892872

Dedication

The Editorial Committee dedicates this handbook to

Dr. Norman W, Frazier

Emeritus Professor ofEntomology, University ofCalifornia, Berkeley

Emeritus Professor ofNematology, University ofCalifornia, Davis

and

Chairman, Editorial Committee, Virus Diseases ofSmall Fruits and Grapevines, 1970

University ofCalifornia, Division ofAgricultural Sciences, BerKeley

R. Casper Corvallis, Oregon

D. Ramsdell August 1987

R. Stace-Smith

R. H. Converse, Chairman
Dr. Norman W. Frazier (1907- )

^rH^n, Agriculture Virus * ■■ ^^^^ Diseases B^ ^^^^•Ä^ir^^^*

ÄSeaS of Small

Service

Agriculture R, H. ConversG, Editor

Handbook

Number 631

For sale by the Superintendent of Documents, U.S. Government Printing Office

Washington, D.C. 20402
Abstract Preface

Converse, R. H., editor, 1987. Virus Diseases of Small Fruits

United States Department of Agriculture, Agriculture Handbook No. 631, 277 p., illus.

This illustrated handbook was compiled by international

authorities on virus and viruslike diseases of small fruits.

Crops covered are in the plant genera Fragaria (strawberry),

Vaccinium (blueberry and cranberry), Ribes (currant and

gooseberry), and Rubus (blackberry and raspberry). The

history, geographic distribution, importance, symptoms,

transmission, cause, detection, and control of virus and

viruslike diseases attacking these crops are discussed.

Keywords: virus, viruslike disease, small fruit, soft fruit.

Fragaria, Vaccinium, Ribes and Rubus, strawberry, blueberry, cranberry, currant, gooseberry, blackberry, raspberry

This handbook is concerned with virus and viruslike diseases

of cultivated Fragaria, Ribes, Rubus, and Vaccinium and is

intended to supersede "Virus Diseases of Small Fruits and

Grapevines" edited by N. W. Frazier and published in 1970

by the University of California Division of Agricultural

Sciences. This handbook, however, considers only the virus

and viruslike diseases of strawberry (Fragaria), blueberries

and cranberries (Vaccinium), currants and gooseberries

(Ribes), and blackberries and raspberries (Rubus). Readers

interested in the vims and viruslike diseases of grapevines

(Vitis) are directed to the recent review by J. K. Uyemoto et

al. 1978, "Grapevine (Vitis) Virus and Virus-Like Diseases,"

Set 1, 29 p. In O. W. Bamett and S. A. Tolin, editors. Plant

Virus Slide Series, College of Agricultural Sciences,

Clemson University, Clemson, S.C. 29631. Many of those

involved in writing this handbook were also authors in the

1970 handbook. Free use has been made of the 1970

handbook material in preparing this handbook; however, the

present authors take full responsibility for their articles. This

handbook was prepared under the auspices of the Small Fruit

Virus Working Group of the International Society for

Horticultural Science (ISHS).

For most papers in this handbook, reviews of the literature

were completed in March 1981.

It is the intention of those of us involved in preparing this

handbook to provide:

1. Information and illustrations to facilitate the identification, management, and control of small fruit virus and

viruslike diseases of the major small fruit crops.

2. Citations to the important primary literature on these

diseases.

3. Notes on major gaps in current knowledge of small fruit

virus and viruslike diseases in the hope of encouraging

additional needed research.

4. Information on nonviral disorders or abnormalities that

may mimic or obscure small fruit virus and viruslike

diseases.

It is the expectation of the Small Fruit Working Group of

ISHS that sufficient progress will have been made in the

decade following publication of this handbook to warrant a

new handbook. Therefore, readers are urged to make

suggestions for improvement and to correct obvious errors

and omissions in this handbook to the senior editor.

I wish to express my thanks and to compliment the many

specialists from all over the world who have contributed to

this handbook. Their knowledge and hard work and that of

the three section editors and Howard Sherman, ARS

technical editor, v/ho worked with me have made this

handbook possible.

R. H. Converse, Chairman

Editorial Committee

Corvallis, Oreg.

VI
Contributing authors

Adams, A. N. East Mailing Research Station, Maidstone,

Kent ME19 6BJ, England.

Baumann, G. Institut für Obstbau und Gemüsebau der

Universität Bonn, D-5300 Bonn, Federal Republic of

Germany.

Casper, R. Biologische Bundesanstalt, Messeweg 11/12,

D-3300 Braunschweig, Federal Republic of Germany.

Chiykowski, L. N. Chemistry and Biology Research

Institute, Research Branch, Canada Agriculture, Ottawa, Ontario KIA 0C6, Canada.

Converse, R. H. USDA-ARS, Department of Botany and

Plant Pathology, Oregon State University, Corvallis,

Oreg. 97331.

Crandall, P. C. Southwestern Washington Research Unit,

Washington State University, 1918 N.E. 78th Street,

Vancouver, Wash. 98665.

Engelbrecht, D. J. Plant Protection Research Institute,

Private Bag X5017, Stellenbosch 7600, South Africa.

Frazier, N. W. Division of Nematology, University of

California, Davis, Calif. 95616

Fulton, J. P. Department of Plant Pathology, University of

Arkansas, Fayetteville, Ark. 72701.

Greber, R. S. Queensland Department of Primary Industry,

Plant Pathology Branch, Meiers Road, Indooroopilly,

Queensland 4068, Australia.

Hancock, J. F. Department of Horticulture, Michigan State

University, East Lansing, Mich. 48824.

Holdeman, Q. L. California Department of Food and

Agriculture, Division of Nursery Services, 1220 N

Street, Sacramento, Calif. 95814.

Johnson, H. A. Driscoll Strawberry Associates, Inc.,

Research Department, 404 San Juan Road, Watsonville,

Calif. 95076.

Jones, A. T. Scottish Crop Research Institute, Invergowrie,

Dundee DD2 5DA, Scotland.

Kim, K. S. Department of Plant Pathology, University of

Arkansas, Fayetteville, Ark. 72701.

Krczal, H. Biologische Bundesanstalt, Institut für Pflanzenschutz im Obstbau, D-6901 Dossenheim, Federal

Republic of Germany.

Leeuw, G. T. N. de. Phytopathological Laboratory Willie

Commelin Schölten, Javalaan 20, Baam, The Netherlands.

Lister, R. M. Department of Botany and Plant Pathology,

Purdue University, West Lafayette, Ind. 47907.

Martin, R. R. Canada Agriculture, Research Station, 6660

N.W. Marine Drive, Vancouver, B.C. V6T 1X2

Canada.

McGrew, J. R. U.S. Department of Agriculture Fruit

Laboratory, BARC-West, Beltsville, Md. 20705.

Meer, F. A. van der. Research Institute for Plant Protection,

P.O. Box 42 6700 AA Wageningen, The Netheriands.

Mellor, F. C. Canada Agriculture, Research Station, 6660

N.W. Marine Drive, Vancouver, B.C. V6T 1X2

Canada.

Morris, T. J. Department of Plant Pathology, University of

California, Berkeley, Calif. 94720.

Murant, A. F. Scottish Crop Research Institute, Invergowrie,

Dundee DD2 5DA, Scotland.

Posnette, A. F. East Mailing Research Station, Maidstone,

Kent ME19 6BJ, England.

Ramsdell, D. C. Department of Botany and Plant Pathology,

Michigan State University, East Lansing, Mich. 48824.

Richardson, J. Department of Entomology, University of

Cahfomia, Berkeley, Calif. 94720.

Schaefers, G. A. Department of Entomology, New York

State Agricultural Experiment Station, Geneva, N.Y.

14456.

Schwartze, C. D. Western Washington Research and

Extension Center, Washington State University, Puyallup. Wash. 98371.

Slack, D. A. Department of Plant Pathology, University of

Arkansas, Fayetteville, Ark. 72701.

Spiegel, S. Agricultural Research Organization, Volcani

Center, P.O. Box 6, Bet Dagan 50-250, Israel.

Stace-Smith, R. Canada Agriculture, Research Station, 6660

N.W. Marine Drive, Vancouver, B.C. V6T 1X2,

Canada.

Stretch, A. W. USDA-ARS, Blueberry and Cranberry

Research Center, Rutgers University, Penn State Forest

Road, Chatsworth, N.J. 08019.

Sylvester, E. S. Department of Entomology, University of

California, Berkeley, Calif. 94720.

Tanne, E. Agricultural Research Organization, Volcani

Center, P.O. Box 6, Bet Dagan 50-250, Israel.

Thresh, J. M. East Mailing Research Station, Maidstone,

Kent ME 19 6BJ, England.

Williams, H. E. (deceased). California Department of Food

and Agriculture, Division of Nursery Services, 1220 N

Street, Sacramento, Calif. 95814.

Wills, A. B. Scottish Crop Research Institute, Invergowrie,

Dundee DD2 5DA, Scotland.
Contents

Page

Section 1.—Virus and viruslike diseases of Fragaria (strawberry) 1

Introduction. R. H. Converse 1

Detection and elimination of virus and viruslike

diseases in strawberry. R. H. Converse 2

Aphid-borne diseases 10

Strawberry mottle. F. C. Mellor and H. Krczal 10

Strawberry vein banding. N. W. Frazier and T. J. Morris 16

Strawberry crinkle. N. W. Frazier, E. S. Sylvester, and J. Richardson 20

Strawberry mild yellow-edge. R. H. Converse, R. R. Martin, and S. Spiegel ... 25

Strawberry Latent C. J. R. McGrew 29

Leafhopper-borne diseases 31

Aster yellows in strawberry. L. N. Chiykowski 31

Strawberry green petal and similar diseases. A. F. Posnette

and L.N.Chiykowski 34

Strawberry lethal decline. CD. Schwartze, N. W. Frazier, and R. H. Converse . 38

¡Strawberry rickettsia yellows and mycoplasma yellows. R. S. Greber 41

(3ther leafhopper-borne diseases of strawberry. L. N. Chiykowski

and A. F. Posnette 45

Nematode-borne diseases 46

European nepoviruses in strawberry. A. F. Murant and R. M. Lister 46

Tomato ringspot virus in strawberry. R. H. Converse and R. Stace-Smith 52

Vectors unknown 55

Strawberry pallidosis. J. P. Fulton 55

Tobacco streak virus in strawberry. R. Stace-Smith, R. H. Converse,

and H. A. Johnson 57

Strawberry chlorotic fleck. J. P. Fulton 60

Minor diseases and those experimentally transmitted only 61

Strawberry leafroll. N. W. Frazier 61

Strawberry feather-leaf. N. W. Frazier 62

Strawberry pseudo mild yellow-edge. N. W. Frazier 63

Tobacco necrosis virus in strawberry. R. H. Converse, R. R. Martin,

E. Tanne, and S. Spiegel 64

wStrawberry witches'-broom and multiplier diseases. R. H. Converse 66

Minor or little-known virus and viruslike diseases of strawberry.

R. H. Converse 68

Virus and viruslike diseases experimentally transmitted

to strawberry. R. H. Converse 69

Nongraft transmissible diseases and disorders 69

Strawberry June Yellows. A. B. Wills 69

Bud and leaf nematodes of strawberry. D. A. Slack and J. P. Fulton 72

Cyclamen mite damage in strawberry. G. A. Schaefers 73

Potato leafhopper injury in strawberry. G. A. Schaefers 75

Miscellaneous arthropod damage in strawberry. G. A. Schaefers 76

Heat spot of Fragaria vesca. J. P. Fulton 78

Strawberry herbicide damage and nutritional imbalances. P. C. Crandall 79

Strawberry literature cited 85

vni
Section 2. — Virus and viruslike diseases of Vaccinium (blueberry and

cranberry) 101

Introduction. D. C. Ramsdell, J. F. Hancock, and A. W. Stretch 101

Aphid-borne diseases 103

Blueberry shoestring. D. C. Ramsdell 103

Leafhopper-borne diseases 106

Blueberry stunt. D. C. Ramsdell and A. W. Stretch 106

Witches'-broom of Vaccinium. G. T. N. de Leeuw 108

Cranberry false blossom. A. W. Stretch 110

Nematode-borne diseases 112

Blueberry leaf mottle. D. C. Ramsdell 112

Necroticringspot of blueberry. D. C. Ramsdell 114

Peach rosette mosaic virus in blueberry. D. C. Ramsdell 116

Tomato ringspot virus in blueberry. D. C. Ramsdell 117

Vectors unknown 119

Blueberry mosaic. D. C. Ramsdell and A. W. Stretch 119

Red ringspot of blueberry. D. C. Ramsdell, K. S. Kim, and J. P. Fulton 121

Ringspot of cranberry. A. W. Stretch 123

Vaccinium literature cited 124

Section 3. — Virus and viruslike diseases of Ribes (gooseberry and black

and red currant) 127

Introduction. R. Casper 127

Detection of virus and viruslike diseases in Ribes. A.N. Adams

and J. M. Thresh 127

Virus and viruslike diseases of gooseberry 129

Aphid-borne diseases 129

Gooseberry vein banding. A. N. Adams and A. F. Posnette 129

Nematode-borne diseases 131

Gooseberry deterioration. F. A. van der Meer 131

Latent infection of gooseberry with arabis mosaic virus. F. A. van der Meer . . 131

Viruslike disorders 132

Gooseberrry mosaic and leaf malformation of gooseberry. A. N. Adams .... 132

Virus and viruslike diseases of black currant 133

Mite-borne diseases 133

Reversion of black currant. A. N. Adams and J. M. Thresh 133

Aphid-borne diseases 136

Green mottle of black currant. A. N. Adams and J. M. Thresh 136

Vein clearing and vein net disease of black currant. A. N. Adams

and J. M. Thresh 137

Nematode-borne diseases 139

Yellow mottle of black currant. A. N. Adams and J. M. Thresh 139

Other nepoviruses isolated from black currant. A. N. Adams

and J. M. Thresh 140

IX
Vectors unknown 140

Black currant yellows. J. M. Thresh 140

Infectious variegation. A. N. Adams and J. M. Thresh 141

Viruslike disorders 142

Viruslike disorders. A. N. Adams and J. M. Thresh 142

Spring vein banding 142

Aphid damage 142

Damage of leaves by eriophyid mites 142

Sectorial chimaera 143

Virus and viruslike diseases of red currant 143

Aphid-borne diseases 143

Red currant vein banding. F. A. van der Meer . 143

Green mottle of red currant. F. A. van der Meer 145

Nematode-borne diseases 146

Spoon leaf of red currant. F. A. van der Meer 146

Infection of red currant with arabis mosaic and strawberry latent

ringspot viruses. F. A. van der Meer 148

Tomato ringspot virus in red currant. H. E. Williams, Q. L. Holdemann,

and R. Casper 149

Leaf pattern of red currant. F. A. van der Meer 150

Vectors unknown 152

Yellow leaf spot of red currant. F. A. van der Meer 152

Interveinai white mosaic. F. A. van der Meer 153

Full blossom of red currant. F. A. van der Meer 155

Viruslike disorders 158

Leaf malformation of red currant. F. A. van der Meer 158

Budlessness of red currant. F. A. van der Meer 160

Aides literature cited 162

Section 4. — Virus and viruslike diseases of Rubus (raspberry and

blackberry) 157

Introduction. R. Stace-Smith 167

Aphid-borne diseases 168

Raspberry mosaic. R. H. Converse, R. Stace-Smith, and A. T. Jones 168

Rubus ytWovj net. R. Stace-Smith and A. T. Jones 175

Black raspberry necrosis. R. Stace-Smith and A. T. Jones 178

Raspberry leaf mottle and raspberry leaf spot. A. T. Jones 183

Raspberry leaf curl. R. Stace-Smith and R. H. Converse 187

Cucumber mosaic virus in raspberry. A. T. Jones 191

Thimbleberry ringspot. R. Stace-Smith 192

Raspberry vein chlorosis. A. T. Jones, A. F. Murant, and R. Stace-Smith 194

Leafhopper-borne diseases 197

Rubus stunt. F. A. van der Meer I97
Nematode-borne diseases 204

Raspberry yellow dwarf and associates diseases of Ruhus caused by arabis

mosaic and strawberry latent ringspot viruses. A. F. Murant 204

Raspberry ringspot and associated diseases of Rubus caused by raspberry

ringspot and tomato black ring viruses. A. F. Murant 211

Cherry leaf roll virus in Rubus. A. T. Jones 220

Tomato ringspot virus in Rubus. R. Stace-Smith and R. H. Converse 223

Tobacco ringspot virus in Rubus. R. Stace-Smith 227

Pollen-borne diseases 229

Raspberry bushy dwarf. A. F. Murant 229

Vectors unknown 235

Tobacco streak virus in Rubus. R. Stace-Smith 235

Wineberry latent virus. A. T. Jones 239

Cherry rasp leaf virus in Rubus. A. T. Jones 241

Bramble yellow mosaic. D. J. Engelbrecht 243

Blackberry calico. R. H. Converse 245

Miscellaneous virus and viruslike conditions and disorders 246

Apple mosaic virus in Rubus. G. Baumann, R. Casper, and R. H. Converse . . . 246

Rubus virus diseases of minor or undetermined significance. R. Stace-Smith . . . 248

Rubus diseases in Great Britain with presumed but unproved viral etiology.

A. T. Jones 250

Viruslike disease symptoms in Rubus in Great Britain. A. T. Jones 251

Rubus literature cited 254

Trade names are used in this publication solely for the purpose specific information. Mention

of a trade name does not constitute a guarantee or warranty of the product by the U.S. Department of Agriculture or an endorsement by the Department over other products not

mentioned.

Copies of this publication can be purchased from the Superintendent of Documents,

Government Printing Office, Washington, DC 20402.

Microfiche copies can be purchased from the National Technical Information Service,

5285 Port Royal Road, Springfield, VA 22161.

Agricultural Research Service has no additional copies for free distribution.

XI
Xll
/Section 1.

iH^irus and Viruslike Diseases of Fragaria

(Strawberry)/;

Introduction

By R. H.jConverse

The period between the publication of "Virus Diseases of

Small Fruits and Grapevines" (Frazier 1970b) and the

publication of this present handbook has been one of major

advances in our knowledge of strawberry viruses and

viruslike diseases. A few important new viruslike diseases

have been described, like strawberry rickettsia yellows and

mycoplasma yellows in Australia. (See "Strawberry Rickettsia Yellows and Mycoplasma Yellows," p. 41.)

Important advances have also been made in biology,

characterization, detection, and control of many major

strawberry virus diseases. (The term "virus" will often be

substituted hereafter for the more accurate but cumbersome

phrase "virus and viruslike diseases.") Important and

economically damaging interactions among viruses in

strawberry have been discovered, for example, between

pallidosis agent and several viruses, particularly strawberry

mild yellow-edge virus. (See "Strawberry Pallidosis," p. 55,

and "Strawberry Mild Yellow-Edge," p. 25.) Vectors have

been identified for viruses that can infect strawberry. Important virus-vector relationships have been discovered, as for

instance, the sites of nepovirus attachment in the alimentary

canals of some vector nematodes. (See Murant "European

Nepoviruses in Strawberry," p. 46.) For another example,

the ability of nonvector aphids to transmit strawberry crinkle

virus that has been injected into their hemoceles has been demonstrated. (See "Strawberry Crinkle," p. 20.)

The discovery that mycoplasmalike organisms and rickettsialike agents are associated with a number of leafhopperbome yellows diseases of plants led to their description in a

number of the yellows diseases of strawberry. (See the

chapters on strawberry leafhopper-bome diseases, p. 31.)

The viruslike particles associated with a number of the major

strawberry virus diseases have been observed. These include:

strawberry mottle (p. 10), strawberry mild yellow-edge (p.

25), strawberry crinkle (p. 20), and strawberry vein banding

virus, whose relationship to the caulimovirus group was also

confirmed by serological studies (p. 16).

In 1970, among the viruses infecting strawberry, only the

nepoviruses could be detected by serological studies (p. 46).

At present, serodetection is also possible for strawberry mild

yellow-edge (p. 25), strawberry vein banding (p. 16), and tobacco streak virus in strawberry (p. 57), and promising

results have been achieved for the serological detection of

strawberry green petal disease agent in Great Britain (M. F.

Clark, D. J. Barbara, and D. L. Davies, unpublished data).

The technologies of enzyme-linked immunosorbent assay

(ELISA) and immunospecific electron microscopy (ISEM)

have been added to existing methods of radioimmunoassay

(RIA) to provide increased sensitivity for the detection of

strawberry viruses against which specific antisera have been

developed. (See "Detection and Elimination of Virus and

Viruslike Diseases in Strawberry," p. 2.)

The control of strawberry virus diseases has been improved

since 1970 by the application of improved methods of heat

therapy and shoot apex culture for virus eradication from

clones, by the development of Fragaria indicator clones of

increased sensitivity and superior methods of leaf grafting to

assess the virus status of suspect clones, and by the

application of ELISA to virus detection in strawberry clones

where suitable antisera had been developed. (See "Detection

and Elimination of Virus and Viruslike Diseases in

Strawberry," p. 2.) Preliminary steps have also been taken

toward the development of strawberry cultivars that will not

support or only poorly support colonization by aphid vectors

of specific viruses, as well as to develop cultivars that possess

genetic immunity or tolerance to virus infection. (See

"Detection and Elimination of Virus and Viruslike Diseases

in Strawberry," p. 2.)

Despite the progress made in the last decade in strawberry

virus research, rapid methods have not yet been developed to

supplement bioassay detection procedures for the detection of

most of the aphid-borne viruses and leafhopper-bome

viruslike diseases of strawberry. The natural means of

spread, aside from clonal propagation, have not been

identified for pallidosis and chlorotic neck diseases, nor have

the causal agents associated with these and a number of other

strawberry diseases been characterized.

I wish to take this opportunity to thank the many research

workers around the world who contributed to the preparation

of the strawberry virus section of this handbook. To those

who wrote, who supplied photographs, and who provided

data from their unpublished research, the readers of this

section are in your debt.

For animal taxa, the following sources were used:

Aphids: Eastop, V. F., and D. H. R. Lambers. 1976. Survey

of the world's aphids. W. Junk, Publishers, The Hague.

537 p.

Cicadellidae: Nielson, M. W., 1968. The leafhopper vectors

of phytopathogenic viruses (Homoptera, Cicadellidae)
taxonomy, biology, and virus transmission. U.S.

Department of Agriculture Technical Bulletin No. 1382,

386 p.

Nematodes: Southey, J. F. 1978. Plant nematology. Ministry

of Agriculture, Fisheries and Food. Her Majesty's

Stationery Office, London. 440 p.

Arthropods: Sutherland, D. W. S., Chairman. 1978.

Common names of insects and related organisms.

Entomological Society of America. 132 p.

For plant taxa, the following source was used:

Kelsey, H. P., and W. A. Dayton, editors, 1942.

Standardized plant names. 2d ed. J. H. McFarland,

Harrisburg, Pa. 673 p.

I wish also to express my thanks to P. W. Oman, Sr.,

Emeritus Professor of Entomology, Oregon State University,

for his considerable assistance with arthropod taxa during the

preparation of this handbook.

Detection and Elimination of Virus and Viruslike

Diseases in Strawberry/;

By R. H.jConverse

Introduction

Wherever cultivated strawberry (Fragaria X ananassa

Duch.) is grown, virus and viruslike diseases cause major

losses in the quantity and quality of the crop. More than 28

virus and viruslike diseases (hereafter collectively called

virus diseases) are discussed in the strawberry section of this

handbook. This number probably is only a portion of the total

number of such diseases affecting this crop worldwide

(Nourriseau 7979), As noted in the description of individual

diseases that foliov^ in this section, not all are major or occur

everywhere strawberries are grown. Strawberry cultivars

differ markedly in their genetic susceptibility to these

diseases, ranging from completely susceptible through

tolerant to immune. Both tolerance and immunity to plant

viruses and to their vectors can be selected. Strawberry plant

breeding programs utilizing such groups of genes are being

investigated at present in several laboratories (Barritt and

Shanks 1980; Barritt and Daubeny 1982; Crock and Shanks

1982).

The economic loss from virus diseases as measured in

decrease in yield and quality of fruit per unit area has been

determined by a number of workers in studies that differ in

viruses, cultivars, and locations chosen. Under the heading

"Economic Importance" in each of the individual chapters of

this section, data bearing on this question are presented. It is

important to remember that few strawberry viruses act singly

or exert their effects under ideal environmental circumstances. The interactions among cultivars, viruses in combinations or strains, and stressful environments can profoundly

influence the degree of economic loss. However, even when

strawberry virus diseases are so severe that yield is

negligible, it is usually impossible to determine by inspecting

the plants what causal agents are present. Therefore, a

number of direct and indirect detection procedures (table 1 )

have been developed to make correct diagnoses. Careful

reviews of this subject have been prepared (Fulton and

McGrew 1970; Fulton 7977).

Methods of Virus Detection

Self-indicating diseases and false symptoms. Some diseases like aster yellows, green petal, lethal decline, rickettsia

yellows, mycoplasma yellows, leafroll, witches'-broom, and

multiplier plant cause characteristic symptoms in strawberry

cultivars. (See these specific chapters.) Problems may arise

in the detection of these diseases in daughter plants that are

taken from recently infected mother plants. Infected daughter

plants will usually exhibit characteristic symptoms but may

not do so at digging time in early spring. Lethal decline

disease (Schwartze and Frazier 1964), for instance, sometimes requires extensive roguing of mother plant-daughter

plant systems in late autumn and winter in the Pacific
Table 1.—Recommended methods of detection and identification of strawberry viruses and viruslike diseases

Antiserum Sap transavailable missible Preferred Transmission Thermotherapy

Diagnostic for ELISA to herb- indicator(s) by vector properties

symptoms or other aceous for leaf graft useful in useful in

Disease in cultivars?* tests? hosts? transmission^ diagnosis? diagnosis? Notes^

Aphid borne:

Crinkle No No No 4, 5 No No Petal streak.

Latent C No No No 5, EMC No No

Mild yellow-edge No Yes-^ No 4,5 No No UC-6 latent

Mottle No No Yes 4, 5 Yes Yes^ by Cf

Pseudo mild yellow- No No No 4, 12, Alp. Yes No 10, 11 latent.

edge.

Vein banding No Yes^ No 6, 12 No No

Leafhopper borne:

Aster yellows Yes No No — No No Distinguish

Green petal Yes No No — No No on herbaceous hosts.

Lethal decline Yes No No — No No

Mycoplasma yellows Yes No No — No No Distinguish

Rickettsia yellows Yes No No

"

No No by electron

microscopy.

Nematode borne:

Arabis mosaic No Yes Yes — No No

Raspberry ringspot No Yes Yes — No No

Straw, latent ringspot No Yes Yes — No No

Tomato black ring No Yes Yes — No No

Tomato ringspot No Yes Yes 4, 5 Alp. No No

Fungus borne:

Tobacco necrosis No Yes3 Yes Yes No Root sap

inoculated to Cq.

Vector unknown:

Chlorotic fleck No No No EMB, EMK No No

Leafroll Yes No No 5 No No

Witches'-broom Yes No No 4, 5 No No

Multiplier plant Yes No No — No No

Feather-leaf Yes No No Alp., 4, 1 No No

June yellows Yes^ No No — No No

Pallidosis No No No 10, 11 No Yes

Tobacco streak No Yes Yes Alp., 4 No No

^The cultivar itself develops symptoms that enable the causal agent to be identified.

2Abbreviations for strawberry indicators: Numbers are for UC indicators 1-12; Alp.

various clones of F. vesca 'East MaUing clone'; Cq = Chenopodium quinoa; Cf =

^From roots only.

^Exceptions noted.

^Heterologous antiserum has been used successfully.

= F. vesca var. semperflorens 'Alpine'; EMB, EMC, EMK

Chaetosiphon fragaefolii.

Northwest of the United States where this disease is a threat

in nursery fields so that infected but symptomless daughter

plants can be culled out.

When diagnosing viruslike symptoms in the field, another

problem confronts the grower. A number of nontransmissible

conditions, including mineral deficiencies and imbalances;

fungus-, bacteria- and pesticide-induced symptoms; and

symptoms caused by arthropod pests, may mimic, complicate, or obscure the diagnosis of transmissible virus disease

symptoms. Several chapters in this strawberry section are

devoted to these abnormalities so as to assist readers in

distinguishing among them.

Virus detection by grafting methods. Although the first

reports of strawberry virus diseases were made in the 1920s'

(Plakidas 1926, 1927), it was not until Harris {1932)

developed the technique for intergrafting stolons that a ready

method of detection of such strawberry diseases by grafting

became available. At first, susceptible cultivars were used as

indicators. Harris and King (79^2) demonstrated the

sensitivity of Fragaria vesca L. 'East Mailing Clone' or

'EMC to many viruses in strawberry cultivars. 'EMC was

widely used as an indicator plant to detect virus diseases by

the stolon grafting method. Unfortunately, 'EMC was

infected with the latent A strain of crinkle virus (Frazier

1953) (see "Strawberry Crinkle," p. 20), so that cultivars

that had been stolon-graft indexed on 'EMC became infected

with latent A.
A number of other indicator clonal lines have been developed

for strawberry virus detection. These include:

'EMB', 'EMK', and 'HEMV clones of 'EMC that have

been freed of the latent A strain of crinkle virus (Frazier

7974b; Fulton 1960; Converse 7979).

'Alpine', F. vesca var. semperflorens (Duch.) Ser., a

runnerless, seed-propagated clonal line (Harris and King

7942; Frazier 7955a).

'UC-l', F. vesca, a runnering seedling of 'Alpine' (Frazier

and Posnette 7958).

'UC-3', F. vesca seedling (Frazier 1974b).

'UC-4', F. vesca x F. virginiana hybrid (Frazier 7974b).

'UC-5', a complex hybrid of F. vesca., F. chiloensis, and F.

virginiana (Frazier 7974b).

'UC-6', F. vesca x F. virginiana hybrid (Frazier 7974b).

'UC-10', F. virginiana (Frazier 1974b).

'UC-ir, F. virginiana (Frazier 1974b).

'UC-12', F. virginiana (Frazier 1974b).

'FV 72', F. vesca (McGrew 1967).

'Ml', F. virginiana — (King and von Ruden 1962) carrying

pseudo mild yellow-edge disease (Frazier 1966b).

The development of the leaf grafting technique (Bringhurst

and Voth 1956) provided a relatively simple grafting system

whereby the donor plant would not be cross-infected by the

indicator plant. The petiole-insert leaflet grafting technique

has been evaluated by several workers (Cropley 1958; Fulton

19572i\ Jorgensen 7957; Miller 7955). It is now generally

used for graft transmission of strawberry viruses. Several of

these investigators reported that successful leaf graft unions

from known infected donors did not always result in

characteristic symptom development in the indicators.

Frazier (7974a), however, demonstrated that transmission

efficiency could be improved, and the length of incubation

time until the appearance of symptoms in the indicator could

be lessened if all leaves except the grafted ones were

removed from the donor at the time of grafting.

Since the improved leaf grafting techniques developed by N.

W. Frazier are best seen to be learned, figure 1 can be used to

follow details of the procedure. Because of its elasticity and

coherence, Sealtex brand tape is widely used for leaf

grafting. For the delicate job of splitting the indicator petiole

and shaping the donor petiole (fig. IF), surgical scalpels are

satisfactory but become dull quickly. Small pieces of new

razor blades broken off to form a sharp point and held in a

suitable tool (figs. ID and F) are frequently used instead of

scalpels. One to three leaflet grafts are generally made per

indicator plant.

After the grafted plants are held in a mist chamber or a humid

atmosphere in the greenhouse for about 1 week, long enough

for graft union to occur, they are placed on the greenhouse

bench and evaluated periodically for symptom development

for 4 to 35 wk, depending on the disease (Converse 7979). A

subtle but essential part of successful disease detection by

leaflet graft is the maintenance of indicators in a vigorous

state of growth before and after grafting. Moderate

temperatures and light intensities, such as are encountered in

spring and autumn in most greenhouses, are key factors in

growing good indicator plants. The presence of tobacco

necrosis virus and its soil fungus vector, Olpidium brassicae

(Wor.) Dang., appears to cause premature death of older

leaves of F. vesca var. semperflorens 'Alpine', mimicking

one of the major symptoms of mild yellow-edge virus. (See

"Tobacco Necrosis Virus in Strawberry," p. 64, and

"Strawberry Mild Yellow-Edge Virus," p. 25.)

Fragaria virginiana L. clones 'UC-10', 'UC-ll', and

'UC-12' have been reported by Frazier (1974b) to develop

symptoms when graft inoculated with pallidosis disease

agent. (See "Strawberry Pallidosis," p. 55.) No F. vesca

clones have been found that produce distinct symptoms when

graft inoculated with pallidosis agent. F. virginiana

indicators are generally poorer than F. vesca indicators for

the detection of other virus and viruslike diseases of

strawberry. Therefore, it is necessary to use both F. vesca

and F. virginiana indicators to detect the known strawberry

virus and viruslike diseases by leaf grafting. A list of

currently popular strawberry virus indicator clones and their

specific uses is found in table 1.

In several situations, indicators that are already infected with

a virus can be used advantageously to detect mild strains of

other viruses that are challenge inoculated into these indicator

plants. Several virus combinations act synergistically to

produce more severe symptoms than the sum of their

individual symptoms. Examples are latent A strain of crinkle

virus acting synergistically with mottle virus; synergism

between crinkle and vein banding viruses; and synergism

between mild yellow-edge virus and pallidosis agent. (See

individual virus chapters in the "Strawberry" section for

further discussion of individual synergistic reactions.)

Cross-protection between strains of the same virus can also

be utilized in the identification of strawberry viruses. For

example, 'EMC infected with the latent A strain of crinkle

virus is a poor indicator for the detection of other strains of

crinkle virus (Frazier and Posnette 1958). On the other hand,

clones of 'East Mailing' F. vesca that have been freed of

latent A, like 'EMB', 'EMK', and 'HEMV are reasonably

satisfactory for crinkle detection.

Some Fragaria indicator clones fail to express symptoms

when inoculated with certain viruses, and these relationships

can also be used to advantage in graft analysis. For example,

'UC-6' is symptomlessly infected by most strains of mild

yellow-edge virus that have been tested so far, and 'UC-10'

and 'UC-ir are symptomlessly infected by pseudo mild

yellow-edge disease. Other examples of symptomlessly

infected indicators can be found in the individual chapters in

this section and in the paper by Frazier (1974b).

The analysis of multiple virus and viruslike infections in a

single strawberry plant is in an unsatisfactory state. Aside

from the viruses like the nepoviruses, tobacco streak, and.
possibly, strawberry vein banding virus and strawberry mild

yellow-edge virus, (see chapters on these viruses) which can

be detected serologically, all of the other virus and viruslike

diseases of strawberry that do not cause diagnostic symptoms

in fruiting cultivars must presently be detected and identified

by a combination of graft and vector transmissions to

indicator hosts. In the cases of multiple infected strawberry

plants that are severely weakened by these viruses, it may be

difficult to obtain leaflets of sufficient vigor and size to make

leaflet grafts to indicators. Moreover, there is no assurance,

even if grafts survive, that the entire complement of viruses

and their strains will become established in the indicator

plant. The same holds true when vector transmission is used.

Conversely, it is not possible to predict with confidence that a

disease complex can be generated by leaflet grafting a

number of virus isolates into a test plant. Evaluation in the

field is still the method of choice for rating strawberry

cultivars and selections for their tolerance to virus and

viruslike diseases, not only because of the technical

difficulties connected with experimental inoculation but

because of the interplay of pathogenic strains and environmental stresses that comes with field testing.

Vector transmission. Aphids, leafhoppers, and nematodes

have been found to transmit various virus and viruslike

diseases to strawberry. Details are given in the "Natural and

Experimental Transmission" portions of the individual

chapters of this section. Because of difficulties in handling

them and the long incubation periods involved, transmission

by leafhoppers and nematodes is seldom used as a diagnostic

tool for identification of strawberry virus and viruslike

diseases. Where the aphids of the genus Chaetosiphon are

vectors, transmission properties are often useful in the

detection of these diseases. As detailed in the various

"Natural and Experimental Transmission" portions of

individual chapters, aphids like C. fragaefolii (Cock.) can be

used to acquire and transmit certain viruses to suitable

indicator plants. This is the method of choice for strawberry

mottle virus identification. Where a complex of aphid-borne

diseases is present in a strawberry clone and detection of the

causal agents involved is desired, sequential feeding of

aphids from this source plant on a succession of indicator

plants may facilitate the separation of the component causal

agents by chance or by differences in their retention and

transmissibility by the vector.

Sap transmission to herbaceous plants. Several viruses

causing diseases of strawberry can be transmitted by sap

inoculation to various herbaceous host plants. As detailed

under "Natural and Experimental Transmission" portions of

these virus chapters, the nematode-bome viruses, tobacco

streak virus, tobacco necrosis virus, and strawberry mottle

virus are sap transmitted. Chenopodium quinoa Willd. is a

good herbaceous test plant for such sap transmissions,

especially when it is growing vigorously under mild

greenhouse temperature and light conditions. Strawberry

plants are usually at their best as sap inoculation sources

when in the early shock stages of infection. Various buffers

are used, but 2 to 3% nicotine alkaloid, often with various

additives (Converse 7979), and 2% polyvinylpyrrolidone

(mol. wt. 10,000) in 0.05M phosphate pH 7 (Martin and

Converse 1982a) are useful buffers. Symptoms usually

develop within 2 wk, but are seldom diagnostic. As described

subsequently, however, sap from infected herbaceous

indicator plants can be used for diagnostic serological tests

when such antisera are available.

In the case of strawberry mottle virus, Chaetosiphon

fragaefolii will transmit this virus to Chenopodium quinoa,

producing diagnostic chlorotic spots on inoculated leaves

within 2 wk after inoculation (Frazier 1968b).

Serological detection methods for strawberry viruses. At

present, only 9 of the 28 named virus and viruslike diseases

of strawberry have had specific antisera prepared against

them, or antisera that will react with them. These are the

nepoviruses, tobacco streak virus, tobacco necrosis virus,

strawberry mild yellow-edge virus, and strawberry vein

banding virus. One of the critical needs in present-day

strawberry virology is the development of specific antisera

against the many economically important strawberry viruses

for which such sera are lacking. This author is of the opinion

that satisfactory detection of viruses and viruslike diseases in

strawberry is dependent upon the production of a complete

set of antisera that span the range of these economically

important diseases or upon the development of alternate,

rapid, sensitive, biochemical detection procedures for the

causal agents of these diseases. The application of

monoclonal antibody techniques (Kennett et al. 1980) to

strawberry viruses offers increased opportunity for developing new and effective antisera.

Where antisera do exist and are available to the investigator,

a number of serological tests are available that detect these

viruses rapidly and with great sensitivity. Enzyme-linked

immunosorbent assay (ELISA) is a technique that is

increasing in popularity for the detection of viruses in

perennial crops, including strawberry (Clark 1981; Barbara

and Clark 1982; Converse and Martin 1982; Johnson et al.

1984). Agar gel double diffusion serology and immunospecific electron microscopy are also useful or promising

serological techniques for strawberry virus detection (Milne

and Luisoni 7977; Converse 1981).

Nonserological biochemical methods of detection of

strawberry viruses. In the rapidly developing field of

nucleic acid biochemistry, several techniques have become

available that offer opportunities for biochemical detection of

strawberry viruses and viruslike diseases by other than

serological means. This approach may become important for

strawberry virus detection because of the general difficulty of

purifying viruses directly from strawberry tissue or transmitting them to more manageable hosts from which purification

could be more readily accomplished. The isolation of

disease-specific nucleic acids, such as double-stranded RNA
B
Figure I.

— Steps in leaf grafting. Fragaria vesca

'UC-4': A. indicator plant before grafting and supplies

and tools: B. pruned toa single leaf before grafting; C.

center leaflet removed to be replaced witha grafted

donor leaflet; D. splitting the petiole; E. preparing the

donor leaf graft insertion by removing all but the center

leaflet; F. trimming the petiole of the donor leaflet intoa

long, sharp spear; G, completely trimmed donor leaflet;

H. stretching Sealtex brand self-cohering tape to wrap

the leaflet graft; /. inserting the donor leaflet into the

petiole and beginning the wrapping procedure (the

donor leaflet should be wedged Hrmly into place before

wrapping); J. wrapping the graft, the Sealtex tape must

be held taut during the entire wrapping process; K. using

two fingers to maintain tension on the Sealtex tape

during the wrapping process while bringing the tape

around the petiole to continue wrapping with the other

hand; Z., leaflet graft completed, graft is then held in an

intermittent mist chamber for 10 days before being

placed on the greenhouse bench. (Photographs courtesy

of Katherine Kowalczyk. agricultural research technician. L'SDA-ARS, Corvallis, Oreg.. according to

methods demonstrated by N. W. Frazier.)

,^
(Morris and Dodds 1979) or viroid RNA (Morris and Smith

7977), has required some modifications of the existing

procedures because of the high content of polysaccharides in

strawberry extracts. The potential for using rapid nucleic acid

detection methods for routine diagnosis of disease agents

where serology is impractical was dramatically illustrated

using cloned DNA for the detection of viroid in potatoes

(Owens and Diener 1981). The potential for using such

procedures for routine diagnosis of strawberry viruses and

viruslike disease offers new opportunity for understanding

the disease complexes and possibly controlling the diseases.

Methods of Virus Elimination in Strawberries

Seed transmission and its elimination. As noted in specific

chapters dealing with these viruses, the nepoviruses viruses,

tobacco streak virus, and June yellows are all seed

transmitted in varying percentages in strawberry when the

seed or pollen parent is infected. None of the aphid-borne,

leafhopper-bome, nor other strawberry virus diseases for

which vectors are not known have so far been found to be

seedbome. Viruses spread in strawberry seed rarely produce

recognizable symptoms in the resulting seedlings; however,

all of these viruses (but not June yellows) can be detected

serologically so that the parents involved in controlled

pollinations can be tested serologically to avoid the

production of symptomless, infected seedling progenies.

Seed from open-pollinated crosses can be evaluated by

ELISA for tobacco streak virus (Johnson et al. 1984), and

probably many of the nepoviruses can be similarly detected

by direct assay of the dormant seed samples.

Methods of elimination of viruses and the causal agents

of viruslike diseases in strawberry clones.

Chemotherapy. Although there is a growing literature in the

chemotherapy of plant viruses (Matthews 1981) the few

reports of chemotherapy of strawberry viruses have either

been negative (Miller and Vaughan 7957; Miller and Garren

1966) or have not been repeated (Fulton 1954). Additional

research on strawberry virus chemotherapy using promising,

recently studied chemicals should be attempted. The

chemotherapy of the viruslike diseases June yellows and

rickettsia yellows is reviewed in the chapters in this section

on those diseases.

Thermotherapy. Some viruses and viruslike agents are

eliminated in plant tissues that are grown at continuous

elevated temperatures around 37° C or do not develop in plant

cells formed at this temperature (Nyland and Goheen 1969).

Posnette (1953b) was the first to eliminate a virus from

strawberry by hot air therapy. Hot water therapy has also

been studied (Miller 1953). Hot air therapy alone and in

conjunction with tissue culture of shoot apices, as noted

subsequently, has been successfully used to develop clones

of many strawberry cultivars that are free of known virus

diseases (table 2). (See individual strawberry chapters for

numerous examples.)

Strawberry plants to be heat treated are generally grown in

large pots without transplanting for several months prior to

treatment to develop a large root system with good

carbohydrate reserves. Inserting the pot into a somewhat

larger pot and filling the intervening space with peat moss

may help reduce damage to the root system during

thermotherapy. Growth chambers are frequently programed

for 18 hr/day of 20,000 lux (ñuorescent plus incandescent

lights) at the leaf surface for the heat treatment. Plants are

often placed in the growth chamber at greenhouse ambient

temperature, and the growth chamber temperature is then

raised a few degrees a day up to 37° C or higher (Bolton

7967).

Strawberry viruses and viruslike diseases differ markedly in

their tolerance to thermotherapy. Strawberry mottle virus

strains (with an exception) are readily inactivated in entire

plants by being grown at 37° C for 10 to 14 days (Mellor and

Frazier 1970b). At the other extreme, strawberry leafroll

disease was not eliminated from plants exposed to 4rC for

20 days (Bolton 7970). Strawberry vein banding virus and

strawberry green petal disease are easily eliminated from

whole strawberry plants by growing them at a constant 37°C

or higher for a few weeks (table 2).

Two horticultural techniques have been useful in improving

the rate of success of elimination of virus and viruslike

diseases by thermotherapy. Intentional destruction of the

growing point of a plant during thermotherapy causes

adventitious buds to develop that can be excised when 3 to 20

mm long and rooted under intermittent mist in the greenhouse

(Mellor and Fitzpatrick 7967). In a second technique, after

thermotherapy the crown is surface-sterilized and sliced into

transverse sections. These sections when placed in sand or

peat in the greenhouse will develop adventitious buds from

which shoots and new plants can be obtained (Smith and

Harland 7958; Posnette and Jha 7960).

Certain viruses and viruslike diseases have been eliminated

from strawberry clones that were grown outdoors in a hot

climate (Fulton 7956; Frazier et al. 7965). This "natural

thermotherapy" eliminated some viruses like crinkle, which

are difficult to eliminate in the growth chamber, but did not

as readily eliminate strawberry mottle virus, which is easily

inactivated in the growth chamber.

Prolonged exposure to cold temperatures has eliminated

potato spindle tuber viroid from infected potato cultivars

(Lizárraga et al. 1980). There is a claim that a similar

treatment freed several cultivars from three aphid-borne

viruses (Kacharmazov and Izvorska 1974). This approach

may be worth tr}dng for the elimination of viruses that are

otherwise difficult to eliminate from desirable clones.

Tissue culture for the elimination of viruses and viruslike

diseases from strawberry clones. Belkengren and Miller

(7962) were the first to eliminate a virus (latent A strain of
Table 2.—Thermotherapy and tissue culture for elimination of viruses and viruslike agents in strawberry

Treatment Disease References

Eradication from

whole plants after a few

weeks at 37°C.

Green petal

Latent A strain of crinkle

Mottle

Vein banding

Posnette and Ellenberger 1963.

McGrew and Scott 1964b.

Mellor and Frazier 7970.

McGrew and Scott 1964.

Bolton 7967.

Shoot apex tissue

culture only.

Crinkle

Latent C

Mild yellow-edge

Mottle

Pallidosis

Vein banding

McGrew 1980.

J. R. McGrew, unpublished data.

Mullin et al. 1974.

McGrew 1980\

Mullin et al. 7974.

Mullin et al. 7974, 7975;

McGrew 1980.

McGrew 7980; R. Mullin,

unpublished data.

Plants grown at 37 °C for

several weeks, followed

by crown bud propagation

or shoot apex tissue

culture.

Crinkle

Feather leaf

Mild yellow-edge

Posnette and Cropley 1958\

Posnette and Jha 1960\

Mellor and Fitzpatrick 7967.

McGrew 1970a.

Posnette and Jha 7960; Mellor

and Fitzpatrick 7967; Miller and

Belkengren 796i; Mullin et al.

7974; Mullin et al. 7976.

Treatments ineffective in

eliminating the disease.

June yellows

Leafroll

Lethal decline

(X disease agenti)

Wills 7962; East Mailing 7969;

East Mailing 7970.

Bolton 7970.

R. H. Converse,

unpublished data.

Nienhaus and Sikora 7979.

iX disease agent is possibly related to lethal decline disease agent.

strawberry crinkle virus) from a Fragaria clone by a

combination of heat therapy and excision of runner tips 0.2 to

10 mm long. They developed whole plants from these tips in

a sterile culture medium that was based on previous tissue

culture work with other plants (White 1943). A number of

specific media utilizing agar (Miller and Belkengren 7962;

Miller and Belkengren 1963; McGrew 7965; Boxus 7974)

and filter paper bridges in liquid media (Mullin et al. 7974,

7976) have been reported.

The regeneration of strawberry plants in tissue culture from

small (500 micrometers (ixm)) excised shoot tips is now a

routine practice in the development of strawberry cultivars

free from known viruses and viruslike diseases. McGrew

{1980) has reviewed these techniques and has described the

system used in his laboratory.

Although thermotherapy alone and tissue culture alone are

sufficient to eliminate many virus and viruslike diseases in

strawberry cultivars, the combination of these two techniques

is sometimes advantageous in developing clones free from a

given virus or viruslike agent (table 2). As a routine

procedure, this author currently heat treats all new

USDA-OSU advanced strawberry selections for 8 wk at 37°C

and excises several 500 |xm shoot apices into tissue culture.

Whole plants are allowed to develop without proliferation in

culture and are potted and held in a humidity cabinet in the

greenhouse when they are sufficiently rooted. Established

plants are indexed for diseases by standard methods. They

are evaluated for trueness to horticultural type, and a typical

clone is then increased to supply official certification

programs in insecticide-treated, screened enclosures by

ordinary runner plant propagation. By this means, clones

may be developed that have an increased likelihood of being

free from all virus and viruslike diseases described and as yet

undescribed.

The advent of rapid micropropagation in tissue culture

(Boxus 7974; Boxus et al. 7977) has made it possible to

maintain and increase a large number of strawberry cultivars
in tissue culture (Mullin and Schlegel 1976). However

desirable this may be for the commercial nurseryman, there is

enough uncertainty about the stability of some strawberry

cultivars during long-term tissue culture micropropagation

(Anderson et al. 1982; Swartz et al. 1981) to suggest to this

author the desirability of maintaining the basic clones of

superior virus-tested strawberry stocks by means of traditional runner propagation methods.

Aphid-Borne Diseases

Strawberry Mottle^ i

By F. C. ^Mellor and H.'jKrczal

Additional Common Names

Mild crinkle (Prentice and Harris 1946) or virus 1 (Prentice

1948) was later identified as mottle virus (MV) combined

with the latent A strain of crinkle virus (see "Strawberry

Crinkle," p. 20). Type 1 (Demaree and Marcus 7957) was

identified by McGrew (1956) as MV with either latent A or

latent C (see "Strawberry Latent C," p. 29).

History and Geographic Distribution

Mottle is the most widespread of the viruses of strawberry,

occurring wherever strawberries are grown. Until virustested stock was provided by heat therapy, most of the older

cultivars were universally infected.

In early reports of virus diseases of strawberry, there was

some confusion between MV and mild strains of crinkle virus

(CV). This was because symptoms of MV were first

described on a clone of Fragaria vesca L. cv. 'EMC that

was infected with latent A, a very mild strain of CV and,

when MV and CV occur together, crinkle symptoms

predominate. Clone 'EMC had been selected as an indicator

at East Mailing in Great Britain because of its superior

sensitivity to strawberry viruses (Harris and King 7942).

When Harris (1938) first transmitted a virus to 'EMC by

grafting from apparently normal plants of the strawberry cv.

'Royal Sovereign', symptoms on the indicator resembled

those of the mild CV described and illustrated by Zeller

(1933). Although Harris recognized that the disease might be

etiologically distinct from severe CV, he referred to it as

"mild crinkle," and for many years this name was used both

for mild strains of CV and for combined infection with MV

and latent A.

MV was subsequently transmitted to 'EMC, not only from

apparently normal cultivars, but also from plants showing

severe degeneration. By serial transfers of infective aphids to

a succession of indicator plants. Prentice (1946) separated the

viruses causing yellow-edge of 'Royal Sovereign' into "mild

crinkle," which persisted in the vector for only a few hours,

and mild yellow-edge, which persisted for several days.

Similarly, Wood and Whitehead (1947) and Mellor and

Fitzpatrick (1951) separated virus complexes causing the

diseases known as "severe crinkle" and "yellows" into

nonpersistent and persistent components. Vector relations of

the component viruses distinguished the nonpersistent "mild

crinkle" or MV from the persistent components, crinkle and

mild yellow-edge. It was not until Frazier (1953) detected the

10
latent A strain of CV in 'EMC that the sensitivity of the

clone was explained, and the symptoms of MV were

distinguished from those of MV with latent A.

The term "mottle" was first used by Thomas (1949) to

describe symptoms on Fragaria vesca L. var. californica

(Cham, and Schlecht.) Staudt, which he used to index

apparently normal 'Marshall' plants. Prentice (1948)

changed the name "mild crinkle" to "virus 1", and finally

(1952) substituted the name "strawberry mottle virus." "Mild

crinkle" was still being applied to MV in publications

appearing as late as 1954 but, where reference was made to

the nonpersistence of the virus in the vector, the virus can be

assumed to be MV.

Economic Importance

MV alone may reduce the marketable yield of strawberries by

20 to 30% (Freeman and Mellor 1962 ;Hom and Carver 1962;

Aerts 1973). When it occurs in combination with crinkle,

vein banding, or mild yellow-edge viruses, the yield is still

further reduced.

Symptoms on Natural and Experimental Hosts

All species oi Fragaria are susceptible to MV although many

are symptomless hosts. The virus is symptomless in all

commercial strawberry cultivars, but severe strains may

reduce vigor and yield.

Innumerable strains or variants of MV on F. vesca cause a

range of symptoms from barely discernible mottle to severe

degeneration. Field plants often carry a mixture of strains.

The variants described here have been divided into mild,

intermediate, and severe strains, but these divisions are

arbitrary. There is actually a continuous range of symptoms

over the entire range of virulence. Symptoms on inoculated

plants remain stable, but milder variants are commonly

separated during aphid transmission (that is, aphids given

access to a group of MV strains may not always transmit all

of them). Isolates can be stabilized, however, by selection

and repeated aphid transmission.

Symptoms appear on F. vesca 1 to 3 wk after aphidinoculation, usually within 7 to 10 days. On F. vesca

'Alpine', or other strains of F. vesca that are free of latent A

virus, the first symptom of mild or intermediate strains is

mottle of one or more leaflets of the youngest leaf, caused by

chlorosis of the net veins. When only one side of the leaf is

affected, the mottled side is smaller than the other. When the

entire leaf is affected, the leaflets usually curl downward and

expansion of the leaflets may be delayed. The youngest

petiole is shorter than normal and may be reflexed. Severe

strains may cause necrosis of one or two young leaves.

On these F. vesca indicators, chronic symptoms of mild

strains consist of general diffuse mottle, varying in severity

from very faint to distinct. Even strains that cause distinct

symptoms may cause little loss of vigor, and the leaves are

Figure 2.—Chronic symptoms of strawberry mottle

virus in Fragaria vesca 'Alpine'. Left, moderate strain;

right, severe strain.

Figure 3.—Chronic symptoms of two strains of

strawberry mottle virus each in two indicators. Left to

right: Moderate strain in Fragaria vesca 'UC-I', severe

strain in F. vesca UC-I", moderate strain in F. vesca

'EMC. severe strain in F. vesca 'EMC.

nearly normal in size and shape. Intermediate and severe

strains cause little or no distinct mottle, but the veins are

finely cleared and often fused (figs. 2 and 3). Intermediate

strains cause moderate loss of vigor and slight crown

proliferation. Leaves are smaller than normal, with some

leaflets narrow at the base (fig. 3, left). Severe strains cause

extreme loss of vigor and much crown proliferation. Leaves

are small and may be distorted (fig. 2, right). Petioles are

irregular in length, slender, and often slightly curled. Stolon

production is scant, and runner plants produce roots very

slowly, if at all.

On F. vesca 'EMC, which is infected with latent A virus,

symptoms of any strain of MV are more severe than they are

on F. vesca clones that are free of latent A (fig. 3). Shock

(early) symptoms on 'EMC usually include epinasty and

unequal leaflet development of the youngest leaf, with

chlorosis of the smaller leaflet (ñg. 4). Severe MV strains

may also cause necrosis of one or more leaflets, curling and

11
Figure 4.—Early symptoms of strawberry mottle virus

in Fragaria vesca "EMC; -4. Mild strain; B. moderate

strain; C. severe strain.

necrosis of stolon tips, and sometimes death of the plant.

Subsequent symptoms become progressively milder until

they stabilize at the symptom expression characteristic of the

strain. In contrast, tobacco streak virus often causes a group

of very young leaves to die, but subsequent growth is

symptomless except for excessive reddening of petioles. (See

"Tobacco Streak Virus in Strawberry," p. 57.) Tomato

ringspot virus can also cause death of young leaves in grafted

F. vesca but with accompanying severe epinasty. (See "Tomato Ringspot Virus in Strawberry, "p. 52.)

On 'EMC, chronic symptoms of mild strains consist of small

chlorotic spots, faintly cleared veins, and mild mottling, with

little distortion of the leaves (fig. 5^4). Intermediate strains

induce small, scarlike, opaque, chlorotic spots that cause

severe distoration of the leaves (fig. 3). Veins are finely

cleared and often fused, leaves are small, vigor is reduced,

and there may be crown proliferation (fig. 55). Severe strains

cause few chlorotic spots and little leaf distortion, but leaves

are very small and marginal dentation is greatly reduced (fig.

3). There is much crown proliferation and extreme debility

(fig. 5C). Chronic symptoms of 12 MV variants in 'EMC are

illustrated in fig. 6.

Symptoms in complexes with other viruses. Together,

mottle and vein banding viruses cause no symptoms in

cultivars, but vigor and yield may be significantly reduced

(Freeman and Mellor 1962). In F. vesca, symptoms of both

viruses can be discerned, but those of mottle predominate.

MV and CV interact synergistically, both in cultivars and in

indicators. Symptoms are of the crinkle type, the severity

depending on the virulence of each component virus. With

the mildest strains of crinkle, however, even virulent strains

of MV may be symptomless in cultivars.

MV plus mild yellow-edge virus cause the disease known as

xanthosis, yellows, or yellow-edge. Addition of the

Pallidosis agent (see "Strawberry Pallidosis," agent (see

"Strawberry Pallidosis," p. 55) may intensify yellows disease symptoms. Symptoms on sensitive cultivars and on indicators are characterized by chlorosis of the younger leaves,

especially near the margins. The plants are dwarfed, leaflets

cupped, petioles short, and the size and number of berries are

markedly reduced.

Experimental hosts. In addition to Fragaria, experimental

hosts include species oí Potentilla, a genus closely related to

Fragaria. Inoculated plants of P. adscherica Somm. and

Lev. developed vein chlorosis. A distortion of the veins of

some of the youngest leaves was observed as an initial

symptom (Maassen 1959). Three species, P. canadensis L.,

P. sterilis (L.) Garcke, and P. táurica Willd. remained

symptomless after infection with MV, but graft transmission

from them to F. vesca induced typical symptoms (Demaree

and Marcus 1951; Whitehead and Wood 1946: Maassen

1959). In an experiment with P. recta L., not all of the

diseased plants developed symptoms. For this reason, further

investigations are needed to ascertain that the observed

alterations (small leaves with shortened petioles) are caused

by MV (Maassen 1959).

12
Figure 5.—Chronic symptoms of strawberry mottle

virus in Fragaria vesca "EMC: A, Mild strain; B.

moderate strain; and C. severe strain.

^S4ii

%^^

«^ «4» «^

Figure 6.—Chronic symptoms of 12 variants of

strawberry mottle virus In Fragaria vesca 'EMC, All

originated from one apparently healthy strawberry

plant, and were separated during aphid transmissions.

Top leaf is normal.

Frazier (1968) reported Chenopodium quinoa Willd., C.

amaranticolor Coste and Reyn., C. album L., Cyamopsis

tetragonoloba (L.) Taub., and Gomphrena globosa L. as

experimental hosts of MV.

Inoculated leaves of C. quinoa developed chlorotic spots

followed by diffuse vein chlorosis and mottling of young

leaves (fig. 7). The chlorotic spots became necrotic, and a

chlorosis and necrosis developed along main veins and

adjacent tissues. The leaves dropped prematurely. Chronic

symptoms consisted of a mosaic pattern of chlorosis, necrotic

spotting, crinkling, and curling of the leaves. The plants were

stunted. On inoculated C. amaranticolor, vein clearing

appeared most frequently in the basal portion of maturing

leaves, followed by small spots which became necrotic with a

narrow red border. After inoculation with MV, young leaves

of C. album developed a vein clearing followed by small,

gradually enlarging spots, which developed pale necrotic

centers with red margins and which frequently coalesced.

Red lesions appeared on main veins and petioles.

On C. tetragonoloba. chlorotic spots on the inoculated leaves

were followed by vein clearing on young leaves. Plants

13
Figure 7.—Symptoms of strawberry mottle virus

aphid-transmitted by Chaetosiphon fragaefolii to Chenopodium quinoa.

(Courtesy R. R. Martin. Agriculture Canada.)

became stunted and dwaifed. The young leaves showed

chlorosis, distortion, epinasty, and necrotic spotting; the

older leaves showed spreading chlorosis with small green

spots and necrotic spotting. The plants died within 4 to 6 wk

after onset of symptoms. G. globosa appeared symptomless,

but the virus was sap-transmitted from it to C. quinoa.

Symptoms developed on Asclepias syriaca L. 2 to 3 wk after

dodder transmission of MV plus strawberry latent A or latent

C virus. These symptoms of chlorotic areas on leaves were

sometimes followed by general chlorosis, necrosis, and

defoliation (Smith and Moore 1952).

Natural and Experimental Transmission

Natural transmission. The most efficient vectors of MV are

the common strawberry aphids of the genus Chaetosiphon

(also previously classified in the genera Pentatrichopus,

Capitophorus, and Myzus). The species largely responsible

for natural spread of MV are C. fragaefolii (Cock.), C.

thomasi H.R.L., and C. minor (Forbes). Chaetosiphon

jacobi H.R.L. is also an efficient vector and is probably a

vector to wild strawberries, but it occurs only in a limited

region of California and has not been found on cultivated

strawberries.

Other aphid species that have been reported as vectors are:

Acyrthosiphon malvae subsp. rogersii (Theob.), Amphorophora agathonica Hottes [also known as A. rubi (Kltb.)],

Aphis gossypii Glov., Chaetosiphon tetrarhodum (Wlk.)

(also known as Pentatrichopus), Acyrthosiphon malvae

zerozalphum Knowl. (also known as Macrosiphum),

Myzaphis rosarum (Kltb.), Myzus (Nectarosiphon) ascalonicus Done, Myzus ornatus Laing, and Rhodobium porosum

(Sand.) Although these species are less efficient vectors than

Chaetosiphon spp., many of them may be significant in the

spread of the virus.

Experimental transmission. Transmission is usually

effected by aphids or by grafting, but transmission by dodder

and by juice extract have also been reported. The virus has

not been transmitted through seed or pollen.

The virus can be transmitted to other herbaceous plants by

sap transmission or dodder. Cuscuta subinclusa Dur. and

Hilg. or C gorovonii Willd. Asclepias syriaca L. (milkweed)

showed symptoms after dodder transmission from strawberry

infected with type 1 virus (Smith and Moore 1952). Graft

transmission from infected to healthy milkweed reproduced

the symptoms, but attempted transmission by dodder back to

strawberry failed. Frazier {1968} reported transmission of

several mottle variants from strawberry to Chenopodium

quinoa Willd. and C amaranticolor Coste and Reyn. by sap

inoculation or by the aphid vector Chaetosiphon jacobi, with

symptoms comparable in severity to those on strawberry.

Symptoms were reproduced by transmission from infected to

healthy Chenopodium, but attempts to reinfect strawberry by

sap, aphids, or grafting failed.

Aphid transmission. Mottle is an aphid-borne virus of the

semipersistent type. Vectors can acquire the virus from an

infected plant and transmit it to a healthy plant during feeding

periods of a few minutes each, but longer periods are more

effective. There is no latent period in the vector, and aphids

usually lose their ability to transmit within a few hours after

leaving the plant. Leaves detached from the infected plant

and supported in vials of water are satisfactory sources of

inoculum. Betti and Costa (1980) reported that detached

leaves of intermediate age were better virus sources than

young or mature leaves, and with such detached leaves they

achieved 95% transmission by C. thomasi.

Vector-virus relationships differ slightly among strains of

MV. The variants differ in their persistence, both in feeding

aphids (Frazier and Posnette 7958) and nonfeeding aphids

(Frazier and Sylvester 7960) and in their incubation periods

in the plant (Frazier 1960b: Mellor and Forbes 1960). These

differences correspond to groupings of variants according to

symptoms. It is not surprising, therefore, that different

investigators have found slightly different vector-virus

relationships.

Frazier and Posnette (1958) reported that the shortest feeding

period for acquisition of the virus by C. fragaefolii was 60

min. The minimum period for transmission was 5 to 10 min,

and the aphids remained infective for up to 6 hr, although the

greatest number of transmissions occurred during the first

hour. They also reported that nymphs were more effective

vectors than adults. In comparative tests, nymphs up to 2

days old transmitted MV to 30 of 60 plants during the first 2

hr of transmission feeding, adults to 14 of 60 plants.

Krczal (1967) found the minimum acquisition period was

only 15 min, the minimum transmission period was 5 min or

less, and aphids remained infective for at least 4 hr. Krczal

14
found that álate or apterous adults, and all stages of nymphs,

were equally efficient as vectors, with 93 to 97%

transmission.

Eulensen (1981) reported for C. fragaefolii a minimum

acquisition period for MV of 15 min, which gave 5%

transmissions; a 4-hr acquisition feed increased transmission

to 41%. He reported a minimum inoculation access period of

7 min with the number of transmissions increasing to 29%

when the transmission feeding period was 15 min and 59%

after 60 min. He found that these aphids remained infective

for only 3 hr and that the number of MV transmissions

decreased sharply after the first hr.

In concurrent tests of two Chaetosiphon spp. as vectors of

MV, Eulensen {1981) found that C. thomasi was a less

efficient vector than C. fragaefolii. C. thomasi required a

minimum acquisition feeding period of 30 min, which gave

4% transmission. The greatest percentage of transmissions,

21%, was reached after a 24-hr acquisition period. The

minimum inoculation access period was 7 min. The

percentage of transmissions increased to 13% with a 15-min

transmission period, but did not significantly increase with

longer periods. C. thomasi remained infective for only 1 hr.

Mellor and Forbes (1960), however, reported that C.

fragaefolii and C. thomasi were equally efficient in

transmitting each of two variants of MV. Recent studies have

shown that the progeny of a single aphid can be classified into

both of these species (Crock and Shanks 1983), suggesting

that the reported variations in vector efficiency for MV may

be attributable to strain differences within a single aphid

species.

Properties of the Causal Agent

Kitajima et al. (1971) found aggregates of isometric,

viruslike particles in thin sections of F. vesca leaves infected

with several different isolates of MV (fig. 8). The

electron-dense portions of these particles, presumably

representing the nucleic acid core, were 17 to 22 nm in

diameter. The center-to-center distance between the closest

particles indicated that the entire nucleoprotein particle was

25 to 30 nm in diameter. Although most often found in

aggregates in the phloem cells, the particles were also seen

frequently in the plasmodesmal lumena of other leaf cells,

including epidermal and parenchymatous tissue.

The virus has not been isolated and purified, and nothing

more is known about its physical and chemical properties.

Detection and Identification

MV in cultivars, whether alone or in combination with other

viruses, can be detected and identified only by transmission

to indicator plants. Frazier (1974) recommended three

selected seedlings of F. vesca as indicators of MV. These

were 'UC-4' (the best), 'UC-5', and 'UC-6'.

4*^

\t

Figure 8.—Viruslike particles associated with strawberry mottle virus-infected leaves of Fragaria vesca.

Bar represents 1000 nm.

(Courtesy E. W. Kitajima, University of Brasilia.)

Since field infections with MV are often accompanied by

other viruses, graft transmission to indicator plants may

cause a confusing symptom picture. MV can best be

identified by aphid transmission. Chaetosiphon fragaefolii is

usually the preferred test aphid. Given an acquisition feeding

period of 4 to 6 hr, and two or three successive 1-hr

transmission periods on indicator plants, the aphids will

transmit only the semipersistent viruses. Of these, MV is

more likely to be transmitted than vein banding or pseudo

mild yellow-edge. Even if one of the latter two viruses were

also transmitted, symptoms of MV could be recognized.

Control Procedures

Control depends not only on the use of virus-indexed planting

stock and control of aphids, but also on isolation from

infected plants. Control of aphids will reduce the rate of virus

spread, but since MV may be transmitted during very short

feeding periods, insecticides do not provide complete

protection against incoming viruliferous aphids. Krczal

(7962; found that plants became infected when exposed to

viruliferous aphids a short time after the plants were sprayed

with the insecticides demeton-S-methyl or parathion. When

plants were exposed to viruliferous aphids 5 hr after

spraying, up to 95% of the plants became infected with MV

(H. Krczal, unpublished data). Unless plants are isolated

from sources of MV, they should be replaced periodically

with new virus-indexed stock to maintain vigor and

productivity.

Therapy. Mottle is one of the most heat-labile of the

strawberry viruses and can usually be eradicated from

infected plants by growing them at 37°C for 10 to 14 days;

however, longer treatment at lower temperatures may be

ineffective. Frazier et al. (1965) tested inactivation of several

viruses in strawberry plants in the field. These were

maintained for 4 mo or more in a naturally high-temperature

environment in the field, where mean summer temperatures

reached 32°C. Surprisingly, CV, which survives much longer

than MV at 37°C in the growth chamber (see "Strawberry

15
Crinkle," p. 20), was eradicated from 41 of 50 plants, and

MV was eradicated from only 1 of 32 plants in this field test.

Remarks

The term "mottle" is used to include what appear to be

numerous strains of a single virus. More than one virus may

be involved, but this is not clearly indicated by present

evidence. There is a very wide range of symptoms, and there

are some differences in vector-virus-plant relationships.

Studies of the properties of MV virions, including their

serology, will be needed to determine their relationships.

\ Strawberry Vein Banding y

By N. W. Crazier and T. J. JMorris

Additional Common Names

Yellow vein banding (Frazier and Posnette 1958), chiloensis

vein banding, and eastern vein banding (Frazier 1960a) are

synonyms of strawberry vein banding virus (SVBV) (Frazier

1955a; Frazier and Converse 1980). Erdbeer-nekrosevirus

(Schöniger 7958) may be a strain of vein banding virus, but

this is uncertain. Leaf curl (virus 5) (Prentice 1952) is a

disease complex formed by SVBV and crinkle virus.

Schöniger noted the similarity of her isolate to leaf curl. Both

Schöniger and Prentice used the East Mailing clone of

Fragaria vesca (EMC), which carries the latent-A strain of

crinkle virus for their indicator plant. The complex of

latent-A and the leaf curl strain of SVBV in EMC causes leaf

curling on young leaves and premature discoloration, vein

purpling, and necrosis of older senescing leaves (Frazier and

Posnette 1958).

History and Geographic Distribution

The leaf-curl strain of SVBV was first transmitted by Prentice

(7952) from a 'Fairfax' plant imported from the United States

into Great Britain where the disease does not occur in nature.

It may occur in continental Europe if Nekrosevirus should

prove to be a strain of SVBV (Schöniger 7955), or if the

semipersistent virus described by Domes (1957) is related to

it. Vein banding virus appears to be native to North America,

where it occurs in many strains. It is common in clones of the

beach strawberry. Fragaria chiloensis (L.) Duch, along the

Pacific coast (Miller and Frazier 7970). It is presumed that

the wild strawberries of Eastern United States: F. vesca L.

subsp. americana (Porter) Staudt, the wood strawberry, and

F. virginiana Duch., the Virginian strawberry, may harbor

the virus. Eastern and western strains of SVBV differ. The

eastern strains are of the leaf-curl type and are more difficult

to detect on indicator plants than the western strains, which

are of the vein-banding type.

SVBV also occurs in Australia, Brazil, and Japan, probably

having been introduced in planting or breeding material.

Economic Importance

The disease is now of minor importance because of low

incidence in commercial strawberries. This is likely due to

the use of certified planting stock. SVBV reduces runner

production, vigor, yield, and fruit quality in commercial

cultivars and can be very severe in mixed infection with

crinkle or latent-C viruses (Bolton 797^; Freeman and Mellor

1962; and Takai 7975).

Symptoms on Natural and Experimental Hosts

Natural infection with SVBV is known only in species of

Fragaria, all of which are probably susceptible. The garden

bumet (Sanguisorba minor Scop.) was established as a

symptomless experimental host by graft inoculation and by

the dark strawberry aphid vector Chaetosiphon jacobi H.R.L.

(Mullin et al. 1980).

Symptoms on cultivars (ofFragaria x ananassa Duch.) and

on F. chiloensis. Few cultivars show dependably diagnostic

symptoms although they may be adversely affected. The

chlorotic pattern of western SVBV is clearly obvious on

'Marshall' in all of the disease complexes tested. Plant vigor

can be severely reduced in infected plants. Western SVBV

interacts strongly with crinkle virus and with decreasing

severity with pallidosis, mottle, and mild yellow-edge

disease agents. In contrast, infections of western SVBV in

'Hood' are detectable with difficulty in the acute stage but are

symptomless in the chronic stage, while Tioga' is initially

symptomless but old leaves develop ^ faint chlorosis of net

veins during the chronic stage.

Symptoms of SVBV have not been detected in any infected

clone of wild or ornamental F. chiloensis.

Symptoms on indicator hosts. The standard strawberry

virus indicator clones are all sensitive to SVBV, but there is

wide variation in sensitivity to different isolates of the virus.

This variation is illustrated for two isolates on Fragaria vesca

'Alpine' (figs. 9 and 11). F. virginiana clone 'UC-12' (fig.

10) and F. vesca clone 'UC-6' are the most sensitive and

diagnostic indicator clones for the virus (Frazier 1974b).

Both are especially useful in diagnoses of eastern strains.

Three symptom types characterize the disease: leaf curl, vein

banding, and necrosis.

1. The leaf curl symptom (epinasty of midribs and twisting

of leaflets usually accompanied by epinasty and reduction of

petioles) is most severe during the early phase of infection,

particularly on F. virginiana indicator plants. It is most

severe and is the dominant early symptom in mixed

infections with crinkle virus (fig. 12). Leaf curl is more

characteristic of eastern isolates than western isolates and is

seldom more than mildly expressed during the chronic phase

of the disease.

2. The vein banding symptom (chlorotic banding along main

veins) is most intensely expressed in the first few leaves to

develop after onset of symptoms (fig. 9A). In leaves

developing later, the banding usually appears as discontinuous streaks or spots. The clarity of the vein banding

16
Figure 9. — A, Leaf of 'Alpine' (Fragaria vesca var.

semperflorens) showing the chlorotic vein banding

pattern of type strawberry vein banding virus; B. leaves

of 'Alpine' infected with a very mild isolate of

strawberry vein banding virus from North Carolina

showing acute symptoms of faint vein clearing of net

veins bordering main veins of basal leaflets of the two

small leaves at the left and faint chronic banding

symptoms in the large leaf at the right.

Figure II. — 'Alpine' plants: Left, healthy; and, right,

infected with a severely stunting isolate of SVBV from

Washington State.

Figure 10.—Fragaria virginiana clone 'UC-12'

infected with strawberry vein banding virus showing

typical vein banding pattern.

Figure 12. — Leaves of Fragaria vesca L. var.

californica {Cham, and Schlecht) Staudt, showing a

severe leaf curl without vein banding due to a double

infection of strawberry vein banding viruses and latent

A crinkle virus.

pattern varies with the virus strain and host plant; the clarity

is more striking in western than eastern isolates.

3. The necrosis symptom develops on mature leaves: Net

veins may become darkened or necrotic and interveinal

tissues may become discolored or necrotic. The leaves may

become partly necrotic or die prematurely. The symptom is

much more evident with eastern isolates than with western

isolates. The symptom persists largely as a premature

coloration of older leaves during chronic infections, and its

severity is increased in combination with crinkle virus.

Symptoms of the leaf curl and necrosis types may be induced

in strawberry by other causal agents, but the vein banding

symptom is relatively diagostic.

During the chronic stage of the disease, symptoms fluctuate

in severity: A series of normal-appearing leaves may

alternate with a series of leaves showing strong symptoms

(fig. 13). The symptomless leaves seem to occur after

transplanting or the application of fertilizer (Mellor and

Fitzpatrick 1961), or may be produced in cycles independently of nutrient or temperature (Stingl and King ¡965a).

17
Figure 13. — An excised crown of 'Alpine' with a

chronic infection of type SVBV. The cluster of small

leaves on short petioles show vein banding symptoms

which are absent from the larger, normal-appearing

leaves that developed 4 wk following a fertilizer

application.

Symptoms in complex with other diseases. The symptoms

of SVBV are additive in the presence of crinkle virus. In F.

vesca, the vein banding pattern is masked or distorted and

crinkle symptoms tend to dominate. This interaction is useful

in the detection of subclinical strains of either virus (Frazier

and Mellor 1970a). Similarly, the vein banding pattern is less

evident in the presence of mottle virus, and the mottle

symptoms tend to dominate. This interaction is also useful

for detecting subclinical strains of either virus.

Natural and Experimental Transmission

SVBV has been transmitted by grafting, by dodder [Cuscuta

subinclusa Dur. and Hilg. (Frazier ¡955a)\, and by the aphid

vectors Chaetosiphon fragaefolii (Cock.) (Prentice 1952),

Amphorophora agathonica Hottes [also known as A. rubi

(Kltb.)], Macrosiphum pelargonii Kltb., Myzus omatus

(Laing) (Frazier 1955a), Amphorophora idaei Born.,

Chaetosiphon jacobi (Frazier and Posnette 1958), Aphis

rubifolii (Thomas), Aulacorthum solani (Kltb.), Myzus

(Nectarosiphon) ascalonicus Done, Myzuspersicae (Sulz.),

and Chaetosiphon tetrarhodum (Wlk.) [also known as

Pentatrichopus tetrarhodus (Wlk.)J (Mellor and Forbes

1960).

Attempts to transmit the disease mechanically with preparations of purified virus (Morris et al. 1980) or isolated nucleic

acid extracts (T. J. Morris, unpublished data) were not

successful.

Strawberry aphids (Chaetosiphon sp.) are probably responsible for most of the field spread of the virus. Other less

efficient vector species often occur in high populations on

Fragaria and could also be important in SVBV epidemiology. The most efficient aphid vectors are Chaetosiphon

fragaefolii, C. jacobi. and C. thomasi. These species, as well

as Myzus omatus, transmit some but not all strains of the

virus, suggesting a subspecific virus-vector relationship

(Frazier 1960a; Mellor and Forbes 1960). This is further

supported by the fact that two eastern isolates of the virus

were not transmitted by C. jacobi (N. W. Frazier,

unpublished data).

SVBV is a virus of the semipersistent type that is acquired

during a 30-min acquisition access feeding period (Frazier

1955a). Retention of the virus by feeding vectors has been

reported to be 1 hr (Prentice 1952) for the leaf curl strain, 8 hr

for the type strain (Frazier 1955a) and 24 hr for the

Nekrosevirus strain (Schöniger 1958). A virus half-life of 10

hr was estimated for the type strain in fasted vectors (Frazier

and Sylvester 1960), and the virus was not retained by C.

jacobi through ecdysis (Frazier 1966a). The incubation

period for symptom development in indicator plants was

reported to be 3 to 5 wk for leaf-curl (Prentice 1952), 2 to 3

wk for vein banding (Frazier 1955a), and 3 to 4 wk for

Nekrosevirus (Schöniger 1958). Betti and Costa (1980) have

reported that plant leaves of intermediate maturity were a

better source for virus acquisition by vector aphids than

young or mature leaves.

Properties of the Causal Agent

SVBV is a member of the caulimovirus group (Kitajima et al.

1973; Frazier and Converse 1980). It has a limited but

distinctive natural host range which distinguishes it from

other caulimoviruses, and it is aphid transmitted in a

semipersistent manner. Typical caulimoviruslike particles,

40 to 50 nm in diameter (fig. 14), have been isolated from

infected strawberry plants, and they had a reported

sedimentation coefficient of 200± 10 S (Morris et al. 1980).

Cytoplasmic inclusion bodies (fig. 15) typical of other

caulimoviruses have been reported in the vascular parenchyma and mesophyll cells of infected plants (Kaname 7975,-

Kitajima et al. 1973; Frazier and Converse 1980; Morris et

al. 1980).

Purification of SVBV from infected leaves of F. vesca has

been accomplished. The isolation of virions from viscous

host extracts included clarification with organic solvents and

fractionation on sucrose-CsCl step gradients and ECTEOLA

cellulose columns (Morris et al. 1980). Yields of virus were

invariably low. Attempts to purify inclusion bodies also

resulted in poor yields (T. J. Morris and R. Mullin,

18
m 9

v# B

#

Figure 14. — Serologically specific electron microscopy of purified preparations of — A, Strawberry vein

banding virus; and B. cauliflower mosaic virus after

fixation in 1% formaldehyde. Both grids were precoated

with cauliflower mosaic virus gamma globulin at 5

Hg/ml, incubated with virus preparations for 2 hr and

stained with uranyl acetate. The bar represents 50 nm.

Figure 15. — An inclusion body in a strawberry leaf

cell exhibiting vein banding symptoms. The virions (45

nm) are present throughout the inclusion; cw, cell wall;

i, inclusion body; v, virions. Bar represents 1 micron.

B

unpublished data). These results, and the fact that a

homogeneous virion population (200± 10 S) could only be

identified in density gradients after fixation in 1% formaldehyde, probably reflect a problem of particle instability. A

more complete characterization of virion proteins and nucleic

acid remains to be accomplished.

Antiserum to SVBV has not been prepared, but a serological

relationship to other caulimoviruses has been demonstrated

(Morris et al. 1980). Purified SVBV reacted in immunodiffusion and ELISA tests with antiserum prepared to the

cabbage-B strain of cauliflower mosaic virus. Similar cross

reactions have been identified using dahlia mosaic virus

antiserum but not with carnation etched ring virus antiserum

(T. J. Morris, unpublished data). SVBV appears to be

serologically distinct from other caulimoviruses tested to

date, but a definitive assignment of serological relationships

will require the production of an SVBV antiserum.

Many strains and/or variants of SVBV have been distinguished on the basis of symptoms, aphid vector specificity

(Frazier and Posnette 1958; Frazier 1960a; Mellor and

Forbes 1960), and in cross-protection tests. In crossprotection tests with seven isolates, the^e was complete or

partial protection whether the virus was introduced by vectors

or by grafting (Frazier and Converse 1980). The relative

importance of strains is not known.

Detection and Identification

The severity of SVBV disease varies widely with host,

isolate, and stage of infection. The virus is best diagnosed by

graft or vector transmission to the indicator clones F.

virginiana 'UC-12' or F. vesca 'UC-6' (Frazier 1974b),

which show characteristic chlorotic vein banding. The virus

can be separated from others by vector transmission.

Chronically infected plants are often a poor source of virus

for vectors (Prentice 1952), but availability can be restored

by graft transmission to a new plant (Frazier and Posnette

7958).

A more rapid serological confirmation of SVBV can be

accomplished in ELISA tests using cauliflower mosaic virus

antiserum. Clarified plant extracts concentrated tenfold by

precipitation with 8% polyethylene glycol (Morris et al.

1980) can give satisfactory results (T. J. Morris and R.

Mullin, unpublished data). Routine serological detection

however, will require the production of an SVBV-specific

antiserum.

Control Procedures

The main control procedure is the use of commercially

available planting stock certified to be free of the virus. The

general incidence of SVBV is very low, and use of such

certified stock is appropriate toward maintaining such a

situation.

19
Elimination of the virus from mother plants by runner tip

culture (Miller and Belkengren 1963) or by heat treatment for

10 days at 42°C (Bolton 1967) has been reported. The

elimination of the type strain of SVBV from experimentally

infected 'Hood' plants by meristem tip culture was 100%

whether or not the plants were preheat treated for 6 wk at

37°C (R. Mullin, unpublished data). In these tests, the

cultured plants were indexed and discarded after 6 mo. This

could prove to be an insufficient incubation period for cloned

meristems, as some dahlia plants similarly treated to

eliminate dahlia mosaic virus remained symptomless for up

to 10 mo (Mullin and Schlegel 1978).

Remarks

Although SVBV is a relatively minor problem in commercial

strawberry production, it is not a virus to be ignored. It can

cause serious losses when associated with other viruses in

disease complexes. In view of the long latent period in shoot

apex propagated plants of the one other caulimovirus tested,

SVBV could become a problem in the production of certified

stock. The production of an antiserum and implementation of

ELISA indexing to detect latent infections could be important

steps in reducing this possibility.

y^Astrawberry Crinkle.y ,

By N. W. Frazier, E. S.|Sylvester, and J.[Richardson

Additional Common Names

The names "crinkle," "mild crinkle," "intermediate crinkle,"

and "severe crinkle" have been applied to diseases of

cultivars caused by various strains of the crinkle virus alone

or in combination with other strawberry virus diseases such

as mottle, vein banding, and mild yellow-edge. In addition to

strains that cause classical symptoms, there are milder strains

that require sensitive indicator plants for detection. These

are, in order of increasing severity: strawberry latent A virus,

mild form (Rorie 7957); strawberry latent A and latent B

viruses (Frazier 1953); strawberry lesion A and lesion B

viruses (Frazier and Posnette 1958); and strawberry vein

chlorosis virus (Prentice 1952; Frazier and Mellor 1970a).

History and Geographic Distribution

Strawberry crinkle virus (SCV) was first reported in the

'Marshall' cultivar in Oregon by Zeller and Vaughan (1932).

Vaughan (1933) demonstrated transmission of the virus by

the strawberry aphid Chaetosiphon fragaefolii (Cock.)

(previously known as Capitophorus fragaefolii, Myzus

fragaefolii, and Pentatrichopusfragaefolii) to 'Marshall' test

plants. Zeller (1933) reported an incubation period of 12 to

15 days in 'Marshall' plants and also recognized that crinkle

was probably composed of two separable components — one

causing a "mild crinkle" — but he did not indicate their

symptom differences.

Crinkle was recorded in Great Britain by Ogilvie et al.

(1934). Later Harris (1937a, b) transmitted the virus by

graft. He pointed out that symptoms were of two types

(designated as mild and severe crinkle) and referred to an

interaction of the two viruses. Prentice and Harris (1946)

transmitted a vims that persisted in the strawberry aphid

vector about 3 hr, and they concluded that it was probably the

mild crinkle virus. This virus. Prentice (1948) designated as

virus 1, and later (1952) he proposed the name "strawberry

mottle," stating that he considered the form causing mild

crinkle to be distinct. He also demonstrated that a form of

severe crinkle could be caused by a complex of virus 1 with a

long-persistent type of virus designated as virus 3 (Prentice

1949), and which he later named "strawberry crinkle"

(Prentice 1952).

SCV occurs worldwide (North and South America, Britain,

Europe, South Africa, New Zealand, Australia, and Japan)

except in regions where strawberry aphids of the genus

Chaetosiphon are not found on strawberry (Sylvester et al.

1976). The East Mailing clone of Fragaria vesca L. 'EMC

was originally selected as a superior indicator because mottle

virus caused more severe symptoms on this clone than any

other. It was not until the discovery that 'EMC was carrying

latent A virus that this sensitivity was explained (Frazier

1953). In the meantime, the clone had been distributed

throughout the world and many cultivars were inadvertently

infected with latent A by stolon grafting to 'EMC.

Economic Importance

SCV is one of the most damaging of the virus diseases

affecting strawberries. As a result of meristem culture to

eUminate SCV from commercial cultivars, and certification

programs to maintain clean planting stock, the losses from

SCV have been minimized in recent years. Where SCV still

occurs, severe strains reduce vigor and productivity and even

mild strains, such as latent A, reduce vigor, runner

production, yield, and fruit size of some varieties (Freeman

and Mellor 1962; McGrew and Scott 1964; Barritt and Loo

1973). On the other hand, Takai (1973) found no significant

differences between crinkle-infected and virus-free

'Kohyoku' lines. SCV most usually occurs in the field with

mottle, vein banding, mild yellow-edge, and/or pallidosis.

Each of these diseases exerts an important additive effect

with SCV. Crinkle is a visual component of several

degenerative disease complexes that have been a limiting

factor in the production of strawberries in many areas.

Symptoms on Natural and Experimental Hosts

SCV is known only in species of Fragaria, none of which is

known to be immune. Strawberry cultivars vary widely in

their sensitivity. More sensitive cultivars, such as 'Hood',

show distinct symptoms with mild strains, while others, such

as 'Shasta', may show no symptoms even when infected with

severe strains. On sensitive cultivars, symptoms are

characterized by chlorotic spots and deformation of leaves

(fig. 16). Small, scattered, opaque, chlorotic to necrotic spots

are associated with veins, and short lengths of cleared or

yellowed veins often radiate from them. Lxaflets are usually

20
Figure 16. — Cv. 'Marshall' plants infected, left to

right, with strawberry crinkle; crinkle and strawberry

mild yellow-edge; crinkle, mild yellow-edge,

strawberry mottle viruses.

and

Figure 17. — Leaf of a cv. 'Marshall' plant exhibiting

the "chlorotic sector" symptom associated with some

strains of crinkle virus.

Figure 18. —Fragaria vesca var. semperflorens cv.

'Alpine' infected with latent A crinkle by the aphid

vector Chaetosiphon jacobi showing early symptoms of

leaflet epinasty (11 and 3 o'clock) and abaxially curled

leaflets (12 o'clock).

unequal in size, distorted, and crinkled. Sectors of leaflets

may be yellowed (figs. 16 and 17), and petioles and leaves

may be reduced in size.

Symptoms on indicator hosts. Clones of F. vesca show

symptoms similar to those described above and vary in

pattern and severity, depending on the virus strain and the

indicator clone. Symptoms of mild strains are most evident

during the early or shock stage of infection (fig. 18) and may

consist only of a slight angular epinasty of a single leaflet on

one or several successive leaves. Symptoms of more severe

strains persist and include several components, not all of

which are diagnostic.

Although chlorotic spotting of the lamina is one of the most

usual symptoms of SCV (fig 19), this symptom, by itself, is

not reliable diagnostically for similar spots can be caused by

mottle or mild yellow-edge infection (fig 20). The spots are

irregularly distributed and associated with veins. At first, the

spots are translucent, later becoming opaque and yellow,

reddish, or necrotic. Crinkling of the lamina and uneven

expansion of the leaflets can be caused by atrophy of the

spots (fig. 21).

Angular epinasty of leaflets is a fairly reliable diagnostic

early symptom of infection. Characteristically, the epinasty

is sharply angular from some point (usually a spot or lesion)

21
Figure 19.—Fragaria vesca 'UC-l', left to right:

Chronic symptoms of three isolates of strawberry

crinkle virus inoculated by Chaetosiphon jacobi.

Figure 20. — Similar symptoms caused by three

different diseases in Fragaria vesca var. semperflorens

cv. 'Alpine' infected by vector inoculations. Left to

right: mild yellow-edge, crinkle, and mottle.

on a midrib and seldom affects more than one leaflet per leaf,

and leaflets often become curled abaxially (fig. 18).

Lesions provide a reliable diagnostic symptom and occur on

stolons, petioles (fig. 22), and leaves. Greenish, reddish, or

necrotic areas or rings may be sunken or swollen and cause

angular bending. Such lesions are most prominent and useful

on F. vesca, occurring less frequently on F. virginiana, F.

chiloensis, and on strawberry cultivars.

Chlorotic sectoring (fig. 17) is not a consistent symptom.

Interveinal yellowing forms wedge-shaped sectors beginning

at some point on a main vein and widening toward the leaflet

margin. This symptom seems to be associated only with

certain strains of crinkle.

Vein chlorosis usually is not conspicuous. Short lengths or

small networks of veins from chlorotic spots can become

finely cleared (fig. 21).

Petal streak is a highly diagnostic symptom of crinkle. It is

particularly useful for the detection of mild infections and of

the presence of crinkle in disease complexes. Short lengths of

Figure 21. — Leaf of Fragaria vesca 'UC-5' with

crinkle virus symptoms of chlorotic spotting and vein

chlorosis.

veins in petals become cleared or translucent permitting the

background color — usually the green of a sepal — to show

through, causing the translucent areas to appear darker than

normal. The streaks may become necrotic, and affected

petals may be deformed and dwarfed (fig. 23).

Symptoms in F. virginiana Duch. cvs. 'Ml', 'UC-10',

'UC-ir, and 'UC-12' are of the characteristically generalized, nondiagnostic syndrome typical of the F. virginiana

reaction to infection with most graft-transmissible diseases.

They consist of general chlorosis, vein clearing, abnormal

development of new leaves, epinasty of leaflets and petioles,

red or yellow old leaves, loss of vigor and stunting (Frazier

1974b). The 'Ml' and 'UC-ll' clones both have superior

sensitivity to SCV, but 'UC-ll' is a much more useful

indicator over a wider range of diseases. The petal-streak

symptom is much less useful in F. virginiana than in F.

vesca.

In complexes with other diseases in F. vesca. Symptom

severity of any complex in cultivars or in indicators depends

on the severity of each disease component (fig. 24) (Frazier

and Melior 1970a).

22
SCV interacts very strongly with strawberry mottle and

strawberry vein banding diseases. The interaction can be

used to advantage in the detection of very mild strains of the

diseases. In combination with mild yellow-edge, the

symptoms of crinkle are partially masked and those of mild

yellow-edge dominate.

Natural and Experimental Transmission

Methods. SCV is easily transmitted by grafting but not by

sap inoculation and only very erratically by aphid vectors

(Frazier and Mellor 1970a). The principal natural vector is C.

fragaefolii. Although C. jacobi H. R. L. also is a vector, it is

found only on wild F. vesca L. var. californica (Cham, and

Schlecht.) Staudt, in the coastal mountains of central

California (Mellor and Frazier 1970b). In recent years, this

species has been used predominately at Berkeley because it is

native to the locality on F. vesca and is an efficient vector of

aphid-borne strawberry viruses. In addition, the dorsum of

mature apterous aphids is uniquely dark-brown, and thus

colony contamination with other species of Chaetosiphon can

be readily detected. Takai (1973) reported C. minor (Forbes)

not to be a vector of crinkle. Babovic {1976) reported

transmission of crinkle by the strawberry root aphid Aphis

forbesi Weed — the first non-Chaetosiphon species to be so

implicated.

Vector-Virus-Plant Relationships

The early detailed vector work on SCV (Prentice 1949;

Prentice and Woolcombe 1951) established it as belonging to

the group of viruses having a persistent vector-virus

relationship, but with an exceptionally long (10 to 19 days)

latent period in C. fragaefolii. The aphids remained infective

for several days. Coupled with an incubation period of 4 to 8

wk in strawberry plants, a transmission cycle could take up to

2'/2 mo. Later tests with C. jacobi (Frazier 1968a) gave a

mean (range) vector latent period of 32 (14 to 59) days, with

lifelong retention of infectivity (recorded maximum of 71

days) with a maximum longevity of 106 days. There was

Í

I

Figure 22. — Stolon tips and segments of petioles from

Fragaria vesca 'UC-1 ' showing the lesion symptoms of

strawberry crinkle virus.

Figure 23. — Flowers from Fragaria vesca var.

semperflorens cv. 'Alpine' plants: left, normal; right,

petal-streak symptoms of strawberry crinkle virus.

Figure 24. — Interactions of a mild strain of mottle

virus with two mild strains of crinkle virus in Fragaria

vesca 'UC-I'. Left to right: mottle alone, with latent A,

and with latent B.

23
. 1 '

WMF mm

Figure 25. — Electron micrograph of

nonenveloped strawberry crinkle

virions in the cytoplasm of the salivary gland of the aphid vector

Chaetosiphon jacobi. Magnification:

X 20,900.

Figure 26. — Enveloped and nonenveloped strawberry crinkle virions in

the petal of Fragaria vesca. Magnification; X 13,000.

evidence that vector efficiency, as well as values for these

other parameters, varied with virus strains. The vector colony

rearing, acquisition, and test feeding periods were carried out

in a sheltered outdoor area (somewhat approximating field

conditions) where the temperature ranged from 9.9° to

18.8°C during the several years of experimentation and was

about 18.3°C in a glasshouse where inoculated plants were

incubated.

More recently, (Sylvester et al. 1974) used serial passage via

needle inoculation to establish that SCV multiplies in C.

jacobi and is a propagative plant rhabdovirus. At 25°C,

inoculated vectors had a median latent period of 6.2 days,

and 10 to 12 days after injection they achieved a maximum

rate of transmission of about 90%. The rate then declined to

12% by 11 to 24 days after injection, and ceased some 6 days

later even though 50% of the insects were still alive. Injected

insects lived for a maximum of 42 days after injection.

Crinkle virus also will multiply in other aphid species when

injected, including Hyperomyzus lactuae (L.), a nonstrawberry-feeding aphid (Sylvester and Richardson ¡981) and

Myzus ornatus Laing, a polyphagous species that will

colonize strawberry (E. S. Sylvester and J. Richardson,

unpublished data). Injected M. ornatus occasionally will

transmit virus to test plants, but with H. lactucae, host plant

specificity precludes valid transmission tests being done.

Properties of the Causal Agent

A variant of the CIO group of SCV (Frazier 1968a) examined

in the electron microscope showed a bacilliform particle

morphology, typical of a plant rhabdovirus (Richardson et al.

1972). SCV presumably belongs to the Rhabdoviridae.

Thin sections of infected C. jacobi vectors revealed

enveloped and nonenveloped virons in the cytoplasm of most

organs (fig. 25). The enveloped particles measured 69± 6 x

190 to 380 nm. Similar particles were found in thin sections

of diseased leaves of F. vesca L. var. semperflorens (Duch.

Ser. cv. 'Alpine' (Alpine strawberry) (fig. 26).

' : *

Tv^tt

Figure 27. — Negatively stained

bullet-shaped virions of strawberry

crinkle from the crushed head of the

aphid vector Chaetosiphon jacobi.

Magnification: x 63,000.

Figure 28. — Nonenveloped strawberry crinkle virions in the

oesophageal wall of an inefficient

aphid vector A/yzMi ornatus. Magnification: X 20,900.

Bullet-shaped particles were exclusively seen in unfixed

negatively stained preparations from infected aphids (fig.

27), and similar particles occasionally can be found in

plant-dip preparations, especially from infected petals.

Enveloped and nonenveloped particles also have been found

in nonvector aphids H. lactucae (Sylvester and Richardson

1981) and M. ornatus (E. S. Sylvester and J. Richardson,

unpublished data) infected by injection (fig. 28).

SCV has not been purified and there is no information on its

physical or chemical properties or its serology; however,

attempted cross-protection tests using C. jacobi and H.

lactucae gave no evidence of interference between SCV and

sowthistle yellow vein, another aphid-borne plant rhabdovirus (Sylvester and Richardson 1982).

Detection and Identification

Some commercial cultivars show symptoms of severe strains

of SCV especially when it is a component of a multidisease

complex. Most, however, are symptomless carriers of mild

strains. Detection depends on graft indexing to sensitive

indicator cultivars. F. virginiana cvs. 'MI' and 'UC-ll' are

the most sensitive indicators, but the symptoms resulting are

generalized rather than diagnostic, F. vesca cvs. 'UC-4',

'UC-5', and 'UC-6' are all very sensitive and show the

diagnostic petal-streak and petiole-lesion symptoms.

Control Procedures

Spread of SCV may be reduced by aphid control, isolation of

plantings from infection sources, and a strawberry plant-free

period in conjunction with an annual planting system where

the local conditions and cultivars permit. The use of certified

planting stock free of SCV is of major importance.

Plants free of SCV can be developed by several techniques.

Heat treatment of infected plants with a constant temperature

of 38°C or temperatures fluctuating daily from 35° to 4rC

eliminates the virus in several months. Propagation of

auxiliary buds from crowns of heat-treated plants reduces the

required length of treatment to a few weeks (Posnette and

Cropley 1958; Posnette and Jha 7960,- Mellor and Fitzpatrick

24
7967; McGrew and Scott 1964). Apical meristems free of

SCV may occasionally be removed from infected plants and

grown on a culture medium, but success of the method is

greatly improved when parent plants are given a short heat

treatment (Belkengren and Miller 1962; Miller and Belkengren 1963; Vine 1968). SCV was inactivated in a high

percentage of plants during a season of growth in a naturally

high temperature climate where summer temperatures

reached a mean of 32°C (Frazier et al. 1965).

jM Strawberry Mild Yellow-Edge ;/

By R. H.jConverse, R. R./Martin, and S. ISpiegel

Additional Common Names

Strawberry virus 2 (Prentice 1948). Mild yellow-edge virus

(MYEV) is a common but not essential component of the

complex known in North America as yellows or xanthosis

and in Great Britain as yellow-edge.

History and Geographic Distribution

Yellows was the first virus disease of strawberry to be

recognized. Home (1922) described the disease in California.

Plakidas (1926, 1927) showed that the disease was

transmissible by the aphid Chaetosiphon fragaefolii (Cock.).

Harris (1933) described a similar graft-transmissible disease

in England, which he called "yellow-edge," and Massée

(1935) showed that yellow-edge was transmitted by C.

fragaefolii. Harris and King (1940) concluded that the two

diseases were analagous, a conclusion supported by later

work (Mellor and Fitzpatrick 7957; and Frazier and Posnette

7958).

MYEV is probably worldwide in distribution in strawberry

cultivars. It is one of the most common viruses in cultivated

strawberries in western North America, Europe, Israel

(Leshem et al. 79(52; Spiegel et al. 1981), South Africa

(Engelbrecht 1967a), Australia (Greber 1979), New Zealand

(Chamberlain 1934), and Japan (Goto and Nemoto 1974).

MYEV and yellows have been reported from eastern North

America, but are uncommon there (Plakidas 1964; Morgan

1965; and Frazier 7975b). Chaetosiphon fragaefolii, a vector

of MYEV, has been found on Fragaria chiloensis (L.) Duch.

in beach areas in southern Chile remote from cultivated

strawberries (R. H. Converse, unpublished results).

The history of the yellows disease is given in detail by

Plakidas (1964).

Economic Importance

The yellows complex is undoubtedly one of the major

diseases of strawberry in most parts of the world; however,

because of the interaction of cultivars, viruses and virus

strains, crop management, and environment, it is difficult to

assess the importance of MYEV in the amount of economic

loss that occurs. MYEV alone is not particularly damaging to

most cultivars, but it seldom occurs alone. The complex of

MYEV with other viruses, for example, mottle (MV), crinkle

(CV), vein banding (VBV), or pallidosis agent (PA), can

cause severe loss of plant vigor, yield, and fruit quality.

In field studies of inoculated plants of cv. 'Hood', Barritt and

Loo (1973) found that MYEV alone did not significantly

reduce plant vigor, fruit yield, or fruit size, but the

combination of MYEV and MV significantly reduced fruit

size. Mullin et al. (1974) reported that meristem-derived

'Fresno' plants outyielded MYEV-infected 'Fresno' in field

trials in California by 15 to 24%. In other field studies,

Martin and Converse (1977) found that the vigor of 'Hood'

plants that had been infected with the yellows complex one or

more years previously was 17% below that of comparable

healthy plants. In plants that had been infected during the

current growing season, fruit percentage and weight were

reduced 16 and 19%, respectively. Aerts (1980) reported that

MYEV reduced yield of 'Gorella' in field tests in The

Netherlands by 30%, mainly by reducing the number of fruit

per infected plant.

In greenhouse studies, Mellor and Fitzpatrick (1961) found

that MYEV further reduced the vigor of 'Marshall' already

infected with MV and CV. Shanks and Crandall (1969) found

that the yellows complex significantly reduced the yield of

'Columbia' but not of the more resistant 'Northwest'.

Lawrence and Miller (1968) found that MYEV with MV

and/or CV did not reduce vigor and yield of 'Northwest' but

did reduce runner production in greenhouse studies.

Symptoms on Natural and Experimental Hosts

Symptoms on natural hosts. In nature, the virus has only

been found in Fragaria. The wild species F. virginiana

Duchesne, F. vesca L., and some clones of F. chiloensis

show symptoms; F. ovalis (Lehm.) Rydb. is a symptomless

carrier.

Most strawberry cultivars are symptomless carriers of

MYEV. At most, slight marginal chlorosis occurs on young

leaves; however, cultivars vary greatly in the amount of

symptom expression and crop loss caused by the yellows

complex (Daubeny et al. 7972). No immune cultivars are

known, and all are believed to suffer a decrease in vigor and

yield when infected by yellows complex.

Experimentally, MYEV can be graft transmitted symptomlessly to Sanguisorba minor Scop. (Mullin et al. 1980).

Symptoms on indicator hosts. Symptoms of typical MYEV

isolates are similar, whether the indicator is F. vesca 'EMC,

'UC-4', or 'Alpine' (fig. 29). Infected 'UC-6' is usually

symptomless and is useful both for this "negative symptomatology" and to maintain MYEV isolates that might kill or

severely weaken 'UC-4' or 'Alpine'.

Prentice (1948) described two symptom types for the MYEV

that he separated from the yellow-edge complex: (1) typical

symptoms, which included small, chlorotic flecks on the

25
Figure 29.—Left, symptoms in hruf^ariu vesia UC-4'

of a mild strain of mild yellow-edge virus 45 days after

grafting. Young leaves are mottled, and a few of the

older leaves show premature senescence. Right, normal

UC-4- plant.

young leaves, chiefly on the smaller veins, with leaflets

slightly cupped and slightly chlorotic, especially toward the

margins, accompanied by gradual loss of vigor; and (2) much

milder symptoms, consisting of slight but definite chlorotic

mottling, some interveinal necrosis of older leaves, but very

little cupping or marginal chlorosis. He also described

somewhat similar but still milder symptoms of a persistent

virus transmitted from "Huxley's Giant', which on the 'East

Mailing' clone ('EMC') of F. vesca caused chlorosis and

slight cupping, but not chlorotic spotting. Frazier and

Posnette (1958), redescribing the same three isolates, added

that the typical form also caused yellowing or reddening and

the premature death of the older leaves. These isolates were

all described on "EMC Symptoms appeared 4 to 8 wk after

inoculation by aphids.

Isolates of MYEV that occur along the Pacific coast of North

America cause a similar range of symptoms. There appear to

be intergrading strains, but experimental evidence is not

sufficient to evaluate their relationships. Mellor and

Fitzpatrick (1951), describing symptoms of the persistent

component separated from the yellows complex in 'Marshall', considered that they most closely resembled symptoms described by Prentice for the persistent virus he isolated

from 'Huxley's Giant'. A strain that commonly occurs on the

Pacific coast resembles typical MYEV described by Prentice

(1948), but symptoms appeared on aphid-inoculated F. vesca

8 to 15 wk after inoculation.

Timing and symptom intensity vary with the virus isolate, the

indicator, and the season. In leaf-grafted indicators, the

symptoms are chlorosis and some necrosis of the net-veins of

one or two leaflets of the youngest leaf. On succeeding

leaves, net-vein chlorosis and necrosis are general, and

affected leaves soon die, so that the symptom picture about 2

mo after inoculation is distinctive. The first three or four

leaves formed after inoculation appear normal, the next few

leaves are dead (fig. 30), and the youngest show epinasty,

net-vein chlorosis and some small, scattered, necrotic spots

and streaks (fig. 31). During later stages of infection, the

youngest leaves may appear nearly normal, but older ones

continue to die prematurely.

Symptoms in complexes with other viruses. MYEV in

complex with the latent A strain of CV causes marginal

chlorosis of the leaves, at least on the cvs. 'Royal Sovereign'

and 'Marshall'. The symptoms of virus 2 on 'Royal

Sovereign', described and illustrated by Prentice (1948),

were probably those of MYEV with latent A.

The combination of MYEV with MV, CV, or both,

sometimes with the addition of PA (see "Strawberry

Pallidosis," p. 55, for a discussion of the role of PA in

yellows), causes the disease known as xanthosis, yellows, or

yellow-edge. Symptom severity varies with the number and

severity of the component viruses and viruslike agents,

length of infection, and susceptibility of the cultivar.

Sensitive cvs., like 'Marshall', 'Hood', and 'Puget Beauty',

are dwarfed and appressed to the ground. The older leaves

are cupped and chlorotic at the margins. Petioles are

abnormally short and stout. Young leaves are small, twisted,

or cupped, with marginal or overall chlorosis. Yield is much

reduced. Less sensitive cultivars exhibit similar but milder

symptoms. Some cvs., like 'Totem', 'Tyee', and 'Northwest', are so tolerant of the yellows complex that infected

plants show no symptoms (Daubeny et al. 1972). No immune

cultivars are known, however, and all are believed to suffer a

decrease in vigor and yield when infected.

Natural and Experimental Transmission

Natural transmission of MYEV is by several species of

aphids, mostly in the genus Chaetosiphon, as a persistent or

circulative virus. MYEV was separated from the yellows

(yellow-edge) complex by serial transfers of infective aphids

26
Figure 30.—Typical stages of symptom production of

mild yellow- edge virus on leaf-grafted Fragaria vesca

'UC-4': A. epinasty of young leaves; B, chlorotic

flecking of young leaves; C, vein necrosis of maturing

leaves; D. scorching of maturing leaves.

to a succession of Fragaria indicator plants by Prentice

(1946, 1948) and by Mellor and Fitzpatrick (1951).

Vector aphids are Chaetosiphon fragaefolii (Cock.), C.

thomasi H.R.L., C. jacobi H.R.L., C. minor (Forbes)

(Frazier 1975b), and Macrosiphum rosae (L.) (Mellor and

Forbes 1960). Myzus persicae (Sulz.) has been found to be a

vector in recent greenhouse studies (R. R. Martin and R. H.

Converse, unpublished results).

Studies of field transmission showed that spread of MYEV

peaked in June in southwestern Washington State, but some

spread occurred there even in winter (Shanks 1965). Field

spread of the virus from infected plants appeared to occur at

random (Converse et al. 1979), although álate Chaetosiphon

spp. may actively seek Fragaria as a host (Shanks 1965;

Shanks and Finnigan 1970).

Experimental aphid transmission is sometimes erratic or

unsuccessful. Some strains of aphids are inefficient vectors,

and some strains of MYEV are less easily transmitted than

others. Krczal {1979) reported that nymphs, apterae, and

alatae of C. fragaefolii all transmitted the virus equally well,

and that single aphids transmitted it to 16% of the test plants.

He obtained 100% transmission by C. fragaefolii with an

acquisition feeding period of 2 days and a transmission

feeding period of 8 days. Frazier and Posnette {1958) found

that C. jacobi acquired MYEV in 8 hr or less. Engelbrecht

27
Figure 31.—Left, typical chronic symptoms in Fragaria

vesca 'UC-4' of a strain of mild yellow-edge virus from

cultivated strawberry in western Oregon. Two mo after

inoculation by leaf grafting, the youngest leaves show

chlorosis and necrosis of secondary veins, while many

mature leaves are scorched and older leaves are dead.

Right, comparably leaf-grafted F. vesca 'UC-6', which

was infected but remained symptomless.

(1967b) reported a latent period for MYEV in C. fragaefoUi

of 24 to 40 hr after an 8 hr acquisition access period. Mellor

and Frazier (1970a) reported that C. jacobi could retain the

virus for 45 days, but efficiency of transmission declined

after 28 days.

To test the effectiveness of inserting only one scion leaflet per

indicator plant, Frazier (1974a) used F. vesca and defoliated

the indicator plants at time of grafting. He found that one

inserted leaflet was adequate for transmission of MYEV, and

that the incubation period was 15 to 30 days, with a mean of

20 days.

MYEV can be graft transmitted to Sanguisorba minor Scop.,

but there are no symptoms (Mullin et al. 1980).

Mechanical transmission of MYEV was reported by Miller

(1951) and Liu (1957), but their results have not been

confirmed. Dodder transmission has not been reported. The

virus is not known to be spread by seed or pollen.

Properties of the Causal Agent

Very little is yet known about the properties of MYEV.

Somewhat distorted isometric particles 23 nm in diameter

have been seen after partial purification of MYEV (fig. 32)

(Martin and Converse, 1982b). No viruslike particles were

observed in the electron microscope in thin-sectioned

strawberry leaf tissue infected with MYEV (Greber 1979).

Because of symptomatology and vector properties, MYEV is

tentatively classified as a luteovirus (Matthews 7979).

Detection and Identification

It is seldom possible to detect and identify MYEV by its

symptomatology in infected cultivars. Transmission to

sensitive clones of F. vesca is therefore necessary for

detection and identification of this virus. On F. vesca

indicator clones, MYEV symptoms usually appear within 3

wk after inoculation by aphid or by leaflet grafting. 'UC-4' is

the most sensitive indicator. 'UC-6' remains symptomless

when infected by most of the isolates of MYEV tested

(Frazier 1974a,b; R. H. Converse and S. Spiegel, unpublished results). F. vesca var. semperflorens 'Alpine', F.

vesca 'UC-5', and F. virginiana 'UC-10' and 'UC-ll' are

also useful indicators for MYEV.

On F. vesca indicators, physiological heat spot may be

confused with early symptoms of MYEV. (See"Heat Spot of

Fragaria vesca,'' p. 78.) Several leafhopper-bome disease

agents, like aster yellows, green petal, tomato big bud, and

Çr

*-^

^%

Figure 32.—Somewhat distorted, isometric particles 23

nm in diameter, from a partially purified preparation of

strawberry mild yellow-edge virus. Bar represents 100

nm.

28
lethal decline (see strawberry leafhopper-bome disease

chapters), may cause foliage symptoms similar to yellows on

some strawberry cultivars, but these diseases also cause

flower phyllody, sterility, or malformation. Tobacco necrosis

virus (see "Tobacco Necrosis Virus in Strawberry," p. 64)

appears to be associated with premature senescence of older

leaves of some Fragaria indicator clones, mimicking MYEV

symptomatology.

Control Procedures

Many of the techniques that are useful for controlling MYEV

also apply to other strawberry viruses and are discussed in the

introductory chapter of the strawberry section of this

handbook. (See "Detection and Elimination of Virus and

Viruslike Diseases in Strawberry," p. 2.)

Elimination of MYEV from strawberry cultivars. Mellor

and Fitzpatrick (1961) found that MYEV survived in

strawberry cultivars exposed to a constant 38°C for 6 mo.

Later work, however, showed that excision of the central

growing point and almost complete defoliation of infected

cultivars during heat treatment for 9 wk at 38°C stimulated

the devlopment of side crowns, which could then be excised

and rooted in sand at normal greenhouse temperatures.

Approximately 50% of the resulting plants were freed of

MYEV. Nearly all axillary crowns excised after heat

treatment of 12 wk or more were free of MYEV (F. Mellor,

unpublished results).

Several cultivars were freed of viruses that are difñcult to

inactivate by thermotherapy by cutting crown disks 0.5 to 1

cm thick and propagating them in a peat-sand rooting

medium (Posnette and Jha 1960). Plants of three cultivars

were freed of MYEV by cutting stolon tips 0.5 to 1 mm or

larger from plants held at greenhouse or at elevated

temperatures and growing them out on culture medium and

then transferring them to pots in the greenhouse (Miller and

Belkengren 1963). The production of cultivars freed from

MYEV and other viruses by a combination of heat treatment

and tissue culture was described by Mullin et al. (1974,

1976).

Because MYEV usually occurs in complex with other

viruses, no controls are unique for MYEV; those discussed

for strawberry crinkle and strawberry mottle viruses are

applicable to MYEV. (See "Strawberry Mottle," p. 10, and

"Strawberry Crinkle," p. 20.)

Remarks

There is a scarcity of published information on the MYEV

particle. Once the antisera now prepared against it (Martin

and Converse 1982b) have been improved to permit rapid

detection of this virus in field samples, research on the

ecology of MYEV will move forward from its present state.

Despite advances in the development of virus-tested planting

stocks and certification schemes, the strawberry yellows

complex remains one of the major causes of economic loss to

the strawberry industry. More thorough evaluation of the

total Fragaria gene pool from which cultivated strawberries

are derived should provide clones with high levels of

resistance to colonization by the aphid vectors of many

strawberry viruses, including MYEV and high levels of

tolerance to the individual viruses. These clones could then

provide the basis for future cultivars.

>-'éStrawberry Latent C//

By J. R.jMcGrew ^

Additional Common Names

Demaree and Marcus Type 2.

History and Geographic Distribution

Typical symptoms of strawberry latent C disease (SLCD)

were first described in Fragaria vesea L. by Harris and King

(1942) from plants imported from the United States of

'Fairfax', 'Dorsett', and 'Premier'. SLCD will be used to

refer both to the disease and its causal agent. Symptoms in

the 'East MalHng' clone of F. vesca ('EMC') were first

illustrated by Demaree and Marcus (1951) who named the

disease type 2. It was found in cultivars throughout the

eastern United States.

McGrew (7958) showed that SLCD, with or without the

latent A strain of strawberry crinkle virus, failed to produce

symptoms in some seedlings of 'EMC, while other seedlings

showed typical epinasty and subsequent dwarfing. SLCD was

readily recovered from symptomless seedlings.

For several years, the geographic distribution of SLCD

corresponded closely with that of 'Howard 17' (also known

as 'Premier') (Bolton 7967; McGrew 1961), of which all

true-to-name plants carried this disease agent (Bell 7955,

Bolton 7964, Craig and Stultz 7964). Spread was detected

occasionally in Arkansas (Fulton 1960), and Nova Scotia

(Craig and Stultz 7964). Indexing at Beltsville, Md., (J. R.

McGrew, unpublished data) detected spread of SLCD in the

late 1970's into strawberry selections in Maryland, New

Jersey, Iowa, Arkansas, and Minnesota. Limited indexing of

selections and cultivars from North Carolina, Florida,

Louisiana, California, and Wisconsin and of cultivars

received from Japan, Taiwan, Germany, England, France,

Poland, and Italy has not detected SLCD.

Natural spread appears limited to eastern North America and

to areas where infected cultivars serve as a source ofinfection.

Economic Importance

The detrimental effect of SLCD as a component of a complex

in 'Catskiir (McGrew and Scott 7959) and alone and in

complex in 'Jerseybelle' (Kender 7964) is significant. Miller

(1960) found moderate to severe degeneration when SLCD

was added to existing virus complexes in 10 selections and

cultivars. However, several cvs., such as 'Premier' and

'Temple', infected with SLCD apparently were sufficiently

tolerant to be commercially acceptable to growers.

29
Figure 33.—Strawberry latent C disease symptoms in

Fragaria vesca 'EMK'. Left, 6 weeks after grafting;

right, chronic symptoms, after several months.

Symptoms on Natural and Experimental Hosts

Most strawberry cultivars appear symptomless when infected

with SLCD. Some nondiagnostic loss of vigor may be found in

others and severe leaf distortion in a few (Miller ¡960) when

SLCD is added to a complex which is itself symptomless.

Symptoms in sensitive clones of F. vesca (fig. 33) inoculated

by leaf grafts include severe epinasty of young leaflets

followed by moderate to severe dwarfing without epinasty,

mottling, or distortion. In F. virginiana Duch. 'UC-10', a

transitory mild yellowing is often seen, but it is not sufficiently

distinct to be diagnostic for SLCD.

At Beltsville, Md., SLCD from many sources has produced

rather uniform symptoms in sensitive indicator clones. The

epinastic shock symptoms are severe and obvious. The later

chronic dwarf symptoms range from severe to moderate, but

still show obvious reduction in size. After the appearance of

dwarfed but otherwise normal leaves, indicators are usually

discarded. Whether some isolates might allow indicators to

return to near normal size leaf production is not known.

N. W. Frazier (unpublished data) has found considerable

variation in severity ofsymptoms from some sources of SLCD

when the number or time that excised-leaf grafts remained in

place were reduced (as in Frazier 1974a). He also found

differences in symptom expression depending on age of leaf

used from a recently infected source plant. Use of older leaves

produced milder symptoms than younger leaves when grafted

individually to indicator plants.

Natural and Experimental Transmission

SLCD spreads in the field, and several aphid species have

been implicated as vectors. Experimentally, it has been

transmitted by runner and excised-leaf grafts and by dodder.

SLCD has been reported to be transmissible by Chaetosiphon

fragaefolii (Cock.). Smith {1952) found that this species

required more than 1 and fewer than 6 days to acquire SLCD,

that infectivity persisted for at least 9 days, and that symptoms

appeared in 23 or more days. Demaree and Marcus {1951)

obtained transmission of SLCD to F. vesca by Chaetosiphon

minor (Forbes) and C. thomasi H.R.L. (their "unnamed

species") collected from plants in the field. Rorie {1957)

suggested that C. minor rarely, if ever, transmits this virus.

N. W. Frazier (unpublished data) was unable to transmit

SLCD from three sources by use of Chaetosiphon jacobi

H.R.L. and several species of leafhoppers, white flies, and

thrips.

Natural spread of SLCD may be rapid under some

conditions—six of nine plants exposed for one season in

Michigan indexed positive (McGrew 1961), or movement

may be rare (Fulton 1960).

Experimental transmission of SLCD is readily achieved by

excised-leaf grafts. Days to symptoms on regular excised leaf

grafts are 24 to 60, mean 34 (McGrew 1970b) and, when all

leaves except grafts are removed, are 15 to 36, mean 21

(Frazier 1974).

Transmission by dodder has been successful using Cuscuta

subinclusa Dur. and Hilg. (29 to 40 days) (Smith and Moore

1952) and with C. campestris Yunck. (35 or more days)

(Fulton 1954).

Properties of the Causal Agent

Cross inoculations or natural complexes indicate SLCD is

distinct from other strawberry viruses, for example: crinkle,

mottle, vein banding (J.R. McGrew, unpublished data) and

pallidosis and mild yellow-edge (N. W. Frazier, unpublished

data). Information is lacking on the nature of the causal agent

and serological relationships of SLCD.

30
Detection and Identification

Strawberry latent C cannot be identified in strawberry cultivars

by symptoms. Transmission to sensitive indicator clones, as

Fragaria vesca clone 'EMC or 'UC-5', is necessary.

Further confirmation of suspected SLCD is to pass it by graft

transmission through an SLCD nonsensitive F. vesca clone,

such as 'Alpine', 'UC-T, 'UC-4' or 'UC-6', and to recover

symptoms in a sensitive clone. Absence of symptoms in the

SLCD nonsensitive clone eliminates the possibility of a

complex with other graft-transmissible agents to which that

clone is sensitive.

Control Procedures

Control procedures include the use of certified planting stock

free of known viruses and viruslike diseases, isolation of new

plantings from infected sources, possibly the use of aphicides,

and periodic replacement of planting stock.

Elimination of SLCD by heattreatment of entire plants was not

successful at 38°C. However, axillary buds that developed on

decapitated crowns and were removed after 3 days at 46.5°C or

above were free of this disease (Bolton 1967).

A combination of heat treatment at 35°C followed by tip

culture was partially successful in eliminating SLCD from a

strawberry cultivar (McGrew 1965). Recent trials (J. R.

McGrew, unpublished data) in which 14 expiants from

SLCD-infected sources were taken without prior heat

treatment (10 of 10 between 0.4 and 0.8 mm, 1 of 2 at 1.0 mm

and 1 of 2 at 1.8 mm) were free of the disease.

Remarks

The frequency of detection of SLCD in the field appears

directly related to the presence of nearby sources in the

planting. The production of cultivar clones free of SLCD and

moderate care in isolation of seedling, selection, and nursery

blocks from known sources, followed by continued replacement of certified fruiting-field stocks, should result in the

disappearance of this disease.

Leafhopper-Borne Diseases

^ Aster Yellows in Strawberry^

By L. N.iChiykowski

(Chemistry and Biology Research Institute, Research Branch,

Agriculture Canada, as C.B.R.L Contribution No. 1295)

Additional Common Names

Eastern (New York) aster yellows; western (California) aster

yellows; August black root; spot dying; chlorotic phyllody.

History and Geographic Distribution

The susceptibility of Fragaria species to aster yellows was

first demonstrated by Frazier and Severin (1945) who

experimentally transmitted a California or western strain to F.

vesca L. var. californica (Cham, and Schlecht.) Staudt,

using the aster leafhopper, Macrostelesfascifrons (Stâl) (also

known as M. divisus DeLong [nee] Uhler). In 1952, a disease

characterized by phylloid ñowers was reported as being

common but not abundant in scattered commercial strawberry plants in central California (Frazier and Thomas 1953).

The authors also stated that similar symptoms had been

observed on various strawberry cultivars and in seedling test

plants on rare occasions over the previous 20 yr. Western

aster yellows was transmitted from such field-infected

strawberry plants to aster and plantain (Plantago major L.)

by means of the aster leafhopper. The same species was also

used to transmit the disease from China aster to F. vesca L.

var. semperflorens (Duch.) Ser. cv. 'Alpine' and return it to

plantain.

In 1949, a disease causing phyllody was observed on

strawberry in Louisiana by Plakidas (1951) and given the

name "chlorotic phyllody." This disease is now generally

believed to have been aster yellows. A severe outbreak of a

disease in strawberry resembling aster yellows and relatively

new to Arkansas was reported by Smith (1954). The cause was

later verified by Fulton (1957b) who also showed that "August

black root" or "spot dying" were the result of aster yellows

infection.

Attempts by Kunkel (1926) to infect strawberry

experimentally with eastern aster yellows using the aster

leafhopper were unsuccessful. Chiykowski (1969), however,

transmitted a disease from naturally infected strawberry cv.

'Sparkle' to aster by means of the aster leafhopper,and the

symptoms produced were typical of eastern aster yellows.

Transmission from an infected ñeabane (Erigeron spp.) plant

found adjacent to the strawberry planting gave similar results.

The geographical range of aster yellows in general covers the

United States and Canada, but the distribution of the different

strains within this range is not clearly understood. Although

aster yellows has not been widely reported as a disease of

31
strawberry, it probably occurs in plantings throughout this

range but is not normally detected because of its low

incidence. Similar, possibly related, diseases occur in Europe,

Japan, and Russia.

Economic Importance

The incidence of aster yellows in strawberry is normally low,

although it may occasionally reach as high as 20% (Smith

1954). Infected plants produce no marketable fruit and

usually die within two mo after symptoms appear. Aster

yellows infection may not always be recognized as such and

instead may be attributed to other causes, as was the case

with August black root and spot dying (Fulton 1957b). It

could also be mistaken for other diseases, such as green petal

(see "Strawberry Green Petal and Similar Diseases," p. 34)

when both diseases occur in the same strawberry planting

(Chiykowski 1969). Thus, the real economic importance of

aster yellows in strawberry may sometimes be underestimated.

Symptoms on Natural and Experimental Hosts

The host range of aster yellows is extensive, consisting of

approximately 300 plant species in at least 50 families.

Included in this list of susceptible species are perennial,

annual, monocotyledonous dicotyledonous, cultivated and

wild plants.

Symptoms on strawberry. Foliage symptoms may appear at

any time during the growing season. New leaves have

shortened petioles, are reduced in size, chlorotic, and

generally cupped (fig. 34). Older leaves may be reddened, be

flat on the ground, and soon turn brown.

The type of flower and fruit symptoms expressed are

dependent on time of infection in relation to initiation of

flower buds. Plants infected late in the fruiting cycle may

show normal petals and some degree of flower sterility.

When infection occurs early in the flower initiation sequence,

the following symptoms may be seen: virescent petals on

partly or fully sterile flowers; virescent petals with small,

green, foliaceous growths from the achenes; or entirely

phylloid flowers. Several symptom stages may be present on

a single plant of even a single inflorescence (fig. 35). Floral

symptoms are important aids in the diagnosis of aster yellows

infection because foliage symptoms alone are not reliably

distinct from those of several other strawberry diseases; for

example, verticillium wilt, yellows (xanthosis) virus complexes, or lethal decline. (See the Aphid-borne Diseases

chapters, p. 10-31, and "Strawberry Lethal Decline," p. 38.)

Symptoms, although of the same general type, may differ in

different cultivars (Frazier and Posnette 1958). In 'Lassen',

the pathogen causes a severe "yellow- edge"-type symptom

accompanied by phyllody and proliferation of flowers, but in

'Shasta', it causes scalding of leaves, cessation of growth,

wilting, and rapid death of the plant; intermediate degrees

have been observed on other cultivars. There is some

Figure 34.—Fragaria vf.íca 'Alpine' experimentally

infected by leafhopper with western aster yellows

disease. (Courtesy, N. W. Frazier, University of

California.)

Figure 35.—Strawberry cv. 'Lassen' infected with aster

yellows disease: A. Various types of floral abnormalities

as well as dwarfed, cupped leaves; B. variation in

symptoms in the flowers of one truss. (Courtesy, N. W.

Frazier. University of California.)

32
Figure 36.—Aster yellows symptoms in China aster: A.

Eastern strain causing numerous, spindly, chlorotic

axillary shoots; B, western strain showing no axillary

growth.

suggestion that pathogen strain may also influence symptom

expression. The cv. 'Sparkle', naturally infected with an

eastern strain of aster yellows, displayed reddish rather than

virescent petals (Chiykowski 1969).

Although aster yellows has not been found occurring

naturally in wild strawberry, it has been experimentally

transmitted to several clones off. vesca (Frazier and Thomas

1953). The first evidence of infection consists of a very mild

veinclearing and a general chlorosis of the affected leaf. The

disease rapidly increases in severity, causing development of

adventitious crowns and chlorotic leaves. Petioles become

progressively reduced in size until they become very minute

shortly before the plants die. Leaflets exhibit upward or

downward cupping, and some petioles are twisted or curved,

tending to assume a horizontal position.

Symptoms on other plant species. Although symptoms on

all plant species are not identical, some appear to be

characteristic of aster yellows infection. Foliage symptoms in

broad-leaved plants consist of veinclearing followed by

chlorosis of the entire leaf and a reduction in leaf size.

Infection often first appears on only one half of the leaf or

plant, but gradually the entire plant becomes chlorotic and

dwarfed. Adventitious growth, consisting of dwarfed,

short-petioled leaves, from the crown of such hosts as carrot

may result in a witches'-broom symptom. Pathogen strain

may affect the type of symptom produced on certain host

species. In aster (Callistephus chinensis Nees), for example,

the eastern strain produces numerous spindly, chlorotic

axillary shoots while the western strain produces only a few

short, fleshy, rosettelike shoots (fig. 36). Also, the western

strain is considerably more severe and produces more

stunting than does the eastern strain.

Natural and Experimental Transmission

Leafhoppers. Twenty-seven species of leafhoppers are

known to transmit the western strain but only one, the aster

leafhopper, is known to transmit the eastern strain

(Chiykowski 1981b). However, the role played by the

various species in the epidemiology of aster yellows in

strawberry is largely unknown. The following three species

have been shown capable of transmitting the pathogen to or

from strawberry: (1) M. fascifrons, from strawberry to aster

(Frazier and Thomas 1953; Chiykowski 1969) and from aster

and celery (Apium graveolen.s L. var. dulce DC) to clones of

F.vesca (Frazier and Thomas 1953); (2) Colladonus

montanus (Van Duzee) from strawberry to plantain and

celery (Frazier and Posnette 1958); and (3) Colladonus

geminatus (Van Duzee), from strawberry to strawberry,

plantain, and celery (Frazier and Posnette 1958). Fragaria

spp., however, do not appear to be very favorable either as

food or breeding hosts of these three leafhopper species,

suggesting that their role as vectors of aster yellows in

33
strawberry is a minor one. Vector species such as

Scaphytopius acutus (Say) (Chiykowski 1962c) and

Aphrodes bicincta (Schrank) (Chiykowski 1977), which can

feed and breed on strawberry, could play a role in areas

where western strains of aster yellows are present.

Grafting. The pathogen can be transmitted from diseased to

healthy strawberry plants by stolon grafts, stolon to petiole

grafts, and excised leaflet grafts. Rapid death of diseased

tissue often does not allow sufficient time for graft union to

occur (Fulton 1957b). The pathogen has also been

transmitted by excised leaf grafts from periwinkle

{Catharanthus roseus (L.) G. Don) to strawberry (Braun and

KepHnger 1962).

Dodder. Cuscuta campestris Yunck. has been used to

transmit the pathogen from strawberry to periwinkle and back

to strawberry (Fulton 1957).

Properties of the Causal Agent

The causal agent, once thought to be a virus, is now

considered to be a mycoplasmalike organism. The organism

has been shown to be present in infected plants and

leafhoppers (Maramorosch et al. 1968\ Hirumi and

Maramorosch 1969). Its general morphological characters

are similar to those exhibited by the green petal organism

(fig. 43). (See "Strawberry Green Petal and Similar

Diseases," p. 34.)

Detection and Identification

Aster yellows can be detected in strawberry by the symptoms

produced on the foliage and on the flowers; however, in

areas where green petal disease occurs (see following

section), identification is more difficult because of general

symptom similarities, overlapping host range, and some

common vectors. Positive identification requires the use of

symptomatology on specific hosts and transmission

characteristics. (See "Strawberry Green Petal and Similar

Diseases," table 3, p. 37.)

Control Procedures

Because of the sporadic occurrence and generally low

incidence of aster yellows in strawberry plants, no control

procedures have been formulated for this crop. The disease

appears to be self-eliminating in strawberry (Frazier and

Thomas 7959), suggesting that incidence is dependent on

disease sources bordering the plantings and the movement of

infective leafhoppers from these sources into the crop. In

other susceptible crops where the disease is of economic

importance, various control methods have been used with

varying degrees of success. These include insecticides for the

reduction of leafhopper vectors, herbicides for the

elimination of inoculum sources, antibiotics, resistant plants,

and various cultural practices (Chapman 1973).

^ istrawberry Green Petal and Similar Diseases^/

By A. F.[Posnette and L. N.jChiykowski

(Contribution by East Mailing Research Station and

Chemistry and Biology Research Institute, Research Branch,

Agriculture Canada, as C.B.R.I. Contribution No. M-1259)

Additional Common Names

Clover phyllody.

History and Geographic Distribution

Phylloid fruit on strawberry (defined as the reversion of floral

organs such as sepals and bracts to leaves) was observed in

Europe more than 300 yr ago and, although some ofthese may

have been affected by green petal disease, they were thoughtto

be genetical abnormalities. The infectious nature of a disease

causing flower sterility and phyllody was recognized in Great

Britain in 1951 and named green petal (Posnette 1953). Most

observers agree that the disease had been present for many

years prior to that date, but not recognized because of the

similarity of symptoms to those caused by Verticillium spp.

Frazier and Posnette (1956, 1957) showed that the causal

agent of green petal was leafhopper transmitted and was also

responsible for the phyllody disease of clover.

In North America, green petal was first reported by Gourley

(7955) in Nova Scotia, although growers had observed

strawberry plants with green petal symptoms and clover plants

with phyllody some years earlier (Lachance 1952). The

transmissibility by leafhoppers and relationship of the two

diseases in Canada was demonstrated by Chiykowski (1962a, b).

Green petal in strawberry has been reported from North

America, Britain, continental Europe, and Russia. In North

America, the disease is recognized in eastern Canada from

Montreal eastward through Quebec and the Maritime

Provinces (Chiykowski et al. 1973). It probably occurs in the

northeastern United States although its presence has not been

recognized due, undoubtedly, to its similarity to aster yellows.

(See "Aster Yellows in Strawberry," p. 31.)

Although green petal of strawberry and a clover phyllody

disease have been shown in certain cases to be caused by the

same pathogen, one cannot unequivocally state that all cases

of phyllody in clover are in fact the same as green petal, since

other diseases can also produce similar symptoms. Thus, in

describing the geographical distribution of green petal one

should only consider reports in which the clover phyllody has

been shown to be the same as green petal.

Economic Importance

The effect of green petal infection on plants is such that they

will produce no marketable fruit. Incidence of the disease

varies from year to year and appears to be dependent on

climatic conditions and cultivars grown. In Great Britain, the

annual incidence is usually between 2 and 5%, but in some

years it can reach as high as 30%. In Prince Edward Island,

Canada, the incidence in the two commonly grown cvs.

34
'Redcoat' and 'Sparkle' reached 28 and 60%, respectively, in

1966 (Willis and Thompson 1966). In 1967, green petal

infection in fruiting fields ranged from 0.2 to 70% (avg. 34%)

in Nova Scotia, 12 to 70% in Prince Edward Island, and 0.5 to

31% (avg. 8%) in New Brunswick (Stultz and MacNab

1970). By the early 1970's, the incidence had dropped

dramatically. An extensive survey of first crop plantings

through Quebec and the Maritime Provinces showed that the

highest incidence observed was less than 3% (Chiykowski et

al. 1973). Cutcliffe and Thompson (1977) reported an

increase in the amount of green petal in Prince Edward Island

in 1976 and suggested that cultivar selection might be

responsible for the higher incidence.

Symptoms on Natural and Experimental Hosts

Natural hosts. Strawberry ladino clover (Trifalhtm repens

L.), red clover {Trifolium pratense L.), and alsike clover

(Trifolium hybridum L.) appear to be the principal natural

hosts of green petal. Although other plant species have been

observed with similar symptoms, proof that the green petal

pathogen is involved is lacking.

Symptoms on strawberry. The most obvious symptom and

the one from which the name is derived is the appearance of

flowers with green petals (fig. 37). Early flower symptoms are

in the form of adherent virescent petals, some of which

eventually become pink. Petal symptoms increase in intensity

on later- developing flowers so that the petals are reduced in

size and become dark green and leaflike (phylloid). Some

flowers are sterile, while others produce a small, hard, green

receptacle which remains dwarfed and does not ripen. The

achenes stand out from the receptacle and appear unusually

large. Although older foliage may remain normal in size and

green or slightly darker green than normal, turning purple in

some cultivars, new foliage is dwarfed, slightly asymmetrical,

cupped, and pale green with chlorotic margins (figs. 38 and

Figure 38.—Mother and daughter btrawberry plants

infected with green petal disease showing green flowers

and foliage with chlorotic itiargins.

Figure 37.—Green petal disease symptoms on strawberry showing green flower petals and affected fruit.

Figure 39.—Foliage symptoms on strawberry infected

with green petal disease. Leaf petioles are short and

leaves are dwarfed, slightly asymmetrical, and have

chlorotic margins.

39). Leaf petioles are extremely short in contrast to normal

foliage. The degree of cupping appears to vary with the

cultivar. For example, cupping can be very pronounced in

'Redchief but mild in 'Sparkle'. Few runners are formed, and

these are stunted and produce only one or two plants. Often the

runner terminates in a rosette or clump ofsmall, short-petioled

leaves (fig. 40). Most infected plants die after a few months.

Symptoms on Trifolium spp. The most characteristic

symptom is phyllody. The degree of phyllody observed on an

infected flower head is dependent on the stage of floral

development at time of infection. In flowers which have begun

development at time of infection, pedicels of individual

flowers and calyx lobes elongate up to three times their normal

length. In advanced infection, these calyx lobes become

leaflike, complete with venation. The standard, keel, and

wings of the flower, while remaining normal in color, are

greatly reduced in size and in advanced infection may be

completely absent. The flower then consists of an enlarged

35
Figure 40.—Left, Normal strawberry runner plant; right,

Runner of plant infected with green petal disease

showing a terminal rosette of small, short-petioled

leaves.

^M • <t

wT^-^-

^^^^^Bg^^'il /. 12-'^

^.^îwm

j

I

Figure 41.—Left, Healthy inflorescence of Ladino

clover; right, two inflorescences infected with green

petal (clover phyllody) disease showing different degrees

of phylloid development.

Figure 42.—Green petal (clover phyllody) disease

symptoms in individual flowers of Ladino clover: Left,

Healthy flower; rest, progressive development of

phyllody showing reduction in petal size, absence of

petals, enlargement of ovary, proliferation of ovary,

replacement of ovary by a leaf, and enlargement of the

calyx.

calyx and enlarged ovary. The ovary may become twice the

normal size and develops a stipe. In advanced infection, the

ovary may proliferate into a simple or trifoliate leaf, or the

ovary may be replaced by a simple leaf (figs. 41 and 42).

Foliage symptoms consist of chlorosis of new leaves with

reduced leaf size and petiole length.

Experimental hosts. The pathogen has a relatively wide host

range with at least 79 species in 22 families shown to be

susceptible (Chiykowski 7967, ¡974). The host list includes

annual and perennial weeds and cultivated species of

monocotyledons and dicotyledons.

Foliar symptoms on these species generally consist of mild

vein clearing, mild chlorosis, stunting as a result of a

shortening of internodes, increased axillary growth, and

reduced leaf size. Thickening of crowns in some species

produces a witches'-broom effect. Many species produce

considerably more flowers than do healthy plants. The most

striking symptoms occur on the flowers. The calyx is greatly

enlarged and leaflike with veins. The petals are enlarged,

green, and take on leaflike characteristics. The ovary becomes

pedicellate and may eventually split open, developing into a

leaflike structure. Often the ovary is replaced by vegetative

growth.

Natural and Experimental Transmission

Leafhoppers. Several leafhopper species have been shown

capable of transmitting the green petal pathogen, but their

roles in spreading the disease in the field have not been fully

evaluated. Only Aphrodes bicincta (Schrank) has been shown

to transmit the pathogen to and from strawberry, although

species such as Macrosteles fascifrons (Stâl), Euscelis

lineolata Brülle, and Euscelis incisas (Kbm.) (also known as E

plebeja [Fall.]) have been shown to transmit from strawberry

to clover and to other hosts, but not back to strawberry. Other

species, such as Macrosteles viridigriseus (Edwards), Macrosteles cristatus (Ribaut), Anoscopus albifrons (L.) (also

known as Aphrodes albifrons [L.]), Scaphytopius acutus

(Say), Paraphlepsius irroratus (Say), and Speudotettix

subfusculus (Fall.), have been shown to transmit the pathogen

from and to clover.

Experimental evidence suggests that A. bicincta is the

principal vector responsible for infecting strawberry and that

the other species are important in maintaining the disease in

clover and weed hosts. Plants can become infected in the field

from June to October, but transmission appears to reach a peak

in August (Chiykowski 1962a, Thompson 1968).

Non-leafhopper transmission. Green petal has been transmitted by the following species of dodder: Cuscuta subinclusa

Dur. and Hilg., from clover to strawberry and to Duchesnea

indica (Andr.) Focke; C. campestris Yunck., to strawberry

cultivars and to Fragaria vesca L.; C. arvensis Beyr. and C.

europaea L., from clover to F. vesca; and C. gronovii Willd.,

from periwinkle (Catharanthus roseus (L.) G. Don.) (also

known as Vinca rosea L.) to periwinkle.

36
Table 3.—Distinctions between green petal and aster yellows

Point of comparison Green petal Eastern aster yellows Western aster yellows

Latent period in vector 28-35 days at 25 °C 14-21 days at 25 °C 14-21 days at 25°C.

Transmission by:

Macrostelesfascifrons Higher by females Sexes equal Sexes equal.

Aphrodes bicincta Yes No Yes.

Scaphytopius acutus Yes No Yes.

Symptoms on:

Trifolium repens petals White and reduced

or absent.

Reduced and green 0)

T. r. calyx Enlarged and leaflike Near normal 0)

Callistephus chinensis:

Incubation period 23 days 16 days 14 days.

Head proliferation Yes No No.

Chlorosis Mild or absent Severe Severe.

Vein clearing Mild Severe Severe.

Axillary growth Slight and green Profuse and chlorotic None.

Catharanthus roseus:

Axillary growth Sparse or absent Profuse Absent.

Chlorosis Mild or absent Severe Severe.

Petals Dark green and leaflike Light green, normal Light green, normal

size and texture. size and texture.

Apium graveolens Resistant Susceptible with long

incubation period.

Highly susceptible.

Nicotiana rustica:

Chlorosis None Severe Severe.

Vein clearing Mild Obvious Obvious.

Flowering Profuse Few Few.

^No comparison made.

The disease has also been transmitted by grafting from

strawberry to strawberry.

Properties of the Causal Agent

The causal agent, once thoughtto be a virus, is now considered

to be a mycoplasmalike organism (fig. 43). The organism has

been shown to be present in infected plants and transmitting

insects (Sinha and PaUwal 1969, 1970; Cousin et al. 1970;

Beakbane et al. 1971).

Detection and Identification

Green petal can be easily confused with some types of aster

yellows disease. The two diseases have an overlapping plant

host range, in some cases an overlapping geographical range,

and some vector species in common. Positive identification

requires the use ofsymptomatology on specific plant hosts and

transmission characteristics (see table 3).

Control Procedures

Insecticides. Studies on controlling green petal through

control of vectors by chemical sprays have been limited.

Collins and Morgan (1958) reported some control of spread in

plots treated with malathion. Razvyazkina (1960) recommended weed-host eradication and general application of

DDT, but gave no data to support these measures. Willis and

Thompson (1966) reported that strawberry plantings transplanted with plants from nurseries treated the previous year

with granular disulfoton applied as sidedressings had fewer

infected plants than those treated with malathion sprays. Field

experiments were conducted over a 2-yr period by Thompson

et al. (1973) to determine the efficacy ofseveral insecticides in

reducing green petal disease. In the first year, disulfoton,

soil-incorporated before planting, was most effective in

reducing the incidence of infected plants. In the following

37
Figure 43. M\coplasnialikcorgunism in phloem cell of

Ladino clover infected with green petal (clover phyllody)

disease. (Bar represents 5(X) nm.)

year, three foliar sprays of DPX-1410 (S-methyl l-(dimethylcarbamoyl)-N-l(methylcarbamoyl) oxy] thioformidate)

(Du Pont of Canada), endosulfan, or oxydemeton-methyl

gave the best results; however, fruit yields were not increased

by any of the treatments.

Antibiotics. Demonstration that the mycoplasma causal

agents of several yellows-type plant diseases are sensitive to

tetracycline antibiotics (Ishiie et al. ¡967) offers another

possible approach to controlling these diseases. Although

antibiotics have not been used for control of green petal under

field conditions, they have been experimentally tried in a

greenhouse environment. Oxytetracycline, tetracycline, and

doxycycline applied as root dips, foliage dips, or sprays to

aster plants immediately after inoculation by leafhoppers

delayed the development of symptoms, while nontetracycline

antibiotics had no effect (Chiykowski 1972, 1973). Root

treatment of infected asters with oxytetracycline resulted in

remission of symptoms, although symptoms eventually

reappeared some weeks later (Sinha and Peterson 1972).

Cultural. Field observations (Chiykowski et al. 1973; Collins

and Morgan 1958; Gourley et al. 1971; Thompson and

Cutcliffe 1972; Willis and Thompson 7966; Cutcliffe and

Thompson 1977) and greenhouse experiments (Chiykowski

and Craig 1975, 1978) suggest that strawberry cultivars differ

in their reaction to green petal infection. While some of the

differences are dependent on the cultivar-pathogen reaction,

variation in disease incidence appears to depend on vector

preference for certain cultivars. Therefore, selection of

cultivars for resistance to both pathogen and vector species

would be highly desirable for reducing green petal incidence.

The selection of growing site can also be important. Various

clover species are known to be highly susceptible to green

petal and also serve as breeding areas for such leafhopper

species as A. bkincta and S. acutus. Culture of strawberries

near or adjacent to such crops should be avoided.

Origin of plants for new plantations should be carefully

chosen. Stultz and MacNab {1970} found that amounts of

green petal diseased plants observed in new plantations,

regardless oftheir location, were characteristic ofthe nurseries

from which the plants originated and were generally low when

obtained from certified nurseries. In contrast, disease

incidence in new plantations with plants taken from common

field stock reached up to 50%.

Heat therapy. Green petal pathogen, originating from

strawberry, was not eradicated from entire periwinkle plants

treated at 40° to 42°C for 3 wk, but 4 of 10 cuttings from these

plants were free of the pathogen. Another isolate originating

from a Helenium species was eradicated from one of three

entire periwinkle plants treated at 40° to 42°C for 3 wk, and all

of 10 cuttings were free of the pathogen (Posnette and

Ellenberger 1963).

lil -'^^Strawberry Lethal Decline,; ,

By C. D.ISchwartze, N. W.lFrazier, and R. H./Converse

Additional Common Names

Northwest disease. X- disease ofstone fruits is possibly related

to lethal decline disease (LDD) (Frazier and Jensen 1970).

History and Geographic Distribution

LDD was first observed in western Washington about 1952 in

'Northwest' strawberry and was subsequently seen in other

cultivars and unnamed strawberry seedlings. This disease was

described by Schwartze and Frazier (/964j. Since 1964, LDD

has been reported in British Columbia and Oregon (Schwartze

and Frazier 1970; Converse and Bartlett 1971).

Economic Importance

LDD is a minor problem in strawberry fruit production, rarely

affecting more than 2% of field plants, although 25% infection

has been observed. This disease has been noted as a factor in

survival of transplants. Late autumn infection in strawberry

nurseries may produce no symptoms until after plants are dug,

stored, and replanted. Transplant failure caused by LDD has

ranged up to 8% (Schwartze and Frazier 7970).

Symptoms on Natural and Experimental Hosts

LDD has been transmitted only to the genus Fragaria, but all

cultivars and all species tested (F. vesca and F. chiloensis) are

susceptible. The incidence of natural infection differs among

cultivars.

Symptoms in cultivars. Symptoms first appear in mid-May

and continue to appear for 2 mo. It is rare to find new

infections from mid-July to mid-October, but new infections

are visible after that into the autumn and winter. In the spring

and in the greenhouse, infected plants develop dwarfed.

38
chlorotic, upward-cupped young leaves with unequal-sized

leaflets. Mature leaves on infected plants may be dull,

chlorotic, and somewhat bronzed above, rolled upward, and

reddish or purplish beneath. This dull or "dirty" chlorosis is a

characteristic symptom of LDD (fig. 44). As the disease

progresses, more mature leaves exhibit these symptoms and

die. Only a few, dwarfed, chlorotic, distorted young leaves

remain before the plant dies.

In the autumn and winter, the premature reddening of the

foliage of LDD-infected plants is often used as a diagnostic

marker to eliminate infected mother plants and their daughter

plant systems. At digging time, daughter plants of infected

Figure 44.—A, "Hcwd' strawberry infected with lethal

decline disease, Elkton, Oreg.. September 1970,

showing bronzing of older leaves and cupping of younger

ones; B. dwarfed, rosetted strawberry seedling infected

with lethal decline disease (above) next to normal plant

(below) in the same row.

mother plants are often conspicuously chlorotic and stunted,

but some infected daughters may be symptomless. Apparently

not all daughter plants in a stolon chain from an infected

mother plant develop LDD, which suggests an uneven

distribution of the pathogen within each plant. Infected

daughter plants die within a month after transplanting as

nursery stock.

In the field, plants that are infected with LDD usually die

before producing flowers or fruit. Plants infected by grafting in

the greenhouse usually have sterile blossoms without petals

(but not virescent petals) on shortened pedicels. Receptacles

may be elongated and necrotic and the calyx lobes reddened.

Cultivars graft-inoculated with LDD in the greenhouse

develop bronzed, wilted leaves (fig. 45). These symptoms are

preceded by degeneration of the older roots, which become

dark brown to black throughout.

Symptoms on Fragaria vesca indicators. Symptoms of LDD

after inoculation by leaflet grafting are about the same as in

strawberry cultivars. Some variations in tolerance to LDD

infection have been noticed among F. vesca clones, but all are

eventually killed by the disease following graft inoculation.

The peach yellow leafroll-type of X-disease, caused by a

mycoplasmalike organism (Nasu et al. 1970), was experimentally transmitted to F. virginiana cv. 'UC-10' and to

'Hood' strawberry by the leafhopper Colladonus montanus

(Van Duzee). On these hosts, it produced symptoms

resembling those of LDD (fig. 46) (Frazier and Jensen 1970).

X-disease transmissions from Prunus species to F. vesca by

dodder and by leaf graft have been reported in Eastern United

States, resulting in mild or unspecified symptoms (Slack 7952;

Braun and Keplinger 1962).

Figure 45.—Strawberry cultivar leaf-graft inoculated

with lethal decline disease 4 mo previously, October

1963, Washington State University.

39
Figure 46.—Peach yellow leafroU strain of Western

X-disease leaf grafted to Fragaria virginiana cv.

'UC-10', causing chlorotic discoloration of older leaves,

severe dwarfing of younger leaves, crown necrosis, and

runner death, soon becoming lethal to the entire plant.

Natural and Experimental Transmission

Natural transmission. The causal agent of LDD was not

transmitted from strawberry to strawberry by the aphid

Chaetosiphon jacobi H.R.L. nor by five species of leafhoppers known to transmit aster yellows disease (see "Aster

Yellows in Strawberry," p. 31): Colladonus geminatus

(Van Duzee), C. montanus (Van Duzee), Euscelidius

variegatus (Kirschbaum), Fiebierella florii (Stâl), and

Macrosteles fascifrons (Stâl), or by a vector of Pierce's

disease: Graphocephala atropunctata (Signoret) [also known

as Hordnia circellata (Baker)] (Schwartze and Frazier 1964).

C. geminatus transmitted the peach yellow leafroll agent

(Western X-disease) to strawberry, causing symptoms similar

to LDD, as already noted (Frazier and Jensen 7970). The

leafhopper Aphrodes bicincta (Schrank) was able to acquire

and transmit LDD from strawberry to strawberry in

preliminary greenhouse tests (R. H. Converse, unpublished

results).

LDD has spread in plants in fumigated soils. This observation

is in keeping with a hypothesis that LDD is not nematode

borne. Furthermore, mapping the locations of LDD-infected

plants in a cultivated strawberry field suggested that most

infections are widely scattered, with 39% clumping of

LDD-infected plants in pairs or triplets (Converse and

Bartlett 1971).

Experimental transmission. LDD has been transmitted by

petiole insert leañet grafting from Fragaria to Fragaria. The

time lapse for appearance of symptoms following graft

inoculation varies from 3 to 16 wk (mean, 8 wk). Because no

symptomless hosts of LDD are known and all susceptible hosts

are severely weakened or killed after inoculation, sequential

graft inoculation of LDD isolates becomes progressively more

difficult. It has been found to be impossible to maintain

isolates for long periods of time in the greenhouse.

Dodder transmission of a strain of X-disease from Prunus to

Fragaria was claimed in Eastern United States, as previously

noted (Slack 1952). Johnson (1969) graft inoculatedMcoíí'ana

tabacum L. with LDD-infected strawberry petioles. Using

Cuscuta subindusa Dur. & Hilg., he was then able to cause

witches'-broom symptoms on one Trifolium repens L., which

then gave rise to dwarfism, leaf distortion, and epinasty in one

mechanically inoculated Lycopersicum esculentum Mill,

plant. This work was not repeated and requires confirmation.

Properties of the Causal Agent

Electron microscopy of sieve tubes of LDD-infected

'Northwest' strawberry revealed mycoplasmalike bodies

averaging 173 nm in diameter (fig. 47) (R. H. Converse,

unpublished data), thus supporting the possible relationship

of LDD to Western X-disease suggested by Frazier and Jensen

(1970) since it would be expected to be caused by a

mycoplasmalike agent (Nasu et al. 1970; Granett and Gilmer

7977; Jones et al. 7974). Western X-disease and its leafhopper

vectors were recently reviewed by Gold (1979). X-disease

occurs in several "strains" in various parts of North America

(Gilmer and Blodgett 7976).

Preliminary attempts to moderate LDD symptoms by heat

therapy and by tetracycline therapy (Nienhaus and Sikora

7979; R. H. Converse, unpublished data) were unsuccessful.

Detection and Identification

No method is superior to direct observation of characteristic

symptoms in infected plants in the field. Transmission by

leaflet graft to F. vesca can be done to confirm field diagnosis

if it is necessary to distinguish between LDD and herbicide

damage.

Figure 47.—Mycoplasmalike bodies in sieve tube of cv.

'Northwest' infected with lethal decline disease. (Bar

represents I micron.)

40
T

Control Procedures

Control is mainly by thorough roguing of infected motherdaughter plant systems in autumn and winter. No successful

therapy of LDD has been reported.

Remarks

The nature and identity of the causal agent of LDD are

unknown. Until precise identification methods are developed

for the causal agent, it will be difficult to determine the natural

reservoirs and means of spread of this disease accurately.

áStrawberry Rickettsia Yellows and Mycoplasma

Yellows

By R. S.lGreber

Additional Common Names

Lethal yellows for both diseases; little leaf or big bud for the

disease associated with mycoplasmalike organisms (MLO).

The etiological relationship, if any, with diseases such as

"bronze leaf wilt" in Great Britain (McGrew and Posnette

1970) and "lethal decline" in the United States (Schwartze

and Frazier 1964, 1970) is unknown. (See 'Other Leafhopper-Bome Diseases of Strawberry," p. 45, and "Strawberry

Lethal Decline," p. 38.). Strawberry rickettsia yellows and

mycoplasma yellows diseases result in the development of

small chlorotic leaves, decline, and death, usually without

development of prominent green petal symptoms.

History and Geographic Distribution

The first description of lethal yellows was in Australia by

Stubbs (1968) and followed the production and use of

planting material free of serious virus disease complexes such

as severe yellow edge. The prevalence of virus diseases

which produced similar symptoms had previously inhibited

the recognition of the diseases associated with MLO and

rickettsialike organisms (RLO) except for the distinctive

green-petal disease. Shanmuganathan and Garrett (1976)

described a little leaf disease in Victorian strawberries, and a

similar disease in Queensland was referred to either as lethal

yellows or "big bud." The latter name related to an

etiological association with MLO from the tomato big bud

disease. Neither of these names seemed particularly

appropriate because the MLO disease of strawberries in the

subtropics was frequently not lethal nor was it associated with

flower bud phyllody or distortion. In Victoria, the MLO

disease is invariably lethal (Shanmuganathan and Garrett

1976). The mycoplasma-associated strawberry lethal yellows, little leaf or big bud diseases are hereafter referred to as

mycoplasma yellows or MLO disease, and the rickettsiaassociated lethal yellows is referred to as rickettsia yellows or

RLO disease.

Rickettsia yellows has been reported only from Queensland

and was distinguished from mycoplasma yellows only

following electron microscope thin section examination

(Greber and Gowanlock 1979) of plants which seemed to

have a slightly atypical yellows symptom. This disease was

frequently lethal under hot conditions. The disease has since

been detected from other locations in Queensland, but is not

easily distinguished from mycoplasma yellows because of

symptom variation overlap between the two (Greber and

Gowanlock 7979).

The Australian diseases are difficult to correlate with those of

the little-leaf or lethal yellows types occurring elsewhere

because of lack of data from electron microscopy of thin

sections or chemotherapy evidence. Bronze leaf wilt

(McGrew and Posnette 7970) probably falls into this group

and perhaps also lethal decline (Schwartze and Frazier 7970)

and witches'-broom (Mellor and Fitzpatrick 7967). (See

chapters on these diseases in the Strawberry section.)

Economic Importance

Both the MLO and RLO diseases occur sporadically and are

of economic importance mainly because they invade runner

production areas isolated from strawberry virus infection.

Apart from losses of plants by death and roguing on the

runner producing farms, it is difficult to avoid distribution of

runners carrying latent infections. These cause more serious

losses on fruit production farms because it is often too late to

replant by the time symptoms are diagnosed. Serious

outbreaks are infrequent and may become less frequent with

present control measures

Symptoms on Natural and Experimental Hosts

Mycoplasma yellows. Older leaves develop some bronze or

purple pigmentation and roll upward around the midvein.

New leaves have small leaflets and shorter petioles. Leaf

margins are yellow or chlorotic and the lamina becomes either

chlorotic or bronzed (figs. 48, 49 A and ß). Flower and fruit

production is inhibited and plants often die, although under

warmer conditions they often persist until rogued out. All

runners attached to affected mother plants eventually develop

symptoms. In graft-infected Fragaria vesca L. seedlings and

cv. 'UC-l' indicators or in strawberry cultivars (fig. 49 B),

symptoms are similar to those occurring in the field.

Figure 48. — Strawberry plant cv. 'Redlands Crimson'

infected with mycoplasma yellows.

41
^éf^-

'9

Figure 49. — A. Symptoms of mycoplasma yellows on

strawberry cv. "Earlisweet'; B. little leaf symptoms of

mycoplasma yellows on strawberry cv. 'Redlands

Crimson' following leaf graft transmission; C mycoplasmalike bodies in sieve tube of strawberry cv.

'Redlands Crimson' infected with mycoplasma yellows.

(Bar represents 1000 nm.); D. detail of mycoplasmalike

bodies in sieve tube of mycoplasma yellows infected

strawberry. (Bar represents 200 nm.)

The end result was invariably lethal with Victorian isolates

(Stubbs 1968: Shanmuganathan and Garrett 1976). N.

Shanmuganathan (personal communication) reports that

flowers on affected plants in Victoria have small petals with a

tinge of green. New leaves of these plants have shortened

petioles and are reduced in size, chlorotic, and generally

cupped. Affected plants wilt suddenly and die within a few

weeks.

Rickettsia yellows. Bronze and purple pigments develop in

older leaves. Younger leaves develop interveinal chlorosis

and tend to bend back along the midvein (fig. 50-4). Leaves

are usually more rigid, tear easily, and may be asymmetric

(fig. 50 B). Under high temperatures (daily max. >30°C),

some petioles and stolons become necrotic, and affected

mother plants frequently wilt and die, leaving a cluster of

chlorotic, infected runners. Flowers are not affected until

plants wilt or become severely debilitated, when they

frequently abort. Often a mild vascular discoloration is

evident when affected crowns are cut and examined.

Symptoms on strawberry cultivars and the indicator F. vesca

cv. 'UC-4' resulting from leaf-graft infection follow a pattern

similar to those in field plants (fig. 50 C). The severity of

symptoms produced and frequency of death are increased by

growing plants at high temperatures. When infected plants

are maintained for several months at temperatures below

25°C, symptoms decrease and most plants eventually show

normal growth, which usually develops following formation

of a new crown from axillary buds.

Natural and Experimental Transmission

The disease symptoms for both the MLO and RLO diseases

begin to develop on leaf-graft inoculated F. vesca and

strawberry plants after 3 to 9 wk. Graft-inoculation from field

plants with severe symptoms of either disease was efficient

42
Figure 50.—A, 'Redlands Crimson' strawberry: Left,

freed of rickettsia yellows by treatment with 1,000 ppm

sodium penicillinate; right, infected with rickettsia yellows; B, 'Tiobelle' strawberry: Left, healthy leaf, right,

leaf infected with rickettsia yellows: C, Fragaria vesca

'UC^' infected with rickettsia yellows; D, closely-packed

rickettsialike bodies, mostly in cross section, in a sieve

tube of strawberry infected with rickettsia yellows. (Bar

respresents 1000 nm.) E, Detail of rickettsialike body

in a sieve tube of 'Redlands Crimson' strawberry infected with rickettsia yellows. (Bar represents 2(X) nm.)

when two grafts were made to medium-age leaves on each

test plant. Inoculation from chronic infections was less

reliable, and RLO-infected plants which had been grown at

less than 25°C were poor sources for leaf-graft transmission.

This was correlated with difficulty in locating the organism in

electron microscope thin sections of midribs and petioles.

Most reported vectors of RLO and MLO diseases are

leafhoppers from the family Cicadellidae. and known

leafhopper vectors of phloem-inhabiting RLO are from the

subfamily Agalliinae (Nielsen 1979). Bronze leaf wilt has

been shown to be transmitted by the leafhoppers Euscelis

spp. and Macrosteles spp. (McGrew and Posnette 1970).

Transmission of MLO diseases in Australia has been

demonstrated only by Orosius spp. (Grylls 1979; Greber and

Gowanlock 1979). The phloem RLO-associated disease,

clover rugose leaf curl (Behncken and Gowanlock 1976), is

-^^Hv

I '; ^. • -' ' • ' •■■■ ^ '

''Z:.iS'^4i^f:^

transmitted by Austroagallia tórrida Evans (Grylls 1979).

Attempts to transmit strawberry rickettsia and mycoplasma

yellows by these vectors were unsuccessful (Greber and

Gowanlock 1979), but the environmental conditions necessary for transmission to strawberry may not have been

fulfilled, even though other plant species were infected in

these tests. Since natural infection only occurs during high

temperatures and the concentration of RLO in leaves at lower

temperatures is poor (R, S. Greber and D. H. Gowanlock,

unpublished data; Markham et al, 1975), it may be necessary

43
to conduct these vector tests at temperatures around 30°C to

achieve transmission to strawberry.

Attempts to transmit clover phyllody organisms to strawberry

in Victoria using Orosius argentatus (Evans), Nesoclutha

pallida (Evans), and Zygina zealandica (Myers), were

unsuccessful, but typical little leaf symptoms developed in

strawberry after dodder (Cuscuta campestris Yunck.) transmissions from white clover with phyllody and tomato with big

bud symptoms (N. Shanmuganathan, personal communication). Transmission from a clover green petal source and

from a source which produced big bud disease of tomato to

strawberry using dodder (C. campestris) was also reported by

Helms (1962). Her transmission resulted in early death of F.

vesca plants, and small green petals developed on most plants

of strawberry cv. 'Climax', which then died after 2 to 4 mo.

The epidemiology of both mycoplasma and rickettsia yellows

indicates that natural infection is highest following periods of

hot, dry weather. At these times, natural vegetation is

becoming dry and unattractive to leafhoppers, and the

irrigated strawberry runner production plantings provide

alternative hosts, which may not be preferred under normal

conditions.

Properties of the Causal Agent

There is a consistent association of MLO with mycoplasma

yellows and RLO with rickettsia yellows. This has been

shown by thin section electron microscopy of both naturally

and experimentally infected plants. No such organisms were

found in sections of healthy plants or those showing

symptom remission following chemotherapy (Greber and

Gowanlock 1979). This indicates a high probability of a

causal association; however, the status of the organisms has

not been demonstrated unequivocally by isolation to cell-free

cultures and reinoculation to produce the diseases. The

symptoms of both diseases show similarities and the

organisms associated with the two diseases have similar

phloem tissue locations.

Strawberry-infecting MLO have typical pleomorphic shapes

in thin section and vary greatly in size and shape, but are

usually in the range of 200 to 500 nm across (fig. 49 C). They

have a single trilaminar membrane and characteristic

radiating fibrils (fig. 49 D).

Strawberry-infecting RLO are found in sieve tubes and are

accompanied by dark-staining granular material. In cells

densely packed with the organism, they appear approximately circular in outline (fig. 50 D), but this could be due to their

alinement, and more of the elongate forms are found in less

densely packed cells (fig. 50 E). The elongate forms (up to

l|x) have ridged cell walls and an inner cell membrane.

Ribosomelike and fibrillar structures are present within the

RLO cells. Assignment of these organisms to systematic

categories within Mycoplasmatales and Rickettsiales may

also be premature until their characteristics have been

investigated in pure cultures; however because their

morphologies closely resemble other members of these

groups, the MLO and RLO terminology has been maintained

in this chapter.

Detection and Identification

Both diseases are readily detected in the field by the

characteristic little-leaf-yellows symptoms, especially in the

absence of virus diseases. They can be visually differentiated

from fungal diseases, such as fusarium wilt, which cause

necrosis of the older leaves rather than purple pigmentation

and rolling of the laminae. This pigmentation and the

chlorotic margins of younger leaves also distinguish the

yellow diseases from bud nematodes infection

(Aphelenchoides besseyi Christie). (See "Bud and Leaf

Nematodes of Strawberry," p. 72.) Neither of the yellows

diseases causes green-petal symptoms. (See "Strawberry

Green Petal and Similar Diseases," p. 34.) Flowers may

abort on plants infected with either strawberry rickettsia yellows or mycoplasma yellows, but flowering is more likely to

continue with RLO infections.

Leaf graft transmission (allow for several weeks of latency),

coupled with isolations to detect fungal parasites, can be used

to confirm infection. However, it is difficult to distinguish

between mycoplasma yellows and rickettsia yellows on

symptoms alone, and etiology must be confirmed by

examination of thin sections in the electron microscope.

Control Procedures

Roguing of affected mother plants and all attached runners

did not prevent distribution of latently infected runners when

the infection period continued until near digging time. No

severe infection, however, has occurred in Queensland after

institution of a spray program on runner production farms,

using 0.3 g dimethoate per liter (0.03%) every 5 days during

summer. This program has not been in operation long enough

to have proved its effectiveness under all conditions.

Continuous maintenance of a high level of insecticide is

practicable during this nonfruiting period.

In Victoria, control measures include insecticide spraying of

uncultivated land adjoining runner crops, clean cultivation of

a buffer strip 10 m wide around the crop, and biweekly

spraying of insecticides on the runner crop (N. Shanmuganathan, personal communication).

Mycoplasma yellows usually terminates in death of the plant,

but roguing is commonly practiced by fruit-growing farmers

as soon as affected plants are recognized. Rickettsia yellows,

on the other hand, can show natural symptom remission

under cooler conditions, and plants will again become

productive.

Treatment of rickettsia yellows-affected individual plants

with penicillin drenches (1000 ppm sodium penicillinate) at

5-day intervals for 8 wk can effect a cure, especially if plants

44
are grown with daily temperature maxima below 30°C. In

plants treated in this way, organisms or symptoms have not

been detected at any time during the subsequent 2 yr of

growth under a variety of environmental conditions. The

procedure should enable infected clones to be freed of this

disease.

Remarks

The fact that the etiology of little leaf, yellows and similar

diseases of strawberries in many countries has still not been

investigated by thin-section electron microscopy causes

difficulty in making comparisons between diseases which

have been described from different locations. While the

green-petal diseases have been well examined, there are few

reports of other MLO-associated diseases of strawberry.

There are also few reports of the effect of antibiotics on these

diseases, and the vector transmission aspect has only been

investigated by a few workers in recent years.

The characteristic yellows symptoms probably result from

the effect on phloem function by the organisms, which are

exclusively located in this tissue. Very similar symptoms are

caused by these two quite unrelated organisms, which infect

strawberry phloem tissue.

Most MLO are sensitive to tetracycline antibiotics, but the

effectiveness of penicillin on an organism could imply that it

has a true cell wall. The RLO which are associated with

strawberry rickettsia yellows have been shown to have true

cell walls. The presence of a cell wall as well as a cell

membrane distinguishes RLO from MLO in thin sections.

The RLO are also associated with a dark-stained granular

material of unknown function in the sieve tubes, which is not

present with MLO.

Now that the etiology of these diseases is understood, control

measures can be instituted. All diseases of this type, which

infect phloem tissue, are transmitted by cicadellid leafhoppers. None of this group of insects is known to breed on

strawberries in Australia, and the inoculum and vectors

probably originated from surrounding vegetation. There are

many possible sources of MLO from other host species. RLO

infect clover in Great Britain and Australia (Markham et al.

7975; Behncken and Gowanlock 1976), and the same or

similar organisms may be the cause of corresponding

diseases in strawberries.

<^.<-

Other Leafhopper-Borne Diseases of Strawberry ^^

By L. N.jChiykowski and A. F.lPosnette

Several leafhopper-bome diseases have been reported

affecting or capable of affecting strawberry, but information

on their economic importance, epidemiology, and relationship with other similar diseases is generally lacking.

Their inclusion in this handbook will serve to alert the reader

to their existence and possibly to stimulate further work to

determine their effects on strawberry production.

Bronze Leaf Wilt

(Clover witches'-broom). Frazier and Posnette (7957)

distinguished two pathogens they transferred from clover to

strawberry; one caused phyllody and green petal in clover

and strawberry, respectively, and the other produced

proliferation (witches'-broom) in clover and bronzing

reddening and wilt in strawberry but no flower symptoms in

either host.

The pathogen was transmitted by dodder. Cuscuta campestris

Yunck., to Fragaria cultivars and by the leafhoppers,

Euscelis lineolatus Brülle, E. incisus (Kbm.), and Macrosteles sp. from clover and strawberry to clover, carrot, celery,

and tomato, but not to strawberry (Posnette and Ellenberger

1963). It was not transmitted by Aphrodes bicincta

(Schrank), and the means by which strawberry plants become

infected in the field is not known. The incidence of the

disease in strawberry is difficult to assess because of its

resemblance to green petal disease in the absence of flowers

(see "Strawberry Green Petal and Similar Diseases," p. 34)

and to Verticillium wilt. Bronze leaf wilt may be more

prevalent than the lack of reports would indicate (McGrew

and Posnette 1970).

The causal agent was assumed to be a virus of the yellows

group because of its transmission by leafhoppers and dodder.

Although no information is available on its morphology, the

agent is now suspected of being a mycoplasmalike organism.

The bronze leaf wilt pathogen appears to interfere with the

transmission of green petal by E. plebeja (Fall.), but the

green petal pathogen does not protect clover plants from

infection by bronze leaf wilt. The latter pathogen retards the

development of E. plebeja and apparently reduces the

insect's longevity (Posnette and Ellenberger 1963).

Delphinium Yellows

Using dodder. Cuscuta campestris Yunck., Posnette and

Ellenberger (1963) transferred a pathogen from a garden

Delphinium hybrid with phyllody to Fragaria cultivars and

Catharanthus roseus. (L.) G. Don. Symptoms in strawberry

were leaf bronzing and rapid death, indistinguishable from

those of bronze leaf wilt. The infected C. roseus plants

became chlorotic and developed small flowers with green

petals; some phyllody occurred but was less pronounced than

with strawberry green petal disease.

The pathogen was transmitted by Macrosteles sexnotatus

(Fall.) from C. roseus to Trifolium repens L. The affected

plant died within 6 mo, after forming progressively smaller

leaves on short petioles and without proliferation of axillary

buds. The causal agent has not been identified.

Clover Yellow Edge

Strawberry has been experimentally infected with a leafhopper-bome disease called clover yellow edge (Chiykowski

7976). The causual agent is a mycoplasmalike organism

(Chiykowski 1981a) and is efficiently transmitted by

45
Aphrodes bicincta. The disease occurs naturally in clovers in

eastern Ontario, Canada, and has been experimentally

transmitted to 15 species of plants in six families, including

the strawberry cvs. 'Cavalier' and 'Redcoat' and Fragaria

virginiana Duch. Symptoms in strawberry include mild

chlorosis and stunting of the whole plant, reduction in leaf

size, chlorosis of leaf margins, asymmetrical leaflets,

reduced runner development, and necrosis of runner tips.

Flowers are reduced in size but never virescent or phylloid.

Plants decline rapidly following the appearance of symptoms

and die prematurely. The symptoms bear considerable

resemblance to those described for lethal decline. (See

"Strawberry Lethal Decline," p. 38.)

Nematode-Borne Diseases

^''El

Í

uropean Nepoviruses in Strawberry; /

By A. F.[Murant and R. M.[Lister ^

In Europe, four nepoviruses are important in strawberry,

namely arabis mosaic virus (AMV), raspberry ringspot virus

(RRV), strawberry latent ringspot virus (SLRV), and tomato

black ring virus (TBRV). All four viruses are nematodebome, have wide host ranges, and infect several kinds of

small fruit. Their general properties and those of the diseases

they cause are described in detail in the Rubus section of this

handbook and only information that is specific to strawberry

is presented here.

AMV and SLRV are transmitted by the same vector,

Xiphinema diversicaudatum (Micoletzky), and therefore tend

to occur together. Similarly, some strains of RRV and TBRV

occur together because they have the same vector,

Longidorus elongatus (de Man). For convenience in

describing the diseases they cause, the viruses are discussed

below in the pairs in which they occur naturally.

Raspberry Ringspot and Tomato Black Ring Viruses

Disease Names

No names have been applied to the disease caused by either

of these viruses in strawberry.

History and Geographic Distribution

RRV was originally described by Cadman (7956) from

raspberry affected by "leaf curl" disease in Scotland, but

soon afterwards Lister (7958) reported it from strawberry

growing in the same general localities. Harrison (7956,

1958a) showed that RRV was soil borne and was often

accompanied in soils by a second soil-borne virus, at first

called beet ringspot virus, but later shown (Harrison 7955c)

to be related to TBRV (Smith 7946). Both viruses occurred in

raspberry, sugarbeet, and many other crops (Harrison 7957)

and also proved to be widespread in strawberry in Scotland

(Lister 1960b, 1960c). The viruses are transmitted by

nematodes of the genus Longidorus; strains of both viruses

occurring in Scotland share the vector L. elongatus (Harrison

et al. 7967; Taylor 7962) and therefore tend to occur

together.

RRV and TBRV are now known to occur throughout Europe

and the U.S.S.R. (see Rubus section). They apparently have

not been found in strawberry outside the United Kingdom

except in the U.S.S.R. (M. A. Keldysh, personal communication), although susceptible cultivars are widely grown

elsewhere, as for example, in the United States (see table 4).

46
Table 4.—Susceptibility of strawberry cultivars to British isolates of RRV

and TBRVi

Cultivar RRV TBRV

Auchincruive Climax -f +

Blakemore + •

Cambridge Early + +

Cambridge Favourite + •

Cambridge Prizewinner + •

Cambridge Rearguard -h +

Cambridge Rival + •

Cambridge Vigour + +

Catskill + •

Dixieland + •

General McMahon ( = Dunbarton Castle) • 4-

Howard 17 (= Premier) + +

Huxley + -

Juspa + •

Madame Lefebvre + +

Marmion • +

Merton Princess + +

Missionary + •

Montrose • +

Pocahontas -h •

Redgauntlet + +

Robinson + +

Royal Sovereign + +

Senga Sengana + +

Senga 54 • +

Sparkle -h •

Surecrop 4- •

Surprise des Halles • +

Talisman -h +

Tennessee Beauty + +

Troubadour • +

Xenion + +

Fragaria chiloensis (L.) Duch. + +

F. vesca L. (various clones) + +

iFrom Lister (1970) with additional unpublished data of J. Chambers.

Note: + = susceptible, - = immune, • = unknown.

Economic Importance

Though RRV and TBRV usually occur together, either alone

can render crops of sensitive strawberry cultivars valueless

within 1 or 2 yr of infection. With large outbreaks, the

economic loss may therefore be considerable; however,

because of their localized occurrence, the viruses are always

of less general importance than others that are more widely

distributed. Moreover, in Scotland, the introduction of

effective control measures has made diseases caused by these

viruses much less common than formerly.

The viruses cause few or no symptoms in the early stages of

infection and may therefore be inadvertently distributed in

infected planting material. This can result not only in loss of

the crop but also in the viruses becoming established in soils

47
already containing vector nematodes. It can also be a

problem in the international exchange of planting material.

Symptoms on Natural and Experimental Hosts

Both viruses infect a wide range of wild and cultivated

plants. For a detailed description of the symptoms caused by

RRV and TBRV in natural and experimental hosts, see the

Rubus section of this handbook, p. 211.

Symptoms on strawberry. Table 4 lists the cultivars known

to be susceptible to British isolates of RRV and TBRV. With

the exception of cv. 'Huxley', which is almost certainly

immune to TBRV, all cultivars that have been adequately

tested are susceptible to both viruses. When exposed to

infective nematode populations, however, some cultivars (for

example, 'Redgauntlet') are more prone to infection and

show more severe symptoms than others. In the field, most

cultivars become infected more readily with RRV than with

TBRV; however, because spread of the viruses is now

effectively controlled in Britain, the field reaction of newer

cultivars is unknown. The following description of the

symptoms in long-established cultivars is based on the

account given by Lister (1970). Similar symptoms may be

caused by infection with either virus or by both viruses

together.

Outbreaks of disease caused by RRV and TBRV occur in

patches ranging from a few square meters to a few hectares in

extent, reflecting the horizontal distribution of the vector in

the soil (fig. 51). When infection arises from the use of

infected planting material, however, infected plants are

typically distributed randomly throughout the crop. Symptoms shown by affected plants vary greatly, depending on the

cultivar and on the time of year. Lister (1970) distinguished

the following broad symptom types, but emphasized that

there was considerable overlap between them.

/. Cv. 'Talisman'. Clearly defined angular chlorotic spots

and rings may be observed (fig. 52 A). Sometimes there are

large areas of chlorosis with sharply defined borders (fig. 52

B), or the whole leaf may become chlorotic (fig. 52 C).

Leaves produced later may show a streaky chlorosis (fig. 52

D), or may be entirely symptomless though they contain

virus (that is "recovery"). The plants become progressively

dwarfed and eventually die. Similar symptoms are seen in the

CVS. 'Early Cambridge', 'Merton Princess', 'Cambridge

Prizewinner', and 'Cambridge Rival'.

2. Cv. 'Auchincruive Climax'. Leaf chlorosis is sometimes

localized, but tends to be generally distributed, appearing as

streaks or as irregularly shaped chlorotic spots (fig. 53);

leaves produced later are symptomless ("recovery"). The

Figure 51. — An outbreak of disease caused by

raspberry ringspot virus and tomato black ring virus

in 'Talisman" strawberry in eastern Scotland. (Copyright Scottish Crop Research Institute.)

48
Figure 52. — Leaves of 'Talisman' strawberry collected in late spring

showing the range of symptoms induced by tomato black ring virus: A,

Angular chlorotic spots; B, large chlorotic areas with sharply defined borders; C, leaf completely chlorotic; and D, streaky chlorosis in a partially

"recovered" leaf. (Copyright Scottish Crop Research Institute.)

~*'^-*t*-^^^,

Figure 53. — Leaf of 'Auchincruive Climax'

strawberry showing irregularly shaped chlorotic

spots and blotches induced by tomato black ring

virus. (Copyright Scottish Crop Research

Institute.)

Figure 54. — Leaf of 'Huxley' strawberry infected with raspberry ringspot virus showing

chlorotic blotches and crinkling. (Copyright

Scottish Crop Research Institute.)

plants are progressively stunted and eventually die. Similar

symptoms are seen in the cvs. 'Cambridge Favourite',

'Camdridge Rearguard', 'Redgauntlet', and 'Madame

Lefebvre'.

3. Cv. 'Huxley' (RRV only). Symptoms include clearly

defined, irregularly shaped chlorotic blotches, often with a

chlorotic center (fig. 54) but without line patterns or rings.

Symptoms are less obvious on leaves produced in midsummer or in warm greenhouse temperatures, but totally

symptomless leaves are not produced. The plants become

progressively stunted and ultimately die.

4. Cv. 'Royal Sovereign'. This cultivar shows symptoms

similar to those in 'Auchincruive Climax', but in addition

develops prominent necrotic spots (fig. 55).

Symptoms in Fragaria vesca L. var. semperflorens (Duch.)

Ser. cv. 'Alpine': Seedlings show yellow blotches in the first

year of infection but are symptomless thereafter.

For information on "Natural and Experimental Transmission," "Properties- of the Causal Agents," "Detection and

Identification," and "Control Procedures," see the Rubus

section of this handbook, p. 211.

Arabis Mosaic and Strawberry Latent Ringspot Viruses

Disease Names

Strawberry mosaic (Posnette 1956); strawberry yellow

crinkle (Harris 1958). These names were applied to diseases

of certain strawberry cultivars that proved later (Jha and

Posnette 1959; Jha 796/) to be infected with AMV. The

different symptoms were caused partly by the response of

different cultivars and partly by virus strain variation. No

name has been given to the disease caused by SLRV in

strawberry

History and Geographic Distribution

AMV was first described from Arabis (rockcress) by Smith

and Markham (1944) and remained a laboratory curiosity

until Cadman (1960) showed that it was the same as

raspberry yellow dwarf virus, a sap-transmissible soil-borne

virus isolated by Harrison (1958b) from raspberry, strawberry, blackberry, and several weed species. Lister (1958,

1960a, 1960b, 1960c) described the results of surveys, which

showed that AMV was widespread in strawberry in England

and also occurred in parts of Scotland and Northern Ireland.

Lister (1964) found that AMV-infected plants of strawberry,

raspberry, and other crops frequently contained a second

49
sap-transmissible soil-borne virus, which he called strawberry latent ringspot virus (SLRV). Both AMV and SLRV are

transmitted by the same nematode, Xiphinema diversicaudatum (Harrison and Cadman 1959; Jha and Posnette 7959;

Lister 1964), which explains why they commonly occur

together in soils.

Both viruses have wide natural host ranges and are widely

distributed in Europe; they have also been reported from

several non-European countries. (See the Rubus section of

this handbook.) Outside the United Kingdom, strawberry

has been reported to be infected with AMV in Germany

(Lister and Krczal 79^52) and the Irish Republic (Staunton and

Moore 7967), and with both AMV and SLRV in Hungary

(Szilagyi 1980) and the U.S.S.R. (M. A. Keldysh, personal

communication). Cultivars known to be susceptible are

widely grown, for example, in the United States (see table 5).

Economic Importance

The effects of AMV are severe enough in some strawberry

cultivars to make the crop worthless within 1 or 2 yr of

infection. SLRV usually occurs in mixed infections with

AMV, but can probably have equally damaging effects on its

own. The viruses are therefore of considerable economic

importance in those areas of southern and southwestern Great

Britain where they are prevalent; however, the adoption of

effective control measures has now made the diseases

induced by these viruses relatively uncommon in strawberry.

The introduction of adequate inspection and certification

schemes for strawberry planting material is an important first

step in eradicating AMV and SLRV, because newly infected

plants may show no symptoms and the viruses can thus be

inadvertently distributed. This can result not only in losses of

crop but also in the introduction of the viruses into soils

already containing vector nematodes. It is also a problem in

the international exchange of plant material.

Symptoms on Natural and Experimental Hosts

Both viruses infect a wide range of wild and cultivated

plants. For a detailed description of the symptoms caused by

AMV and SLRV in natural and experimental hosts, see the

Rubus section of this handbook, p. 204.

Symptoms on strawberry. Table 5 lists the strawberry

cultivars known to be susceptible to AMV; little information

is available for SLRV, except that the cvs. 'Cambridge

Favourite', 'Cambridge Vigour', and 'Tantallon' are susceptible.

As with RRV and TBRV, outbreaks of disease caused by

AMV and SLRV occur as patches in the crop, reflecting the

horizontal distribution of the nematode vector, except of

course when infection results from the use of infected

planting material. Strawberry plants show a very wide

variation in response to infection with AMV, depending on

the cultivar and on the strain of virus involved; however, the

Table 5.—Strawberry cultivars and Fragaria species

susceptible to AMVi

Strawberry cultivars

Black Prince

Blakemore

Bradley Cross

Cambridge 497

Cambridge Early Pine

Cambridge Favourite

Cambridge Prizewinner

Cambridge Profusion

Cambridge Rearguard

Cambridge Rival

Cambridge Vigour

Captain Cook

Catskill

Charles Lane

Deutsche Evern

Dixieland

Dybdahl

Early Cambridge

Glasnevin *A'

Gorella

His Excellency

Howard 17 (= Premier)

Huxley

Indra

John Innes 580

Jucunda

Juspa

King George

Fragaria spp.

F. chiloensis (L.) Duch.

F. corymbosa Los.

F. cuneifolia Nutt.^

F. moschata Duch.

F. moupinensis (Franch.) Card.

F, nilgerrensis Schlecht.

Lihama

Madame Lefebvre

Merton Princess

Midland

Missionary

Northwest

Oberschlesien

Perle de Prague

Pocahontas

Prodige

Red Dragon

Redgauntlet

Robinson

Royal Sovereign

Sans Rivale

Senga 242

Silver Jubilee

Sir Joseph Paxton

Sparkle

Surecrop

Surprise des Halles

Talisman

Tantalion

Tardive de Leopold

Tennessee Beauty

Triomphe de Tihage

Troubadour

Xenion

F. nipponica Makino

F. nubicola Lindl.

F. orientalis Los.

F. platypeltata Rydb.

F. vesca L.

F. virginiana Duch.

F. viridis Duch.

iprom Lister (1970) and Posnette and Manwell (1971), with

additional unpublished data of J. Chambers.

^A natural hybrid of chiloensis x virginiana.

50
Figure 55. — Leaves of 'Royal Sovereign' strawberry

infected with raspberry ringspot virus showing necrotic

spots and chlorosis. (Copyright Scottish Crop Research

Institute.)

plants are usually stunted and show chlorotic leaf mottle or

mosaic symptoms. The reduction of growth may range from

slight stunting to such extreme dwarfing (ñg. 56) that the

plants die within a year or two of infection. The leaves are

often twisted, cupped, or crinkled. Chlorotic markings on the

leaves range from a diffuse chlorotic mottle (fig. 57) to vivid

yellow spots, blotches, and streaks (fig. 58). The prominent

blotching symptom induced by AMV in the cv. 'Royal

Sovereign' (fig. 58) was called strawberry mosaic by

Posnette (1956), but the virus in these plants induced only

diffuse mottle and necrotic spotting in graft-inoculated plants

of cv. 'Cambridge Favourite' (Jha 1961). Leaf symptoms are

most readily seen in late spring before the fruit is set, and

again in autumn, but tend to disappear in midsummer,

although the stunting is still evident.

The reactions of strawberry cultivars to infection with SLRV

are largely unknown. The virus was found originally in plants

of cv. 'Cambridge Vigour', which were stunted and had

yellow blotches on the leaves; but AMV, which causes

similar symptoms, was also present. Lister (1970) found that

plants graft-inoculated with SLRV alone showed the same

kind of symptom (fig. 59).

Symptoms on Fragaria vesca 'Alpine'. Some clones show

chlorotic symptoms when infected with AMV, but most are

symptomless except for loss of vigor. Plants infected with

SLRV remained symptomless in greenhouse tests.

No immunity to AMV was detected among 13 species of

Fragaria (table 5; Posnette and Manwell 1971), giving little

hope that genes for immunity to this virus occur in Fragaria.

For information on Natural and Experimental Transmission,

Properties of the Causal Agents, Detection and Identification,

and Control Procedures, see the Rubus section of this

handbook, p. 204.

Figure 56. — Plants of 'Cambridge Favourite' strawberry: Left, healthy; right, infected with arabis mosaic

virus, showing extreme stunting. (Copyright Scottish

Crop Research Institute.)

Figure 57. — Plant of 'Talisman' strawberry infected

with arabis mosaic virus in the field and showing

chlorosis and miniaturization. (Copyright Scottish Crop

Research Institute.)

Ü

HIH^HIHBV-rtriPm ^^k

Miv^feiinjBN

3^^^^^'»-;¿jV. i^^fjte^Hk I

^ BB^^^Ils

mi^S^m'^' JêÎê^^ JpvSI^^^^^HIB^BH

B^yX ;^_,

Figure 58. —

i

"Strawberry

M

mosaic" disease in cv.

'Royal Sovereign' infected with arabis mosaic virus.

(Copyright East Mailing Research Station.)

51
Figure 59. — Chlorotic blotches on leaf of 'Cambridge

Vigour' strawberry graft-inoculated with strawberry

latent ringspot virus. (Copyright Scottish Crop Research

Institute.)

^^k Tomato Ringspot Virus in Strawberry,/

By R. H.lConverse and R.jStace-Smith

Additional Common Names

Peach yellow-bud mosaic in Fragaria chiloensis (L.) Duch.

(Frazier et al. 1961) was later shown to be the same as tomato

ringspot virus (TomRSV) by Cadman and Lister (1961,

1962). The disease in strawberries caused by TomRSV has

been given no common name.

History and Geographic Distribution

TomRSV was found in symptomless F. chiloensis along the

coast of northern California (Frazier et al. 1961). Field

infection of four strawberry cultivars by TomRSV was

reported in western Oregon (Converse 1981); moreover,

TomRSV from red raspberry has been successfully graftinoculated to nine strawberry cultivars in the greenhouse and

was lethal to eight of them (Mellor and Stace-Smith 1963).

TomRSV probably infects wild and cultivated strawberry

wherever it occurs with its dagger nematode vector over a

large part of the Western Hemisphere.

Economic Importance

Since the natural infection ofstrawberry cultivars by TomRSV

has only recently been reported (Converse 1981), surveys to

determine its occurrence and damage to cultivated strawberries have not yet been made. TomRSV is one of the most

common and severe virus diseases of red raspberry and

blueberry in Oregon. (See "Tomato Ringspot Virus inRubus,"

p. 223; and "Tomato Ringspot Virus in Blueberry," p. 117.)

Therefore, crop loss to TomRSV in strawberry can be

expected in Oregon and similar areas.

Symptoms on Natural and Experimental Hosts

Symptoms on natural hosts. Strawberry^ Wild F. chiloensis

is symptomless when infected. Symptoms in cultivated

strawberries range from none ('Lassen' and 'Sequoia'); to

dwarfing, reduction in runner production, and occasionally

mottled leaves in the spring ('Puget Beauty') (fig. 60), where

symptoms usually resemble those caused by the common

aphid-borne strawberry viruses like crinkle, mottle, and mild

yellow-edge; and to death of whorls of outer leaves and

subsequent death of plants, resembling Verticillium wilt

disease symptoms, in 'Olympus' (fig. 61).

Other hosts. TomRSV has an extensive host range among

woody and herbaceous plants, including many common

shrubs and weeds, often seedbome and without symptoms.

(See "Tomato Ringspot Virus in Rubus," p. 223, for a

further discussion of natural hosts.)

Symptoms on experimental Fragaria hosts. F. chiloensis

clones have been found in grafting tests to vary from immune,

to symptomless, to weak with varying amounts of vein

chlorosis (Frazier and Mellor 1970b). F. vesca indicator

clones 'EMC, 'EMK', 'EM-l', 'UC-l', 'UC-3', 'UC-4',

'UC-5', and 'UC-6' all respond similarly to leaf-graft

inoculation by TomRSV. Initial symptoms about 2 wk after

grafting are epinasty, unequal leaflet development, a rather

distinctive blotchy leaf mottling (fig. 62), and, sometimes,

necrosis of leaf blade tissue. Symptoms do not follow a precise

pattern and may resemble symptoms of other strawberry virus

diseases. Chronic symptoms are usually mild, but fluctuate

seasonally, both in severity and kind. Leaflets are neither

Figure 60.—Tomato ringspot virus causing mottling in

leaf of 'Puget Beauty' strawberry.

52
Figure 61.—Dying 'Olympus' strawberry plants infected with tomato ringspot virus (24-mm-diameter coin

included for size comparison).

Figure 62.—Symptoms of tomato ringspot virus inoculated by leaf grafting to Fragaria vesca cv. 'UC-4'.

mottled nor distorted, but are slightly rounder and smaller than

normal. The youngest petioles are redder, shorter, and more

upright than normal, and are usually swollen. The abnormal

thickening of petioles is a symptom diagnostic of TomRSV

infection. Other seasonal symptoms include: premature

yellowing and death of older leaves; transient epinasty of

unfolding leaves and transient curling of runner tips;

inflorescences on shortened, thickened stalks or peduncles,

with an increased number of flowers having slightly phylloid

sepals, an increased number of small, often virescent, petals;

and distinct vein chlorosis, most pronounced on 'Alpine',

which may only appear on a series of several leaves (Frazier

and Mellor 1970b).

Figure 63.—Shock symptoms (dead leaf) of tomato

ringspot virus inoculated by leaf grafting to Fragaria

virginiana cv. 'UC-1 !'.

TomRSV is usually lethal in leaf-graft inoculated F.

virginiana L. cvs. 'UC-10' and 'UC-ll'. First, some younger

leaves become necrotic (fig. 63), and, then the whole plant

dies. Chronic symptoms in the 'M-T clone of F. virginiana

graft-inoculated with TomRSV differ from those in other

members of the genus. Initial symptoms are similar to those

in the more sensitive commercial cultivars; spreading

necrosis appears at runner tips and as spots on young leaves,

and soon kills all the leaves except those that were fully

mature at the time of infection. Although crowns also appear

to have been killed, after a few weeks numerous, miniature,

adventitious shoots are produced. These bear dwarfed,

deformed, chlorotic-mottled leaves which, 3 mo after

infection, give the crowns of plants the appearance of rosettes

(Frazier and Mellor 1970b).

Symptoms in complex with other viruses. In leaf graft tests

on F. vesca, no interaction was detected between TomRSV

and the latent A strain of strawberry mottle virus. Symptoms

of each virus were additive in such complex infections (Frazier

and Mellor 1970b).

Natural and Experimental Transmission

Natural transmission. TomRSV is transmitted to F.

chiloensis and to strawberry cultivars by the American dagger

nematode (Xiphinema americanum Cobb) (Frazier and

Maggenti 7962; Converse 1981). X. rivesi Dalmasso, a

closely related species, has recently been found associated

with TomRSV transmission to other crops (Forer and Stouffer

1982). The field infection rate of cultivated strawberries by

53
nematode-transmitted TomRSV is slow—30% in 19 mo

(Converse 798/). Single American dagger nematode adults

and all four larval stages can acquire TomRSV after feeding on

cucumber roots (Cucumis sativas L.) for 1 hr and can transmit

it to test cucumbers within feeding periods of 1 hr (Téliz et al.

7966).

The following strawberry cultivars were infected by TomRSV

transmitted by viruliferous American dagger nematodes in

greenhouse tests: 'Olympus', 'Puget Beauty', 'Rainier',

'Totem', 'Tyee', and Oregon-USDA selections 4356, 4459,

4681,4682, and 6108 (R. H. Converse, unpublished results).

TomRSV is seed transmitted in F. vesca and in cultivated

strawberry, often without symptoms (Mellor and Stace-Smith

796i). We can expect TomRSV to occur in some strawberry

runner plants used to establish new plantings, particularly

those taken from fields with high American dagger nematode

populations.

Experimental transmission. TomRSV can be transmitted by

sap inoculation from young, infected strawberry leaves to

several herbaceous test plants.

Test plant

Chenopodium quinoa

Willd.

Cucumissativas L. cv.

'National Pickling'

Nicotiana tabacum L.

cv. 'Xanthi NC

Symptoms

Local lesions on inoculated leaves

followed by systemic shoot tip

necrosis (fig. 64).

Yellow local lesions on inoculated

cotyledons followed by necrosis

and withering of cotyledons,

mosaic, distortion, necrosis, and

stunting of the leaves (fig. 65).

Local lesions on inoculated leaves

followed by ring and line patterns

on leaves and eventual appearance

of symptomless leaves (fig. 66).

Several buffers can be used for these sap inoculations: 3%

nicotine alkaloid + O.OIM K2HPO4 + O.OIM cysteine

hydrochloride, pH.9; and 2% polyvinylpyrrolidone (mol. wt.

10,000) in 0.05 M phosphate buffer, pH 7 (Brunt and

Stace-Smith 7976; Converse 7979; Martin and Converse

7952a).

Pollen from TomRSV-infected strawberry plants is

viruliferous, as determined by sap inoculation to herbaceous

test plants and by serological tests; however, TomRSV has not

been found to infect strawberry plants pollinated by

viruliferous strawberry pollen (Frazier and Mellor 1970b).

Properties of the Causal Agent

TomRSV is a nepovirus 28 nm in diameter. (See "Tomato

Ringspot Virus in Rubus," p. 223, for a detailed presentation

of the properites of this virus.) Properties are also summarized in Commonwealth Mycological Institute and the Association of Applied Biologists Descriptions of Plant Viruses, No. 18 (Stace-Smith 7970). The virus is a good antiFigure 64.—Necrosis of Chenopodium quinoa that had

been sap-Inoculated with tomato ringspot vims.

Figure 65.—Yellow local lesions and systemic symptoms on Cucumis salivus that had been sap-inoculated

with tomato ringspot virus.

Figure 66.—Local lesions on leaves of Nicotiana tabacum sap inoculated with tomato ringspot virus.

54
gen, and antiserum can be prepared following the standard

procedures just referenced or can be purchased from organizations like the American Type Culture Collection,

Rockville, Md. Antisera prepared against TomRSV isolates

from a number of hosts have reacted well against TomRSV

isolates from strawberry.

Detection and Identification

TomRSV can seldom be identified by symptoms in infected

strawberry cultivars. This virus can be readily detected and

identified in leaves of suspect strawberry plants by preparing

sap from them to use in enzyme-linked immunosorbent assay

(ELISA) (Clark and Adams 7977; Converse 1981). Leaf

grafting to F. vesca 'Alpine' or other F. vesca indicators can

be used for detection and identification of this virus when the

more sensitive and rapid ELISA procedures are not available.

(See "Symptoms on Experimental Hosts" in this chapter.)

Control Procedures

Because no Fragaria clones have been found that were

completely infected by TomRSV, it has not been necessary to

attempt to eradicate this virus from Fragaria clones. Heat

inactivation of TomRSV in vivo was accomplished in peach

after 21 days at 38°C (Nyland and Goheen 1969).

The principal control measures are: (1) control of the

American dagger nematode by fumigation or avoidance of

infested soils (Murant and Taylor 1965; Thomason and

McKenry 7975); (2) use of certified nursery stock free from

TomRSV and grown in fumigated soil; and (3) use of immune

cultivars. The cvs. 'British Sovereign' and 'Sparta' were

found to be immune to leaf-graft infection by TomSRV

(Mellor and Stace-Smith 1963). Immunity to TomRSV may

be fairly widespread in strawberry cultivars and can be

purposely incorporated into advanced selections by plant

breeders.

Remarks

Serological tests to detect TomRSV should be included in

future strawberry virus surveys in North America, as it is

probable that this virus is widespread, damaging, and largely

unrecognized in many strawberry growing areas where

TomRSV is known to occur.

Vectors Unknown

y

/

Strawberry PallidosiS/v

By J. P.jFulton

Additional Common Names

None.

History and Geographic Distribution

Although pallidosis was detected in the United States and in

Australia in 1957 (Frazier and Stubbs 7969), the disease

appears to be indigenous to North America. Its occurrence in

Australia was associated with cultivars obtained from the

U.S. Department of Agriculture at Beltsville, Md. (Frazier

and Stubbs 1969). In addition to its occurrence in Eastern

United States, it has been reported from Western United

States (Frazier and Stubbs 7969; Mullin et al. 7975), from

midwestern United States (Fulton and Moore 1982), and

from eastern Canada (Craig 1981).

Economic Importance

Comparative studies of pallidosis-free and pallidosis-infected

'Redcoat' and 'Midway' cultivars at Kentville, Nova Scotia

(Craig 1981), indicated that pallidosis had no significant

effect on total yield, marketable yield, or fruit size. Frazier

and Stubbs (7969) indicated that certain strawberry cultivars

developed very mild symptoms under greenhouse culture,

whereas others remained symptomless. In Australia, mild

symptoms and a lack of vigor were noted in field plantings of

'Midland'. 'Klonmore', and Tennessee Beauty'. Mullin et

al. (7975) and Craig (1981) suggested that the economic

importance of pallidosis is as a result of the synergistic

response when in combination with other viruses. Definitive

studies of such synergistic effects have not been reported,

however.

Symptoms on Natural and Experimental Hosts

Pallidosis is latent in most commercial cultivars of

strawberries, but very mild symptoms were observed in the

CVS. 'Marshall', 'Lassen', 'Hood', and 'Northwest' (Frazier

and Stubbs 1969). In standard indicator clones of Fragaria

vesca L., pallidosis produces either no symptoms or very

mild and transient symptoms. None of the F. vesca indicators

are of value in detecting pallidosis. F. virginiana Duch.

indicators, particularly the 'UC-10' and 'UC-ll' clones,

develop severe symptoms when inoculated with pallidosis

(fig. 67). In these clones, the new leaves become recurved,

reduced in size, and chlorotic (fig. 68). Runners are pale and

shortened. When infected by severe isolates, some plants

may die. Symptoms are most severe in greenhouse-grown

plants during the winter. During the summer, symptoms fade

unless plants are heavily shaded.

55
Figure 67. —Fragaria Virginia 'UC-10': Left, plant

showing twisted, chlorotic leaves 46 days after infection

with pallidosis disease by leaflet grafting; right, healthy

plant.

Figure 68.—Fragaria virginiana 'UC-10': Three

leaves on the left are from a plant leaf-grafted with a

leaflet infected with pallidosis disease. These leaves

show dwarhng, distortion, and chlorosis 46 days after

grafting; healthy leaf is on the right.

Natural and Experimental Transmission

Pallidosis is readily transmitted by grafting. Symptoms

generally appear between 18 and 30 days. There are

conflicting reports regarding the spread of the pallidosis agent

under greenhouse conditions. Frazier reported that pallidosis

spread in his greenhouse in California (Frazier and Stubbs

1969). Movement of pallidosis has not been recorded in our

greenhouses or screenhouses in Arkansas (J. P. Fulton,

unpublished data). Natural spread in the field has been

recorded in the United States and Canada, but the amount of

spread appears to vary. Although field spread was not

observed in California (Mullin et al. 1975), the disease has

been detected in several cultivars widely grown on the west

coast of the United States (Frazier and Stubbs 1969). Some

spread was recorded in Nova Scotia (Craig 1981), but the rate

of spread was slow. The rate of spread in Arkansas is

apparently much greater (Fulton and Moore 1982). The

pattern of spread is suggestive of an aerial vector although

none has been detected (J. P. Fulton, unpublished data).

Properties of the Causal Agent

Although pallidosis is usually referred to as a virus, the only

indication that it is a virus is its transmission by grafting.

Observations with the electron microscope have generally

failed to demonstrate any viruslike particles or any

ultrastructural changes suggestive of virus infection (J. P.

Fulton, unpublished data).

Detection and Identification

Pallidosis can be reliably detected only by grafts to F.

virginiana ('UC-10', 'UC-ll', and certain other F. virginiana clones) (Frazier 1974b). The symptoms in F.

virginiana, however, are not diagnostic. At present, a

graft-transmissible entity producing symptoms in the F.

virginiana clones but failing to produce symptoms in F.

vesca indicators is assumed to be pallidosis (see Remarks).

Control Procedures

Contaminated clones are readily freed from pallidosis by

shoot apex culture. Mullin et al. (1974, 1975) report almost

100% elimination of pallidosis by excising shoot apices 0.23

to 1.0 mm in length. The pallidosis agent was as readily

eliminated without heat treatment as with such treatment.

Observations in Arkansas indicate that pallidosis-free clones

can be maintained in screenhouses without fear of recontamination. In California, this is not true. There is no

indication of the degree of isolation required to maintain a

field planting free of pallidosis.

Remarks

Since the symptoms of pallidosis in F. virginiana indicators

are not diagnostic, this entity is very poorly defined. Failure

to produce symptoms in F. vesca associated with the

production of symptoms in F. virginiana is the basis for

designating this entity, but it is known that other viruses may

act similarly. The latent A strain of strawberry crinkle virus is

of this type. (See "Strawberry Crinkle," p. 20.) Pçrhaps

mild strains of other viruses can evoke this response from

these two species of indicators. More than one entity may

currently be in the literature under the term "pallidosis."

Henriques and Schlegel (1975) observed long, flexuous

viruslike particles 10 to 11 nm in diameter in phloem cells of

a pallidosis-infected strawberry. Two types of inclusions

resembling ultrastructural features associated with beet

yellows infection in beet were also observed. Frazier (1975a)

reported possible transmission of pallidosis by the leafhopper

Coelidia olitoria (Say). Neither of these two reports has been

confirmed, and additional studies will be required to

determine their significance.

56
V£Tobacco Streak Virus in Strawberry y <

By R. IStace-Sxnith, R. H.^Converse, and H. A.ijohnson

Additional Common Names

Strawberry necrotic shock virus (Frazier et al. 1962).

components from the different strains may yield infectious

hybrid strains. Symptoms of TSV on natural and experimental hosts are diverse. Some species show mottling,

ringspot, or necrotic symptoms as a shock reaction, but the

plants usually recover and exhibit no chronic symptoms.

History and Geographic Distribution

Frazier et al. {1962) applied the name " necrotic shock" to a

disease of strawberry in California that was characterized by

being essentially symptomless on commercial cultivars, but

inducing a severe necrotic reaction when grafted into

Fragaria vesca L. indicator clones. Although the vector was

not determined, evidence suggested that both the virus and

the vector had host plants other than Fragaria spp. The virus

was also detected in nursery plantings in Oregon and

Washington and in commercial plantings in Oregon (Converse 1969). Stace-Smith and Frazier (1971) isolated tobacco

streak virus (TSV) from necrotic-shock infected F. vesca.

More recently, TSV has been isolated from commercial

strawberry cultivars in Queensland (Greber 1979).

Although the recorded geographic distribution of TSV in

strawberry is restricted to Western United States and

Queensland, Australia, the virus is known to have a far wider

geographic distribution (Fulton 1971).

Economic Importance

Under field conditions, virus symptoms are rare in

commercial cultivars. Experimentally infected cultivars show

mild transient symptoms or a shock reaction followed by

recovery. Tests in California showed TSV-infected strawberry plants to yield about 7500 kg less fruit per hectare and to

develop one-quarter the number of runners as healthy plants

(Johnson et al. 1983). When TSV is combined with other

strawberry viruses, the effect of double infections on F.

vesca indicator clones (Frazier et al. 1982) or the cultivar

'Redlands Crimson' (Greber 7979) may be mildly additive.

Although TSV is often mild or symptomless in commercial

cultivars, it contributes to a decline in productivity of field

plantings. TSV also frequently invades nursery plantings of

otherwise virus-free stock (Frazier et al. 1962; Converse

1969) being propagated in areas that are isolated from

commercial strawberry plantings.

Symptoms on Natural and Experimental Hosts

TSV has a wide natural host range, including both

herbaceous and woody plants (Fulton 1948). The virus is

known to occur naturally on such diverse crops as tobacco,

cotton, dahlia, clover, tomato, pea, bean, grape, and

raspberry, as well as weed species and native plants. The

experimental host range is extensive; in one study where 169

species were inoculated, the virus was subsequently

recovered from 87 species representing 21 families (Fulton

1948).

Symptoms on Strawberry

TSV infections in commercial strawberry cultivars cannot be

detected in field plantings. Symptoms on experimentally

infected cultivars depend to a large extent on the isolate used

as inoculum. In Australia, some cultivars show leaflet

epinasty, petiole stunting, necrosis on the tips of expanding

leaves, or etched rings and lines on the leaf surface (Greber

7979). In the United States, 'Marshall' strawberry leafgrafted with Frazier's-type isolate of TSV (A-8) developed

foliar line patterns (R. H. Converse, unpublished data).

Other cultivars show only transient symptoms on a single leaf

(Frazier et al. 1962). Following shock symptoms, the

infected strawberry plants recover and show no symptoms of

infection.

Indicator clones of F. vesca are more sensitive to TSV

infection than are strawberry cultivars. Plants that are

inoculated by leaf grafting show symptoms as soon as 6 to 14

days or as long as 30 days under short photoperiod conditions

(Frazier 1974a; Greber 7979; H. A. Johnson and J. I.

Espejo, unpubHshed results). A California isolate of TSV

induced a severe necrotic shock reaction in 'Alpine' (fig. 69

A), while a Canadian isolate caused chlorotic spots in grafted

'UC-l' (fig. 69B). A Queensland, Australia, isolate does not

induce necrosis but induces epinasty, petiole stunt, and

chlorosis. As with the commercial cultivars, indicator clones

of F. vesca that have been grafted or mechanically inoculated

recover to produce new growth that appears entirely normal.

Although no symptoms are apparent, recovered plants and

the vegetative progeny from such plants generally remain

infected with TSV.

Natural and Experimental Transmission

Strawberry seed from crosses involving TSV-infected pollen

or ovule parents are infected up to 35%, and TSV can readily

be detected by ELISA in surface-sterilized, ungerminated

seed lots. Mother plants pollinated with TSV-infected

strawberry pollen did not become infected in these

experiments, even when their seed was infected (Johnson et

al. 1983). No information is available on the mechanism of

natural infection in strawberry, although thrips are reported

as vectors of TSV in several annual crops (Costa and Neto

1976; Kaiser et al. 7982). The fact that the virus can be

recovered from isolated plantings established with virustested planting material suggests that the source of initial

infections is a host other than strawberry.

Several strains or variants, differing in host range and

symptomatology, have been isolated. Combinations of

57
Figure 69.—A, Necrosis of young leaves in Fragaria

vesca var. semperflorens cv. 'Alpine' 2 wk after leaf

grafting from a California strawberry plant infected with

tobacco streak virus. B. Yellow spots in leaf of f. vesca

'UC-I' after leaf grafting with an isolate of tobacco

streak virus from strawberry in British Columbia,

Canada.

Experimental transmission is achieved by grafting or by sap

inoculation. The leaf-petiole graft is reliable; symptoms can

be enhanced if indicator plants are pruned to one expanded

leaf at the time of grafting (Frazier 1974a). Sap transmission

from infected strawberry to herbaceous indicator hosts is

more reliable when newly infected leaves of graft-inoculated

plants are used as a source of inoculum. A buffer, consisting

of 0.05 M phosphate plus 2% polyvinyl pyrrolidone (mol.

wt. 10,000) pH 7.0, has been found to be satisfactory for

mechanical transmission of TSV from strawberry to

herbaceous plants (Martin and Converse 1982a). Sap

transmission of TSV from herbaceous test plants into

strawberry is more difficult, but it has been achieved using

either infected cucumber sap or purified virus (Greber 1979).

Properties of the Causal Agent

TSV is the type member of the ilarvirus group (Matthews

1979). The virus has four nucleoprotein components; each

component contains mainly one RNA species. The three

fastest-sedimenting components are required for viral

replication. A mixture of the three largest RNA's is not

infective, but can be activated by the viral coat protein or by

the smallest TSV-RNA. The three largest RNA species have

molecular weights of about 1.1, 0.9, and 0.7 x 10" daltons;

the subgenomic RNA is mol. wt. 0.3 x 10" daltons. All

particles have the same density (in CsCl, 1.36 g/cm');S2o°,w

values lie within the range 80 to llOS. Particles are

quasi-isometric; different components differ in diameter

within a range of 26 to 35 nm. Protein subunit molecular

weight is about 30.000 daltons. The virus is weakly to

moderately immunogenic. and different strains show varying

degrees of serological relatedness.

Detection and Identification

Since TSV usually induces no obvious symptoms in

strawberry cultivars, either graft or sap transmission or

serological methods must be used to detect the virus. Frazier

(1974b) evaluated several Fragaria indicator clones. All of

those tested ('Alpine,' 'EMC, 'UC-l', 'UC-4', 'UC-5',

'UC-6", 'UC-ir, and 'UC-l2') showed a strong reaction

following graft inoculation. F. vesca var. semperflorens cv.

'Alpine' was the most satisfactory indicator. Symptoms

induced on this host were sufficiently distinctive to

distinguish the California isolate of TSV from most other

strawberry viruses. Greber (1979) reported that the F. vesca

clones were more useful than the F. virginiana clones. Of

those tested, 'UC-4' showed the most obvious and distinctive

symptoms after infection with the Queensland isolate of

TSV.

Use of sap transmission techniques to detect TSV in

strawberry plants is possible, but it is not as reliable as graft

transmission. Unless ELISA techniques are used, however,

the virus must be recovered from strawberry and transmitted

to herbaceous hosts to identify it. Sap transmission may be

achieved by macerating infected strawberry tissue in 0.05M

phosphate buffer containing 2% polyvinyl pyrrolidone (mol.

58
wt. 10,000, pH 7.0) and applying the inoculum to

herbaceous test plants. Use of this buffer has allowed sap

transmission to TSV even from mature, infected strawberry

leaves in the summer (Martin and Converse 1982a). The virus

induces necrotic local lesions that appear within a few days

after inoculation of indicator hosts such as cucumber

(Cucumis sativas L.) (fig. 70 A), Gomphrena globosa L. (fig.

70 B), Nicotiana tabacum L. cv. 'Havana' (ñg. 70 C, D),

Chenopodium quinoa Willd., and C. amaranticolor Coste

and Reyn. Symptoms induced on herbaceous indicator hosts

are not adequate for positive identification of all strains of

TSV. Cross-protection tests are of limited value because

some strains fail to protect against other strains. Serological

tests are more reliable, but since some strains fail to react or

react weakly when tested with antisera prepared against other

strains, it may be necessary to use more than one antiserum

source. Globulin from an antiserum against a Rubus strain of

TSV has given clear-cut results in ELISA tests against a

number of U.S. Pacific coast strawberry TSV isolates

(Johnson et al. ¡983).

Control Procedures

To date, no satisfactory control measures have been devised

to prevent the introduction of TSV into plantings used for

nursery stock propagation. Since these plantings are located

in areas where there is no commercial strawberry production,

infected native hosts may, apparently, serve as reservoirs for

infection. The virus is known to be prevalent in the native

trailing blackberry (Rubus ursinus Cham, and Schlecht.)

(Brunt and Stace-Smith 1976; Converse and Bartlett 1979),

and this, or other native plants, could be the virus sources.

Eradication of naturally infected plants from the immediate

vicinity of strawberry nursery plantings may be effective.

It is unlikely that TSV eradication from strawberry would

ever be necessary since strawberry clones are not universally

infected. TSV contamination could be a problem, however,

in a strawberry breeding program if a promising seedling

became infected prior to being multiplied. Should the

necessity arise, the virus could be eradicated by the heat

treatment-shoot tip culture technique. Greber (7979) found

Figure 70.—Symptoms on herbaceous indicators after

leaf sap inoculation from a strawberry infected with

tobacco streak virus: A. Local lesions on inoculated

Cucumis .çûi/vui cotyledons; B, local lesions on

moc\i\aXed Gomphrena glohiK.a Icai: ( , locil lesions on

Nicotiana tabacum cv. 'Havana' inoculated leaves; and

D, systemic symptoms on inoculated 'Havana' plant.

59
that the Australian strawberry strain of TSV was intermediate

between severe mottle virus and mild yellow-edge virus in

ease of eradication. (See "Strawberry Mottle," p. 10, and

"Strawberry Mild Yellow-edge," p. 25.) However, TSV

was not eliminated in plants grown outdoors in the hot summer growing conditions of the Imperial Valley in California

(Frazieretal. 7965).

Remarks

Major gaps in our knowledge are the mode of initial

introduction of TSV into isolated plantings of virus-tested

material and subsequent spread from strawberry to strawberry. Evidence suggests that the initial source of inoculum is

not wild strawberry but species unrelated to Fragaria.

Solutions to these problems have an important bearing on the

nature of spread of TSV as well as on its control. Selective

eradication of the inoculum source is more readily achieved

than eradication of all potential sources of inoculum.

A1 Strawberry Chlorotic Fleck ¡i

By J. P.|Fulton

Additional Common Names

None.

History and Geographic Distribution

This virus disease was described by Horn and Carver (1962)

from a strawberry cultivar grown at Tunica, La. It was later

detected in other cultivars, including 'Dabreak', 'Headliner'

(Horn 7965), 'Tangi', and a numbered selection (J. R.

McGrew, personal communication), but only from

Louisiana. There are no reports of its occurrence elsewhere.

Economic Importance

Chlorotic fleck disease signiñcantly reduced both plant and

fruit yields of the cv. 'Headliner' (Horn and Carver 7962).

The cv. 'Tangi' produced 40 to 70% more plants when free

of chlorotic fleck disease (J. R. McGrew, personal

communication).

Symptoms on Natural and Experimental Hosts

Chlorotic fleck disease produces no overt symptoms in

commercial cultivars. In Fragaria vesca L. indicators, young

leaves are distorted and down-curled. Vein clearing followed

by the appearance of small chlorotic spots is sometimes

evident (fig. 71). On 7^. virginiana L. indicators chlorosis,

down-curling and distortion of young leaves are observed.

Symptoms in these indicators are generally evident 3 to 4 wk

following grafting. There is a remission of symptoms with

time.

Figure 71.—Strawberry chlorotic fleclc symptoms on

the Beltsville strain of the East Mailing (BEM) clone of

Fragaria vesca. (Courtesy N. L. Horn, Louisiana State

University.)

Properties of the Causal Agent

On the basis of aphid and graft transmission of the disease to

indicators, chlorotic fleck disease is assumed to be caused by

a virus.

Detection and Identification

Chlorotic fleck disease is detected by grafting to indicators,

preferably F. vesca 'EMB' or F. vesca 'EMK'. The causal

agent of this disease is very incompletely characterized and it

cannot be distinguished from other viruses with confidence.

(See Remarks.)

Control Procedures

The causal agent seems to be evenly distributed throughout

the plant, including the meristem, and cannot be eliminated

by tip culture alone. Heat treatment at 35°C for 40 days or

longer may eliminate the virus (J. R. McGrew, unpublished

data).

Remarks

Although chlorotic neck disease is apparently distinct from

others which have been described, not enough is known to

unequivocally separate it from other viruses or mixtures.

Neither symptomatology on F. vesca and F. virginiana nor

elimination of causal agents by therapy permit unequivocal

differentiation between chlorotic fleck and similar symptoms

produced by mottle virus, latent A strain of crinkle virus, or

vein banding virus, alone or in combination.

Natural and Experimental Transmission

The disease has been successfully transmitted by grafting and

by the aphid Aphis gossypii Glov. The type of vector

relationship has not been determined (Horn 7965).

60
Minor Diseases and Those Experimentally

Transmitted Only

r

ÁStrawberry LeafroU/;

By N. W.jkazier

Additional Common Names

None.

History and Geograpliic Distribution

Strawberry leafroll disease (SLRD) was first observed in

Ontario, Canada, on a plant of 'Parson's Beauty' strawberry,

and again on 'Premier' by Berkeley and Plakidas (1942) who

observed the same disease in Geneva, N.Y., in 1940. Its

occurrence in three plantings in Ontario and New Brunswick

was recorded by Bolton (1964). The only report of the

disease outside of northeastern North America was in the

Alma-Ata district of Kazakstán, U.S.S.R., by Eliseeva et al.

(1974).

Economic Importance

Because of its restricted distribution and sporadic, rare

occurrence, SLRD must be considered to be of very minor

importance economically. Bolton however, (1964) observed

infections of 10 to 60% of plants in three plantings. The

affected plants failed to yield any fruit and produced only a

few, distorted runners. Intrinsically, the disease is very

damaging to infected plants.

Symptoms on Natural and Experimental Hosts

The known natural hosts of SLRD are commercial cultivars

of strawberry, Fragaria X ananassa Duch., all of which

appear to be very susceptible. They can also be used as

experimental hosts by graft transmission. Berkeley and

Plakidas (1942) reported having transmitted SLRD to the

scarlet strawberry Fragaria virginiana Duch. Frazier (1974b)

reported the F. virginiana indicator clones 'UC-IO',

'UC-ir, and 'UC-12' to give strongly positive symptoms

and the woods strawberry. Fragaria vesca L. indicator clone

'UC-5', to be uniquely sensitive, producing diagnostic

symptoms. F. vesca clone 'UC-3', a parent of 'UC-5'

(Frazier 1947b), and F. virginiana clone '2AI7', selected at

the University of California, Berkeley, but not distributed to

other laboratories, also show excellent, typical symptoms of

SLRD (see "Natural and Experimental Transmission").

Symptoms are basically the same on natural and experimental

hosts. The diagnostic symptom is the downward rolling of

leaflet margins, especially pronounced basally. In extreme

examples, the leaflet may be tubular with the lamina

narrowed and both margins rolled along their entire length,

even overlapping. The leaves are chlorotic, rugose with

cleared net veins, and petioles considerably shortened (fig.

72). Less severely rolled leaves have irregularly, sometimes

deeply serrated margins. Affected leaves are reduced, and

symptoms may appear on only a portion of a leaflet. Often,

diffusely chlorotic areas, usually banding main veins, may be

detected. This symptom becomes clearly evident as a

"peacock" pattern on clone '2AI7' (fig. 73) when typical

leaftoll symptoms are absent.

Natural and Experimental Transmission

No natural vector is known. There probably is no single

vector because SLRD appears to be caused by a complex of

at least three different agents, each of which could have a

different means of infection and spread.

N. W. Frazier (unpublished data) tested the ability of the dark

strawberry aphid, Chaetosiphon jacobi H. R. L., to transmit

SLRD over nonpersistent, semipersistent, and persistent

acquisition and inoculation feeding periods. No apparent

transmission of any disease resulted. Parallel tests of

mechanical transmission using sap from leafroll diseased

plants to commonly used herbaceous test plants were made.

Tobacco mosaic virus infections were occasionally produced;

however, Frazier did not clearly demonstrate that strawberry

was the actual source of the tobacco mosaic virus infection.

Figure 72. — Symptoms of strawbeny leafroll on

Fragaria vesca clone 'UC-5'.

Figure 73. — Symptoms of peacock pattern associated

with leafroll on Fragaria virginiana clone '2A17'.

61
y

Infected plants of some clones, such as 'UC-3' and 'UC-5',

irregularly produce flushes of normal-appearing leaves but

have never been observed to grow out of SLRD. A high level

of transmission by grafting was obtained from leaves

showing leafroll symptoms, but when normal-appearing

leaves were used for scions, transmission was very erratic. A

double-crowned 'UC-5' plant with one crown in the chronic

stage of SLRD infection and the other without symptoms

yielded transmission from the crown with symptoms, but not

from the symptomless crown.

Plants of clone '2A17' occasionally recovered from typical

leafroll symptoms, leaving a peacock pattern (fig. 73) in

evidence. Several plants then recovered from peacock

symptoms and appeared as somewhat chlorotic normal

plants. The remission process was never observed to revert.

In grafting tests, SLRD could be transmitted only from leaves

showing leafroll; peacock leaves transmitted either peacock

pattern or pallidosis disease (see "Strawberry Pallidosis," p.

55); leaves from recovered plants showing neither leafroll

nor peacock pattern transmitted only pallidosis disease.

'UC-ir plants graft-inoculated with leafroll-infected leaflets

developed only severe symptoms of pallidosis disease, but

not leafroll or peacock pattern. Neither leafroll nor peacock

pattern could be recovered from the plants. Only pallidosis

disease was transmitted, which cross-protected against type

isolates of pallidosis disease and was strongly additive with

isolates of mild yellow-edge, characteristics confirming a

diagnosis of paUidosis for the transmitted disease.

Frazier {1974a) gave the incubation period for the development of leafroll symptoms as from 42 to 180 (mean 62)

days — a relatively long period for strawberry virus diseases.

Bolton (1970) reported the appearance of symptoms about 15

days after grafting — a period much closer to the mean of 22

days given for pallidosis disease by Frazier (1974a).

The work at Berkeley, Calif., was done with a single plant of

an unknown cultivar which appeared to be infected with at

least three distinct entities causing pallidosis, peacock

symptoms, and SLRD. Whether the entities causing

pallidosis disease or peacock symptoms are necessary for the

causation of SLRD was not clear.

Properties of the Causal Agent

Not known.

Detection and Identification

The disease is visible in cultivars and can be identified by its

unique symptoms on the cultivar or on 'UC-5' or other

adequate indicator hosts by graft transmission.

Control Procedures

The disease is not inactivated at 4rc for 20 days. The fact

that symptoms are exhibited by cultivars allows efficient

control of SLRD by roguing out the diseased plants (Bolton

1970).

VÚL

// Strawberry Feather-Leaf

By N. W.IFrazier

Additional Common Names

Sparkle virus disease.

History and Geographic Distribution

McGrew (1970a) reported that the disease was first detected

in Arkansas in field-grown 'Midway'. It was also found in

some plants of the first distribution of 'Sparkle' by the U.S.

Department of Agriculture; in a single plant of 'Red Star'

from Maryland; in 3 of 10 plants of 'StarKrimson' from

Missouri; and in 2 of 8 'Paymaster' from Michigan.

Economic Importance

Unknown. Presumably very minor.

Symptoms on Natural and Experimental Hosts

The disease causes no symptoms in 'Sparkle' and only a

slight mottle in 'Midland'.

In indicator clones, Fragaria vesca L. clones show the

typical feather-leaf symptoms which include: dwarfing;

leaves narrowed, straplike, somewhat rugose, with deeply

serrated margins; and leañets fused at the base (fig. 74).

Although these symptoms are typical, they are not

necessarily diagnostic unless accompanied by vein clearing

or fasciation, translucent spots on young leaves (like heat

spot disease; see "Heat spot oí Fragaria vesca,'' p. 78), and

often deeply and unequally serrated margins. Infections may

be very obscure or very severe initially and often are first

evident on one or more side crowns. Plants may develop a

succession of diseased and normal-appearing leaves or

normal-appearing crowns and diseased crowns on the same

plant. When such diseased and normal-appearing crowns are

propagated by runners (fig. 75) and leaves from both kinds of

plants are used to inoculate healthy test plants, feather-leaf

disease is transmitted as readily from the normal-appearing

leaves as from the leaves with symptoms. 'Alpine' and

'UC-l' show the best symptoms of the indicators tested

(Frazier 1974b).

Fragaria virginiana clones 'UC-10', 'UC-ll', and 'UC-12'

were susceptible to infection but showed only symptoms of

pallidosis (see "Strawberry Pallidosis," p. 55). When such

plants were indexed on F. vesca plants, typical feather-leaf

symptoms developed.

Natural and Experimental Transmission

There is no information on natural transmission. Experimental transmission has been by grafting. Both McGrew

(1970a) and Frazier (1974a) found transmission to require

very extended incubation periods: McGrew, 35 to 240 days;

Frazier, 86 to 268 days. In Frazier's work, nondiagnostic

symptoms did appear more rapidly in some of the

plants — indicative of the presence of more than a single

disease-causing entity. Mechanical transmission was reported by Reed and Felix (1961), but their work has not been

corroborated.

62
Figure 74. — Leaves of Fragaria vesca ('EMK', left;

'UC-l', right) with classic symptoms of feather-leaf

disease. (Courtesy University of California Division of

Agricultural Sciences.)

Figure 75.—Fragaria vesca 'UC-l' sister plants

propagated by runners from a normal-appearing (left)

and a feather-leaf diseased (right) crown on the same

mother plant.

Properties of the Causal Agent

No information.

Detection and Identification

Both are dependent upon the production of characteristic

symptoms on standard F. vesca indicators, particularly

'Alpine' or 'UC-l'. Incubation periods can be very long,

over 8 mo. Symptoms in indicator plants are often difficult to

detect with confidence. McGrew (1970a) stated that in

combination with mottle, vein banding, or crinkle, there is no

apparent effect by feather-leaf disease on the symptoms

expressed by the other viruses.

Control Procedures

There is little information, but as reported by McGrew

{1970a), feather-leaf is susceptible to heat treatment at 38°C

for 5 to 9 wk followed by culture of 28 to 300 mg excised

buds.

Remarles

The somewhat unreliable production of detectable symptoms

and the sometimes very long period before they appear

following graft inoculation, make feather-leaf disease one of

the most difficult of the strawberry diseases to detect with

confidence.

^

^ Strawberry Pseudo Mild Yellow-Edge -,

By N. W.Crazier

Additional Common Names

None.

History and Geographic Distribution

Strawberry pseudo mild yellow-edge disease (SPMYED) was

described by Frazier (1966b, 1970a) who transmitted the

causal agent from plants of the 'M-l' indicator clone of

Fragaria virginiana Duch. This is the only record of the

occurrence of this disease. The 'M-l ' clone originated from a

wild plant found in Minnesota by King and von Ruden

(1962), which may have been infected prior to its collection.

Economic Importance

Not known.

Symptoms on Natural and Experimental Hosts

'M-l' is the only naturally infected host reported. Although

yellow to reddish coloration of old leaves with necrotic areas

on veins was commonly seen on 'M-l ' plants (Frazier 1966),

their association as symptoms of SPMYED was not

demonstrated. During later work with three F. virginiana

clones derived from 'M-l', similar symptoms were noted by

Frazier (1974b) on 'UC-12' plants (fig. 76) but not 'UC-10'

or *uc-ir.

Figure 76. — Plants of Fragaria virginiana clone

•UC-12' that are (left) healthy (center) infected with

mild yellow-edge disease; and (right) infected with

pseudo mild yellow-edge disease. Note the more severe

effect of the mild yellow-edge disease and the scalded,

dead leaves with large necrotic spots associated with

veins on the pseudo mild yellow-edge infected plant.

63
Experimental hosts are the F. vesca L. and F. virginiana

indicator clones evaluated by Frazier (1974b). All of the F.

vesca plants show very similar symptoms of SPMYED,

which appear only on older leaves as mottled discolorations

in shades of yellow and red followed by premature necrosis

of the leaves. The mottling often clearly shows a

vein-yellowing pattern, but typically appears as a stipple

pattern of isolated or merged, irregular spots or areas. The

pattern is least severe near the margin of the lamina (fig. 77).

These symptoms on the older leaves are remarkably similar

to those of mild yellow-edge disease. SPYMED can be

distinguished from diseases caused by severe strains of mild

yellow-edge virus (see "Strawberry Mild Yellow-edge," p.

25) by the absence of symptoms on young leaves and a less

debilitating effect on plant growth (fig. 76), but is difficult to

distinguish from symptoms caused by mild strains of mild

yellow-edge virus.

The causal agent of SPMYED does not affect the symptom

expression of pallidosis disease in 'UC-10' or 'UC-ll' (see

"Strawberry Pallidosis," p. 55.) (Frazier 1975b). Otherwise, symptoms in complexes with other diseases have not

been determined.

Natural and Experimental Transmission

There is no information on natural transmission, but natural

spread is probably by species of strawberry aphids —

Chaetosiphon spp. Chaetosiphon jacobi H.R.L., the dark

strawberry aphid, was the experimental vector, but does not

occur in Minnesota, the only place where SPMYED is known

to occur naturally.

Experimental transmission has been accomplished by leaflet

grafting and by the vector C. jacobi. The disease has the

semipersistent type of vector relationship: It can be acquired

in less than 2 hr and retained for 6 but not 18 hr by the vector

(Frazier 1966b). 'Alpine' test plants developed symptoms

about 3 wk (15 to 27 days) following inoculation.

Properties of the Causal Agent

No information.

Remarks

SPYMED appears not to be of economic importance.

Figure 77. — Stipple pattern of discoloration on an old

leaf of "Alpine' strawberry Fragaria vesca var.

semperflorens, characteristic of pseudo mild yellowedge infection.

i^^ Tobacco Necrosis Virus in Strawberry//

By R. H.¡Converse, R. R.JMartin, E.'Tanne, and S.

^piegel '

Additional Common Names

Strawberry rosette necrosis virus (Faccioli 1974).

History and Geographic Distribution

Tobacco necrosis virus (TNV) was first reported in Fragaria

by Fulton (¡952) in Arkansas, and subsequently by Frazier

(1955b) in California, primarily as a greenhouse disease of F.

vesca indicator root systems and was thought to be of no

economic importance. TNV occurs in cultivated strawberries

in the field in Italy (Faccioli 1970, 1974), Bulgaria

(Yankulova and Schmelzer 1974), and Japan (Kaname and

Kishi 1973; Komuro et al. 1973). Satellite of tobacco

necrosis virus (STNV) has also been reported to be associated

with TNV in strawberry roots in Japan (Komuro et al. 1973)

Detection and Identification

The disease can be detected by graft or vector transmission to

F. vesca clones and to F. virginiana 'UC-12'. Identification

can be accomplished by inoculating F. vesca plants, which

will develop characteristic symptoms, and F. virginiana

'UC-10' or 'UC-ir plants, which will not develop

symptoms. The 'UC-6' clone of F. vesca grafted with

SPMYED develops the characteristic symptoms already

discussed, but remains symptomless when grafted with most

mild yellow-edge virus sources.

Control Procedures

No information: No field control is necessary, but it can be

assumed that the disease could be eliminated by heat

treatment and meristem culture.

Economic Importance

In Japan, TNV and STNV have been associated with a

dwarfing disease (the Sukumi disease) of cultivated strawberry, but conclusive etiologic experiments are lacking

(Kaname and Kishi 1973; Komuro et al. 1973). In Italy, a

strain of TNV, called strawberry rosette necrosis virus, has

been associated with dwarfing, leaf malformation and

necrosis, and root necrosis of F. vesca and strawberry

cultivars (Faccioli 7970). The occurrence of aphid-borne

strawberry viruses, however, was not investigated in these

experiments. In the United States and Israel, TNV has been

found to occur in Fragaria spp. and cultivars in the

greenhouse. In several standards, vesca indicator clones like

'Alpine', TNV was associated with premature death of older

64
leaves and interfered with the use of this indicator to detect

strawberry mild yellow-edge and pseudo mild yellow-edge

diseases, (fig. 78)

TNV occurs commonly in roots of potted strawberries grown

in the greenhouse. F. vesca roots are particularly prone to

infection (fig. 78).

Symptoms on Natural and Experimental Hosts

In strawberry cultivars, the presence of TNV and its fungal

vector Olpidium brassicae (Wor.) Dang, in strawberry roots

causes necrosis of small roots (Faccioli 1969). In Italy, TNV

infection of F. vesca and cultivars was also linked with

dwarfing, leaf malformation, necrosis, and mottling (Faccioli

7969, 7970). The possible association of TNV with the

Sukumi disease of cultivated strawberry in Japan was

previously mentioned under "Economic Importance."

TNV has a very wide natural and experimental host range

among angiosperms (Price 1940). A number of herbaceous

test plants develop necrotic local lesions when sap-inoculated

with TNV. Chenopodium quinoa Willd. is a good experimental host for TNV by strawberry root sap inoculation.

Small, necrotic, local lesions develop on C. quinoa leaves a

few days after inoculation with sap from TNV-infected

strawberry roots (fig. 79). Roots of mung bean (Phaseolus

aureus Roxb.) are readily infected by Olpidium plus TNV

and quickly develop characteristic chocolate-brown root

lesions after such infections (fig. 80) (Teakle 7962).

Natural and Experimental Transmission

TNV is spread naturally by zoospores of the obligately plant

parasitic fungus Olpidium brassicae, which has a wide host

range (Harrison 1977). Untreated greenhouse potting soils

are frequently infested with TNV-carrying Olpidium resting

spores, and plants grown in such soils are readily infected by

Olpidium and TNV. Infection of strawberry roots by TNV

has been obtained in soils air dried for 30 days (Komuro et al.

1973). Occurrence of TNV in small infected pieces of roots

in the soil could explain these results since TNV fails to

survive in air-dried soil even for 2 days (Smith et al. 1969).

TNV can be transmitted from infected strawberry roots by

grinding them, using a mortar and pestle, with a suitable

buffer like 3% nicotine alkaloid in water, or 0.05 M

phosphate buffer -I- 2% polyvinyl pyrrolidone (mol. wt.

10,000), and inoculating the resulting sap to suitable

indicator plants like C. quinoa, C. amaranticolor Coste and

Reyn., and bean {Phaseolus vulgaris L.) (Fulton 1952;

Frazier 1955b; Faccioli 7969). Local lesions (fig. 79) appear

within 3 to 5 days on TNV-inoculated leaves.

Figure 78. — Necrotic older leaves ol trucaría vesca

'Alpine' infected by tobacco necrosis virus.

Figure 79. — Chenopodium quinoa: Left, leaf infected with tobacco necrosis virus by sap inoculation

from infected strawberry roots; right, healthy leaf.

Properties of the Causal Agent

TNV and STNV have been studied in great detail. TNV is an

isometric particle (26 nm in diameter) with a sedimentation

coefficient (s2oo,w) of 118S. Its specific absorbance at 260 nm

is 5.0 to 5.5. TNV usually occurs in very high concentrations

Figure 80. — Mung bean seedlings showing large black

root lesions after infection by Olpidium brassicae and

tobacco necrosis virus in infested soil; two healthy

seedlings on the right.

65
in infected roots (dilution end point of infected sap often

reaches 1:1,000,000 in herbaceous hosts, but is usually low

in Fragaria). TNV is quite heat stable in vivo (thermal

inactivation point in infected sap is 85° to 95°C). TNV mol.

wt. is 7 X 10^ daltons, with single-stranded RNA mol. wt. of

1.4 X 10^ daltons (Kassanis 1970b). STNV is a smaller

isometric particle 17 nm in diameter. Its specific absorbance

at 260 nm is 6.5; S(2oo,w) = 50 S, and STNV mol. wt. is 1.97

X 10' daltons, with RNA mol. wt. of 0.28 x 10' daltons

(Kassanis 1970a). Two major serotypes of TNV are known

which cross-react poorly. STNV is serologically unrelated to

TNV. When STNV is present with TNV, STNV may

comprise the bulk of the virions present, so that serological

detection may require sera containing antibodies against

STNV as well as the proper TNV serotypes. TNV and STNV

may occur in infected plants as free RNA as well as intact

virions. Therefore, ELISA tests for TNV in infected

strawberry root sap are often faint or even negative when

bioassays on C. quinoa are positive.

Detection and Identification

TNV with or without STNV can best be detected in

strawberry by grinding roots of suspected plants (1:5, w:v) in

0.05 M phosphate buffer + 2% polyvinyl pyrrolidone (mol.

wt. 10,000), with a mortar and pestle, and a little Celite

(diatomaceous earth powder) and rubbing leaves of Chenopodium quinoa. TNV causes small local lesions on leaves 3 to 5

days after inoculation (fig. 79). TNV appears to be present

more often at higher concentrations in infected F. vesca roots

than in roots of infected strawberry cultivars. If only one or

two local lesions develop on inoculated C. quinoa, they can

usually be successfully subtransferred by mechanical inoculation to other C. quinoa leaves for confirming studies such

as physical property determinations, agar gel, or other

serological identification tests, including serologically specific electron microscopy.

Control Procedures

Use of pasteurized, autoclaved, or fumigated soil for

greenhouse experimental work with strawberries is necessary

to prevent infection. The infected Olpidium brassicae

zoospores carrying TNV and often STNV are able to move in

films of water from infected to healthy plants, particularly on

wooden greenhouse benches. Strawberry plants can be

maintained free from TNV infection under such conditions

by growing them on inverted clay pots or glass jars (Frazier

1955b). TNV is not known to be seed transmitted, and

TNV-free 'Alpine' strawberry plants can be obtained by

growing them from seed in Olpidium-frcc soil on greenhouse

benches free from Olpidium-infQcicd plants.

The need for, and the methods of control of, TNV in

strawberry cultivars in the field have not been investigated.

No information is available on the elimination of TNV from

infected strawberry clones by heat therapy.

Remarks

The role of TNV in causing diseases of cultivated

strawberries is not known. Feeder root necrosis has not been

reported to occur in infected cultivars in the United States.

There are now enough reports on the occurrence of TNV in

field-grown strawberry cultivars throughout the world to

warrant more serious study of this virus, of STNV, and of

their vector, Olpidium brassicae, in causing strawberry

diseases, alone or in combination with virus and other

diseases of strawberry. The infection of strawberry plants by

TNV in soils that have been air dried or pasteurized also

requires additional study.

Vá

Strawberry Witches'-Broom and Multiplier Diseases//

By R. H.{Converse

Additional Names

For multiplier disease: multiplier plant, bushy plant, and

spindly plant diseases. For strawberry witches'-broom: no

other name.

History and Geographic Distribution

Witches'-broom disease (WBD) was first reported in Oregon

(Zeller 1927) and has been found in California (N. W.

Frazier, unpublished data). A similar disorder was later

described in The Netherlands (Kronenberg 1943). This

disease is rare from all three reporting areas. Multiplier

disease (MD) was first noted in Minnesota, Wisconsin,

Illinois, and New York (Demaree and Marcus 1951) and has

been subsequently reported and studied in Wisconsin (Sehgal

and Boone 1963; Boone 7970).

Economic Importance

Multiplier disease occurs rarely and is found mainly in the

Great Lakes region of the United States and in British

Columbia in Canada. Both diseases are readily detected, and

infected plants can be readily rogued. Because of their rarity,

neither is economically significant.

Symptoms on Natural and Experimental Hosts

On natural hosts. Both diseases are only known to infect

Fragaria spp. Witches'-broom diseased strawberry cultivars

are dwarfed, very bushy in appearance, and have numerous

branched crowns, with small leaves on spindly petioles (fig.

81). Runners when formed are very short, and severely

broomed daughter plants become established close to

infected mother plants. Plants of strawberry cultivars infected

by MD are dwarfed and exhibit crown proliferation. Leaflets

cup upwards on short, erect petioles. Runners are short and

flowers are reduced in number and size, but fruit normally

(fig. 82).

On experimental hosts. Witches'-broom diseased leaves

grafted to Fragaria vesca var. semperflorens (Duch.) Ser.

cv. 'Alpine' and F. chiloensis (L.) Duch. caused crown

proliferation with numerous small leaves on thin petioles

66
Figure 81. —Left, strawberry witches'broom disease

(Marshall strain) on cv. 'Marshall'; right, healthy

'Marshall'. (Courtesy D. M. Boone, University of

Wisconsin.)

Figure 82. — A, Multiplier disease on cv. 'Sparkle' B,

Healthy cv. 'Sparkle'. (Courtesy D. M. Boone,

University of Wisconsin.)

(Miller ¡959; Frazier 1974). Leaf graft transmission from

infected 'Puget Beauty' to 'Marshall' cultivars led to similar

symptoms (Miller 7959). Typical crown proliferation and

stunting were caused when MD was grafted into several

strawberry cultivars and F. vesca clones, including 'EMC,

'UC-l' F. vesca var. alba (Duch.), F. vesca ssp. bracteata

(Heller) Staudt, F. chiloensis, and F. orientalis Losink

(Sehgal and Boone 1963).

Natural and Experimental Transmission

The modes of natural transmission of WED and MD are

unknown, although WBD does spread slowly in the field

(Zeller 1927). Experimentally, WBD was transmitted by leaf

graft (Miller 1959, Frazier 1974) and stolon graft (Demaree

and Marcus 1951). Zeller (1927) claimed to have transmitted

WBD experimentally by Chaetosiphon fragaefolii (Cock.),

although his data show only the development of short,

epinastic leaflets on spindly petioles rather than crown

proliferation. He may have mistakenly transmitted one of the

aphid-borne viruses. Mellor and Forbes {I960) were unable

to transmit WBD by either C. fragaefolii or C. thomasi.

Sehgal and Boone {1963) transmitted MD by dodder

{Cuscuta subinclusa Dur. and Hilg.) to Fragaria vesca

'EMC and to strawberry but not to several herbaceous hosts.

Transmission of MD was not achieved by means of the

aphids Aphis gossypii Glov., A. forbesi Weed, several

Chaetosiphon species, or the aster leafhopper Macrosteles

fascifrons (Stâl) (Sehgal and Boone 1963; N. W. Frazier,

unpublished data).

Properties of the Causal Agent

Strawberry WBD and MD both cause symptoms typical of

yellows diseases that are commonly transmitted by leafhoppers and are caused by mycoplasmalike organisms (MLO)

(Whitcomb and Davis 1970). As expected, temporary

symptom remission of WBD was achieved by treatment of

infected strawberry plants with oxytetracycline at 50 ppm in

root mist culture (Huhtanen and Converse 1971). Structures

resembling MLO were found in the phloem of WBD-infected

strawberry petioles (fig. 83) (Doi and Okuda 1973; R. H.

Converse, unpublished data). MD has not yet been similarly

studied.

Detection and Identification

So far, geography is the best criterion for identifying diseases

associated with crown proliferation symptoms in strawberry

Figure 83. — Electron micrograph of mycoplasmalike

bodies in sieve tubes of F. vesca cv. "Alpine' infected

with Miller isolate of witches'-broom disease. Bar

represents 200 nm.

67
cultivars in North America. As previously noted, WBD has

been recognized only in The Netherlands and on the Pacific

coast of the United States and not in Canada. MD is known

only from the Great Lakes region of the United States and

from British Columbia. Crown proliferation; small leañets

borne on short, spindly petioles; and shortened runners are

symptoms common to both diseases. No fruit are produced

on WBD-infected cultivars, whereas normal-sized fruit are

produced by a few, small ñowers on MD-infected cultivars.

F. chiloensis is said to be a good test plant for MD by leaflet

grafting (Sehgal and Boone 1963), producing a tuft of small

spindly leaves. There are no literature reports of grafts of

WBD to F. chiloensis.

Control Procedures

Both of these diseases cause pronounced and characteristic

symptoms in infected strawberry cultivars. Both of them

spread slowly in the field. Accordingly, the use of certified

planting stock and roguing infected plants are adequate

control measures. There is no published information on the

elimination of either causal agent from infected plants. If

they are caused by MLO, however, both should be readily

heat inactivated in infected plants (Nyland and Goheen

1969).

Remarks

The slight differences in symptomatology between WBD and

MD that are reported in the literature could be ascribed to the

environmental conditions and choice of cultivars in the areas

where the work was done. The precise relationships between

the causal agents of WBD and MD must await further

etiologic studies of both diseases. Frazier believes that the

WBD with which he worked in California was a complex of

several undetermined causal agents (Frazier 1974).

"y^^&Minor or Little-Known Virus and Viruslike Diseases of

Strawberry«/

By R. H.jCpnverse

Several virus and viruslike diseases of strawberry, not

discussed elsewhere in this section, have seldom been

reported in the literature. Some of these diseases may have

been important when reported, or may have been curiosities

then and now, or may be of unrecognized importance in some

strawberry growing areas at present. More data are required

to establish their economic importance. Often, the relationships of these diseases and their causal agents to

well-described diseases and pathogens remain to be determined. Key literature citations are given below. Many of

these diseases were also discussed, sometimes in more detail

than here, in Frazier (1970b).

Disease

Strawberry

necrosis

(Nekrosevirus

der Erdbeere)

Strawberry

band mosaic

(Bandmosaik

der Erdbeere)

Strawberry

stunt

Strawberry

vein necrosis

(called NEPO

Virus No. 1

by R. M.

Lister 1970)

NEPO Virus

No. 2

Notes

Symptomless in cv.

'Herzberg's Triumph'

and was mechanically

transmitted to bean and

a few other herbaceous

test plants in Germany.

Relationships unknown.

Causes mosaic

symptoms on leaves of

cv. 'St. Anthony of

Padua' in Hungary and

is graft transmissible to

cv. 'Muncheberg Early'

but not to F. vesca.

Relationships unknown.

Infected cultivars were

dwarfed with erect

leaves, graft

transmitted, and also

claimed to be aphid

transmitted. Reported in

Minnesota (Skiles and

King 7952) and possibly

in Germany (Domes

7957), but the first

report at least was

probably multiplier plant

disease in complex with

other viruses (Boone

7970). (See "Strawberry

Witches'-broom and

Multiplier Diseases, ' '

p. 66.)

Found in one strawberry

plant (possibly cv.

'Champion') once in

Minnesota and

graft-transmitted to F.

vesca, causing apical

necrosis and recovery,

and sap transmissible to

several herbaceous

hosts, similar to tobacco

streak virus in many of

its properties. (See

"Tobacco streak virus in

Strawberry," p. 57.)

Graft transmitted to cv.

'Madame Moutout' and

to F. vesca, causing leaf

vein chlorosis,

asymmetry, and

followed by recovery;

sap transmitted to many

herbaceous plants,

causing necrosis and

tumors in beans.

Relationships unknown.

Reported once in

northern Italy.

Author and

year

Maassen

7959, 7967

Maassen and

Nemeth 7967

Zeller and

Weaver 7947

Stingl and

King 1965b

Canova and

Tacconi 7965;

Lister 7970

68
Tobacco

mosaic virus

Virus groups

1-6

Loosely associated with

Sukumi strawberry

degeneration disease in

Japan. See "Strawberry

Leafroll,"p. 61, for a

report of its occasional

association with this

disease. Also isolated

from F. vesca.

Virus isolates from 39

strawberry cultivars

indexed on F. vesca

were cataloged into 6

groups, and previously

reported viruses in

strawberry were

compared with them.

Comuet and

Morand 1960;

Reed and

Felix 1961;

Kaname and

Kishi 1973

Schöniger and

Bauer 1955

Nongraft Transmissible Diseases and Disorders

ÁVirus and Viruslike Diseases Experimentally

Transmitted to Strawberry

By R. H. Converse

Strawberries, particularly Fragaria vesca L., have frequently

been used as experimental host plants for viruses (hereafter

used to include viruses and viruslike agents) from a number

of other crops. Transmission has usually been by petiole

insert leaf grafting, but aphids, dodder, and sap have also

been used. It is possible to obtain virus transmissions to

Fragaria from other Rosaceous genera, like Rubus. Table 6

lists literature reports of strawberry as a host of experimentally transmitted viruses not otherwise mentioned in this

section.

.^^

Strawberry June Yellows y

By A. B.[Wills

Additional Common Names

Leaf variegation, yellow leaf, gold leaf, spring yellows,

transient yellows, 'Blakemore' yellows.

History and Geographic Distribution

Reports of variegation in strawberry species and cultivars in

eighteenth and nineteenth century literature were noted by

Stevens (1933) and in a comprehensive review of June

Yellows by Darrow (1955). These reports are generally brief

but June Yellows can be recognized with confidence from the

description by Darwin (1896) of a variegated strawberry

clone observed in 1859. Symptoms attributable to June

Yellows have since been reported in cultivars or materials

raised in the course of breeding or genetical studies. The

earliest of such reports were by Richardson (1920, 1923) in

England and Alderman (1926) in North America. The

condition now occurs worldwide wherever strawberry

breeding is done.

Economic Importance

Vigor and yield decline in affected clones as the disease

progresses. In severely affected clones, plants are dwarfed

and yields negligible. Serious economic losses can occur

when a widely grown cultivar becomes affected and

degenerates rapidly. A notable instance of this occurred in

Britain when cv. 'Auchincruive Climax' became affected;

symptoms were first seen in 1950, and by 1955 nearly all

stocks had deteriorated so far as to be valueless (Wills 1962).

The disease is a constant hazard in plant breeding, as

significant numbers of progenies may have to be culled when

it appears.

Symptoms

Symptoms are seen most clearly during the period of rapid

spring growth; in most cultivars they disappear during the

summer but may reappear in the autumn. Symptom

expression is temperature sensitive and all but very severely

affected plants become green when kept at a high temperature

only to develop June Yellows again at ambient temperatures

(Braak 7955).

Affected leaves are either uniformly pale-yellow when they

unfold and become mottled green and yellow as they mature

(fig. 84), or are mottled from the outset. The mottled areas

are clearly delineated and tend to form sectorial patterns (fig.

85). The symptoms may become more conspicuous on

successive leaves, but they usually disappear as the leaves

age and may not occur on later-formed leaves. Permanent

69
Table 6.—Viruses or viruslike agents experimentally transmitted to strawberry

but not known to infect strawberry naturally

Plant source

Virus or viruslike agents

transmitted

Fragaria

indicator References

Apple and

rose.

Apple mosaic

(= rose mosaic).

F. vesca

and CVS.

Cropley et al. 1960;

Fulton 7952; Nyland and

Engelbrecht 1958.

Apricot Apricot ring

pox.

F. vesca

and CVS.

Nyland and

Engelbrecht 1958.

Blackberry Alpine mosaic agent F. vesca

'Alpine'.

R. H. Converse,

unpublished data.

Black raspberry.

Mild streak F. vesca

and CVS.

Braun and Keplinger 1962.

Chokecherry X-disease Strawberry cvs. Braun and Keplinger 1962.

Peach Prunus ringspot F. vesca

and CVS.

Nyland and Engelbrecht 1958.

Tomato ringspot

( = peach yellow

bud mosaic).

F, vesca

and CVS.

Nyland and Engelbrecht 1958.

X-disease F. vesca 'EMC Slack 1952.

Plum Line pattern

(= plum line pattern).

F. vesca

and CVS.

Nyland and Engelbrecht 1958.

White spot F. vesca and cvs. Nyland and Engelbrecht 1958.

Red raspberry Senescence disorder F. vesca 'Alpine' R. H. Converse, unpublished

data.

Raspberry vein chlorosis F. vesca 'Alpine' Stace-Smith 1961.

Green mosaic F. vesca and cvs. Braun and Keplinger 1962.

Unknown disease,

probably caused by tomato

ringspot virus. (See 'Tomato

Ringspot Virus in Strawberry,"

p. 52.)

F, vesca Vaughan and Wiedman 1955.

Rubus yellow net F. vesca Stace-Smith and Mellor 7957.

Rose Various sources F. vesca 'UC-l', 'UC-2' Frazier 1963.

Sour cherry Prune dwarf ( = sour

cherry yellows).

F. vesca

and cvs.

Nyland and Engelbrecht 1958.

Sweet cherry Rugose mosaic

(= prunus ringspot).

F. vesca and cvs. Nyland and Engelbrecht 1958.

Big bud F. vesca 'EMS-l', 'UC-l' Helms 1962.

White clover — F. vesca Krczal 1960.

70
1 ituit o,T. —June Yellows showing variation in leaf

symptoms on a single strawberry plant.

Figure 85. — June Yellows showing sectorial leaf

mottling.

white streaks, usually accompanied by distortion of the leaf,

appear spasmodically in some affected cultivars and have

been observed unaccompanied by mottling symptoms in

others.

The disease is progressive. Symptoms on affected plants

become increasingly severe over a period of years; the plants

become stunted and eventually die. The period elapsing

before the disease first appears and the subsequent rate of

progress vary greatly between cultivars.

Natural and Experimental Transmission

Natural transmission is known to occur only sexually, the

disease being inherited through both pollen and seed parents.

The proportion of affected seedlings in a progeny varies with

the severity of symptoms in the parent plants and may even

differ between progenies grown from seeds obtained from

different flower trusses on one plant (Wills ¡962). The

disease can also occur in seedlings raised from symptomless

plants of an affected cultivar or from nonaffected cultivars.

The relationship between mottling and white streak symptoms of leaves is still obscure because the two kinds of

symptom can occur either together or separately.

Properties of the Causal Agent

Demaree and Darrow (1937) suggested that the cause might

be a mutation making possible the appearance of a recessive

character. Williams (7955) and Wills (1962) believed that an

extra-nuclear plasmagene with a threshold for expression

provided the best explanation of disease behavior, but both

authors recognized an influence of plant genotype on disease

development. More recently. Brown (1977) has postulated an

interaction between a nuclear and a plasmid gene.

Attempts to transmit June Yellows by insects have been

unsuccessful (Plakidas 1932; Morris and Afanasiev 1944;

Cuba 1933; Demaree and Darrow 1937; Berkeley 1931), as

have sap inoculations (Plakidas 1932; Guba 1933) and grafts

(Berkeley 1928; Plakidas 1929; Guba 1933; Demaree and

Darrow 1937; Reid 1951; Williams 7955).

Thomberry et al. (1951) reported finding spherical particles

in a variegated clone. Huhtanen and Converse (1971)

observed partial and temporary remission of symptoms after

applying a root spray of oxytetracycline and suggested that

mycoplasmalike organisms might be involved in disease

etiology. Recent attempts to associate viruses or viroids

with June Yellows in extracts from affected plants have so far

been unsuccessful (R. 1. Hamilton and T. J. Morris,

unpublished results).

Detection and Identiñcation

No direct tests are known for latent June Yellows, but

progeny testing by selfing has long been advocated as a

means to detect carriers (Demaree and Darrow 1937). Bauer

(1960) concluded that sib-crosses in S, or back-crosses were

more satisfactory because the plants obtained could be

exploited in breeding nonsusceptible cultivars. He further

advocated crossing S| breeding materials to tetraploid

Fragaria vesca L. var. semperflorens (Duch.) Ser. as a

control test. Wills (1962) preferred a test cross to a cultivar

known to have a genotype that permitted symptom

development in susceptible offspring.

The disease is easily confused with other genetic variegations, some herbicide damage symptoms (see "Strawberry

Herbicide Damage and Nutritional Imbalances," p. 79), or

with the nonvariegated spring pallor shown by some

genotypes. No other yellows condition shows both the

seasonal variation and the sectorial symptom pattern

characteristics of June Yellows.

Control Procedures

June Yellows showed no permanent response to prolonged

growth at high temperatures (Wills 1962) or to heat treatment

followed by meristem tip culture (East Mailing Research

Station 7969, 7970).

71
Propagation from nonaffected stock has proved effective in

prolonging the useful life of some cultivars, for example,

'Blakemore' and 'Cambridge Favourite'. Careful inspection

and roguing during spring are necessary for the production of

certified planting material.

Remarks

Although June Yellows is not a wholly accurate name, it is

the one most commonly used and it is desirable that it should

be standardized.

,41- Bud and Leaf Nematodes of Strawberry y

By D. A.gl_ack and J. P.JFulton

Additional Common Names

Diseases associated with various species of bud and leaf

nematodes have been termed spring dwarf, spring crimp,

strawberry eelworm disease, red plant, summer dwarf,

summer crimp, and Blättalchenkrankeit.

A more severe disease when nematodes are associated with a

bacterium is termed cauliflower disease, strawberry bunch,

and Blumenkohlkrankheit.

History and Geographic Distribution

Ritzema Bos (1890) first described a nematode from

strawberry plants with cauliflower disease. Later, Crosse and

Pitcher (1952) and Pitcher and Crosse (1958) demonstrated

that this particular disease resulted from the interaction of a

bacterium and nematode. Other studies in North America

(Brooks 1931; Christie and Crossman 1936; Christie 1943)

attributed milder disease symptoms to bud and leaf

nematodes alone.

The cauliflower disease attributed to the nematode-bacterial

association occurs in northern Europe only. Spring and

summer dwarf are present in both northern and southern

strawberry growing areas in the United States.

Economic Importance and Symptoms on Natural and

Experimental Hosts

Although spring dwarf occurs more commonly in northern

United States and summer dwarf more commonly in southern

United States, the symptoms of these two diseases are

similar. Initially the plant lies flat on the ground (fig. 86 A,

B). Older leaves may take on a reddish coloration. New

leaves are dwarfed with varying amounts of twisting,

cupping, and crinkling (fig. 87). The main buds may die and

secondary buds produce stunted, multiple-crowned plants.

Fruit on affected plants are sometimes malformed (Slack et

al. 1957).

The cauliflower disease is characterized by plants with

crowns reduced to stunted, fleshy rosettes. The bulk of such a

structure is composed of short, swollen leaf petioles, gall

tissue, and rudimentary blossoms.

' 1 'Z A- iT^-

Figure 86. —A, Summer dwarf (dwarfed strawberry

plants in center) caused by Aphelenchoides besseyi: B,

left, spring dwarf caused by Aphelenchoidesfragariae.

right, normal strawberry plant.

Figure 87. — Spring dwarf of cultivated strawberry

showing twisted young leaves.

72
Natural and Experimental Transmission

Nematodes are spread to daughter plants produced from

infected mother plants. Some dissemination of the nematodes

occurs as a result of splashing rain and water movement. The

nematodes persist for only short periods in the soil. Spread

into new plantings is primarily the result of utilizing infested

plants.

Properties of Causal Agent

Three species in the genus Aphelenchoides are associated

with the diseases described here. Spring dwarf is caused by

A. fragariae (Ritzema Bos) Christie, while A. besseyi

Christie is the cause of summer dwarf. In northern Europe,

A. fragariae or A. ritzemabosi (Schwartz) Steiner and Buhrer

are associated with the strawberry eelworm disease. Joint

infections of either of these two nematodes and Corynebacterium fascians (Tilford) Downson cause the cauliflower

disease. A. besseyi from rice does not infect strawberry and

vice versa. Undoubtedly, a strain difference exists.

Detection and Identification

Buds from suspected plants are dissected and macerated in

water in a Petri dish or watchglass. After approximately 15

min, the material is observed at a low magnification for

active nematodes. The characteristics of the several species

and useful keys for their identification have been developed

by Allen (7952).

Control Procedures

Bud nematode problems are effectively controlled by careful

attention to plant production. Certification programs should

be cognizant of the nematode problems and allow no

tolerance in inspection of certified plantings. When an

occasional diseased plant is noted in fruit-producing fields,

control can generally be effected by roguing.

Dá-Cyclamen Mite Damage in Strawberry..

By G. A.lSchaefers ^

Additional Common Names

Steneotarsonemus (also known as Tarsonemus) pallidus

(Banks), Steneotarsonemus (also known as Tarsonemus)

fragariae (Zimmerman). Beer (1954) concluded that the

European S. fragariae is synonymous with S. pallidus. This

opinion is widely held although some authors consider them

distinct species (Van Eyndhoven and Groenwold 1959), and

the name T. fragariae is still frequently used in European

literature. The common name approved by the Entomological

Society of America is cyclamen mite. Other names used in

the literature include strawberry mite, strawberry crown

mite, and strawberry tarsonemid mite.

History and Geographic Distribution

The early history of this important pest of strawberry was

reviewed by Smith and Goldsmith {1936). They noted that

the mite had been observed on garden strawberries in Finland

as early as 1892. In the United States, the pest was first

observed on strawberries by Darrow in 1928; however, it was

long known as a pest of ornamental plants in greenhouses.

The mite occurs throughout North America and Europe and

has been reported from Africa, Australia, and Hawaii. As an

outdoor pest, its distribution may be limited in areas of

extremely high temperatures or low humidities. In the

artificial environment of greenhouses, the mite could

theoretically occur throughout the world.

Economic Importance

Before suitable control methods were discovered, cyclamen

mite was considered to be the most important pest of

strawberries in California, the leading strawberry producing

State in the United States. Reports on yield losses due to this

pest are varied and range up to 70% (Savzdarg 1957). In

Great Britain, detailed studies (Alford 7972) showed that

severely injured plants exhibited 53% yield reduction, while

moderately injured plants showed a 45% yield reduction. It

was found that 63 mites per leaflet resulted in a 36%

reduction in yield, compared to that obtained with 4 mites per

leaflet. Although the mite is still considered a major pest on

strawberry, with the development of modem pest management strategies devastating losses are no longer inevitable.

Symptoms on Natural and Experimental Hosts

Cyclamen mite is primarily a greenhouse pest and under such

conditions has a great range of host plants (Smith 1933).

Outdoors, in addition to strawberry, they attack Delphinium

and, more recently, the author has observed them on

raspberry, although not in damaging numbers.

Because of the humidity requirements of the mite, its feeding

activity is usually restricted to the protected areas within the

folds of the youngest leaves. When injury is mild, the leaves

continue to grow and unfold, but are reduced in size and have

shortened petioles. The leaf may be dark green, and have a

rugose, blistered appearance (fig. 88). The veins often

assume a reddish brown color, and the plant itself appears

dense as a result of the shortened petioles. Occasionally, the

leaf edges have been observed to roll downward (fig. 89),

thus suggesting leafroll virus symptoms. (See "Strawberry

Leafroll," p. 61.) More severe symptoms result in a pale

greenish-yellow color of the newly unfolding leaves (fig. 90).

They are more severely reduced in size and distorted with the

margins cupped upward. With high mite densities, even more

severe symptoms may result. The petioles often fail to exceed

2.5 cm in length, and the new leaves do not unfold normally.

They are much reduced in size, and present a silvery

appearance because of the dense pubescence on their

undersides. Later they die and turn brown, at which time they

become quite brittle. In addition to foliar injury, the mites

may also attack the blossoms causing them to darken around

the base with resultant failure of fruit development.

Properties of Causal Agent

Osterwalder (1928) described a "crinkle disease" of strawberry which he attributed to the mite's feeding activity. Because

73
Figure 88. — Rugose symptom on leaf caused by

low-density cyclamen mite infestation.

Figure 89. — Leaf-rolling symptom caused by cyclamen mite.

of the local symptoms of the "disease," Harmson (1934)

concluded that the injury resulted from feeding and was most

likely not virus-induced. Massée (1933) considered the

possibility that the mite was responsible for the presence of

yellow-edge virus but was unable to confirm it. It is now

concluded that the injury results when the mite penetrates the

epidermis of the leaf and extracts the cell contents. Death of

the leaf probably results under conditions of high mite

density and reduced leaf growth, allowing for the release of

high concentrations of destructive enzymes by the mite.

Under conditions of low populations of mites and/or rapid

leaf growth, the mites feeding activities appear to have a

stimulatory effect on the epidermal cells resulting in their

hypertrophy and proliferation (fig. 91 A and 5). This reaction

results in the distorted, blistered appearance of mildly

infested leaves.

Natural Spread

Because of the size of the adult mites, about 200 to 250

microns in length, as well as their dependence on a humid

environment, they are unable to move any great distances

under exposed conditions. Transmission probably occurs

through the transfer of infested plant materials. The mite is

generally introduced into a planting by means of infested

Figure 90. — Severe crown symptoms due to high

cyclamen mite density.

Figure 91. — Cyclamen mite damage: A. Cross section

of a noninfested leaf. B. cross section of an infested leaf

with proliferation of epidermal cells (enlarged).

74
nursery plants. Within-field spread then occurs through leaf

contact and runner plants. Limited spread may occur via

other agents, such as agricultural implements, clothing, bees,

and other insects.

Detection and Identification

Because of the small size of the mites, some degree of

magnification is desirable when attempting to determine their

presence. They may be most readily detected during periods

of high population density. This occurs during fruit

development, at which time vegetative growth is greatly

curtailed. The different forms may be seen by opening the

young, still-folded leaves. They may be seen clustering in

large numbers (fig. 92) near the base of the leaflets. The adult

female is oval in shape, has four pairs of legs, is pinkish or

pale-amber to brown and has a glistening surface texture. The

eggs that are generally present in greatest numbers are oval.

transparent in color, and nearly one-half the size of the

female. The presence of the mite may be more readily

detected through recognition of the plant symptoms described

above.

Control Procedures

Cyclamen mite has been historically difficult to control, but a

number of organic pesticides are now known to be effective

(Schaefers 1963); however, these require the application of

high gallonage drenches to the crown area. This may be most

effectively accomplished during strawberry bed renovation,

at which time the canopy foliage is removed and the crown

growth is fully exposed. Granular systemic insecticides offer

considerable promise for eradication in nursery stock.

Organophosphate insecticides are particularly destructive to

predatory mites. Several early studies suggest that differences in cultivar tolerance and/or resistance may exist, but.

unfortunately, little research has been conducted on this

aspect of cyclamen mite control.

Remarks

The great variety of symptoms resulting from the feeding of

this pest could mislead the observer to consider the

possibility of viral causes.

jlli

z'

Figure 92. — Cyclamen mite.s on underside of young

leaflet (enlarged).

Potato Leafhopper Injury in Strawberry^.

By G. A.iSchaeîers

Additional Common Names

None.

History and Geographic Distribution

This insect pest earns its notoriety from the extensive

damage, that is. "hopperbum," it causes on potato (Ball

191IÁ). Poos and Wheeler {1943) were the first to rear the

leafhopper from Fragaria. The economic significance of this

association was reported by Campbell and Taylor (1962).

The potato leafhopper, Empoasca fabae (Harris), is not

broadly distributed throughout the United States, occurring

primarily in the East and Midwest. The insect overwinters in

the South, migrating to the Northern States each year, usually

starting around early May. On strawberry, they are most

active during July and August.

Economic Importance

The potato leafhopper for many years has been considered the

most important economic species of the genus because of the

damage it causes on potatoes, beans, clover, and alfalfa,

(Delong 1931). Significant yield reductions have been

attributed to the feeding of this pest on many crops.

Leafhopper feeding on strawberry has been observed to

reduce plant growth and inhibit runner production. To date,

however, detailed studies have not been conducted to

determine its effects on strawberry yield. Under defined

conditions, and with certain cultivars, the insect requires

control procedures, and thus may be classified as a major pest

(Schaefers 1981).

Symptoms on Natural and Experimental Hosts

The potato leafhopper has been reared from or collected on

138 host species (Poos and Wheeler 1943) and has been

shown to produce a great variety of symptoms, depending on

the host species as well as the time of the attack. These

authors discuss the "diseaselike" injury caused on various

hosts, such as "yellows" on alfalfa; "hopperbum," "leafroll,"

or "tipbum" on potato; "dwarfing" on peanuts; and "fruit

spotting" on oranges.

In contrast to other Empoasca species, which are mesophyll

feeders and cause a simple stippling of the leaf blade, E.

fabae feeds in the vascular tissue, and causes a much more

severe plant response. On commercial strawberry cultivars,

feeding by both adults and nymphs produces a reduction in

petiole length and leaf size (fig. 93). In greenhouse studies,

as few as one or two nymphs were capable of nearly total

inhibition of new growth. The leaves bend downward at right

angles to the midvein and exhibit a general distortion. In

more mature leaves, chlorosis begins at the edges and

gradually moves down or towards the midvein (fig. 94). In no

instance is the symptom referred to as "hopperbum"

applicable to the symptoms caused by E. fabae feeding on

75
strawberry. Symptoms may be confused with those of early

vein-banding disease (see "Strawberry Vein Banding," p. 16)

but distinct vein-banding symptoms are not evident.

Properties of the Causal Agent

Plant symptoms resulting from leafhopper feeding have been

attributed to one of three possible causes. These include

inoculation of a pathogen, inoculation of a toxin, or

mechanical blockage of the vascular system. While the

vector hypothesis has been generally discounted, there

remains good evidence for the support of the latter

hypotheses. More recently (Medler 1941; Hollebone et al.

1966), it was proposed that saliva injected during feeding

resulted in cell hypertrophy, which in turn interrupted

translocation. This is in contrast to simple plugging of the

vascular system with leafhopper stylet sheath material. In an

expansion of the early "toxaemia" theory, entomologists

have suggested that insect secretions are involved in the

production of plant growth regulators, which may result in

Figure 93. — Leafhopper injury on new growtii.

various symptoms, including growth inhibition. It is now

known that internal feeding by sucking insects is a complex

process, and consequently each of the above may be an

oversimplification of the facts.

The leafhopper cannot overwinter in the northern United

States, and must migrate north each year from areas of

Louisiana and Florida. The migrating forms move into the

earliest available green crops, such as alfalfa, and from there

into secondary crops as they become available. Eggs are

deposited into the leaves and stems of strawberry, and the

emerging nymphs feed on the undersides of the leaves.

Young plants seem to suffer most severely.

Detection and Identification

Upon observing the symptoms described above, one should

examine the undersides of the leaves for the presence of the

insect. The adults are smaller and lighter green. They may be

distinguished from other insects occurring on strawberry by

their habit of running sideways when disturbed. The presence

of cast skins will indicate the past presence of the insect.

Control Procedures

The leafhopper is easily controlled by a number of

insecticides. Local recommendations should be consulted.

Preliminary observations suggest that marked differences in

tolerance exist among cultivars.

r.W^Miscellaneous Arthropod Damage in Strawberry,/

By G. A.jSchaefers

Diseaselike symptoms are commonly associated with feeding

by members of the insect order Hemiptera. No less than 20

species are recognized as pests of strawberry. Members of

this order feed by means of piercing and sucking type

mouthparts. During this process, a complex of chemicals

may be injected into the plant, which can have a profound

influence on its physiological development. These chemicals

include stylet sheath material, which is mainly protein and

oxidizing enzymes, and watery saliva, which consists largely

of hydrolyzing or digestive enzymes, amino acids, and,

possibly, plant hormones (Miles 1972). The phytopathogenic

effects of a few of the more important hemipterans and mites

are reviewed here.

Mealybug

Members of the family Pseudococcidae, or mealybugs, are

among the most serious pests of plant life. Several species of

the genus Pseudococcus occur on strawberry.

Hildebrand (1939) noted the similarities in symptoms

between injury by mealybug feeding and crinkle virus. (See

"Strawberry Crinkle," p. 20.) In both instances, small

chlorotic spots may occur on the young unfolding leaves. In

mealybug injury, however, the spots continue to enlarge.

These eventually coalesce, and mosaiclike symptoms may

Figure 94. — Leafhopper injury on mature leaf.

76
Figure 95. — Adult mealy bug on lower surface of a

leaflet (enlarged).

result. Some dwarfing of the plant occurs with mealybug

feeding, but the leaves do not show the rugosity that is

characteristic of crinkle.

Mealybugs are small (2 mm), soft-bodied insects that appear

on the stems and crown growth (fig. 95). They are

characterized by flattened, elongate oval bodies covered by a

white powdery wax, which extends from the sides in a series

of short filaments with usually two longer ones at the

posterior end.

Following chemical control, new growth will be symptomless.

Shallot Aphid

While the strawberry aphid Chaetosiphon fragaefolii (Cock.)

is important as a virus vector, even large numbers of these

aphids free of viruses fail to produce any significant effect on

plant development. In contrast, the shallot aphid, Myzus

(Nectarosiphon) ascalonicus Doncaster, can have a severe

effect on both the quality and quantity of strawberry yields

(Alford 7976). Dicker (1950), upon first observing the plant

injury caused by this aphid, noticed the resemblance to the

symptoms of severe crinkle virus (see "Strawberry Crinkle,"

p. 20). Similariy, Mellor and Fitzpatrick (1961) pointed out

the possibility of confusing these symptoms with those of

crinkle virus or of certain virus complexes. Dicker noted that

the petioles became shortened, and the laminae were small,

puckered, twisted along the midribs, and curled. Some

strawberry cultivars exhibit red or purplish flecks on the

leaves. He concluded that the injury was purely mechanical

and that symptoms disappeared with control of the aphid.

The severity of the symptoms, however, would strongly

suggest that salivary injections may be involved.

Spittlebug

A spittlebug, Philaenus leucophthalmus L. attacks all

portions of the strawberry plant and produces distortion or

death of the stems and leaf blades (Mundinger 1946). Zeller

{1933) reported that spittlebug injury resembles crinkle virus

symptoms (see "Strawberry Crinkle," p. 20) in that the

Figure 96.

feeding.

Deformed leaf caused by spittlebug

leaves become crinkled and dark green (fig. 96). Some fruit

deformity results from the presence of spittlebug. While

detailed studies have not been conducted, it appears that the

deformity results from spittlemass interference with pollination rather than from some salivary secretion. Spittlebug

injury may be readily distinguished from virus disease by the

decided absence of systemic activity and the normality of the

new growth. Fresh or dried spittle masses on the leaf surfaces

provide evidence for the involvement of spittlebug. It is

readily controlled with a number of insecticides.

Tarnished Plant Bug

Several species of plant bugs (Miridae) are known to attack

strawberries. These include Lygus hesperus Knight, Lygus

elisus Van Duzee, and the tarnished plant bug, Lygus

lineolaris (P. de B.). Allen and Gaede (1963) concluded that

L. hesperus feeding during the blossom stage could cause the

production of deformed fruit. The problem is a major one in

many areas, and in a "normal" season, one nymph per

blossom cluster can cause 30 percent injured fruit with about

a 9 percent reduction in mean berry weight (Schaefers 7980).

Injury by the tarnished plant bug is characterized by the

presence of a number of well-developed achenes, which are

closely located due to lack of development of that area of the

receptacle (fig. 97). Upon dissection, the achenes will be

found to be hollow. While detailed feeding studies have not

been conducted, the bug may secrete a digestive enzyme

during feeding, which functionally blocks the stimulation of

receptacle growth by plant hormones. While a number of

pathogens can result in the production of "seedy" fruit,

tarnished plant bug injury is distinguished by the localized

patches of seeds. Resistant cultivars have not yet been found.

77
but control can be readily obtained through the application of

effective pesticides during blossom and early fruit development.

Spider Mites

Spider mites are worldwide in distribution and are considered

to be major economic pests on many field and orchard crops

as well as ornamental plants. The twospotted spider mite,

Tetranychus urticae Koch, and the strawberry spidermite,

Tetranychus turkestani Ugarov and Nikolski, are probably of

greater concern to North American strawberry growers than

any other arthropod pest on this crop.

rasping of the leaf surface followed by a sucking of the cell

contents. In contrast with the insects discussed previously,

there is no indication that any phytopathogenic secretions are

involved.

In higher population densities, symptoms on the upper leaf

surface will be a bronzing and drying of the leaf tissues. Such

feeding reduces plant vigor and yield and leads to stunting

and possible death of the plants. Although some resistant

cultivars have been identified (Kishaba et. al. 1972), a

number of acaricides may be effectively used in integrated

pest management systems (Kennedy et al. 1976).

Feeding injury resulting from low infestation levels of mites

may result in temporary confusion with crinkle symptoms

(Mellor and Fitzpatrick 1961). (See "Strawberry Crinkle,"

p. 20). Infected leaves are reduced in size and may present a

speckled or stippled appearance (fig. 98). The mites feed on

the lower surface of the older leaves. Feeding involves a

Figure 97. — Tarnished plant bug injured berries.

Heat Spot of Fragaria vesca

By J. P. Fulton

Small chlorotic spots appearing on the leaves of Fragaria

ve.^ca L. indicators as a result of physiological stress can

sometimes be mistaken for virus symptoms (fig. 99). These

symptoms have been termed "heat spot" (Smeets and

Wassenaar 1956) and are most commonly seen when plants

are moved from a cool to a warm environment. Plants that are

potbound or lacking in sufficient nutrients often respond with

heat spot at temperatures above 24°C. Since this is a stress

response, plants which have been inoculated with mild forms

of certain viruses or viruslike agents such as mild

yellow-edge virus or pallidosis agent (see "Strawberry Mild

Yellow-edge," p. 25, and "Strawberry Pallidosis," p. 55)

will also exhibit this type of spotting. To avoid the confusion

this symptom may cause when indexing for viruses, utilize

young, vigorously growing plants as indicators, add ungrafted controls, and hold plants at temperatures near 20°C.

Figure 99. — Heat spot symptoms on Fragaria vesca

cv. 'EMK'.

Figure 98. — Right, Spidermite injury on leaflet; left.

normal leaflet.

78
Té.

Strawberry Herbicide Damage and Nutritional

Imbalances;;

By P. CJCrandall

Herbicide injury and the toxicity or deficiency symptoms that

result from nutrient imbalances may occur in strawberry

fields and are occasionally mistaken as symptoms of virus

infection. Awareness of these possibilities and knowledge of

symptomatology and conditions under which these situations

may occur help to prevent mistaken diagnoses of field

problems.

Herbicide Injury

Herbicides that are registered for use on strawberries have

been tested for crop tolerance over a wide range of

conditions. Only after a number of years of such testing are

they approved for use by growers. Recommended application

rates are established to provide a good margin of safety below

phytotoxic levels. The instructions on the product label

include all precautions considered necessary for effective

weed control and to prevent crop damage. In spite of this,

strawberries are occasionally damaged by herbicides. Such

phytotoxicity results from any one of a number of causes

(Yarish 1980; Skroch and Sheets 1977).

Overapplication. Herbicides are plant killers. If too much is

applied, crop injury can occur. Overapplication is a frequent

cause of damage to strawberries. It can result from failure to

follow the product label directions or miscalculation of the

amount of herbicide put into the sprayer tank. The sprayer

may not be adjusted to apply the correct amount of material

per hectare. Since wettable powder herbicides are very

abrasive, they casue the nozzle openings to erode rapidly,

thus the application rate is increased. There is a tendency for

the tractor to travel slower when going up a slope and at the

ends of rows. Overapplication can also result from

overlapping at the ends of the spray boom. (Lockerman et al.

1975). Sometimes, excessive herbicide application occurs

when residual chemicals are applied to soil which already has

a high chemical level as the result of application on a

previous crop.

Drift. Injury from drift can occur at considerable distance

from the place of application. The phenoxy herbicide, 2,4-D,

is especially prone to drift either as minute droplets or as

vapor. Such drift causes leaf and stem or fruit deformities on

strawberries (figs. 100 and 101). The tendency to drift is

increased by high temperature, windy conditions, and/or high

nozzle pressures at the time of application.

Moisture and soil texture. The tolerance of strawberries to

residual herbicides depends on the ability of the plants to

endure low concentrations of the chemical and on the low

solubility of the herbicide, which causes the active

ingredients to be released slowly. Under normal soil and

moisture conditions, an equilibrium is maintained that

controls weeds in the surface layers of the soil with no

Figure 100. — Twisting of strawbeny petioles caused

by 2,4-D. (Courtesy W. A. Skroch, North Carolina

State University, Raleigh.)

Figure 101. — Misshapen strawberry fruit resulting

from 2,4-D application during time of blossom bud

formation. (Courtesy W. A. Skroch, North Carolina

State University, Raleigh.)

damage to the deeper-rooted strawberries. Damage can

occur, however, if the roots are exposed, if the soil is not

adequately settled around the plants, or if the soil has a coarse

texture. Under loose soil conditions, especially if excessive

moisture occurs soon after the herbicide is applied, the

chemical is carried down into close proximity to the roots and

causes injury. Danger from this source of injury is greater

with the more soluble herbicides. Chemicals with long

residual activity may accumulate to toxic levels as a result of

repeated applications in soils high in organic matter or clay

fractions.

79
Stage of strawberry plant growth. Susceptibility to

phytotoxicity is related to the stage of plant growth, age of

plants, and sensitivity of the cultivar, and it varies with the

time of year and the chemical. Factors involved include

rainfall, temperature, dormancy of the aboveground parts of

the plants, activity of the root system and other actively

growing sites, and the internal physiological processes of the

plant.

Simazine, a residual herbicide, can be used safely in the

Pacific Northwest of North America if applied to strawberries during late summer or early winter. When applied during

the spring, it causes marginal chlorosis or necrosis of the

leaves and considerable stunting of the strawberry plants (fig.

102). This chemical accumulates in soils that have high

exchange capacities and, in perennial plants like strawberry,

repeated use may cause toxicity. Simazine cannot be safely

used on strawberries in Eastern United States where different

growing conditions result in crop injury.

Napropamide, if applied during the time of runner

development, prevents many of the runner plants from

rooting.

The phenoxy herbicide 2,4-D can be safely applied to

strawberries right after harvest or during the winter. Some

leaf deformation may occur but is not serious. When applied

in the autumn during blossom bud differentiation, it causes

abnormally large, deformed fruits at harvesttime (fig. 101).

Dinoseb is satisfactory if applied to fully dormant plants;

however, when applied to growing plants or semidormant

plants it causes stunting and yield reduction.

Cultivar tolerance. Cultivars differ in their sensitivity to

herbicides. This tolerance is related to concentration of the

chemical, internal metabolism, growth habit, age, hairiness

of the leaves, and other anatomical features. Most older

cultivars have been evaluated for herbicide tolerance, but

newly introduced cultivars should be carefully observed for

herbicide sensitivity.

Additional factors. Other factors that influence phytotoxicity are chemical incompatabilities, temperature, humidity,

plant vigor, and cultural practices.

Symptomatology. Visible symptoms of herbicide injury on

strawberries vary widely. Some of the common symptoms

are vein clearing (terbacil, fig. 103), marginal chlorosis or

necrosis (chloroxuron, fig. 104), interveinal chlorosis or

necrosis (simazine, fig. 102), leaf or fruit deformity and

epinasty of stems, (2,4-D, figs. 100, 101), root damage and

inhibition of root growth or stunting of plants (napropamide,

fig. 105), or dying of plants. These symptoms may occur in

definite patterns across the field or may affect plants in a

random pattern.

Figure 102. — Simazine injury on strawberry leaves.

Figure 103. — Vein clearing of strawberry leaves

caused by terbacil. (Courtesy J. W. Braun, Washington

State University. Vancouver.)

Figure 104. — Chloroxuron injury of strawberry

leaves. (Courtesy R. S. Byther, Washington State

University, Puyallup.)

80
Figure 105. — Typical strawberry leaf coloration that

accompanies stunting. Stunting was caused by napropamide. (Courtesy J. W. Braun, Washington State

University, Vancouver.)

extreme nutritional imbalances vary considerably among

cultivars and may sometimes be complicated by the presence

of more than one imbalance.

Deficiency symptoms. A description of nutrient deficiency

symptoms of strawberries is helpful in diagnosing field

problems. The following list includes composite descriptions

derived from those published by Johanson {1963 and 1980),

Johanson and Walker {1963), Lineberry and Burkhart

{1943), Iwakiri and Scott (7957), Hoagland and Snyder

{1933), Lott (7946), Davidson {1941), Boyce and Matlock

(7966), Davis and Hill {1928), and Ulrich et al. (7980). More

complete descriptions are included in the above publications.

Most Common Nutrient Deficiency Symptoms on

Strawberries

Deficient

nutrient Symptoms

Diagnosing the problem. Careful observation of injury

patterns in the field sometimes helps to diagnose the problem.

The injury may occur in streaks that are related to the spray

boom length or to spray boom overlap. Injury may be worse

at the ends of rows or when the sprayer is moving up a slope.

Any of these injury patterns may indicate herbicide damage.

Sometimes, it is possible to relate injury to soil texture or

drainage. Often, the only way to determine the cause is to

analyze the complete herbicide application schedule, including previous cropping history. Lockerman et al. {1975) list a

number of pertinent questions to ask and field symptoms for

which to look. Jennings and Nyvall (7977) and Skroch and

Sheets (7977) emphasize the importance of "lookalike"

symptoms that may be mistaken for herbicide injury.

Nutrient Imbalances

Nutrient imbalances may cause visible symptoms of either

deficiency or toxicity. Such symptoms indicate that a

radically imbalanced situation has existed for some time.

This imbalance results from either too much or too little of

the nutrient in the soil, or from the application of another

nutrient or material that produces an antagonistic effect on

the absorption, translocation, or utilization of the nutrient.

The chemistry of such imbalances has been studied

extensively. The absorption and accumulation of each

nutrient are influenced by the absorption of every other

nutrient (Shear et al. 1948).

Deficiency and toxicity symptoms are visible responses to

this imbalanced nutrition. These visible expressions of

Nitrogen Young leaves small, pale, yellowish green

on stiff, upright petioles. Plants stunted

(fig. 106). Old leaves may have red

serrations or be completely bright yellow or

orange-red, later turning brown, with

necrotic margins. Calyx on ripe fruit

reddish.

Figure 106.—Nitrogen deficient strawberry plants on

right showing small, light green leaves and stunted

growth; normal plant on left. (Courtesy A. Ulrich,

University of California, Berkeley.)

Phosphorus Dark, bluish purple to blackish upper leaf

surfaces (fig. 107). Bottoms of leaves

reddish purple, often blue in veins of older

leaves. Leaves small, cupped downward,

reduced number of flower buds.

81
raí *h: V

^^^K*^ T3IH|!^^n|

between blades and crown remains green.

Young leaves remain green. Upward cupping of leaf margins.

Figure 107. — Phosphorus deficiency. Bluish-purple

coloration of upper strawberry leaf surfaces. (Courtesy

F. D. Johanson.)

Potassium Marginal chlorosis of mature leaves changing to reddish purple. Leaf margins scorch

and turn upward. Areas between veins

reddish brown except for a green triangle at

base of leaflet (fig. 108). Lower midrib and

short section of petiole darkens and becomes dry. Younger leaves unaffected or may

show some interveinal chlorosis. Older

leaves die forming a collar around base of

plant. Some leaflets develop a red band

across the middle of the underside.

Figure 109. — Magnesium deficiency. Marginal and

interveinal chlorosis on older strawberry leaves, young

leaves unaffected. (Courtesy A. Ulrich, University of

California, Berkeley.)

Boron Tipbum of early, unfolding leaves. Marginal and interveinal chlorosis of young

leaves (fig. 110). Growing points die

causing development of small, chlorotic,

deformed, and cupped leaves near the

center of plants. Short, brittle petioles and

blasting of flowers with deformed fruits.

Roots short and stubby with multiple

branching.

Figure 108. — Potassium deficiency. Reddish-brown

strawberry leaves with bright green triangle at base of

leaflet. (Courtesy F. D. Johanson.)

Magnesium Interveinal chlorosis of mature leaves

beginning near upper margin, becoming

reddish brown and necrotic. Serrations

green during early stages. Interveinal areas

develop necrotic patches giving a blotchy

leaf pattern (fig. 109). Short petiole section

Figure 110. — Boron deficiency. Tipbum and interveinal chlorosis on young strawberry leaves, older

leaves with puckered, squared-off tips.

82
Calcium Newly emerged leaves develop tipbum and

severe crimping of the tips of the leaflets

(fig. 111). Brown lesions on leaf and fruit

petioles with globules of sirupy sap exuding from large veins and petioles (fig. 112).

Older leaves develop chlorotic areas or a

purplish band across the center of the leaf

blades, which later becomes necrotic. Fruit

stunted with imperfect achene set.

Zinc Young leaves pale green or yellow; serrations remain green. Leaf blades narrow,

concave, and elongated. Larger veins

remain green (ñg. 113). Reddening between veins may occur in some cultivars.

Leaves become stunted.

^w^p^ vSp

Figure 111. — Calcium deficiency. Mature strawberry

leaf with tipbum. (Courtesy A. Ulrich, University of

California, Berkeley.)

Figure 113.—Zinc deficiency. Young strawberry

leaves pale green or yellow, serrations green. Leaf

blades narrow and elongated, normal leaf on left.

(Courtesy F. D. Johanson.)

Manganese Chlorosis of young leaves followed by fine,

green-netted veining or discontinuous vein

clearing (fig. 114). In later stages, the vein

clearing may develop into purple stippling

between larger veins. Leaf margins become

necrotic and curl upward. Scorching develops inward from outer margins of

leaflets (fig. 115).

Figure 114. — Manganese deficiency. Fine, greennetted veining or discontinuous vein clearing on

strawberry leaflet (enlarged). (Courtesy A. Ulrich, University of California, Berkeley.)

Figure 112. — Calcium deficiency. Brown lesions with

globules of sap on strawberry petioles. (Courtesy A.

Ulrich, University of California, Berkeley.)

83
Figure 115. — Manganese deficiency. Marginal scorching of strawberry leaves. (Courtesy A. Ulrich,

University of California, Berkeley.)

Iron Young leaves develop interveinal chlorosis

and are light yellow to nearly white (fig.

116), followed by marginal necrosis. New

leaves are stunted. Older leaves remain

green for some time.

Figure 116. — Iron deficiency. Young strawberry

leaves light yellow to nearly white. (Courtesy F. D.

Johanson.)

Nutrient toxicity. Micronutrients also damage strawberry

plants when present in excessive amounts. Among the most

common are boron, copper, and manganese. Visual

symptoms of such toxicities are not very specific. They tend

to involve stunting, marginal necrosis, and death of the

plants.

Salt toxicity. Salt toxicity results from a buildup of excess

soluble salts in the soil, which causes severe stunting or leaf

burn (Bernstein 1980). Stunting is related to the concentration of soluble salts in the soil solution and is often

accompanied by typical chloride leaf bum (fig. 117). Such

salt accumulations often result from the use of saline

irrigation water. Buildups occur in heavier soils where

leaching is slow, where not enough natural rainfall or

irrigation water is available to leach salts out of the root zone,

or in soils with a high water table. In high water table

situations, the water evaporates from the soil surface leaving

an accumulation of salts behind.

Albinism. Strawberries sometimes produce white or lightcolored fruits that are normal in size but are insipid, mushy,

and spoil rapidly after picking (fig. 118). This problem

results from sugar levels that are inadequate for normal

ripening (Ulrich et al. 1980). It often occurs during periods of

cloudy weather on excessively vigorous plants. It can also

occur on plants with a heavy set of fruit and poor leaf

development. The latter is typical of plants that have received

inadequate chilling before or after planting. Excessive levels

of bromide ion in the soil following methyl bromide

fumigation can also lead to the production of albino fruits.

Diagnosing nutrient problems. Specific plant and leaf

symptoms are helpful for determining nutrient problems.

Often, a careful observer can associate such symptoms with

soil texture and drainage. Symptoms are usually not uniform

from plant to plant or between areas of the field. When they

appear to be related to changes in soil texture and drainage,

nutritional problems should be suspected. Addition of

deficient nutrients or correction of soil conditions to avoid

deficiencies or toxicities should result in normal plant

growth. Foliar symptoms can be confirmed by plant and soil

chemical analyses. Such information helps to separate

nutritional problems from virus or other disease problems.

Nutritional symptoms related to nutritional imbalances may

also be accentuated as a result of insect, disease, mechanical

or freeze damage, or action of vertebrate pests on roots.

These possibilities should always be considered.

Importance of health virus indicator plants. Since

nutritional and other cultural problems can sometimes be

mistaken for virus disease expression, it is important that

plants to be used as indicator plants be healthy and normal in

appearance. Such plants must be grown under adequate

nutrition, light, and moisture conditions. Optimum levels

vary with cultivar and must be determined from experience.

84
Figure 117. — Marginal necrosis of strawberry leaves

typical of chloride (salt) injury. (Courtesy L. E.

Francois. USDA Salinity Laboratory, Riverside, Calif.)

Figure 118. — Albino strawberry fruits caused by

inadequate carbohydrate levels during ripening. (Courtesy R. D. Nelson, Driscoll Strawberry Associates.)

Strawberry Literature Cited

Aerts, J. 1973. Invloed van een enkelvoudig virus en van een

vimscomplex op de produktie bij acht aardbeivarieteiten.

(Effect of a single virus and a virus complex on the yield of

eight strawberry varieties.) Mededelingen Fakulteit Landbouwwetenschappen Gent 38: 1631-1645. [In Dutch].

1980. Invloed van Zwak-geelrandvirus op de

produktie bij aardbeien. [Effect of strawberry mild yellowedge virus on the production of strawberries.) Mededelingen

Faculteit Landouwwetenschappen Gent 45:369-375. [In

Dutch.)

Alderman, D. H. 1926. New fruits produced at the

University of Minnesota Fruit Breeding Farm. Minnesota

Agricultural Experiment Station Bulletin No. 230, 47 p.

Alford, D. V. 1972. The effect of Tarsonemus fragariae

Zimmerman (Acarina:Tarsonemidae) on strawberry yields.

Annals of Applied Biology 70:13-18.

1976. Some observations on the effect of pests on

strawberry yields. Annals of Applied Biology 84:437-455.

Allen, M. W. 1952. Taxonomic status of the bud and leaf

nematode related to Aphelencoides fragariae (Ritzema Bos

1890). Proceedings of the Helminthological Society of

Washington 19:108-120.

Allen, W. W., and S. E. Gaede. 1963. The relationship of

Lygus bugs and thrips to fruit deformity in strawberries.

Journal of Economic Entomology 56:823-825.

Anderson, H. M., A. J. Abbott, and S. Wiltshire. 1982.

Micropropagation of strawberry plants in vitro — effect of

growth regulators on indicence of multi-apex abnormality.

Scientia Horticulturae 16:331-341.

Babovic, M. V. 1976. Investigation of strawberry virus

diseases in Yugoslavia. Acta Horticulturae 66:19-24.

Ball, E. D. 1918. Leaf bum of the potato and its relation to

the potato leafhopper. Science 48:194.

Barbara, D. J., and M. F. Clark. 1982. A simple indirect

ELISA using F(ab')2 fragments of immunoglobulin. Journal

of General Virology 58:315-322.

Barritt, B. H., and H. A. Daubeny. 1982. Inheritance of

virus tolerance in strawberry. Journal of the American

Society for Horticultural Science 107:278-282.

85
and H. Y. s. Loo. 1973. Effects of mottle, crinkle,

and mild yellow-edge viruses on growth and yield of Hood

and Northwest strawberries. Canadian Journal of Plant

Science 53:605-607.

and C. H. Shanks, Jr. 1980. Breeding strawberries

for resistance to the aphids Chaetosiphon fragaefolii and C.

thomasi. HortScience 15:287-288.

Bauer, R. 1960. Grundlagen und Methoden der Züchtung bei

der Gartenerdbeere {Fragaria ananassa Duch.). Zeitschrift

für Pflanzenzüchtung 44:73-100.

Beakbane, A. B., M. D. Mishra, A. F. Posnette, and C. H.

Slater. 1971. Mycoplasma-like organisms associated with

chat fruit and rubbery wood diseases of apple, Malus

domestica Borkh., compared with those in strawberry with

green petal disease. Journal of General Microbiology

66:55-62.

Beer, R. E. 1954. A revision of the Tarsonemidae of the

Western Hemisphere (Order Acariña). University of Kansas

Science Bulletin 36:1091-1387.

Behncken, G. M., and D. H. Gowanlock. 1976. Association

of a bacterium-like organism with rugose leaf curl disease of

clovers. Australian Journal of Biological Sciences 29:137-

146.

Belkengren, R. O., and P. W. Miller. 1962. Culture of apical

meristem of Fragaria vesca strawberry plants as a method of

excluding latent A virus. Plant Disease Reporter 46:119-121.

Bell, H. K. 1955. Howard 17 and Premier strawberry: Are

they one and the same? Fruit Varieties and Horticultural

Digest 10:57-58.

Berkeley, G. H. 1928. Strawberry mosaic. Report of the

Dominion Botanist, Canada, 1927:128-130.

1931. Suspected strawberry mosaic. Report of the

Dominion Botanist, Canada, 1930:125-126.

and A. G. Plakidas. 1942. Strawberry leaf roll: a new

disease. Phytopathology 32:631-633.

Bernstein, L. 1980. Salt tolerance of fruit crops. U.S.

Department of Agriculture, Agriculture Information Bulletin

No. 292, 8 p.

Bettie, J. A., and A. S. Costa. 1980. Efeito da idade da folka

na aquisiacäo dos virus do mosqueado e da faixa-das-nevuras

do morangueiro pelo afidio vetor. [Effect of leaf age on

acquisition of strawberry mottle and vein banding viruses by

the aphid vector.] Fitopatología Brasileira 5(l):25-30. [In

Portuguese.]

Bolton, A. T. 1964. Virus diseases of strawberries in eastern

Canada. Canadian Plant Disease Survey 44:83-90.

1967. The inactivation of vein banding and latent C

viruses in strawberries by heat treatment. Canadian Journal

of Plant Science 47:375-380.

1970. Strawberry leafroll, p. 46. In N. W. Frazier,

editor. Virus diseases of small fruits and grapevines.

University of California Division of Agricultural Sciences,

Berkeley, 290 p.

1974. Effects of three virus diseases and their

combinations on fruit yield of strawberries. Canadian Journal

of Plant Science 54:271-275.

Boone, D. M. 1970. Witches'-broom and multiplier diseases

of strawberry, p. 25-26 In N. W. Frazier, editor. Virus

diseases of small fruits and grapevines. University of

California, Division of Agricultural Sciences, Berkeley,

290 p.

Boxus, P. 1974. The production of strawberry plants by

in-vitro micropropagation. Journal of Horticultural Science

49:209-210.

M. Quoirin, and J. M. Laine. 1977. Large-scale

propagation of strawberry plants from tissue culture, p.

130-140. In J. Reinert and Y. P. S. Bajaj, editors. Applied

and fundamental aspects of plant cell, tissue, and organ

culture. Springer Verlag, New York, 803 p.

Boyce, B. R., and D. L. Matlock. 1966. Strawberry

nutrition, p. 518-548. In N. F. Childers, editor. Nutrition of

fruit crops. Horticultural Publications, Rutgers University,

New Brunswick, N.J., 888 p.

Braak, J. P. 1955. Effect of temperature and light on June

Yellows in strawberries. Euphytica 4:189-196.

Braun, A. J., and J. A. Keplinger. 1962. Transmission of

viruses to strawberry by excised leaf grafts from plants other

than strawberry. Phytopathology 52:726. [Abstract.]

Bringhurst, R. S., and V. Voth. 1956. Strawberry virus

transmission by grafting excised leaves. Plant Disease

Reporter 40:596-600.

Brooks, A. N. 1931. Crimp — a nematode disease of

strawberry. Florida Agricultural Experiment Station Bulletin

No. 235, 27 p.

Brown, G. R. 1977. The disorder strawberry streak of

Fragaria x ananassa Duch., anatomical characteristics of the

leaves, environmental influence on expression and a genetic

hypothesis for control. Transactions of the Missouri

Academy of Science 10/11:277.

86
Brunt, A. A., and R. Stace-Smith. 1976. The occurrence of

the black raspberry latent strain of tobacco streak virus in

wild and cultivated Rubus species in British Columbia. Acta

Horticulturae 66:71-76.

1969. Green petal and aster yellows diseases both

found in strawberry, p. 2-3. In Annual Report of the

Committee for Horticultural Research. 1968. Canadian

Horticultural Council.

Cadman, C. H. 1956. Studies on the etiology and mode of

spread of Scottish raspberry leaf curl disease. Journal of

Horticultural Science 31:111-118.

1960. Studies on the relationship between soil-borne

viruses of the ringspot type occurring in Britain and

continental Europe. Virology 11:653-664.

and R. M. Lister. 1961. Relationship between

tomato ringspot and peach yellow-bud mosaic virus.

Phytopathology 51:29-31.

1972. Effects of three tetracyclines and their method

of application on the development of clover phyllody and

aster yellows symptoms in aster. Canadian Journal of Plant

Science 52:29-33.

1973. Effectiveness of antibiotics applied as

post-inoculation sprays against clover phyllody and aster

yellows. Canadian Journal of Plant Science 53:87-91.

1974. Additional host plants of clover phyllody in

Canada. Canadian Journal of Plant Science 54:755-763.

and R. M. Lister. 1962. Relationships and particle

sizes of peach yellow-bud mosaic and tomato ringspot

viruses. Plant Disease Reporter 46:770-771.

1976. Transmission characteristics and host range of

the clover yellow edge agent. Canadian Journal of Botany

54:1171-1179.

Campbell, R. E., and E. A. Taylor. 1962. Strawberry insects

and how to control them. U.S. Department of Agriculture

Farmers' Bulletin No. 2184, 20 p.

Canova, A., and R. Tacconi. 1965. Riecerche sui virus della

fragola. IL Un virus trasmissibile per sueco. [Researches on

strawberry viruses. II. A sap-transmissible virus.] Phytopathologia Mediterránea 4:31-37. (In Italian.) (English

Summary) (Abstract in Review of Applied Mycology 45:388

entry No. 2179, 1966.)

Chamberlain, E. E. 1934. A virus disease of strawberry in

New Zealand. New Zealand Agriculture 49:226-231.

Chapman, R. K. 1973. Integrated control of aster yellows.

Proceedings of the North Central Branch, Entomological

Society of America 28:71-92.

Chiykowski, L. N. 1962a. Clover phyllody and strawberry

green petal diseases, caused by the same virus in eastern

Canada. Canadian Journal of Botany 40:1615-1617.

1962b. Clover phyllody virus in Canada and its

transmission. Canadian Journal of Botany. 40:397-404.

1962c. Scaphytopius acutus (Say), a newly discovered vector of celery-infecting aster-yellows virus. Canadian

Journal of Botany 40:799-801.

1965. Transmission of clover phyllody virus by the

leafhopper, Paraphlepsius irroratus (Say). The Canadian

Entomologist 97:1171-1173.

1967. Some host plants of a Canadian isolate of the

1977. Transmission of a celery-infecting strain of

aster yellows by the leafhopper Aphrodes bicinctus.

Phytopathology 67:522-524.

1981a. Association of mycoplasma-like organisms

with clover yellow edge disease. Canadian Journal of Plant

Pathology 3:139-144.

1981b. Epidemiology of diseases caused by

leafhopper-bome pathogens, p. 105-159. In K. Maramorosch

and K. F. Harris, editors. Plant diseases and vectors: Ecology

and epidemiology. Academic Press, New York, 360 p.

S. R. Colpitts, L. J. Coulombe, and others. 1973.

Strawberry green petal disease in Quebec and the Maritime

Provinces, 1971-72. Canadian Plant Disease Survey 53:63-

66.

and D. L. Craig. 1975. Reaction of strawberry

cultivars to clover phyllody (green petal) agent transmitted by

Aphrodes bicincta. Canadian Plant Disease Survey 55:66-68.

and D. L. Craig. 1978. Plant and insect age as factors

in the transmission of clover phyllody (green petal) agent to

strawberry by Aphrodes bicinctus. Canadian Journal of Plant

Science 58:467-470.

Christie, J. R. 1943. Spring dwarf and summer dwarf of

strawberries. U.S. Department of Agriculture Circular No.

631, 10 p.

and L. Crossman. 1936. Notes on the strawberry

clover phyllody virus. Canadian Journal of Plant Science

47:141-148.

strains of the bud and leaf nematode, Aphelenchoides

fragariae. Proceedings of the Helminthological Society of

Washington 2:69-72.

87
Clark, M. F. 1981. Immunosorbent assays in plant

pathology. Annual Review of Phytopathology 19:83-106.

and A. N. Adams. 1977. Characteristics of the

microplate method of enzyme-linked immunosorbent assay

for the detection of plant viruses. Journal of General

Virology 34:475-483.

Collins, W. B., and G. T. Morgan. 1958. Green petal of

strawberry in New Brunswick. Plant Disease Reporter

42:339-341.

Converse, R. H. 1969. Occurrence of necrotic shock virus in

the Pacific Northwest. Plant Disease Reporter 53:608-610.

1979. Recommended virus indexing procedures for

new USDA small fruit and grape cultivars. Plant Disease

Reporter 63:848-851.

1981. Infection of cultivated strawberries by tomato

ringspot virus. Phytopathology 71:1149-1152.

and A. B. Bartlett. 1971. Occurrence of strawberry

lethal decline disease in Oregon. Plant Disease Reporter

55:560.

and A. B. Bartlett. 1979. Occurrence of viruses in

some wild Rubus and Rosa species in Oregon. Plant Disease

Reporter 63:441-444.

and R. R. Martin. 1982. Use of the Barbara-Clark

F(ab')2 indirect ELISA test for detection of viruses in small

fruits. Acta Horticulturae 129:21. [Abstract.]

J. Seely, and L. W. Martin. 1979. Evidence for

random local spread of aphid-borne mild yellow-edge virus

in strawberries. Phytopathology 69:142-144.

Comuet, P., and J. D. Morand. 1960. Infection naturelle des

fraisiers {Fragaria spp.) par le virus de la mosaïque du tabac.

Comptes, Rendus Herbdomadaires des Seances de

l'Académie des Sciences de Paris 250:1583-1584.

Costa, A. S., and V. da Costa Lima Neto. 1976. Transmiäo

do virus da necrose branca do fumo por Frankliniella sp.

[Transmission of tobacco streak virus to tobacco by

Frankliniella sp.] IX Congreso Sociedad Brasiliero Fitopatología, I p. [In Portuguese.]

Cousin, M. T., J. P. Moreau, A. Faivre-Amiot and T.

Staron. 1970. Mise en évidence de mycoplasmes dans des

fraisiers attients de la maladie des "Pétales Verts" récemment

signalée en France. Comptes Rendus de l'Académie des

Sciences de Paris 270:2000-2001.

Craig, D. L. 1981. Strawberry cultivar reaction to pallidosis

disease. Canadian Plant Disease Survey 61:41-42.

and H. T. Stultz. 1964. Aphid dissemination of

strawberry viruses in Nova Scotia. Canadian Journal of Plant

Science 44:235-239.

Crock, J. E., C. H. Shanks, Jr. and B. H. Barritt 1982.

Resistance in Fragaria chiloensis and F. X ananassa to the

aphids Chaetosiphon fragaefolii and C. thomasi. HortScience 17:959-960.

and C. H. Shanks, Jr. 1983. Setal variations in clonal

lineages of the strawberry aphids Chaetosiphon fragaefolii

(Cockerell) and C. thomasi (Hille Ris Lambers) (Homoptera:

Aphididae). Annals of the Entomological Society of America

76:225-227.

Cropley, R. C. 1958. Erratic transmission of strawberry

viruses by grafting excised leaves. East Mailing Research

Station, Report for 1957, p. 124-125.

C. E. Ellenberger, and A. Jha. 1960. Strawberry

mottle and apple mosaic viruses in strawberry. East Mailing

Research Station, Report for 1959, p. 96-97.

Crosse, J. E., and R. S. Pitcher. 1952. Studies in the

relationship of eelworms and bacteria to certain plant

diseases. I. The etiology of strawberry cauliflower diseases.

Annals of Applied Biology 39:475-484.

Cutcliffe, J. A., and L. S. Thompson. 1977. Incidence of

green petal disease in strawberry in Prince Edward Island,

1976. Canadian Plant Disease Survey 57:1-2.

Darrow, G. M. 1955. Leaf variegation in strawberry — a

review. Plant Disease Reporter 39:363-370.

Darwin, C. 1896. The variation of animals and plants under

domestication, p. 263-264. Second edition, vol. 2, D.

Appleton, New York, 495 p.

Daubeny, H. A., R. A. Norton, and B. H. Barritt. 1972.

Relative differences in virus tolerance among strawberry

cultivars and selections in the Pacific Northwest. Plant

Disease Reporter 56:792-795.

Davidson, O. W. 1941. Nutrient-deficiency symptoms in

deciduous fruits, p. 191-237. In G. Hambridge, editor.

Hunger signs in crops. American Society of Agronomy and

National Fertilizer Association, Washington, D.C., 390 p.

Davis, M. B., and H. Hill. 1928. Nutritional studies with

Fragaria. Scientific Agriculture 8:681-692.

Delong, D. M. 1931. A revision of the American species of

Empoasca known to occur north of Mexico. U.S. Department of Agriculture Technical Bulletin No. 231, 59 p.

88
Demaree, J. B., and G. M. Darrow. 1937. Leaf variegation

in strawberry not considered a virus disease. Plant Disease

Reporter 21:400-403.

and C. P. Marcus. 1951. Virus diseases of

strawberries in the United States, with special reference to

distribution, indexing, and insect vectors in the East. Plant

Disease Reporter 35:527-537.

Dicker, G. H. L. 1950. The shallot aphid, Myzus ascalonicus

Doncaster, a pest of cultivated strawberries. East Mailing

Research Station Report for 1949, p. 139-140.

Doi, Y., and S. Okuda. 1973. Electron microscopic study of

mycoplasma-like organisms (MLO) in yellows-diseased host

plants. Shokubutsu Byogai Kenkyu 8:203-221. [In

Japanese.] [Abstract in Review of Plant Pathology 53:451,

entry No. 2111, 1974.]

Domes, R. 1957. Eine Abbauerscheinung bei der Erdbeersorte Madame Moutout. Phytopathologische Zeitschrift

31:113-122.

East Mailing Research Station. 1969. Production of

virus-free clones. Annual report for 1968, p. 39.

1970. Production of virus-free clones. Annual report

for 1969, p. 54.

Eastop, V. F., and D. Hille Ris Lambers. 1976. Survey of

the world's aphids. W. Junk, Publishers, The Hague. 537 p.

Eliseeva, Z. N., M. T. Kulikova, and I. S. Slobozhanina.

1974. Virus diseases of strawberries in the Amia Ata

District. Vestnik Sel'skokhozyaistvennoi Nauki Kazakhstana

17:51-54. [In Russian.] [Abstract in Review of Plant

Pathology 53:546 entry No. 2630, 1974.]

Engelbrecht, D. 1967a. Studies on virus diseases of

strawberries in the western Cape Province. I. Degeneration

of locally bred strawberry cultivars. South African Journal of

Agricultural Science 10:345-356.

1967b. Studies on virus diseases of strawberries in

the western Cape Province. II. The latent period of mild

yellow-edge and crinkle viruses in the vector Chaetosiphon

fragaefolii (Ckll.). South African Journal of Agricultural

Science 10:575-582.

Eulensen, J. B. 1981. Differential transmission of strawberry

mottle virus by Chaetosiphon thomasi Hille Ris Lambers and

Chaetosiphon fragaefolii (Cockerell). Master of Science

thesis, Oregon State University, 30 p.

Faccioli, G. 1969. Caratteristiche sintomatologiche e principali proprieta fisiche di un virus isolato da radici di fragola

{Fragaria vesea L.) e della sua variante instabile. [Characteristic symptoms and physical properties of a virus isolated

from roots of strawberry {Fragaria vesea L.) and some of its

unstable variants.] Phytopathologia Mediterránea 8:162-170.

[In Itahan.]

1970. Necrosi della rosetta: Nuova infezione da virus

sulla fragola. [Necrotic rosette: a new virus infecting

strawberry.] Extract of the Proceedings of the Fourth

National Strawberry Conference, Cesena, Italy, May 21-23,

1970, p. 351-355. [In Italian.]

1974. Identificazione e caratteristiche fisico-cimiche

di un ceppo di virus della necrosi della tobacco isolato di

fragola. [Identification and physiochemical characterization

of a tobacco necrosis virus culture isolated from strawberry.]

Phytopathologia Mediterránea 13:71-76. [In Italian.]

Forer, L. B., and R. F. Stouffer. 1982. Xiphinema spp.

associated with tomato ringspot virus infection of Pennsylvania fruit crops. Plant Disease 66:735-736.

Frazier, N. W. 1953. A latent virus of Fragaria vesca. Plant

Disease Reporter 37:606-608.

1955a. Strawberry vein banding virus. Phytopathology 45:307-312.

1955b. Tobacco necrosis virus on strawberries. Plant

Disease Reporter 39:143-147.

1960a. Differential transmission of four strains of

strawberry vein banding virus by four aphid vectors. Plant

Disease Reporter 44:436-437.

1960b. Differential transmission of nineteen variations of strawberry mottle virus by Aphis gossypii Glover.

Plant Disease Reporter 44:12-13.

1963. Strawberry as a possible useful host of rose

viruses. Plant Disease Reporter 47:585-586.

1966a. Nonretention of two semipersistent strawberry biruses through ecdysis by their aphid vector. Phytopathology 56:1318-1319.

1966b. Pseudo mild yellow-edge: A new strawberry

virus disease in the Fragaria virginiana indicator clone M-1.

Phytopathology 56:571-572.

1968a. Transmission of strawberry crinkle virus by

the dark strawberry aphid Chaetosiphon jacobi. Phytopathology 58:165-172.

1968b. Transmission of strawberry mottle virus by

juice and aphids to herbaceous hosts. Plant Disease Reporter

52:64-67.

89
1970a. Strawberry pseudo mild yellow-edge, p.

12-13. /« N. W. Frazier, editor, Virus diseases of small fruits

and grapevines. University of California Division of

Agricultural Sciences, Berkeley, 290 p.

ed. 1970b. Virus diseases of small fruits and

grapevines. University of California, Division of Agricultural Sciences, Berkeley, 290 p.

1974a. Detection of graft-transmissible diseases in

strawberry by a modified leaf grafting technique. Plant

Disease Reporter 58:203-207.

1974b. Six new strawberry indicator clones evaluated for the detection and diagnosis of twelve grafttransmissible diseases. Plant Disease Reporter 58:28-31.

1975a. Possible transmission of strawberry pallidosis

by the leafhopper Coelidia olitoria. Plant Disease Reporter

59:40-41.

and A. F. Posnette. 1957. Transmission and

host-range studies of strawberry green petal virus. Annals of

Applied Biology 45:580-588.

and A. F. Posnette. 1958. Relationships of the

strawberry viruses of England and California. Hilgardia

27:455-514.

and H. H. P. Severin. 1945. Weed-host range of

California aster yellows. Hilgardia 16:621-650.

and L. L. Stubbs. 1969. Pallidosis — A new virus

disease of strawberry. Plant Disease Reporter 53:524-526.

and E. S. Sylvester. 1960. Half-lives of transmissibility of two aphid-borne viruses. Virology 12:233-244.

and H. E. Thomas. 1953. Strawberry: a host of

western aster yellows virus. Plant Disease Reporter 37:272-

275.

1975b. Strawberry mild yellow-edge in North

Carolina. Plant Disease Reporter 59:41-42.

and R. H. Converse. 1980. Strawberry vein banding

virus. Descriptions of plant viruses No. 219. Commonwealth

Mycological Institute and the Association of Applied

Biologists, Kew, Surrey, England.

and H. E. Thomas. 1959. Fate of strawberry plants

infected with aster yellows virus in nursery beds. Plant

Disease Reporter 43:645.

CE. Yarwood, and A. H. Gold. 1961. Yellow-bud

virus endemic along California coast. Plant Disease Reporter

45:649-651.

and D. D. Jensen. 1970. Strawberry, an experimental host of peach Western X-disease. Phytopathology

60:1527-1528.

P. S. Jorgensen, H. E. Thomas, and H. A. Johnson,

Jr. 1962. Necrotic shock — a virus disease of strawberries.

Plant Disease Reporter 46:547-550.

and A. R. Maggenti. 1962. Nematode transmission

of yellow-bud mosaic virus to strawberry. Plant Disease

Reporter 46:303-304.

V. Voth, and R. S. Bringhurst. 1965. Inactivation of

two strawberry viruses in plants grown in a natural

high-temperature environment. Phytopathology 55:1203-

1205.

Freeman, J. A., and F. C. Mellor. 1962. Influence of latent

viruses on vigor, yield and quality of British Sovereign

strawberries. Canadian Journal of Plant Science 42:602-610.

Fulton, J. P. 1952. A tobacco necrosis virus associated with

strawberry plants. Plant Disease Reporter 36:313-314.

and F. C. Mellor. 1970a. Strawberry crinkle, p.

18-23. InN.W. Frazier, editor. Virus diseases of small fruits

and grapevines, University of California, Division of

Agricultural Sciences, Berkeley, 290 p.

and F. C. Mellor. 1970b. Tomato ringspot virus in

strawberry, p. 43-45. In N. W. Frazier; editor. Virus diseases

of small fruits and grapevines. University of California

Division of Agricultural Sciences, Berkeley, 290 p.

and A. F. Posnette. 1956. Leafhopper transmission

of a clover virus causing green petal disease in strawberry.

Nature 177:1040-1041.

1954. A study of virus diseases of strawberry in

Michigan. Ph.D. thesis, Michigan State College, 94 p.

1956. Yearly variations in amount of virus in

Arkansas strawberry fields. Phytopathology 46:12 [Abstract.]

1957a. An evaluation of the use of excised-leaf grafts

in strawberry virus studies. Phytopathology 47:521. [Abstract.]

1957b. Aster yellows virus affecting strawberries in

Arkansas. Plant Disease Reporter 41:521-523.

1960. Strawberry virus dissemination in Arkansas.

Phytopathology 50:477-479.

90
1977. Strawberry viruses. HortScience 12:470-471.

and J. R. McGrew. 1970. Introduction: virus and

viruslike diseases of strawberry, p. 1-4. /« N. W. Frazier,

editor, Virus diseases of small fruits and grapevines.

University of California Division of Agricultural Sciences,

Berkeley, 290 p.

and B. J. Moore. 1982. Strawberry virus dissemination in Arkansas. Plant Disease 66:847-848.

Fulton, R. H. 1954. Studies on inactivation of the strawberry

type 2 viruses in vivo. Phytopathology 44:489.

Fulton, R. W. 1948. Hosts of the tobacco streak virus.

Phytopathology 38:421-428.

1952. Mechanical transmission and properties of rose

mosaic virus. Phytopathology 42:413-416.

1971. Tobacco streak virus. Commonwealth Mycological Institute and the Association of Applied Biologists,

Descriptions of Plant Viruses No. 44, 4 p.

Gilmer, R. M., and E. C. Blodgett. 1976. X-disease, p.

145-157. In T. Pine, editor. Virus diseases and noninfectious

disorders of stone fruits in North America. U.S. Department

of Agriculture, Agriculture Handbook No. 537, 433 p.

Gold, R. E. 1979. Leafhopper vectors and western X

disease, p. 587-602. In K. Maramorosch, and K. F. Harris,

editors, Leafhopper vectors and plant disease agents.

Academic Press, New York, 654 p.

Goto, T., and M. Nemoto. 1974. [Studies on strawberry

virus diseases — Degeneration of strawberry in Hokkaido].

Hokkaido National Agricultural Experiment Station Bulletin

No. 109:97-105. [In Japanese; EngUsh Summary.]

Gourley, C. O. 1955. Green petal of strawberry in Nova

Scotia. Plant Disease Reporter 39:808-809.

C. W. Bishop and D. L. Craig. 1971. Susceptibility

of some strawberry cultivars to green petal. Canadian Plant

Disease Survey 51:129-130.

Granett, A. L., and R. M. Gilmer. 1971. Mycoplasmas

associated with X-disease in various Prunus species.

Phytopathology 61:1036-1037.

Greber, R. S. 1979. Virus diseases of Queensland

strawberries and the epidemiological effects of the strawberry

runner approval scheme. Queensland Journal of Agricultural

and Animal Sciences 36:93-103.

and D. H. Gowanlock. 1979. Rickettsia-like and

mycoplasma-like organisms associated with two yellowstype diseases of strawberries in Queensland. Australian

Journal of Agricultural Science 30:1101-1109.

Grylls, N. E. 1979. Leafhopper vectors and the plant disease

agents they transmit in Australia, p. 179-212. In K.

Maramorosch, and K. Harris, editors, Leafhopper vectors

and plant disease agents. Academic Press, New York, 654 p.

Guba, E. F. 1933. Suspected mosaic of the strawberry.

Phytopathology 23:654-661.

Harmson, E. E. 1934. Onderzoek naar de oorzaak van

ziekzeverschijnselen bij aardbeien. [Research on the cause of

disease symptoms in strawberries.] Tijdschrift over Plantenziekten. 40:137-152. [In Dutch.]

Harris, R. V. 1932. Grafting as a method of investigating a

possible virus disease of the strawberry. Journal of Pomology

and Horticultural Science 10:35-41.

1933. The strawberry "yellow-edge" disease. Journal

of Pomology and Horticultural Science 11:56-76.

1937a. Studies in strawberry virus diseases III.

Transmission experiments with "crinkle," 1935. East Mailing Research Station Report for 1936, p. 211-221.

1937b. Virus diseases in relation to strawberry

cultivation in Great Britain — a synopsis of recent

experiments at East Mailing. East Mailing Research Station

Report for 1936, p. 201-211.

1938. A bibliographical note on the distinction

between mild and severe strawberry crinkle. East Mailing

Research Station, Report for 1937, p. 201-202.

1958. Plant pathology. East Mailing Research

Station, Report for 1957, p. 22-27.

and M. E. King. 1940. Review of research on

strawberry virus diseases, 1932-39. East Mailing Research

Station, Report for 1939, p. 66-68.

and M. E. King. 1942. Studies in strawberry

diseases. V. The use oí Fragaria vesea L. as an indicator of

yellow-edge and crinkle. Journal of Pomology and Horticultural Science 19:227-242.

Harrison, B. D. 1956. Soil transmission of Scottish raspberry

leaf-curl disease. Nature (London) 178:553.

1957. Studies on the host range, properties and mode

of transmission of beet ringspot virus. Annals of Applied

Biology 45:462-472.

91
1958a. Further studies on raspberry ringspot and

tomato black ring, soil-borne viruses that affect raspberry.

Annals of Applied Biology 46:571-584.

1958b. Raspberry yellow dwarf, a soil-borne virus.

Annals of Applied Biology 46:221-229.

1958c. Relationship between beet ringspot, potato

bouquet, and tomato black ring viruses. Journal of General

Microbiology 18:450-460.

1977. Ecology and control of viruses with

soil-inhabiting vectors. Annual Review of Phytopathology

15:331-360.

Huhtanen, D. P., and R. H. Converse. 1971. Temporary

symptom remission of strawberry June Yellows and

witches'-broom by use of oxytetracycline. Phytopathology

61:1137-1139.

Ishiie, T., Y. Doi, K. Yora, and H. Asuyama. 1967.

Suppressive effects of antibiotics of the tetracycline group on

symptom development in mulberry dwarf disease. Annals of

the Phytopathological Society of Japan 33:267-275.

Iwakiri, B., and L. E. Scott. 1951. Mineral deficiency

symptoms of the Temple strawberry grown in sand culture.

Proceedings of the American Society for Horticultural

Science 57:45-52.

and C. H. Cadman. 1969. Role of a dagger nematode

(Xiphinema sp.) in outbreaks of plant diseases caused by

arabis mosaic virus. Nature (London) 184:1624-1626.

W. P. Mowat, and C. E. Taylor. 1961. Transmission

of a strain of tomato black ring virus by Longidorus

elongatus (Nematoda). Virology 14:480-485.

Helms, K. 1962. Strawberry, clover, and pea as hosts of big

bud virus. Australian Journal of Biological Sciences

15:278-281.

Henriques, M., and D. E. Schlegel. 1975. Studies on the

nature of the strawberry pallidosis disease. Proceedings of

the American Phytopathological Society 2:114 [Abstract.]

Hildebrand, A. A. 1939. Notes on mealybug injury on

strawberry, and its resemblance to crinkle. Canadian Journal

of Research Section C, Botanical Sciences 17:205-211.

Hirumi, H., and K. Maramorosch. 1969. Mycoplasma-like

bodies in the salivary glands of insect vectors carrying the

aster yellows agent. Journal of Virology 3:82-84.

Hoagland, D. R., and W. C. Snyder. 1933. Nutrition of

strawberry plants under controlled conditions. Proceedings of

the American Society for Horticultural Science 30:288-294.

Hollebone, J. E., J. T, Medler, and A. C. Hilbrandt. 1966.

The feeding of Empoascafabae (Harris) on broad bean callus

in tissue culture. The Canadian Entomologist 98:1259-1264.

Horn, N. L. 1965. A mottle-type symptom produced on

Fragaria virginiana by virus obtained from commercial

strawberries. Phytopathology 56:1062. [Abstract.]

and R. G. Carver. 1962. Effect of three viruses on

plant production and yields of strawberries. Plant Disease

Reporter 46:762-765.

Home, W. T. 1922. Strawberry troubles. California

Agricultural Experiment Station Report 1921-22:122-123.

Jennings, I. M., and R. F. Nyvall. 1977. Misapplied row

crop herbicides. Iowa Cooperative Extension Service Pamphlet No. 738, 12 p.

Jha, A. 1961. Arabis mosaic virus in strawberry. Journal of

Horticultural Science 36:219-227.

and A. F. Posnette. 1959. Transmission of a virus to

strawberry plants by a nematode {Xiphinema sp.). Nature

(London) 184:962-963.

Johanson, F. D. 1963. Strawberry nutrient deficiency

symptoms. Washington Agricultural Extension Service

Bulletin No. 561, 24 p.

1980. Hunger in strawberries. K. and H. Printers,

Everett, Wash. 37 p.

and R. B. Walker. 1963. Nutrient deficiency and

foliar composition of strawberries. Proceedings of the

American Society for Horticultural Science 83:431-439.

Johnson, F. 1969. Transmission studies of strawberry lethal

decline. Phytopathology 59:1034. [Abstract.]

Johnson, H. A., Jr., R. H. Converse, A. Amorao, and

others. 1984. Seed transmission of tobacco streak virus in

strawberry. Plant Disease 68:390-392.

Jones, A. L., G. R. Hooper, and D. A. Rosenberger. 1974.

Association of mycoplasmalike bodies with little peach and

X-disease. Phytopathology 64:755-756.

Jorgensen, P. A. 1957. Strawberry virus transmission by

insert graft. Plant Disease Reporter 41:1009-1010.

Kacharmazov, V., and N. Izvorska. 1974. The use of tip

meristems of strawberry for producing virus-free plants, p.

25-31. In Virusni bolesti po rasteniyata. Bulgarian Academy

of Science, 1974. Sofia. [In Bulgarian.] [Abstract in Review

of Plant Pathology 55:1027, No. 5284, 1976.]

92
Kaiser, W. J., S. D. Wyatt, and G. R. Pesho. 1982. Natural

hosts and vectors of tobacco streak virus in Eastern

Washington. Phytopathology 72:1508-1512.

Kaname, T. 1975. [Particles discovered in Fragaria vesea

infected with strawberry latent A virus (SLAV) and

strawberry vein banding virus (SVBV)]. Annals of the

Phytopathological Society of Japan 41:288. [Abstract.] [In

Japanese.]

Komuro, Y., M. Iwaki, and T. Makino. 1973. [Occurrence

of tobacco necrosis virus in roots of strawberry collected in

the Watari District of Miyagi Prefecture.] Annals of the

Phytopathological Society of Japan 39:134. [Abstract.] [In

Japanese.]

Krczal, H. 1960. Eine vom Weissklee SLUî Fragaria vesea L.

übertragbare Viróse. Zeitschrift für Pflanzenlcrankheiten

67:599-602.

and K. Kishi. 1973. [On tobacco necrosis virus and

tobacco mosaic virus isolated from strawberries.] Annals of

the Phytopathological Society of Japan 39:134. [Abstract.]

[In Japanese.]

1962. Untersuchungen über den Massenwechsel und

die Bekämpfung der Erdbeerblattlaus Pentatriehopus fragaefolii (Cock.). Anzeiger für Schädlingkunde 35:145-148.

[English summary.]

Kassanis, B. 1970a. Satellite virus. Commonwealth Mycological Institute and the Association of Applied Biologists.

Descriptions of Plant Viruses, No. 15.

1970b. Tobacco necrosis virus. Commonwealth

Mycological Institute and the Association of Applied

Biologists. Descriptions of Plant Viruses, No. 14.

Kelsey, H. P., and W. A. Dayton, editors. 1942.

Standardized plant names. Second edition. J. H. McFarland,

Harrisburg, Pa., 673 p.

Kender, W. J. 1964. Effects of specific viruses, virus

complexes, and nitrogen nutrition on the growth, mineral

composition, and ñowering of strawberry. Proceedings of the

American Society for Horticultural Science 84:302-309.

Kennedy, G. G., E. R. Oatman, and V. Voth. 1976.

Suitability of plictran and pirimor for use in a pest

management program on strawberries in southern California.

Journal of Economic Entomology 69:269-272.

Kennett, R. H., T. J. McKeam, and K. B. Bechtol, editors.

1980. Monoclonal antibodies. Plenum Press, New York,

423 p.

King, T. H., and D. H. von Ruden. 1962. Fragaria

virginiana, an indicator host for strawberry latent A virus.

Plant Disease Reporter 46:772-776.

Kishaba, A. B., V. Voth, A. F. Howland, and others. 1972.

Twospotted spidermite resistance in California strawberries.

Journal of Economic Entomology 65:117-119.

Kitajima, E. W., J. A. Betti, and A. S. Costa. 1971.

Isometric, viruslike particles in leaf tissues oí Fragaria vesea

L. infected with strawberry mottle virus. Ciencia e Cultura

23(5):649-655.

J. A. Betti, and A. S. Costa. 1973. Strawberry vein

1967. Untersuchungen über die Vektorleistungen der

Erdbeerblattlaus Pentatriehopus fragaefolii (Cock.). Übertragungsversuche mit dem strawberry mottle. Mitteilungen

aus der Biologischen Bundesanstalt für Land-und Forstwirtschaft 121:140-145. [English summary.]

1979. Transmission of the strawberry mild yellow

banding virus, a member of the cauliñower mosaic virus

group. Journal of General Virology 20:117-119.

edge and crinkle virus by the strawberry aphid Chaetosiphon

fragaefolii. Acta Horticulturae 95:23-30.

Kronenberg, H. E. 1943. Autoreferaat van de voordracht

voor de Nederlandisch Plantenziektenkundife Vereniging op

28 November 1942 te Amsterdam. Virusziekten in aardbeien. [Report on the lecture before the Netherlands Society

for the Study of Plant Diseases November 28, 1942, at

Amsterdam. Virus diseases in strawberries.] Tijdschrift over

Plantenziekten 49:74-76. [In Dutch.]

Kunkel, L. O. 1926. Studies on aster yellows. American

Journal of Botany 13:646-705.

Lachance, R. O. 1952. Common clover. Floral abnormality.

31st Annual Report of the Canadian Plant Disease Survey,

1951, p. 25.

Lawrence, F. J., and P. W. Miller. 1968. Effects of virus

infection on the strawberry cultivar Northwest. Plant Disease

Reporter 52:811-813.

Leshem, J., G. Loebenstein, E. Cohen, and I. Slomnitzky.

1962. [Degeneration of strawberry in Israel.] Hassadeh

43(2):181-183. [In Hebrew.]

Lineberry, R. A., and L. Burkhart. 1943. Nutrient

deficiencies in the strawberry leaf and fruit. Plant Physiology

18:324-333.

Lister, R. M. 1958. Soil-borne virus diseases in strawberry.

Plant Pathology 7:92-94.

1960a. Occurrence of soil-borne virus diseases of

strawberry in Britain. Plant Pathology 9:102-105.

93
1960b. Soil-borne virus diseases. Scientific Horticulture 14:90-96.

1960c. Strawberries and soil-borne virus diseases.

Agriculture (Her Majesty's Stationery Office) 67:15-29.

1964. Strawberry latent ringspot: a new nematodebome virus. Annals of Applied Biology 54:167-176.

1970. Nematode-bome viruses as pathogens in

strawberry, p. 32-42. In N. W. Frazier, editor, Virus

diseases of small fruits and grapevines. University of

California Division of Agricultural Sciences, Berkeley,

290 p.

and H. Krczal. 1962. Über des Auftreten des

Arabis-Mosaiks bei der Erdbeere in Deutschland. Phytopathologische Zeitschrift 45:190-199.

Liu, S. C. Y. 1957. Biochemical variability, biological

reactions of certain strawberry viruses and their mechanical

transmission. PhD thesis, University of Minnesota, 69 p.

[Dissertation Abstracts 19 (Part 1):613-614. (1958/59).]

Lizafraga, R. E., L. F. Salazar, W. M. Roca, and L.

Schilde-Rentschler. 1980. Elimination of potato spindle

tuber viroid by low temperature and meristem culture.

Phytopathology 70:754-755.

Lockerman, R. H., A. R. Putnam, R. P. Rice, Jr., and W. F.

Meggitt. 1975. Diagnosis and prevention of herbicide injury.

Michigan Cooperative Extension Service Bulletin No. E809,

19 p.

Lott, W. L. 1946. Strawberries need small amounts of Mn

and Zn. North Carolina Agricultural Experiment Station

Annual Report 69, p. 66.

Maassen, H. 1959. Beitrage zur Kenntnis der Erdbeervirosen. Phytopathologische Zeitschrift 36:322-380.

1961. Untersuchungen über ein von Erdbeeren

isoliertes mechanisch übertragbares Nekrosevirus. Phytopathologische Zeitschrift 41:271-282.

and M. Németh. 1961. Das Bandmosaik der

Erdbeere. Phytopathologische Zeitschrift 42:57-61.

Maramorosch, K., E. Shikata, and R. R. Granados. 1968.

Structures resembling mycoplasma in diseased plants and in

insect vectors. Transactions of the New York Academy of

Science 30:841-855.

Markham, P. G., R. Townsend, and K. A. Plaskitt. 1975. A

rickettsialike organism associated with diseased white clover.

Annals of Applied Biology 81:91-93.

Martin, L. W., and R. H. Converse. 1977. Inñuence of

recent and chronic virus infection on strawberry growth and

yield. Phytopathology 67:573-575.

Martin, R. R., and R. H. Converse. 1982a. An improved

buffer for mechanical transmission of viruses from Fragaria

and Rubus. Acta Horticulturae 129:69-74.

R. R., and R. H. Converse. 1982b. Purification,

some properties, and serology of strawberry mild yellowedge virus. Acta Horticulturae 129:75. [Abstract.]

Massée, A. M. 1933. Further observations on the strawberry

mite. East MalHng Research Station, Report for 1932,

20:117-131.

1935. On the transmission of the strawberry virus

"yellow-edge" disease by the strawberry aphid, together with

notes on the strawberry tarsonemid mite. Journal of

Pomology and Horticultural Science 13:39-53.

Matthews, R. E. F. 1979. Classification and nomenclature of

viruses. Intervirology 12:247-248.

1981. Plant virology. Second edition. Chapter 14.

Inactivation, p. 516-560. Academic Press, New York, 897 p.

McGrew, J. R. 1956. Analysis of viruses causing Demaree

and Marcus type 1 and type 2 symptoms in Fragaria vesca.

Plant Disease Reporter 40:173-175.

1958. Reactions of Fragaria seedlings to a single

strawberry virus isolate. Phytopathology 48:462-463. [Abstract.]

1961. Maintenance of virus-free strawberry plants

under nursery and field conditions. Transactions of the

Peninsula Horticultural Society 1960, 50(5):39-43.

1965. Eradication of latent C virus in the Suwannee

variety of strawberry by heat plus excised runner-tip culture.

Phytopathology 55:480-481.

1967. A sensitive strawberry virus indicator clone of

Fragaria vesca from the USSR. Plant Disease Reporter

51:288-290.

1970a. Strawberry feather-leaf, p. 46-47. In N. W.

Frazier, editor. Virus diseases of small fruits and grapevines.

University of California Division of Agricultural Sciences,

Berkeley, 290 p.

1970b. Strawberry latent C. p. 16-18. In N. W.

Frazier, editor. Virus diseases of small fruits and grapevines.

University of California, Division of Agricultural Sciences,

Berkeley, 290 p.

94
1980. Meristem culture for production of virus-free

strawberries, p. 80-85. Proceedings of the conference on

nursery production of fruit plants through tissue culture —

applications and feasibility. U.S. Department of Agriculture,

Science and Education Administration, Northeast Region.

Agricultural Research Results, ARR-NE-11, 119 p.

Miller, P. W. 1951. Studies on the mechanical transmission

of strawberry yellows. Plant Disease Reporter 35:179.

1953. Effect of hot water on virus-infected

strawberry plants and viruses. Plant Disease Reporter

37:609-611.

and A. F. Posnette. 1970. Leafhopper-bome virus

diseases of strawberry, p. 26-32. In N. W. Frazier, editor.

Virus diseases of small fruits and grapevines. University of

Cahfomia, Division of Agricultural Sciences, Berkeley,

290 p.

and D.H. Scott. 1959. Effect of two virus complexes

on the responses of two strawberry varieties. Plant Disease

Reporter 43:385-389.

and D. H. Scott. 1964. The effect of strawberry latent

A virus on growth and fruiting of seven varieties of strawberries. Plant Disease Reporter 48:929-932.

Medler, J. T. 1941. The nature of injury to alfalfa caused by

Empoasca fabae (Harris). Annals of the Entomological

Society of America 34:439-450.

Mellor, F. C, and R. E. Fitzpatrick. 1951. Studies of virus

diseases of strawberries in British Columbia. II. The

separation of the component viruses of yellows. Canadian

Journal of Botany 29:411-420.

and R. E. Fitzpatrick. 1961. Strawberry viruses.

Canadian Plant Disease Survey 41:218-255.

and A. R. Forbes. 1960. Studies of virus diseases of

strawberries in British Columbia. III. Transmission of

strawberry viruses by aphids. Canadian Journal of Botany

38:343-352.

and N. W. Frazier. 1970a. Strawberry mild

yellow-edge, p. 14-16. In N. W. Frazier, editor. Virus

diseases of small fruits and grapevines. University of

California, Division of Agricultural Sciences, Berkeley, 290

Pand N. W. Frazier. 1970b. Strawberry motde, p.

4-8. /« N. W. Frazier, editor. Virus diseases of small fruits

and grapevines. University of California, Division of

Agricultural Sciences, Berkeley, 290 p.

and R. Stace-Smith. 1963. Reaction of strawberry to

a ringspot virus from raspberry. Canadian Journal of Botany

41:865-870.

Miles, P. W. 1972. The saliva of Hemiptera. Advances in

Insect Physiology 9:183-255.

1958. Comparative efficiency of excised leaf petiole

grafts and stolon grafts for transmitting certain strawberry

viruses. Plant Disease Reporter 42:1043-1047.

1959. Outbreak of witches'-broom disease in Puget

Beauty strawberry in Oregon. Plant Disease Reporter

43:996-997.

1960. Rapid degeneration of some strawberry

varieties and selected seedlings infected with latent C virus in

combinations with other viruses. Plant Disease Reporter

44:796-799.

and R. O. Belkengren. 1962. Obtaining virus-free

strawberries by excising and culturing of apical meristem of

plants infected with the yellow-edge, crinkle, and vein

banding viruses and certain other virus complexes. Phytopathology 52:743-744.

and R. O. Belkengren. 1963. Elimination of

yellow-edge, crinkle, and veinbanding viruses and certain

other virus complexes from strawberries by excision and

culturing of apical meristems. Plant Disease Reporter

47:298-300.

and N. W. Frazier. 1970. Strawberry vein banding,

p. 8-10. In N. W. Frazier, editor. Virus diseases of small

fruits and grapevines. University of California, Division of

Agricultural Sciences, Berkeley, 290 p.

and R. E. Garren. 1966. Studies on the inactivation

of strawberry viruses by chemotherapy. Plant Disease

Reporter 50:843-847.

and E. K. Vaughan. 1957. Yellows virus complex in

Marshall strawberry plants not inactivated by growthregulating, antibiotic, and certain other chemicals. Plant

Disease Reporter 41:17-18.

Milne, R. G., and E. Luisoni. 1977. Rapid immune electron

microscopy of vims preparations, p. 265-281. In K.

Maramorosch, and H. Koprowski, editors. Methods in

virology, vol. 6. Academic Press, New York and London,

542 p.

Morgan, G. T. 1965. Effects of strawberry aphid control on

virus spread and yield. Journal of Economic Entomology

58:195-196.

95
Morris, H. E., and M. M. Afanasiev. 1944. Yellows, a

non-infectious disease of the Progressive everbearing strawberry in Montana. Montana State Agricultural Experiment

Station Bulletin 424:1-11.

Morris, T. J., and J. A. Dodds. 1979. Isolation and analysis

of double-stranded RNA from virus-infected plant and fungal

tissue. Phytopathology 69:854-858.

R. H. Mullin, D. E. Schlegel, and others. 1980a.

Isolation of a caulimovirus from strawberry tissue infected

with strawberry vein banding virus. Phytopathology 70:156-

160.

and E. M. Smith. 1977. Potato spindle tuber disease:

procedures for the detection of viroid RNA and certification

of disease-free potato tubers. Phytopathology 67:145-150.

Mullin, R. H., N. W. Frazier, and D. E. Schlegel. 1975.

Meristem culture of Fragaria chiloensis infected with

pallidosis. Plant Disease Reporter 59:268.

N. W. Frazier, and D. E. Schlegel. 1976. Heat

treatment increases the success of strawberry meristem tip

culture. Proceedings of the American Phytopathological

Society 2:116. [Abstract].

T. J. Morris, and D. E. Schlegel. 1980. Current

research on strawberry virus diseases. IV. Experimental

transmission of five strawberry viruses to Sanguisorba

minor, the garden bumet. California Strawberry Advisory

Board, Strawberry News Bulletin 26, No. 14, 2 p.

and D. E. Schlegel. 1976. Cold storage maintenance

of strawberry meristem plantlets. HortScience 11:100-101.

and D. E. Schlegel. 1978. Meristem-tip culture of

dahlia infected with dahlia mosaic virus. Plant Disease

Reporter 62:565-567.

S. H. Smith, N. W. Frazier, and D. E. Schlegel.

1974. Meristem culture frees strawberries of mild yellowedge, pallidosis, and mottle diseases. Phytopathology

64:1425-1429.

Mundinger, F. G. 1946. The control of spittle insects in

strawberry plantings. Journal of Economic Entomology

39:299-305.

Murant, A. F., and C. E. Taylor. 1965. Treatment of soil

with chemicals to prevent transmission of tomato black-ring

and raspberry ringspot viruses by Longidorus elongatus de

Man. Annals of Applied Biology 55:227-237.

Nasu, S., D. D. Jensen, and J. Richardson. 1970. Electron

microscopy of mycoplasma-like bodies associated with insect

and plant hosts of peach western X-disease. Virology

41:583-595.

Nielson, M. W. 1968. The leafhopper vectors of phytopathogenic viruses (Homoptera, Cicadellidae) taxonomy,

biology, and virus transmission. U.S. Department of

Agriculture Technical Bulletin No. 1382, 386 p.

1979. Taxonomic relationships of leafhopper vectors

of plant pathogens, p. 3-23. In K. Maramorosch, and K.

Harris, editors, Leafhopper vectors and plant disease agents.

Academic Press, New York, 654 p.

Nienhaus, F., and R. A. Sikora. 1979. Mycoplasmas,

spiroplasmas, and Rickettsia-like organisms as plant

pathogens. Annual Review of Phytopathology 17:37-58.

Nourriseau, J. G. 1979. Un nouveau dépérissement du

fraisier aux causes indéterminées. Phytoma, 44.

Nyland, G., and D. Engelbrecht. 1958. Symptoms of some

fruit tree virus diseases in strawberry. Phytopathology

48:396. [Abstract.]

and A. C. Goheen. 1969. Heat therapy of virus

diseases of perennial plants. Annual Review of Phytopathology 7:331-354.

Ogilvie, L., T. Swarbrick, and C. R. Thompson. 1934. A

note on a strawberry disease resembling the American

crinkle. Long Ashton Research Station Report for 1933, p.

96-97.

Osterwalder, A. 1928. Die Krauselkrankheit der Erdbeeren.

Schweitzerische Zeitschrift für Obst-und Weinbau 37(23):

395-398.

Owens, R. A., and T. O. Diener. 1981. Sensitive and rapid

diagnosis of potato spindle tuber viroid disease by nucleic

acid hybridization. Science 213:670-671.

Pitcher, R. S., and J. E. Crosse. 1958. Studies in the

relationship of eelworms and bacteria to certain plant

diseases. II. Further analysis of the strawberry cauliñower

disease complex. Nematologia 3:244-256.

Plakidas, A. G. 1926. Strawberry "yellows," a degeneration

disease of the strawberry. Phytopathology 16:423-426.

1927. Strawberry xanthosis (yellows) a new,

insect-borne disease. Journal of Agricultural Research

35:1057-1090.

1929. Report on strawberry virus disease project.

Plant Disease Reporter 13:129-131.

1932. The June Yellows of strawberries. Phytopathology 22:22.

96
1951. Chlorotic phyllody of strawberry. Plant

Disease Reporter 35:495-496.

1964. Strawberry diseases. Louisiana State University Press, Baton Rouge, 195 p.

Poos, R. W., and N. Wheeler. 1943. Studies on host plants

of the leafhoppers of the genus Empoasca. U.S. Department

of Agriculture Technical Bulletin No. 850, 51 p.

Posnette, A. F. 1953a. Green petal, a new virus disease of

strawberries. Plant Pathology 2:17.

1953b. Heat inactivation of strawberry viruses.

Nature (London) 169:837-838.

1956. Strawberry mosaic virus disease. East Mailing

Research Station, Report for 1955, p. 120.

and R. Cropley. 1958. Heat treatment for the

inactivation of strawberry viruses. Journal of Horticultural

Science 33:282-288.

and C. E. Ellenberger. 1963. Further studies of green

petal and other leafhopper-transmitted viruses infecting

strawberry and clover. Annals of Applied Biology 51:69-83.

and A. Jha. 1960. The use of cuttings and heat

treatment to obtain virus-free strawberry plants. East Mailing

Research Station, Report for 1959, p. 98.

and W. E. Manwell. 1971. Fragaria species

susceptible to arabis mosaic virus. East Mailing Research

Station, Report for 1970, p. 120-122.

Prentice, L W. 1946. Resolution and synthesis of virus

complexes causing strawberry yellow-edge. Nature (London)

158:24.

1948. Resolution of strawberry virus complexes IL

Virus 2 (mild yellow-edge virus). Annals of Applied Biology

35:279-289.

1949. Resolution of strawberry virus complexes. IIL

The isolation and some properties of virus 3. Annals of

Applied Biology 36:18-25.

1952. Resolution of strawberry virus complexes. V.

Experiments with viruses 4 and 5. Annals of Applied Biology

39:487-494.

and R. V. Harris. 1946. Resolution of strawberry

virus complexes by means of the aphid vector Capitophorus

fragariae Theb. Annals of AppUed Biology 33:50-53.

and T. M. Woollcombe. 1951. Resolution of

Price, W. C. 1940. Comparative host ranges of six plant

viruses. American Journal of Botany 27:530-541.

Razvyazkina, G. M. 1960. [Strawberry green-petal virus and

its dissemination.] Moscow Journal of Agricultural Sciences

5:139-140. [In Russian, with English summary.]

Reed, H. E., and E. L. Felix. 1961. Late symptom

expression in strawberry virus indexing. Phytopathology

51:645. [Abstract.]

Reid, R. D. 1951. June Yellows in Climax plants. The

Fruit-Grower 2894:1056-1057.

Richardson, C. W. 1920. Some notes on Fragaria. Journal

of Genetics 10:39-46.

1923. Notes on Fragaria, Journal of Genetics

13:147-152.

Richardson, J., N. W. Frazier, and E. S. Sylvester, 1972.

Rhabdoviruslike particles associated with strawberry crinkle

virus. Phytopathology 62:491-492.

Ritzema Bos, I. 1890. De Bloemkoolziekte der aardbeien,

veroorzaakt door Aphelenchus fragariae nov. spec. [Strawberry cauliflower disease, caused by Aphelenchusfragariae,

new species.] Maandblad Natuurwetenschappen 16:107-117.

[In Dutch.]

Rorie, F. G. 1957. Resolution of certain strawberry viruses

by the aphid vector Capitophorus minor Forbes. Plant

Disease Reporter 41:683-689.

Savzdarg, E. E. 1957. [Ways of freeing berry fruits from

mites in relation to peculiarities of their biology and

ecology.] Izvestiya Timiryazevsk. SeLskokhoz. Acad.

1(14):5-17. [In Russian.]

Schaefers, G. A. 1963. Seasonal densities and control of the

cyclamen mite, Steneotarsonemus pallidus (Acarina:Tarsonemidae) on strawberry in New York. Journal of Economic

Entomology 56:565-571.

1980. Yield effects of tarnished plant bug feeding on

June-bearing strawberry varieties in New York State. Journal

of Economic Entomology 73:721-725.

strawberry virus complexes. IV. The latent period of virus 3

in the vector. Annals of Applied Biology 38:389-394.

1981. Pest management systems for strawberry

insects, p. 377-393. In D. Pimentel, editor, C.R.C.

handbook of pest management in agriculture. Vol. 3,

C.R.C. Press, Boca Raton, Fla., 656 p.

Schöniger, G. 1958. Erdbeervirosen in Deutschland. III. Das

Erdbeer-Nekrosevirus: Ein weiteres nichtpersistentes Virus.

Phytopathologische Zeitschrift 32:325-332.

97
and R. Bauer. 1955. Erdbeervirosen in Deutschland

I. Befund nach Propfung verschiedener Sorten mif Fragaria

vesca L. Phytopathologische Zeitschrift 23:443-454.

Schwartze, C. D., and N. W. Frazier. 1964. Lethal decline,

a graft-transmissible disease of strawberry. Plant Disease

Reporter 48:833-836.

Skroch, W. A., and T. J. Sheets. 1977. Herbicide injury

symptoms and diagnosis. North Carolina Cooperative

Extension Service Publication Ag 85, 31 p.

Slack, D. A. 1952. Dodder transmission of a virus from

X-diseased peach and sand cherry. Phytopathology 42:475.

[Abstract.]

and N. W. Frazier. 1970. Lethal dechne of

strawberry, p. 50-51. In N. W. Frazier, editor, Virus

diseases of small fruits and grapevines. University of

California, Division of Agricultural Sciences, Berkeley,

290 p.

Sehgal, O. P., and D. M. Boone. 1963. Multiplier disease of

strawberry in Wisconsin. Plant Disease Reporter 47:46-48.

Shanks, C. H., Jr. 1965. Seasonal populations of the

strawberry aphid, and transmission of strawberry viruses in

the field in relation to virus control in western Washington.

Journal of Economic Entomology 38:316-322.

and P. C. Crandall. 1969. Effect of aphid transmitted

viruses on the strawberry cultivars Northwest and Columbia.

Plant Disease Reporter 53:639-640.

and B. Finnigan. 1970. Probing behavior of the

strawberry aphid. Annals of the Entomological Society of

America 63:734-737.

Shanmuganathan, N., and R. G. Garrett. 1976. Little leaf of

strawberry. Australian Plant Pathology Society Newsletter 5

(Suppl.) Abstract 83.

Shear, C. B., H. L. Crane, and A. T. Myers. 1948.

Nutrient-element balance: Application of the concept to the

interpretation of foliar analysis. Proceedings of the American

Society for Horticultural Science 51:319-326.

Sinha, R. C, and Y. C. Paliwal. 1969. Association,

development, and growth cycle of mycoplasma-like organisms in plants affected with clover phyllody. Virology

39:759-767.

and Y. C. Paliwal. 1970. Localization of a

mycoplasma-like organism in tissues of a leafhopper vector

carrying clover phyllody agent. Virology 40:664-672.

and E. A. Peterson. 1972. Uptake and persistence of

oxytetracycline in aster plants and vector leafhoppers in

relation to inhibition of clover phyllody agent. Phytopathology 62:377-383.

Skiles, R. L., and T. H. King. 1952. Strawberry stunt virus

in Fragaria vesca. Plant Disease Reporter 36:406-407.

C. Seymour, H. Fields, and J. P. Fulton. 1957.

Summer dwarf of strawberry. Plant Disease Reporter

41:398-401.

Smeets, L., and L. M. Wassenaar. 1956. Problems of heat

spot in Fragaria vesca L. when indexing strawberry

selections for viruses. Euphytica 5:51-54.

Smith, F. 1933. The cyclamen mite and broad mite and their

control. U.S. Department of Agriculture Circular No. 301,

13 p.

Smith, H. E. 1952. Aphid transmission of strawberry viruses

from commercial plants to Fragaria vesca L. (East Mailing

clone). Phytopathology 42:20. [Abstract.]

1954. New strawberry disease in Arkansas. Plant

Disease Reporter 38:630-631.

and J. D. Moore. 1952. Dodder transmission of

strawberry viruses. Phytopathology 42:20. [Abstract.]

Smith, K. M. 1946. Tomato black ring: a new virus disease.

Parasitology 37:126-130.

and R. Markham. 1944. Two new viruses affecting

tobacco and other plants. Phytopathology 34:324-329.

Smith, L. M., and E. V. Goldsmith. 1936. The cyclamen

mite, Tarsonemus pallidus and its control on field strawberries. Hilgardia 10:53-94.

Smith, M. C, and S. C. Harland. 1958. Can this mean

Climax free of yellows? Grower and Prepacker 49:549-550.

Smith, P. R., R. N. Campbell, and P. R. Fry. 1969. Root

discharge and soil survival of viruses. Phytopathology

59:1678-1687.

Southey, J. F. 1978. Plant Nematology. Ministry of

Agriculture, Fisheries and Food. Her Majesty's Stationery

Office, London. 440 p.

Spiegel, S., R. H. Converse, B. Raccah, and others. 1981.

Virus diseases in strawberries. Phytoparasitica 9(3):253.

Stace-Smith, R. 1961. Studies on Rubus virus diseases in

British Columbia. VIL Raspberry vein chlorosis. Canadian

Journal of Botany 35:559-565.

98
1970. Tomato ringspot virus. Commonwealth

Mycological Institute and the Association of Applied

Biologists, Descriptions of Plant Viruses, No. 18.

and N. W. Frazier. 1971. Tobacco streak virus

isolated from strawberry infected with necrotic shock.

Phytopathology 61:757-758.

and F. C. Mellor. 1957. Studies on Rubus virus

diseases in British Columbia. IV. Transmission of raspberry

mosaic viruses to Fragaria vesea L. Canadian Journal of

Botany 35:287-290.

Staunton, W. P., and J. F. Moore. 1967. The occurrence of

arabis mosaic virus and its nematode vector Xiphinema

diversicaudatum in Ireland. Irish Journal of Agricultural

Research 6:121-122.

Stevens, N. E. 1933. Leaf variegation appears in the

Blakemore strawberry. Plant Disease Reporter 17:145-147.

Stingl, H., and T. H. King. 1965a. Influence of temperature

on mild mottle and veinbanding in Fragaria vesca and

Fragaria virginiana. Phytopathology 55:919-922.

and T. H. King. 1965b. Vein necrosis: A new virus

disease of strawberry. Phytopathology 55:1269-1276.

Stubbs, L. L. 1968. Lethal yellows disease of strawberry.

Australian Plant Disease Recorder 20:33-34.

Stultz, H. T., and A. A. MacNab. 1970. Incidence of green

petal disease in cultivated strawberry in the Maritime

Provinces in 1967. Canadian Plant Disease Survey 50:46-47.

Sutherland, D. W. S., chairman. 1978. Common names of

insects and related organisms. Entomological Society of

America, 132 p.

Swartz, H. J., G. J. Galletta, and R. H. Zimmerman. 1981.

Field performance and phenotypic stability of tissue

culture-propagated strawberries. Journal of the American

Society for Horticultural Science 106:667-673.

Sylvester, E. S., N. W. Frazier, and J. Richardson. 1976.

Strawberry crinkle virus. Commonwealth Mycological Institute and the Association of Applied Biologists, Descriptions

of Plant Viruses No. 163, 4 p.

and J. Richardson. 1981. Inoculation of the aphids

Hyperomyzus lactucae and Chaetosiphon jacobi with isolates

of sowthistle yellow vein virus and strawberry crinkle virus.

Phytopathology 71:598-602.

J. Richardson, and N. W. Frazier. 1974. Serial

passage of strawberry crinkle virus in the aphid Chaetosiphon

jacobi. Virology 59:301-306.

Szilágyi, K. 1980. Small fruit cultivation in Hungary. Acta

Horticulturae 95:21-22.

Takai, T. 1973. Studies on strawberry virus diseases in

Japan. Bulletin of Horticultural Research Station (Ministry of

Agriculture and Forestry) Series C (Morioka) No. 8, 59-104.

Taylor, C. E. 1962. Transmission of raspberry ringspot virus

by Longidorus elongatus de Man (Nematoda:Dorylaimoidea). Virology 17:493-494.

Teakle, D. S. 1962. Necrotic symptoms of tobacco necrosis

virus in roots. Phytopathology 52:1037-1040.

Téliz, D., R. G. Grogan, and G. F. Lownsbery. 1966.

Transmission of tomato ringspot, peach yellow-bud mosaic,

and grape yellow-vein viruses by Xiphinema americanum.

Phytopathology 56:658-663.

Thomas, H. E. 1949. The strawberry virus complex.

Phytopathology 39:863. [Abstract.]

Thomason, I. J., and M. McKenry. 1975. Chemical control

of nematode vectors of plant viruses, p. 423-439. In F.

Lamberti, C. E. Taylor, and J. W. Seinhorst, editors,

Nematode vectors of plant viruses. NATO Advanced Study

Institutes Series A: Life Sciences, vol. 2, Plenum Press,

London, 460 p.

Thompson, L. S. 1968. Strawberry green petal virus

transmission in the field. Plant Disease Reporter 52:393-394.

and J. A. Cutcliffe. 1972. Incidence of green petal

disease in some strawberry cultivars and selections in Prince

Edward Island, 1970-71. Canadian Plant Disease Survey

52:4-5.

J. A. Cutcliffe, CO. Gourley, and R. A. Murray.

1973. Evaluation of several insecticides for control of

strawberry green petal disease. Canadian Plant Disease

Survey 53:16-18.

Thomberry, H. H., A. E. Vatter, and D. M. Beeson. 1951.

Virus-like particles in strawberry plants with foliar variegation. Phytopathology 41:35.

Ulrich, A., M. A. E. Mostata, and W. W. Allen. 1980.

Strawberry deficiency symptoms: a visual and plant analysis

guide to fertilization. University of California Division of

Agricultural Sciences, No. 4098, Berkeley, Calif., 58 p.

Van Eyndhoven, G. L., and H. Groenwald. 1959. On the

morphology of Steneotarsonemus pallidus and S. fragariae

(Acarina:Tarsonemidae). Entomologische Berichten

19:123-124.

99
Vaughan, E. K. 1933. Transmission of the "crinkle" disease

of strawberry. Phytopathology 23:738-740.

and H. W. Wiedman. 1955. A disease of strawberry

caused by a virus from red raspberry. Plant Disease Reporter

39:893-895.

Vine, S. J. 1968. Improved culture of apical tissues for

production of virus-free strawberries. Journal of Horticultural

Science 43:293-297.

Whitcomb, R. F., and R. E. Davis. 1970. Mycoplasma and

phytarboviruses as plant pathogens persistently transmitted

by insects. Annual Review of Entomology 15:405-464.

White, P. R. 1943. A handbook of plant tissue culture.

Jacques Cattell Press, Lancaster, Pa., 277 p.

Whitehead, T., and C. A. Wood. 1946. Virus diseases of the

strawberry. I. The field problem in North Wales. Journal of

Pomology 22:119-133.

WilHams, H. 1955. June Yellows: a genetic disease of the

strawberries. Journal of Genetics 53:232-243.

Wills, A. B. 1962. Genetical aspects of strawberry June

Yellows. Heredity 17:361-372.

Wood, C. A., and T. Whitehead. 1947. Etiology of

strawberry virus diseases. Nature (London) 160:761-762.

Yankulova, M., and K. Schmelzer. 1974. [Determination of

a mechanically transmitted strawberry virus in Bulgaria.] In

Virusni bolesti po rasteniyata. Bulgarian Academy of

Science (1974), p. 33-42, Sofia. [In Bulgarian.] [Abstract in

Review of Plant Pathology 55:1027 (No. 5285), 1976.]

Yarish, W. 1980. A field guide to recognizing herbicide

action and injury. Alberta Agriculture. (Canada) Agdex

641-7, 58 p.

Zeller, S. M. 1927. Preliminary studies on witches'-broom

of strawberry. Phytopathology 18:329-335.

1933. Crinkle disease of strawberry. Oregon State

Agricultural Experiment Station Bulletin No. 319, 14 p.

and E. K. Vaughan. 1932. Crinkle disease of

strawberry. Phytopathology 22:709-713.

Willis, C. B., and L. S. Thompson. 1966. Observations on

strawberry green petal in Prince Edward Island. Canadian

Plant Disease Survey 46:137.

. and L. E. Weaver. 1941. Stunt disease of strawberry.

Phytopathology 31:849-851.

100
^M

(Section 2

[^7. V- Virus and Viruslike Diseases of Vaccinium

(Blueberry and Cranberry)

/

Introduction i

By D. C.|Ramsdell, J. F.^iancock, and A. WJStretch

History of Blueberry and Cranberry Culture

Blueberries and cranberries belong to the genus Vaccinium in

the heath family Ericaceae. There are several agriculturally

important subgenera in Vaccinium, including Cyanococcus

(true blueberries), Oxycoccus (cranberries), and Euvaccinium

(bilberries and whortleberries). Members of all these

subgenera grow wild in North America, whereas only

Oxycoccus and Euvaccinium occur naturally on the European

continent.

The berries of numerous Vaccinium species have been

harvested from the wild by humans since early history, but

only a few species have been extensively cultivated. The most

important species, according to Camp's (1945) classification

system, are highbush (V. corymbosum L. and V. australe

Small), lowbush {V. angustilfolium Ait.), rabbiteye (V. ashei

Reade), and cranberry (V. macrocarpon Ait.). Others

cultivated to a limited extent in North America or harvested

from the wild are dryland (V. altomontanum Ashe and V.

pallidum Ait.), evergreen (V. ovatum Pursh), mountain {V.

membranaceum Dougl.), Canada (V. myrtilloides Michx.),

and Constable's {V. constablaei A. Gray). In Europe, three

additional species are harvested from the wild—bilberry {V.

myrtillus L.), cowberry (V. vitis idaea L.), and European

cranberry {V. oxycoccus L.).

The cranberry V. macrocarpon has been cultivated in North

America since the early 19th century. Commercial production

began in the Cape Cod region of Massachusetts, and it has

since spread to other parts of Massachusetts, Wisconsin, New

Jersey, Washington, and Oregon. Originally, wild selections

made up most ofthe cranberry acreage, but improved cultivars

now dominate most of the production regions. Massachusetts

and Wisconsin produce the most cranberries.

The lowbush blueberry (V. angustifolium) has been cultivated

in the Northeastern United States since the middle of the 19th

century. The major lowbush blueberry regions are still in the

Northeastern United States and Eastern Canada, although

limited acreages are also in Wisconsin, Minnesota, West

Virginia, and Michigan. Most of the lowbush production is

based on native plants growing on their original location,

however, lowbush blueberry cultivars have been planted on a

very limited scale.

The highbush blueberry (primarily V. corymbosum) has only

been widely cultivated for the last 50 yr. The first serious

efforts were made in the early 1900's by F. W. Coville of the

U.S. Department of Agriculture and Elizabeth C. White at

Whitesbog, N.J. Today, in 1982, the most important

highbush blueberry regions in North America are located in

Michigan and New Jersey. North Carolina, British Columbia, Oregon, and Washington also have significant

acreages, and Arkansas has a small but growing industry.

Most of the highbush blueberry acreage is now composed of

hybrid selections, although approximately 10% of the

cultivated blueberries in Michigan is the wild selection

'Rubel'.

Rabbiteye blueberries (V. ashei) have been cultivated for a

shorter period of time than any of the other domesticated

Vaccinium species. Until recently, cultivation was limited to

plants transplanted from the wild in restricted areas of Florida,

Georgia, and Alabama, but improved cultivars have been

developed in the last 30 yr which have resulted in some

expansion within the Southeastern United States and into other

States, including Texas and Arkansas.

Outside of the United States and Canada, blueberry and

cranberry cultivation has been limited. Highbush blueberries

have been planted to some extent in Europe in the last 20 yrs,

but the cranberry (V. macrocarpon) is still quite rare. Most of

the Vaccinium berries eaten in Europe are shipped from North

America or are harvested from wild populations of native

species.

Virus and Viruslike Diseases of Blueberry and Cranberry

A considerable amount of knowledge concerning Vaccinium

virus and viruslike diseases (especially blueberry) and their

etiology has been developed since the writing of "Virus

Diseases of Small Fruits and Grapevines" (Frazier 1970).

Further knowledge of virus-vector relationships has also been

advanced during this period.

The viral etiology of blueberry shoestring has been well

documented. The virus has been thoroughly characterized and

an aphid vector identified (Lesney et al. 1978; Ramsdell

7979; Ramsdell and Stace-Smith 1979b).

Mycoplasmalike organisms (MLO) have been associated

with blueberry stunt (Chen 1971; Hartmann et al. 1973).

blueberry witches'-broom (Kegler et al. 1973; Blattny and

Vana 1974; de Leeuw 1975), and cranberry false blossom

(Chen 1971). Leafhopper vector(s) for each of these diseases

have been strongly implicated or proved.

Three new virus diseases of highbush blueberry and their

causes have been reported as having nematode vectors or

putative nematode vectors since the 1970 book was published.

101
A new disease called blueberry leaf mottle has been described

(Ramsdell and Stace-Smith 1979a), and the virus has been

characterized (Ramsdell and Stace-Smith 1981). Although the

physical and chemical properties of the virus indicate that it is

a putative member of the nepovirus group (Harrison and

Murant 1977), nematode transmission has not been proven as

of this writing (D. C. Ramsdell, unpublished data). Peach

rosette mosaic virus has been shown under experimental field

conditions to cause disease in two blueberry cultivars

(Ramsdell and Gillett 1981). Tomato ringspot virus has been

shown to be associated with a disease of highbush blueberry,

showing symptoms somewhat similar to those of necrotic

ringspot disease (Johnson 7972).

The causal agent and vector of blueberry mosaic remain

unknown. Red ringspot disease has recently been shown to

be associated with a large spherical virus embedded in

inclusion bodies (Kim et al. 1981). The vector has not yet

been identified for this virus. Similar virions and inclusion

bodies have been associated with ringspot disease of

cranberry, indicating that these two diseases may have a

common causal agent (K. S. Kim, unpublished data).

Although rabbiteye blueberry is being planted in significant

quantities in Southeastern United States, to date the only

reports of virus or viruslike diseases occurring in this

blueberry type show that blueberry stunt can be experimentally graft transmitted to it (Dale and Mainland 1981; R. M.

Milholland, unpublished data).

Whereas in a previous review of this field, "Minor Virus

Diseases of Ericaceae in Europe" and "Leaf-Spotting Diseases

of Low-Bush Blueberry" were covered as subjects (Frazier

7970), these will not be covered in this handbook because of

their relative lack of importance.

Indexing and Detection Procedures

For detection and indexing of blueberry viruses for which

antisera exist, enzyme-linked immunosorbent assay (ELISA)

may be used successfully. ELISA works very well in the

detection of blueberry shoestring virus, tobacco ringspot virus

(necrotic ringspot disease), tomato ringspot virus, peach

rosette mosaic virus, and blueberry leaf mottle virus.

Alternatively, all of the previously fisted viruses, with the

exception of blueberry shoestring virus, are sap-transmissible

to herbaceous indicator hosts, the two most useful being

Chenopodium quinoa Willd. and cucumber (Cucumis sativas

L.). A small amount of young terminal leaf tissue should be

taken from several locations on a bush to be indexed. The

tissue should be ground in a small amount (2-3 ml) of 0.05 M

phosphate buffer (ph 7.2) containing 2 to 3% nicotine

alkaloid, using a mortar and pestle. The resulting sap-buffer

mixture is then rub-inoculated to leaves of the herbaceous

plants that have been previously dusted with 300 to 600 mesh

carborundum or diatomaceous earth. After 7 to 14 days,

symptom-bearing leaves can be collected, sap expressed, and

tested with agar gel double diffusion serology plates, using

antisera to the previously listed viruses.

For blueberry mosaic, stunt disease, and witches'-broom, for

which no antisera are available, and red ringspot virus [for

which serological detection methods are in the process of

being developed (D. C. Ramsdell, unpublished data)],

budding or whip grafting techniques to sensitive blueberry

cultivars (see below) offer the best method of detection.

Alternatively, for detection of stunt and witches'-broom,

electron microscopy of ultrathin sections could be used to

detect the MLO in the sieve tubes of diseased leaf tissue

although this is a slow, costly method.

For stunt and mosaic diseases, chip budding or whip grafting

from dormant diseased or suspected diseased cultivars onto

healthy 'Cabot' highbush blueberry is effective. A 2-yr

observation period is necessary to allow symptoms to develop.

For red ringspot disease, chip budding or whip grafting onto

healthy 'Blueray', 'Cabot', or 'Darrow' is effective. Again, a

2-yr observation period is advisable (A. W. Stretch,

unpublished data).

For detection of cranberry viruses and MLO, no serological

methods are available. Because of their thin and wiry stems,

cranberries are not suitable subjects for graft transmission.

Until better detection techniques are developed, electron

microscopy of suspected diseased tissue could be used for the

detection of false blossom MLO in sieve tubes from ultrathin

sections of leaf tissue. For detection of ringspot of cranberry,

observation of symptoms on the crop plants is the only

available method.

Certification Programs

At present (1982), no program exists for growing virus-tested

certified clean stock. Michigan and New Jersey have nursery

inspection programs, but symptomless or latent infections are

missed without the requisite indexing to assume freedom of

infection from virus and viruslike entities. Arkansas with its

fledgling blueberry industry is promulgating a mother block

system of growing inspected stock (J. P. Fulton, personal

communication). North Carolina has developed a system of

combating stunt by indexing their cultivars on 'Cabot' and

keeping their clean "nuclear" stock in screenhouses for a

source of expansion stock to be grown in the field without a

screenhouse for 1 yr. This is then sold as "registered" stock

(R. M. Milholland, personal communication).

The recent expansion of research on Vaccinium virus diseases

by USDA, ARS, at Corvallis, Oreg., has given impetus to

develop a stringent thermotherapy, indexing, and certification

program, involving most commonly used blueberry cultivars.

This program will be a joint effort between the USDA, the

North American Blueberry Council, and research and

regulatory personnel from Michigan, New Jersey, Oregon,

and Washington (R. H. Converse, personnel communication). This program should result in the orderly distribution

of clean, true-to-name cultivars of blueberry stock, which

can then be expanded by nurseries in the various States.

Thereafter, it is expected that appropriate personnel in those

States will ensure that such stock remains clean.

102
Aphid-borne Diseases

^^i.

Blueberry Shoestring ;

By D. C.[Ramsdell By

Additional Common Names

None

History and Geographic Distribution

The disease in highbush blueberry {Vaccinium corymbosum

L.) was described by Hutchinson (1950) and later was shown

by Vamey (1957) to be of virus or viruslike etiology. The

disease is most prevalent in Michigan and New Jersey and has

been found in Washington (P. Bristow, and D. C. Ramsdell,

unpublished data) and North Carolina (R. M. Milholland,

unpublished data). A recent survey for the disease in Oregon

failed to show its occurrence there (Converse and Ramsdell

1982). The disease has been reported in Nova Scotia (Lockhart

and Hall 7962) in lowbush blueberry (Vaccinium angustifolium Ait.). There have been no reports of shoestring in

blueberries from other parts of the world.

Economic Importance

Shoestring virus in Michigan has infected about 145,000

plants on 10,000 acres and has caused a loss of approximately

$3 million (D. C. Ramsdell, unpublished data). Economic loss

in New Jersey is not as great as in Michigan, but it is

substantial.

Symptoms on Natural and Experimental Hosts

On highbush blueberry, there are several symptoms. The most

prominent symptom consists of elongated (0.2 x 1.2 cm)

reddish streaks on current year and 1-yr-old stems (fig. 119),

especially on the side exposed to the sun. At

blossom time, some petals will exhibit red streaks (fig. 120).

Affected leaves are straplike (shoestring symptom, fig. 121),

curled, or crescent shaped. Many leaves on a bush may be

found with this symptom, or it may show on only as few as one

or two shoots near the crown. A few leaves may show red vein

banding or reddish streaking along the midrib and, on

occasion, oak leaf patterns. Immature berries on infected

bushes may develop a premature reddish-purple cast (fig.

122). Shoestring disease has been observed in highbush cvs.

'Blueray', 'Burlington', 'Coville', 'Earliblue', 'Jersey',

'June', 'Rancocas', 'Rubel', and 'Weymouth'. Cvs. 'Bluecrop' and 'Atlantic' possess field immunity. Yield of infected

bushes is greatly decreased. Bushes become progressively

diseased along a row. Missing bushes in such a pattern are

typical of shoestring infection (fig. 123). Healthy bushes

replanted in a field with disease show symptoms after about 4

yrs.

There are no known herbaceous hosts (Lesney et al. 1978).

Figure 119.—A current-year stem of cv. 'Jersey'

showing elongated reddish streaks typically caused by

shoestring disease.

Figure 120.—Blossom streaking symptoms (arrow)

often associated with shoestring disease.

103
Figure 121.—Leaf-strapping symptom on cv. 'Jersey'

caused by shoestring disease.

Figure 122.—Red or purple fruit coloration symptom

associated witii shoestring infection.

Natural and Experimental Transmission

Natural transmission: Natural transmission in highbush

blueberry is by the blueberry aphid, Illinoia pepperi

(MacGillivray) (D. C. Ramsdell, unpublished data). Spread

in the field is from bush to bush and is not a random

phenomenon according to mathematical analysis of spread

(Lesney et al. I97H). Nematode vectors (Xiphinema spp.) are

not associated with the disease, and pollen does not contain

the virus (D.C. Ramsdell, unpublished data; Lesney et al.

1978). The initial mode of spread is through infected,

vegetatively propagated planting stock. After the stock is

planted, transmission from infected bushes is mediated by the

blueberry aphid.

Experimental transmission: Only blueberry seedlings and

young, lush, vegetatively propagated woody cuttings will

become infected when rub-inoculated with purified virus.

Rub inoculation of lush blueberry seedlings or rooted cuttings

of a susceptible cultivar, for example, 'Jersey', with purified

virus will result in transmission and disease symptoms within

5 or 6 mo (Lesney et al. 1978). Chip budding and whip

grafting from diseased plants to healthy small 'Jersey' bushes

will produce symptoms within 1 yr (Varney 1957).

Properties of the Causal Agent

Blueberry shoestring virus (BBSSV) is not a member of any

recognized virus group. It is a single component, isometric

virus with a diameter of 27 nm (Ramsdell and Stace-Smith

1979b; Ramsdell 1979). The virus sediments at 120 5 and

contains single-stranded RNA that makes up 20% of the

molecular weight of the virion. Molecular weights of the RNA

and protein subunit are 1.45 x 10" and 30,000 daltons,

respectively. In ultrathin sections of infected leaf tissue,

viruslike particles were found in epidermal, palisade, and

mesophyll cells (Hartmann et al. 1973). Particles were found

in xylem, but not in phloem cells. Epidermal leaf cells and root

xylem cells contained crystalline arrays of particles.

Detection and Identification

Although BBSSV is a good immunogen and antisera are

available, agar gel diffusion tests of triturated, infected

blueberry tissue do not detect the virus. However, enzymelinked immunosorbent assay (ELISA) (Ramsdell and StaceSmith 7979b) will readily detect the virus in symptomless

tissue. Blossom tissue possesses the highest virus titer for the

purpose of detection, but young leaf tissue works well also.

Bushes should be sampled thoroughly, that is, a half-dozen

samples taken from various locations on a bush. The virus is

unequally distributed in infected bushes (D. C. Ramsdell,

unpublished data). The time of year for sampling is not

critical, as long as sampling is thorough.

Control Procedures

Roguing by itself has not proven to be a successful means of

control. A combination of thorough roguing of symptombearing bushes, followed by a rigorous insecticide-based

aphid control program using an airblast ground sprayer.

104
Figure 123.—Typical pattern of shoestring spread in the

field. The disease progresses from bush to bush along

the row. (Note missing bushes below arrow).

appears to be the best method to halt significant further spread

in a field showing disease. If a field is sufficiently diseased so

as to be uneconomical, complete removal of bushes followed

by replanting with an immune cultivar, for example,

'Bluecrop', would be the best strategy; however, ifsusceptible

cultivars must be grown, then a thorough aphid vector control

program would be necessary.

No information has been developed for thermotherapy.

105
Leafhopper-Borne Diseases

V

i^^

Blueberry Stunt// ,

By D. C.JRanisdell and A. W.jStretch

Additional Common Names

None

History and Geographic Distribution

The viruslike nature of stunt was first described by Wilcox

{1942). Stunt was first observed in New Jersey, but is now

known to exist in eastern Canada, Maine, Massachusetts, New

Hampshire, New York, Michigan, North CaroHna, Pennsylvania, Maryland, Virginia, and most recently in Arkansas

(Gocio and Dale 1982).

Economic Importance

Stunt can cause severe yield reduction in the most susceptible

cultivars. In northern areas with cold winters, for example,

Michigan, the disease is not present in epidemic proportions.

The disease is relatively more serious in New Jersey. In these

two States, roguing diseased bushes and insecticidal control of

the sharp-nosed leafhopper ScapZ/y/opiMS magdalensis (Prov.)

have been effective control strategies.

Symptoms on Natural and Experimental Hosts

All cultivars of highbush blueberries are susceptible.

'Rancocas' is the only cultivar with a high degree of

resistance. Stunt occurs naturally in Vaccinium vacillans

Torr., V. atrococcum Helbr., V. stamineum L., and V.

myrtilloides Michx. Symptoms have been observed on

graft-inoculated V. amoenum Ait., V. altomontanum Ashe,

and V. elliotii Chap. (Hutchinson et al. 1960), and V. ashei

Reade (Dale and Mainland 1981; R. M. Milholland,

unpublished data).

One plant of V. darrowi Camp has been successfully

infected using dodder (M. T. Hutchinson, unpublished data),

and periwinkle (Catharanthus roseus (L.) G. Don) has also

been infected by means of dodder.

Symptoms on highbush blueberry. Overall dwarfing of the

bush is a primary symptom, hence, the name stunt (figs. 124

and 125). Downward leaf cupping and puckering is a

Fig. 124.—Overall stunting effect due to stunt disease on

a bush of "Wolcott' cv. The branch in the right center

showing twiggy growth is infected. The branch above it

in the upper center is healthy. (Courtesy R. D.

Milholland, North Carolina State University.)

106
characteristic symptom along with a reduction in leaf size (fig.

126). Leaves on infected bushes are often chlorotic, with

chlorosis most pronounced along the leaf margins and between

lateral veins. Midribs and lateral veins usually retain normal

green coloration. Chlorotic areas often turn a brilliant red in

the late summer. Stem intemodes become shortened, and

growth of normally dormant buds causes twiggy branching.

Symptoms on rabbiteye blueberry. On the cv. 'Garden

Blue', the disease in later stages of development is

characterized by a slight reduction in leaf size and intemode

length and marginal chlorosis, but no leaf cupping (Dale and

Mainland 1981).

Symptoms on wild Vaccinium spp. Symptoms on wild

species of Vaccinium are generally like those on highbush

cultivars.

Symptoms on Catharanthus. Leaves of infected C. roseus

are pale green, marked with patches or transverse bands of

dark green. Leaf size is not markedly reduced and virescence

does not occur, but flowers are smaller and fewer than on

healthy plants.

Natural and Experimental Transmissions

Natural transmission: To date, the only known vector is the

sharp-nosed leafhopper Scaphytopius magdalensis (Hutchinson ¡955; Maramorosch 1955). Apparently, the vector is

present in all blueberry growing areas where stunt is present.

It has recently been found in the relatively new Arkansas

growing area (Dale and Moore 1978).

Experimental transmission: The causal organism is easily

graft transmitted. Plants grafted at bud break may show

symptoms in 2 to 3 mo. If grafts are made later in the season,

symptoms may be delayed until the following year. Kunkel

in 1947 (Tomlinson et al. 1950) was the first to use dodder

(probably Cuscuta campestris Yunck.) to transmit the causal

organism to C. roseus. Cuscuta suhinclusa Dur. and Hilg.

has also been used successfully.

Properties of the Causal Agent

Ultrathin sections made from stunt-infected cv. 'Jersey' bud

and leaf tissue revealed mycoplasmalike organisms (MLO) in

sieve elements (Chen 1971). The MLO ranged from spherical

to oval or had irregular morphology. The diameter ranged

from 160 to 700 nm (fig. 127). No MLO were found in healthy

tissue. Ultrathin sections of diseased tissue from 'Collins' and

'Concord' cultivars revealed similar MLO pleomorphic

bodies and what appeared to be crystalline inclusion bodies

(Hartmannet al. 1972).

Detection and Identification

The most characteristic symptoms of the disease consist of

chlorotic leaf margins and interveinal areas of the leaf. Leaf

area is reduced and leaves are cupped downward. General

stunting of infected bushes and twigginess (a proliferation of

Fig. 125.—Stunling effect and "twigginess" (stem

proliferation) on a stunt-infected cv. 'Jersey' bush.

Fig. 126.—Leaf yellowing and cupping of leaves

typical of stunt infection.

107
Â

Fig. 127.—Mycoplasmalike organism in phloem sieve

element from infected blueberry petiole tissue. Bar

represents 1000 nm. (Courtesy J. X. Hartmann.)

twigs) are all part ofthe symptomatology. If symptoms are not

definite, grafting onto cvs. 'Cabot' or 'Jersey' may result in

stronger symptoms. Alternatively, aniline blue stained

freehand sections viewed under UV-flourescence light

microscopy have been reported as a possible method of

detection (Gocio and Dale 1982). One-way ELISA tests with

an antiserum made to Spiroplasma citri failed to detect the

causal organism in stunt infected blueberry leaf sap

(Converse and Ramsdell 1982).

Control Procedures

In Michigan and New Jersey, a combination of field

inspections, roguing of infected plants and a diligent

insecticidal spray program to control leafhoppers has been

effective in controlling stunt. In warmer climates, such as in

North Carolina and Arkansas, control of disease spread may

be more difficult. Strict inspection of source bushes is

necessary before any propagating wood is taken. Thermotherapy would probably be effective because of the MLO etiology

of stunt.

1- Witches'-Broom of Vaccinium^.

by G. T. N. deJLeeuw

Additional Common Names

Blueberry little leaf, heksenbezemziekte van de bosbes;

Hexenbesenkrankheit der Heidelbeere; Kleinblattrigkeit der

Heidelbeere; metlovitost borúvky, malolitost bonîvky.

History and Geographic Distribution

Blattny and Stary {1940} described witches'-broom in

Vaccinium myrtillus L. as a virus disease. More recent work,

however, strongly indicates that some diseases of Vaccinium

spp., formerly ascribed to virus infections, are actually caused

by mycoplasmalike organisms (MLO).

Witches'-broom has been found in The Netherlands,

Germany, Czechoslovakia, Yugoslavia, Scotland, and

France. The disease occurs in lowlands and on slopes of hills

and mountains, most frequently, in dry locations in Scotch

pine forests. The distribution depends on a suitable

environment for the leafhopper vectors.

Economic Importance

According to Blattny and Blattny (1970), Witches'-broom

disease is of great economic importance in Czechoslovakia.

Many thousands of tons of V. myrtillus berries are harvested

annually, with a large proportion for the export market. In

some areas losses may exceed 15% of the crop. Losses in V.

vitis-idaea L., V. uliginosum L., and Vaccinium oxycoccus L.

are negligible.

Symptoms in Natural and Experimental Hosts

Infected V. myrtillus plants show a very dense, bushy growth.

This is due to the erect position of the excessively formed new

branches. The excessive ramification of the plants is

associated with a striking reduction in size of branches and

leaves. The leaves may have a length of 4 mm or even less,

instead of the usual 15 to 20 mm (fig. 128). Branches of plants

affected in a later stage of growth have only an erect position

instead of the plagiotropic position on normal, healthy plants.

Plants affected earlier in their development remain small, are

heavily branched and have smaller leaves. Young plants at the

edge of a diseased group of plants remain extremely small

(about 5 cm), have very small leaves, and do not form

subterranean suckers (fig. 129). Diseased plants drop their

leaves later in autumn than healthy plants, which may lead to

frost damage. Sometimes the leaves show some reddening due

to an increased anthocyanin formation. Diseased plants do not

flower at all. (Bos 7960).

Blattny and Blattny (1970) distinguished two types of

witches'-broom in V. myrtillus. Type A symptoms include

severe vertical branching and brooming; severe stunting, with

plants reaching only 2 cm in height, leaves only 1.5 mm long

rather than the normal 15 to 20 mm; frequent reddening of the

leaves; partial drying and dieback; and sterility, with the

exception of a few small flowers and berries on mildly affected

plants. Type B symptoms include less vertical branching; less

stunting, with plants reaching 10 cm; leaves 6 mm long;

light-green leaves because of paler intercostal tissues; a

light-pink color rather than a reddening of the leaves; little

drying up and no death of plants; and a few flowers and berries

smaller than normal.

In localities where type A symptoms occur, plants are not

affected by the disease characterized by type B symptoms, and

the reverse holds true where type B is found. Type A

symptoms are prevalent in Czechoslovakia, West Germany,

The Netheriands, and East Germany. Type B occurs in

Czechoslovakia, East Germany, and Yugoslavia. V. vitisidaea, V. uliginosum, and V. oxycoccus show similar

symptoms, that is, upright growth of shoots, brooming,

stunting, reduced leaf size, leaf reddening, and sterility.

108
Fig. 128.—Twigs of a healthy (left) and witches'-broom

diseased V. myrtillus plant (right).

Fig. 129.—Extremely small plants from the edge of a

group of V. myrtillus plants affected by witches'-broom.

Natural and Experimental Transmission

Blattriy (1963) proved that the leafhopper Idiodonus cruentatus Panz. can transmit the disease to V, myrtillus; however, the

disease also occurs abundantly where /. cruentatus has not

been found. Probably other leafhoppers are vectors as well.

Experiments have indicated that the leafhoppers Empoasca

solani (Curt.), Neophilaenus exclamationis Thumb.,

Aphrodes bicincta (Schrank), Euscelis ssp., and Macropsis

fuscula (Zett.) do not transmit the disease.

Warm periods in summer, autumn, and in dry springs are

favorable for leafhoppers. The disease increases after such

weather conditions. Excessive tree felling in the forest also

supports the occurrence of leafhoppers and causes an increase

in the number of diseased plants.

Witches'-broom in V. myrtillus may also be transmitted by

grafting (Bos 7960,- Uschdraweit 1961; Blattny and Blattriy

1970), or by implantation of bast (phloem) tissue into stems

(Blattny and Stafy 1940). The incubation times vary according

to the season in which grafts are made and to environmental

conditions.

Attempts to transmit the disease by means of Cuscuta

campestris Yuncker, C. epithymum Murray, and C. subinclusa Dur. and Hilg. were unsuccessful. Up to now, 1981, no

disease has been found in seedlings obtained from the very few

viable seeds from lightly diseased plants.

Fig. 130.—Electron micrograph of mycoplasmalike

organisms in sieve tubes of witches'-broom diseased V.

myrtillus plants. Bar represents 500 nm.

Properties of the Causal Agent

Kegler et al. (1973), Blattny and Vana (1974), and de Leeuw

(1975) detected mycoplasmalike organisms (MLO) in the

sieve tubes of V. myrtillus plants affected by witches'-broom

(fig. 130). The consistent association of MLO with

witches'-broom symptoms and the absence of these organisms in the sieve tubes of healthy plants make it very likely

that MLO are the causal agents of this disease. Whether these

organisms are related to the etiologic agents of blueberry

stunt and cranberry false blossom has yet to be investigated.

(See "Blueberry Stunt," p. 106, and "Cranberry False Blossom," p. 110.)

Detection and Identification

The disease may be detected by graft or vector transmission to

V. myrtillus, V. vitis-idaea, V. uliginosum, or V. oxycoccus.

The presence of MLO in the sieve tubes of suspected plants

can be detected with the aid of fluorescence microscopy or

electron microscopy.

Control Procedures

The eradication of diseased plants as soon as they are

recognized is desirable. Prevention of leafhopper migration

may reduce the extent and distribution of the disease. Control

of vectors is particularly important where it is necessary to

prevent the spread ofthe disease from wild hosts to plantations

of cultivated V. corymbosum L. There are no studies on the

therapy of this disease.

Remarks

Early evidence of witches'-broom in V. myrtillus was found

in Czechoslovakia in herbarium species dated 1925 and

1926. V. myrtillus f. parvifolium Domin (f. microphyllum

auct.), characterized by very minutes leaves; as well as V.

109
l^

myrtillus f. erectum Otruba with erect twigs; and V. myrtillus

f. pygmaeum Ostenf. are probably affected by witches'-

broom (Blattñy and Blattny 1970). When grown under

unsuitable conditions, V. myrtillus and V. vitis-idaea can be

dwarfed and infertile. By the absence of the vertical growth

and brooming, such plants can be distinguished from plants

with witches'-broom disease.

Witches'-broom, blueberry stunt, and cranberry false blossom

cause similar symptoms in their respective hosts, but are

transmitted by different leafhoppers. A strain relationship

between these MLO is possible but has not yet been

demonstrated.

r

b

Cranberry False Blossom,/

ByA. W.fetretch

Additional Common Names

Wisconsin false blossom.

History and Geographic Distribution

Shear (1908) first described and named the disease. Its

transmissibility and mode of transmission were established by

Dobroscky (1929). Chen (1971) determined that false blossom

was associated with mycoplasmalike organisms (MLO) rather

than viruslike particles as originally surmised. False blossom

appears to be indigenous to Wisconsin. The disease was

probably distributed from Wisconsin to other U.S. cranberry

growing areas in diseased vines (Stevens 1931). The disease is

now found in Massachusetts, New Jersey, New York

(including Long Island), Oregon, Washington, and Nova

Scotia.

Economic Importance

In the early 1900's, this disease caused serious losses which

reached a peak in the 1920's and early 1930's. Since that

period, control of the vector has reduced the spread to a point

where losses are small. Large-scale planting of resistant

cultivars has reduced its economic impact.

Symptoms on Natural and Experimental Hosts

False blossom disease is known to occur only on American

cranberry (Vaccinium macrocarpon Ait.) and European

cranberry {Vaccinium oxycoccus L.). Kunkel (1945) was able

to transmit false blossom through dodder {Cuscuta campestris Yunck.) to 28 species of plants in 10 different families.

In nature, the host range appears limited by vector feeding

preferences and natural resistance.

Symptoms in cranberry. False blossom is most easily

recognized at bloom when the flowers on infected plants

assume an upright position because the pedicels are straight

(fig. 131), rather than arched, as on a normal plant (fig. 131).

The calyx lobes of diseased flowers become enlarged, the

petals are short and streaked with red and green, and the

stamens and pistils are abnormal, usually resulting in a sterile

flower. Normally latent axillary buds are also stimulated and

give rise to branches with a witches'-broom effect (fig. 132).

The leaves on these branches are closely appressed to the stem.

In autumn, they take on a reddish hue before normal autumn

coloration develops. Terminal flower buds are enlarged, in an

advanced stage of development, and very susceptible to spring

frost injury, since they are protected by only one layer of scale

leaves as compared with four layers in a normal flower bud.

Symptoms in complex with ringspot virus have not been

determined. (See "Ringspot of Cranberry" p. 123).

Symptoms on experimental hosts. The false blossom MLO

caused all of the 28 species artifically inoculated through the

use of dodder (Kunkel 1945)io become chlorotic, to assume a

more upright habit of growth than is normal, and to produce

marked effects of flowering and fruiting organs. At present,

no information is available on suitable indicator hosts.

Natural and Experimental Transmission

Natural Transmission: Dobroscky (1929) proved that the

blunt-nosed leafhopper Scleroacus vaccinii (Van Duzee), also

known as Euscelis striatulus Dobroscky (nee Fallen), was a

vector of false blossom disease. No other vectors have been

implicated. The shortest time from feeding of the leafhopper

vector to symptom development on cranberry was 30 days,

and the longest was a year or more (Dobroscky 1931).

Experimental Transmission: False blossom has been transmitted from cranberry to periwinkle {Catharanthus roseus (L.) G.

Don, tomato {Lycopersicum esculentum Mill.), and other

plant species, using dodder (Cuscuta campestris) (Kunkel

1945). Graft transmission from cranberry to cranberry has not

proven useful because of the difficulty of grafting thinstemmed cranberry vines. Kunkel (1945) was able to graft

transmit the MLO into periwinkle, tomato, and other

herbaceous plants.

Properties of the Causal Agent

The MLO described by Chen {1971) have not been grown in

pure culture and then reintroduced into cranberry to prove a

positive causal association with diseased plants. The MLO

were found in the sieve-tube elements, and their shapes

ranged from spherical to oval to irregular. Each body was

surrounded by a single unit membrane. The size range of

these MLO was 80 to 300 nm (fig. 133).

Detection and Identification

The disease is detected most successfully at the bloom stage

when the normal arching of the flower pedicel is replaced by

an upright habit of growth. Witches'-brooming and upright

growth above the level of normal vines make diseased plants

stand out. Identification is based on symptoms in cranberry.

Electron microscopy of diseased tissue can detect MLO, but

cannot distinguish among them. Development of a cultural

method for the MLO and production of specific antisera

should provide a means for positive serological identification

of the false blossom causal organism.

110
Fig. 131. — Cranberry false blossom symptoms on

cranberry. Diseased uprights with abnormal flowers and

straight pedicels (right). Heahhy uprights with normal

flowers and arched pedicels (left). (Courtesy D. M.

Boone.)

Control procedures

Chemical control of the leafhopper with parathion applied at

the dangle stage before bloom is the primary method of

control. FoUowup sprays 10 to 14 days and 4 wk after

midbloom with parathion or azinphosmethyl are also needed

for leafhopper control. The growing of cultivars that are less

attractive as food plants than cultivars like 'Howes' has been

very important in control. 'Shaw's Success' is the most

resistant cultivar, followed in descending order by 'McFarlin' and 'Early Black'. 'Howes' is the most susceptible.

Flooding a bog in June — just before the flower buds open

and after the leafhopper eggs have hatched — has proved

effective, but timing is critical and vine damage is a distinct

possibility. No information is available on therapy of this

disease.

Fig. 132. — Witches'-brooming associated with

cranberry false blossom (right) compared with normal

upright production (left). (Courtesy D. M. Boone.)

Fig. 133. — Electron micrograph of mycoplasmalike

organisms in sieve tubes of false blossom diseased

cranberry leaves. Bar represents 500 nm. (Courtesy T.

A. Chen.)

Ill
Nematode-Borne Diseases

rá

Blueberry Leaf Mottle,/

By D. C.]Ramsdell

Additional Common Names

None.

History and Geographic Distribution

The disease was observed for the first time in 1977 in a 4-ha

planting of mature cv. 'Rubel' bushes near Hartford, Mich.

The bushes exhibited a general decline and dieback condition

and leaf mottling. The disease has been found in cv. 'Jersey'

bushes in a few other plantations. Symptoms consisted of

some bush stunting and smaller leaves, but leaf deformation

and pronounced mottling were absent. The symptomatology

of this disease is different from that of other virus-caused

diseases of blueberry. As of this writing, the disease has been

diagnosed and serologically confirmed in a total of five fields

in southwestern and western central Michigan. It has not

been reported from other blueberry growing areas. A

serologically distantly related virus, grapevine Bulgarian

latent virus, has been isolated from Vitis vinifera L.

grapevines near Pleven, Bulgaria (Martelli et al. 1977, 1978;

Ramsdell and Stace-Smith 1979a). A virus serologically

closely related to BBLMV (but reported as a strain of

grapevine Bulgarian latent virus) (Uyemoto et al. 1977) has

also been isolated from a single Vitis labrusca L. 'Concord'

grapevine in New York State.

Economic Importance

Bushes infected with blueberry leaf mottle virus (BBLMV)

are stunted and very unproductive. Bushes that have been

infected for several years die, probably due to winter injury

as a result of their weakened condition.

Symptoms on Natural and Experimental Hosts

BBLMV has a fairly narrow host range (Ramsdell and

Stace-Smith /979a). Mostly herbaceous indicators in the

genus Chenopodium show symptoms. Cucumis sativus L.

'Straight Eight' may show chlorotic local lesions on

inoculated cotyledons. Nicotiana clevelandii Gray shows

systemic pinpoint necrotic local lesions I to 2 mm in

diameter in new leaves.

Symptoms on highbush blueberry. Cv. 'Rubel' shows the

most striking symptoms. Bushes that have been infected for

several years develop a severe dieback of older stems,

leaving stunted, deformed new growth coming from the

crown area (fig. 134). Leaves show a mottling pattern and

sometimes chlorotic roughly circular "windows" (ñg. 135).

In the most severe cases, leaf malformations such as leaf

strapping and curling can occur. Productivity is nil. Healthy

Figure 134. — A cv. Rubel' blueberry bush showing

effect of stem diebaclc and stunted regrowth as a result

of blueberry leaf mottle disease.

seedlings of the cv. 'Rubel', if rub-inoculated with purified

virus, will show a leaf mottling within several months after

inoculation (fig. 136) (Ramsdell and Stace-Smith 1979a).

Cv. 'Jersey' exhibits milder symptoms. Stem dieback is not

very prevalent. There is some stunting and growth reduction

present. Leaves are somewhat smaller, and slight leaf

mottling of lower leaves occurs in the crown area.

Productivity is greatly reduced.

The pattern of spread appears to be random in affected fields.

Attempts to transmit the virus using Xiphinema americanum

Cobb have given negative results (T. C. Vrain, unpublished

data, and J. M. McGuire, unpublished data). Pollen grains

were extremely high in virus content in 13 out of 15

symptom-bearing bushes sampled, according to ELISA tests

(D. C. Ramsdell, unpublished data). Disease spread is

probably mediated by honey bees, which are an integral part

of highbush blueberry culture.

Symptoms on Indicator Hosts

The following herbaceous indicators are useful:

Chenopodium quinoa Willd.

Chlorotic local lesions, mottle, and apical death within 7

to 10 days.

112
Figure 135. — Leaf mottling and chlorotic "windows"

in leaves from a cv. 'Rubel' blueberry bush with

blueberry leaf mottle disease.

Chenopodium amaranticolor Coste and Reyn.

Systemic mottle within 10 to 14 days.

Nicotiana clevelandii Gray

Pinpoint necrotic local lesions, 1 to 2 mm in diameter,

on noninoculated leaves within 14 to 21 days.

Natural and Experimental Transmission

Natural Transmission: Unknown. Although BBLMV possesses physical and chemical properties of a nepovirus,

similar to tomato ringspot and cherry leaf roll viruses

(Harrison and Murant ¡979; Ramsdell and Stace-Smith

1981), the suspected nematode vector, Xiphinema americanum. is not associated with the disease (D. C. Ramsdell,

unpublished data). The pattern of spread in the field is

random rather than circular, the latter being typical of a

nematode-mediated pattern of spread. The fact that pollen

has been found to contain high levels of virus indicates that

natural spread may be by pollen. Although not yet

demonstrated, the disease is no doubt spread by infected

propagating material.

Experimental Transmission: Bud and graft transmission tests

have not been done. Sap transmission from infected

Figure 136. — A cv. 'Rubel' leaf showing mottling

symptoms a few months after a healthy seedling was

rub-inoculated with purified blueberry leaf mottle virus.

blueberry to herbaceous host plants is easily done by grinding

young terminal leaf tissue in 0.05 M Tris-HCl buffer pH 7.0,

with 2% (v/v) nicotine alkaloid added. A mortar and pestle

works well for grinding the tissue.

Properties of the Causal Agent

BBLMV is a putative member of the nepovirus group

(Ramsdell and Stace-Smith 1981). It has three types of

isometric particles with sedimentation coefficients of 53,

120, and 128 S. The virions contain two pieces of

single-stranded RNA with molecular weights of 2.15 and

2.35 X lO*" daltons, respectively. The protein coat subunit

has a molecular weight of 54,000 daltons. BBLMV is

serologically distantly related to grapevine Bulgarian latent

virus. The virus has a narrow host range, causing known

diseases in blueberry and grape only.

Detection and Identification

Visual inspection will give a strong indication that the disease

is caused by BBLMV, but sap transmission to the

aforementioned herbaceous indicators is useful for detection

of BBLMV. Final confirmatory results using such serological

tests as agar gel double diffusion are necessary. BBLMV is a

113
good immunogen. Antisera with titers of 1:1024 are easily

obtained. Instead of using herbaceous indicators, ELISA

tests made directly with young infected blueberry leaf tissue

or blossoms works well (D. C. Ramsdell, unpublished data).

Control Procedures

Until the mode of spread is proved, all that can be done is to

inspect fields visually for infected bushes and then rogue

them. If the disease is indeed pollen spread, the effect of

honey bees upon spread will need to be scrutinized carefully.

No information is available on thermotherapy.

L

V Necrotic Ringspot of Blueberryyy

By D. C.[Ramsdell

Additional Common Names

Pemberton disease.

History and Geographic Distribution

The disease was first discovered in a commercial field in New

Jersey and was brought to the attention of researchers in

1955. Varney and Raniere {I960) demonstrated its virus or

viruslike etiology. Lister et al. (1963) demonstrated the

association between tobacco ringspot virus (TRSV) and

necrotic ringspot disease. The disease occurs in Connecticut,

Illinois, Michigan, and New Jersey. It has recently been

reported in Arkansas (McGuire and Wickizer 1979) and in

Oregon (Converse and Ramsdell 1982).

Economic Importance

Necrotic ringspot disease causes a slow, but steady decline in

bush productivity in susceptible cultivars, for example,

'Pemberton', 'Stanley', 'Rubel', 'Concord', and 'Collins'.

In some cases, bush death occurs, especially in Northern

States such as Michigan which have extremely cold winters.

Until recently, cv. 'Jersey' was thought to be resistant to

necrotic ringspot, but a severe strain of TRSV was found to

be associated with a decline disease of 'Jersey' (Ramsdell

7978).

Symptoms on Natural and Experimental Hosts

TRSV, the causal agent, has a broad host range, causing

diseases in both herbaceous and woody plants (Stace-Smith

1970b). TRSV isolates causing necrotic ringspot, found by

Lister et al. {1963), infected the following herbaceous hosts

as a result of mechanical inoculation: Nicotianci tabacum L.,

A^. rustica L., N. clevelandii Gray, Petunia hybrida Vilm.,

Datura stramonium L., Phaseolus vulgaris L., Cucumis

sativus L., Chenopodium amaranticolor Coste and Reyn.,

and C. quinoa Willd. The TRSV isolate associated with the

decline of cv. 'Jersey' was found to cause more severe and

rapid necrosis in herbaceous hosts than standard necrotic

ringspot isolates of TRSV (Ramsdell 1978).

Symptoms on highbusb blueberry. Cultivars that are

susceptible, for example 'Pemberton', exhibit stem dieback

Figure 137. —Cv. Pemberton showing leaf deformation symptoms (arrow) due to necrotic ringspot disease

caused by tobacco ringspot virus.

and stunting. Leaves are deformed and somewhat thickened

(fig. 137). Leaves become chlorotic and show necrotic spots.

Some of these may drop out giving a shot-hole or tattered

effect (fig. 138). On other susceptible cultivars, for example,

'Concord' and 'Stanley', symptoms are expressed as short

intemodes and small straplike leaves (fig. 139).

Symptoms on Indicator Hosts

The following herbaceous indicator hosts and their reactions

to TRSV are useful for preliminary identification of the

causal virus, but serological confirmatory tests are necessary:

Chenopodium quinoa Willd.

Necrotic lesions on inoculated leaves; apical dieback

within 6 to 7 days.

Cucumis sativus L. cv. "National Pickling'

Chlorotic lesions 1 to 3 mm in diameter on inoculated

cotyledons, followed by systemic chlorosis and necrotic

lesions on new leaves.

Nicotiana tabacum L. cv. 'Burley'

Necrotic ringspot on inoculated leaves, mosaic symptoms

on new leaves.

114
Figure 138. — Cv. 'Pemberton' showing leaf necrosis

and shot-hole effect (arrow) due to necrotic ringspot

disease caused by tobacco ringspot virus.

Natural and Experimental Transmission

Natural transmission: Natural spread is thought to be by

Xiphinema americanum Cobb. This nematode has been

shown to be most consistently associated with the disease in

blueberry (Griffin et al. 1963; Tjepkema et al. 1967; Raniere

1964). McGuire (1964) has shown that single nematodes can

transmit TRSV from herbaceous to herbaceous hosts. The

disease spreads slowly in a roughly circular manner in the

field. The disease is also spread through vegetatively

propagated hardwood cuttings.

Experimental transmission: The disease can be bud or graft

transmitted to 'Pemberton' or other susceptible cultivars.

TRSV can be successfully sap transmitted from young leaf

tissue from terminals of stems or from suckers coming from

the crown. Dormant buds are also a good source of tissue for

successful transmission to herbaceous indicators (D. C.

Ramsdeli, unpublished data). Phosphate buffer (0.05 M, pH

7.2) containing 2% (v/v) nicotine alkaloid is a satisfactory

buffer for grinding leaf tissue with a mortar and pestle for sap

inoculation to the aforementioned herbaceous indicators.

Figure 139. — Cv. 'Stanley' showing shortened

terminal growth and small straplike leaves (arrow) due

to necrotic ringspot disease caused by tobacco ringspot

virus.

Properties of the Causal Agent

TRSV is a member of the nepovirus group (Harrison and

Murant 1977). It is a multicomponent virus with three

particles about 28 nm in diameter, sedimenting at 53, 91 and

126 5 (Stace-Smith /970a). The single-stranded RNA is

composed of two different molecular weight species, 1.4 x

10" and 2.4 x 10" daltons, and both are necessary for

infection. The protein coat is composed of 42 subunits, each

having a molecular weight of about 55,000 daltons. The virus

causes disease primarily in woody or semiwoody plants, but

also causes some diseases in herbaceous ornamentals and

agricultural crop plants. Natural transmission is by the

nematode Xiphinema americanum.

Detection and Identification

Susceptible cultivars exhibit disease symptoms that are fairly

characteristic. Visual inspection in commercial plantings will

give a primary indication that necrotic ringspot disease is

present. For more definitive diagnosis, however, sap

inoculation to herbaceous indicators and confirmation by

serology as previously outlined is the best method for

detection. Alternatively, enzyme-linked immunosorbent

assay (ELISA) works very well (D C. Ramsdell, unpublished

data; Converse and Ramsdell 1982). Bud, blossom, and leaf

tissue from shoot terminals is the best for both herbaceous

plant and ELISA indexing. Alternatively, bud or graft

indexing may be done to detect symptomless infection by

budding or grafting onto healthy cultivars which will readily

show symptoms, for example, 'Cabot', 'Concord', 'Pemberton', or 'Stanley'.

Control Procedures

Roguing of diseased bushes, several bushes beyond those

that are showing symptoms, is required to remove symptomlessly infected bushes. Soil fumigation with high rates of

nematicides 1 yr after bush removal is necessary to halt

115
further spread of the disease. For new plantings, disease-free

stock planted into nematode vector-free soil will prevent the

disease.

No information is available concerning thermotherapy of

blueberry tissue to rid it of TRSV.

\ÁPeach Rosette Mosaic Virus in Blueberryyy

By D. C.jRamsdell

Additional Common Names

None.

History and Geographic Distribution

This virus occurs only in southwestern Michigan and

southeastern Ontario, Canada. The disease has only been

observed in blueberries in an experimental planting where

blueberries were planted in infested soil in a vineyard site

(Ramsdell and Gillett 1981).

Economic Importance

No information.

Symptoois on Natural and Experimental Hosts

Peach rosette mosaic virus (PRMV) has a very narrow

experimental and natural host range (Dias 7975). In nature,

the virus occurs in woody plants (grape and peach) and in

some weed species (Ramsdell and Myers 1978). Sap

transmission of the virus by rub inoculation is readily done

using Chenopodium quinoa Willd.

Symptoms on blueberry. Symptoms have been observed

only on highbush cvs. 'Jersey' and 'Berkeley'. In cv. 'Jersey',

leaves become strap shaped (fig. 140 A) and/or deformed into

a crescent shape (fig. 140ß). In cv. 'Berkeley', the leaves are

spoon shaped and smaller than normal (fig. 140 C).

Symptoms on diseased leaves are not equally distributed over

an infected bush. No necrotic or chlorotic lesions have been

observed on leaves. These latter two symptoms are peculiar

to tobacco and tomato ringspot virus induced diseases,

respectively (see these two disease chapters). No twig or fruit

symptoms have been observed as a result of PRMV infection.

Symptoms on Indicator Hosts

The only two reliable herbaceous indicator hosts are:

Chenopodium quinoa Willd.

Faint chlorotic local lesions occur in inoculated leaves

within 4 to 10 days followed by epinasty and abscission.

Uninoculated terminal leaves become mottled and twisted.

Death of the terminal growing point usually occurs within

about 2 wks.

Chenopodium amaranticolor Coste and Reyn.

Faint chlorotic local lesions may or may not occur in

inoculated leaves within 4 to 10 days. Uninoculated

terminal leaves show mottling, and often death of the

terminal growing point will occur after about 2 wks.

Natural and Experimental Transmission

Natural transmission: Natural transmission of PRMV is by

Xiphinema americanum Cobb. Healthy peaches and grapes

become infected when planted in infested soils (Cation 7942,

1951). Steam or chlordane treatment of infested soil from

peach orchards prevented transmission (Fulton and Cation

1959). Large populations of X. americanum are found

associated with soils around PRMV-diseased grapevines

(Ramsdell and Myers 1974). Healthy Vitis labrusca L. cv.

'Concord' and some French hybrid grapevines became

infected within 3 yr when planted in soil infested with X.

americanum (D. C. Ramsdell, unpublished data).

Experimental transmission: Hand-picked X. americanum

transmitted PRMV from Chenopodium quinoa to C. quinoa,

but not to healthy grapes. The percentage of transmission was

low and erratic (Dias 1975).

Properties of the Causal Agent

PRMV is a member of the nepovirus group (Harrison and

Murant 1977). The following physical and chemical

properties have been reported (Dias 7975; Dias and Cation

1976). The virus has three types of isometric particles about

28 nm in diameter, sedimenting at 52, 115, and 135 5. The

middle and bottom components have estimated percent RNA

values of 37 and 44%, respectively. The single coat

polypeptide has a molecular weight of about 55,000 daltons.

The virus has a narrow natural host range, being restricted to

peach, grape, and some weed species. Shortened intemodes

and leaf malformation (rosetting in peach) are the main

symptoms caused on these woody hosts. Natural transmission is by the nematode vector X. americanum.

Detection and Identification

The symptoms described for PRMV-caused disease of

blueberry should not be considered diagnostic. Any bushes

suspected of having the disease should be tested by grinding a

small amount of young terminal leaf tissue in 0.05 M

phosphate buffer pH 7.2 containing 2% (v/v) of nicotine

alkaloid, and rub-inoculating carborundum-dusted C. quinoa

and C. amaranticolor plants. Symptom-bearing herbaceous

tissue should be tested serologically to confirm the presence

of PRMV. Alternatively, ELISA tests can be run directly on

suspected infected blueberry tissue (Ramsdell and Gillett

7987; Ramsdelletal. 7979).

Control Procedures

If PRMV is found infecting a blueberry field, suspect bushes

should be tested by the previously mentioned methods to

determine the extent of infection. Infected bushes should then

be removed. Root pieces should be thoroughly removed also.

After a season has passed and the soil has been well worked,

preplant soil fumigation should be done using nematicides at

high rates to kill vector nematodes thoroughly. After

sufficient aeration time, new plants free of PRMV could be

replanted in the area. No information is available on

thermotherapy of PRMV.

116
Figure 140.—Symptoms of peach rosette mosaic virus

infection in highbush blueberry; A. Leaf strapping; B.

malformation in cv. 'Jersey'; and C, spoon-shaped

leaves on terminal growth of cv. 'Jersey'.

iVte: <^ Tomato Ringspot Virus in Blueberry y

By D. C.]Ramsdell

Additional Common Names

None.

History and Geographic Distribution

The disease with tomato ringspot virus (TomRSV) was

reported for the first time in 1972 in a field near Mossyrock,

Wash. (Johnson 1972). It was more recently reported from

Oregon (Converse and Ramsdell 1982). There has been no

other report of TomRSV-associated disease in blueberry.

Economic Importance

No quantitative data exist for deleterious growth or yield

effects due to TomRSV infection of blueberries.

Symptoms on Natural and Experimental Hosts

TomRSV has a wide experimental and natural host range;

species in more than 35 dicotyledonous and monocotyledonous families are susceptible (Stace-Smith 1970b).

Symptoms in blueberry. The blueberry bushes reported

infected by Johnson (1972) in Washington exhibited the

following symptoms: Leaves were in some cases malformed

and exhibited roughly circular chlorotic spots (2 to 5 mm in

diameter); in addition, stems, twigs and branches exhibited

circular, brownish necrotic spots of similar size (figs. 141

and 142). Younger terminal leaves exhibited a tendency

toward leaf-strapping and a mottle pattern (fig. 143)

(observed by the author; not part of Johnson's 1972

description). Bud grafts made in summer from infected

blueberries to plants of the red raspberry cv. 'Puyallup'

produced ringspot and oak leaf patterns in the foliage the

following spring (Johnson 1972).

Symptoms on Indicator Hosts

See the listing of useful herbaceous indicator hosts in the

Rubus disease section, "Tomato Ringspot Virus in Rubus,"

p. 223.

Natural and Experimental Transmission

Natural transmission: Natural transmission is thought to be

via the dagger nematode Xiphinema americanum Cobb. High

populations were associated with two of the three blueberry

fields where TomRSV was found associated with the disease

in Oregon (Converse and Ramsdell 1982). Infected planting

stock is also undoubtedly another source of spread.

Experimental transmission: The red raspberry cv. 'Puyallup' was successfully bud-inoculated from a TomRSVdiseased source bush. The following season the leaves

showed ringspots and oak leaf patterns (Johnson 1972). The

virus was also successfully sap transmitted from young

diseased blueberry leaves to Nicotiana tabacum L., Chenopodium quinoa Willd., and Cucumis sativus L. (Johnson

117
Figure 141.—Cv. 'Earliblue' infected with tomato

ringspot virus. Note circular chlorotic lesions on the

leaves and necrotic circular lesions on stems.

Figure 142.—Leaves of cv. "Earliblue' showing a

closcup view of chlorotic circular lesions associated

with tomato ringspot virus infection.

7972). The causal virus has been successfully transmitted

using herbaceous plants (Téliz et al. 1966). but it has not

been transmitted using blueberry plants.

Properties of the Causal Agent

See the Rubus disease section, "Tomato Ringspot Virus in

Rubus," p. 223.

Detection and Identification

The most practical and quickest way to detect TomRSV from

blueberry is to perform enzyme-linked immunosorbent assay

(ELISA) tests on suspected diseased buds or young leaf tissue

(Converse and Ramsdell 1982). Alternately, diseased bud or

young leaf tissue can be ground in a small amount of 0.05 M

phosphate buffer containing 2% nicotine alkaloid (v/v) and

rub-inoculated onto carborundum-dusted Chenopodium

quinoa, Ciicumus sativus cv. 'National Pickling", and

Nicolianci tahucum cv. "Burley" indicator plants. Sap

expressed from symptom-bearing tissue can then be tested

against TomRSV antiserum in agar gel diffusion plates for

confirmation that TomRSV is present.

Control Procedures

Roguing of diseased bushes several bushes beyond those that

are showing symptoms is a necessary measure to remove

symptomlessly infected bushes. Soil fumigation with high

rates of nematicides 1 yr after bush removal is necessary to

halt further spread of the disease. For new plantings,

disease-free stock planted into nematode vector-free soil will

prevent the disease. No information is available concerning

thermotherapy of blueberry tissue to rid it of TomRSV.

118
Vectors Unknown

Figure 143.—Young leaves of cv. 'Earliblue' showing

leaf-strapping and mottling symptom associated with

tomato ringspot infection.

2 4-Billlueberry Mosaic/^

By D. C.|Ramsdell and A. W.^tretch

Additional Common Names

Variegation.

History and Geographic Distribution

The disease was recognized as a variegation and thought to

be of genetic origin before it was shown to be of viruslike

etiology (Varney 1957). It has been observed in plantings of

cultivated blueberries throughout Eastern United States,

Michigan, Indiana, Oregon, and in British Columbia,

Canada.

The disease has been observed on older cultivars of highbush

blueberry, for example, 'Cabot', 'Concord', 'Earliblue',

'Pioneer', 'Rubel', and 'Stanley'. Another differentappearing type of mosaic disease on cv. 'Coville' may be of

genetic origin. The disease has been observed occasionally

on Vaccinium vacillans Torr., which is a lowbush dryland

type.

Economic Importance

No quantitative data are available. Diseased bushes have a

noticeable reduction in yield — the fruit is of poor quality

and such fruit may ripen late.

Symptoms on Natural and Experimental Hosts

Symptoms include mild to brilliant mottle and mosaic

patterns of chrome yellow, yellow and yellow green.

Sometimes, the leaves will also have areas of pink (fig. 144).

The distribution of symptoms on a bush is spotty. Symptoms

may show on the major portion of a bush or on only one or

two stems. Symptoms may be ephemeral, showing in a given

year, not showing the next year, and then reappearing a year

later. On cv. 'Coville', the mosaic pattern is less brilliant.

Rather than a bright yellow mosaic, the pattern is a light

green alternating with a deep green (figs. 145 A and B) and

may be a genetic disorder.

Natural and Experimental Transmission

Cvs. 'Herbert', 'Stanley', and 'Burlington' graft-inoculated

at bud break showed symptoms on 27, 31, and 51 days,

respectively (Raniere 7960). Ten additional cultivars inoculated at the same time failed to develop symptoms during the

course of the experiment. Mosaic is not sap or dodder

transmissible to herbaceous hosts. There is no known vector,

but the disease does spread slowly in the field.

Properties of the Causal Agent

Attempts at purification of virus particles by several methods

using symptomatic blueberry leaf tissue have failed to yield

119
Figure 144.—Chrome yellow, yellow, and green

mosaic patterns on leaves of cv. 'Rubel' blueberry infected with blueberry mosaic.

any detectable virus particles (D. C. Ramsdell, unpublished

data). Electron microscopic examination of ultrathin sections

made from symptomatic leaf tissue, petioles, and roots did

not yield any definitive virions. Packets of roughly spherical

viruslike particles, 28 to 30 nm in diameter, were found, but

these could have been ribosomal structures altered as a result

of the disease (none were formed in similarly treated healthy

tissue) (K. K. Baker and D. C. Ramsdell, unpublished data).

Detection and Identification

Symptoms are generally distinct and diagnostic. Confirmatory diagnosis in plants with mild symptoms may be done by

graft inoculating 'Stanley', 'Cabot', or a similar indicator

cultivar.

Control Procedures

Since blueberry mosaic is not known to be latent in

blueberry cultivars, prompt removal of visibly infected

bushes may be worthwhile. No information is available on

thermotherapy.

1."^

Figure 145. — A and B, Light- and dark-green

mosiac symptoms on leaves of cv. 'Coville', which

probably has a genetic disorder that can be confused with regular blueberry mosaic.

120
1ë

Red Ringspot of Blueberry /

By D. C.|Ramsdell, K. S.]kim, and J. P.|Fulton

Additional Common Names

Ringspot (Hutchinson and Vamey 1954).

History and Geographic Distribution

The symptoms of this disease were first described by

Hutchinson (1950), and its virus or viruslike nature was

determined by Hutchinson and Vamey (1954). The disease is

most important from an economic standpoint in New Jersey,

and it is widespread in recent plantings in Arkansas (Kim et

al. 1981). The disease has also been reported from Michigan,

Connecticut, Massachusetts, New York, North Carolina, and

most recently in Oregon (Converse and Ramsdell 1982), but

it is not of much economic importance in these States.

Paulechova (1972) has reported the occurrence of red

ringspot in Czechoslovakia on wild Vaccinium myrtillus L.;

however, she did not establish that the disease was caused by

the virus by graft transmission, but only showed that a fungal

pathogen was not present.

Economic Importance

No actual bush loss or crop loss data are available for this

disease, from the standpoint of growth reduction, yield loss,

or fruit damage.

Symptoms on Natural and Experimental Hosts

The cultivars most commonly observed showing symptoms

include 'Blueray', 'Bluetta', 'Burlington', 'Cabot', 'Coville', 'Darrow', 'Earliblue', and 'Rubel'. The cv. 'Jersey'

exhibits apparent immunity, and 'Bluecrop' has shown

excellent field resistance. The disease has been observed in

wild blueberry plants in New Jersey. These plants belong to

the V. australe Small and V. corymbosum L. group. Red

ringspot disease of blueberry and cranberry ringspot may be

caused by the same virus. The disease symptoms are similar,

and similar inclusion bodies are found in ultrathin sections

from diseased cranberry (K. S. Kim and A. W. Stretch,

unpublished data); however, cross-graft experiments have

not yet been conducted to establish this relationship.

Attempts to rub transmit purified red ringspot virus (RRSV)

to herbaceous hosts have been unsuccessful (Kim et al.

798/).

On highbush blueberry, the disease causes the following

symptoms: Stems 1 yr old and older often exhibit red ring

spots (fig. 146) or red blotches that are roughly circular, but

not ringlike (fig. 147). Reddish-brown circular spots, 2 to 6

mm in diameter, develop on older leaves in mid- to late

summer (fig. 148). Younger leaves usually do not show the

red spots. Sometimes spots, if sufficiently numerous,

coalesce. These circular spots often have a green center.

These spots are most prominent only on the upper surface of

the leaf. Powdery mildew Microsphaera aini DC ex Wint.

var. vaccinii (Schw.) Salm.) can cause similar symptoms on

Figure 146. — Stem of a red ringspot infected cv.

'Blueray' bush exhibiting typical well-defined ringspots

(arrow).

the leaves; however, the leaf spots caused by this disease are

prominent on both sides of the leaf. The cv. 'Rancocas' may

show fruit symptoms as part of the disease syndrome,

consisting of circular light areas of blotching on the fruit. The

cv. 'Bluetta' sometimes shows a red ringspotlike disorder

typified by red leaf spotting, which is probably caused by a

genetic disorder. There are no ring spots on the stems

associated with the genetic disorder.

There are no known experimental herbaceous or woody

experimental hosts (other than blueberry).

Natural and Experimental Transmission

Natural transmission; The disease appears to spread

actively in New Jersey; however, in Michigan the disease

does not spread at all in the field. Mapping of spread in New

Jersey plantings indicates that spread is generally from bush

to bush within the row (A. W. Stretch, unpublished data).

Since spread does not occur in Michigan in fields with

populations of the blueberry aphid (lllinoia pepperii

MacGillivray) present, it is unlikely that this aphid is the

vector. In New Jersey, where active spread occurs in the

field, mealybug (probably Dy.smicoccus sp.) is the suspected

vector (A. W. Stretch, personal communication).

121
Figure 147. — Stem of a red ringspol infected cv.

Blueray' bush exhibiting red blotches that are not

ringspots (arrow).

Experimental transmission: The only experimental transmission is by chip budding or whip grafting to healthy

susceptible highbush blueberry cultivars.

Properties of the Causal Agent

Red ringspot virus (RRSV) is an isometric virus 42 to 46 nm

in diameter (Kim et al. 1981). The virions are found

embedded in inclusion bodies (fig. 149) in ultrathin sections

made from symptom-bearing infected leaf tissue. The

circular inclusion bodies are found in both the cytoplasm and

in the nucleus. There are two centrifugal components in

ultracentrifuged linear-log sucrose density gradients (Kim et

al. 1981). In ultracentrifuged cesium chloride step gradients,

the virus forms two distinct bands of densities 1.3 and 1.4

g/cm\ whereas in a sibling tube of cauliflower mosaic virus

(CaMV) a single band was formed at 1.35 gm/cm'. In

one-way tests, purified RRSV did not react with CaMV

antiserum in agar gel double diffusion tests nor in

enzyme-linked immunosorbent assays (ELISA) (Kim et al.

1981). In two-way agar gel tests with RRSV and CaMV

antiserum, no serological relationship was shown between

the two viruses (D. C. Ramsdell, unpublished data).

Figure 148. — Red ringspot infected leaves of cv.

'Blueray' showing typical reddish-brown circular leaf

spots, which appear on older leaves in the late summer.

Younger leaves will usually not exhibit these spots.

i

Figure 149. — An inclusion body from a red ringspot

infected blueberry leaf showing embedded virions

(arrow). Bar represents 500 nm.

Detection and Identification

Symptomatology is a useful means of detecting red ringspot,

provided that one is cognizant of the possible confusion with

the symptoms caused by powdery mildew infection of leaves.

Symptoms seen in cv. 'Bluetta' must be confirmed by further

tests to eliminate the possibility that they are the result of a

genetic disorder. If one is testing plants for a clean stock

program, tests beyond visual inspection are necessary to

detect symptomless infection. Budding or whip grafting from

stems from suspected diseased bushes to healthy very

susceptible cultivars, for example, 'Blueray', 'Burlington',

'Cabot', or 'Darrow' should be done in the spring just before

bud break. Symptoms may develop within 3 mo, but longer

observation is advisable. Methods of direct detection using

ELISA are being developed (D. C. Ramsdell, unpublished

data).

122
Control Procedures

The use of disease-free plants and roguing of diseased bushes

from the field are the only currently recommended measures

for control, until the vector is determined. Stretch and Scott

(1977) have published a method for producing red

ringspot-free softwood cuttings based upon extensive indexing. They have also shown that heat treatment of red

ringspot diseased plants at 37°C for 8 wk did not eliminate

RRSV from propagants taken from resulting new shoot

growth.

J

^^

Ringspot of Cranberry//

By A. W. IStretch '

Additional Common Names

None.

History and Geographic Distribution

The disease was first reported to occur on cranberry in New

Jersey in 1962 by Stretch (1964). It was observed in

Wisconsin in 1963 by Boone (1966). No other published

reports of occurrence have been made, but there is a strong

possibility that the disease could be found in areas where

vines originating in New Jersey were grown.

Economic Importance

Ringspot causes malformation and necrosis of berries of the

cv. 'Searles', and adversely affects the keeping quality of

fresh berries (Boone 1967). Distribution of the disease is so

limited, however, particularly in 'Searles', that the total

economic loss is negligible.

Symptoms on Natural and Experimental Hosts

Cranberry fruits from affected plants show pale, circular

patches or whitish rings. The rings on the cv. 'Howes' (fig.

150) are usually larger and more distinctive than those on

'Searles'. Where the berries are only slightly colored, the

area within the rings is a much deeper red than the area

outside. Affected berries of 'Searles' are often malformed

(fig. 151), and many of them show necrosis at the blossom

end (fig. 151). In extreme cases, entire berries are necrotic.

Ringspot symptoms are also produced on the leaves (fig.

152). These become apparent when the leaves assume their

reddish autumn color; the rings stay green, while the

remainder of the leaf turns red. No information on symptoms

in experimental hosts is available.

Symptoms on Indicator Hosts

At present, no information is available.

Natural and Experimental Transmission

At present, no information is available.

Properties of the Causal Agent

The causal agent has not been positively identified. K. S.

Kim (unpublished data) has observed viruslike particles and

^1^^^

Figure 150. — Ringspot on the fruit of the cranberry cv.

'd

"Howes'. (Courtesy D. M. Boone.)

^P^'^W^

I

a

(^f^f^ %^

Figure 15!. — Ringspot symptoms on the cranberry cv.

'Searles' showing necrosis (bottom two rows) compared

with healthy fruit (upper row). (Courtesy D. M.

Boone.)

associated inclusion bodies in diseased cranberry leaf tissue.

The observed bodies are similar to the caulimovirus type

recently reported associated with blueberry red ringspot

disease (Kim et al. 1981).

Detection and Identification

Ring symptoms produced on the fruit and leaves are good

indicators. The rings are particularly prominent on the cv.

'Howes'.

Control Procedures

The use of diseased vines should be avoided in planting new

cranberry beds. No information is available on thermotherapy of this disease.

123
Figure 152. — Leaf symptoms of ringspot of cranberry.

(Courtesy D. M. Boone.)

Vaccinium Literature Cited

Blattny, C, Jr., 1963. Die Übertragung der Hexenbesenkrankheit der Heidelbeeren {Vaccinium myrtillus L.) durch

die Zikade Idionus cruentatus Panz. Phytopathologische

Zeitschrift 49:203-205.

and V. Vana. 1974. Mycoplasma-like organisms in

Vaccinium myrtillus L. infected with blueberry witches'-

broom. Biología Plantarum (Praha) 16:476-478.

Blattny, C, Sr., and B. Stafy. 1940. Atlas skodlivych

cinitelfl ovocnych plodin. [Atlas of factors detrimental to

fruit production.] |ln Czech.) Prague.

and C. Blattny, Jr. 1970. Blueberry witches'-broom.

p. 177-179. In Virus diseases of small fruits and grapevines.

Frazier, N. W., editor, University of California, Division of

Agricultural Sciences. Berkeley, 290 p.

Boone, D. M. 1966. Ringspot disease of cranberry. Plant

Disease Reporter 50:543-545.

1967. A cranberry ringspot disease injuring the

Searles variety. Cranberries 31:14-15.

Bos, L. 1960. A witches'-broom virus disease of Vaccinium

myrtillus in The Netherlands. Tijdschrift over Plantenziekten

66:259-263.

Camp, W. H. 1945. The North American blueberries with

notes on the other groups of Vacciniacae. Brittonia

5:203-275.

Cation, D. 1942. The rosette mosaic disease of peach.

Michigan Agricultural Experiment Station Quarterly Bulletin

No. 180, 24 p.

1951. Rosette Mosaic, p. 14-16. In Virus diseases

and other disorders with viruslike symptoms of stone fruits in

North America. U.S. Department of Agriculture, Agriculture

Handbook No. 10, 276 p.

124
Chen, T. A. 1971. Mycoplasma-like organisms in sieve tube

elements of plants infected with blueberry stunt and

cranberry false blossom. Phytopathology 61:233-236.

Converse, R. H., and D. C. Ramsdell. 1982. Occurrence of

tomato and tobacco ringspot viruses and of dagger and other

nematodes associated with cultivated highbush blueberries in

Oregon. Plant Disease 66:710-712.

Dale, J. L., and J. N. Moore. 1978. Blueberry disorder

possibly caused by mycoplasma. Arkansas Farm Research

27:16.

and C. M. Mainland. 1981. Stunt disease m

rabbiteye blueberry. HortScience 16:313-314.

Dias, H. F. 1975. Peach rosette mosaic virus. Descriptions of

Plant Viruses No. 150. Commonwealth Mycological Institute

and the Association of Applied Biologists. Kew, Surrey,

England. Unpaged.

and D. Cation. 1976. The characterization of a virus

responsible for peach rosette mosaic and grape decline in

Michigan. Canadian Journal of Botany 54:1228-1239.

Dobroscky, I. D. 1929. Cranberry false blossom spread by a

leafhopper. Science 70:635.

1931. Studies on cranberry false blossom disease and

its insect vector. Boyce Thompson Institute Contributions

3:59-83.

Frazier, N. W., editor. 1970. Virus diseases of small fruits

and grapevines. University of California Division of

Agricultural Sciences. Berkeley, 290 p.

Fulton, R. H., and D. Cation. 1959. Destruction of inoculum

or possible transmitting agent of peach rosette mosaic virus

by soil drenching with chlordane. Plant Disease Reporter

43:991-992.

Gocio, M. J., and J. L. Dale. 1982. Investigation of

blueberry stunt disease in Arkansas. Plant Disease 66:244-

245.

Griffin, G. D., J. E. Huguelet, and J. W. Nelson. 1963.

Xiphinema americanum as a vector of necrotic ringspot virus

of blueberry. Plant Disease Reporter 47:703-704.

Harrison, B. D., and A. F. Murant. 1977. Nepovirus group.

Descriptions of Plant Viruses No. 185. Commonwealth

Mycological Institute and the Association of Applied

Biologists. Kew, Surrey, England. Unpaged.

Hartmann, J. X., J. F. Bath, and G. R. Hooper 1973.

Electron microscopy of virus-like particles from shoestring-diseased highbush blueberry, Vaccinium corymbosum

L. Phytopathology 63:432-436.

G. R. Hooper, and J. E. Bath. 1972. Occurrence and

nature of mycoplasma-like organisms in stunt disease of

Michigan highbush blueberry. Michigan Academician 4:461-

467.

Hutchinson, M. T. 1950. Can you recognize the symptoms

of stunt disease? Proceedings of the Nineteenth Annual

Blueberry Open House 19:9-11.

. and E. H. Vamey. 1954. Ringspot: A virus disease

of cultivated blueberry. Plant Disease Reporter 38:260-263.

1955. An ecological study of the leafhopper vectors

of blueberry stunt. Journal of Economic Entomology 48:1-8.

A. C. Goheen, and E. H. Vamey. 1960. Wild

sources of blueberry stunt virus in New Jersey. Phytopathology 50:308-315.

Johnson, F. 1972. Tomato ringspot virus of blueberries in

Washington. Phytopathology 62:1004. [Abstract.]

Kegler, H., H. M. Müller, H. Kleinhempel, and T. D.

Vederevskaja. 1973. Untersuchungen über den Kirschenverfall und die Hexenbesenkrankheit der Heidelbeere. Nachrichtenblatt für den Pflanzenschutzdienst in der DDR 27:5-8.

Kim, K. S., D. C. Ramsdell, J. M. Gillett, and J. P. Fulton.

1981. Virions and ultrastructural changes associated with

blueberry red ringspot disease. Phytopathology 71:673-678.

Kunkel, L. O. 1945. Studies on cranberry false blossom.

Phytopathology 35:805-821.

Leeuw, G. T. N. de. 1975. Presence of mycoplasma-like

organisms in phloem of witches'-broom diseased Vaccinium

myrtillus plants in The Netherlands. Phytopathologische

Zeitschrift 83:91-94.

Lesney, M. S., D. C. Ramsdell, and M. D. Sun. 1978.

Etiology of blueberry shoestring disease and some properties

of the causal virus. Phytopathology 68:295-300.

Lister, R. M., L. C. Raniere, and E. H. Vamey. 1963.

Relationships of viruses associated with ringspot diseases of

blueberry. Phytopathology 53:1031-1035.

Lockhart, C. L., and I. V. Hall. 1962. Note on an indication

of shoestring virus in the lowbush blueberry Vaccinium

angustifolium Ait. Canadian Journal of Botany 40:1561-

1562.

Maramarosch, K. 1955. Transmission of blueberry stunt

virus by Scaphytopius magdalensis. Journal of Economic

Entomology 48:106.

MartelH, G. P., D. GallitelU, P. Abracheva, V. Savino, and

A. Quaquarelli. 1977. Some properties of grapevine

Bulgarian latent virus. Annals of Applied Biology 85:51-58.

A. Quaquarelli, and D. GallitelU. 1978. Grapevine

Bulgarian latent virus. Descriptions of Plant Viruses No.

186. Commonwealth Mycological Institute and the Association of Applied Biologists. Kew, Surrey, England. Unpaged.

125
McGuire, J. M. 1964. Efficiency of Xiphinema americanum

as a vector of tobacco ringspot virus. Phytopathology

54:799-801.

and S. L. Wickizer. 1979. Occurrence of necrotic

ringspot of blueberry in Arkansas. Arkansas Farm Research

29:3-5.

Paulechova, K. 1972. The occurrence of red ringspot virus

disease of blueberry in Czechoslavakia. Biología (Bratislava)

27:791-793.

Ramsdell, D. C. 1978. A strain of tobacco ringspot virus

associated with a decline disease of 'Jersey' highbush

blueberry. Plant Disease Reporter 62:1047-1051.

1979. Physical and chemical properties of blueberry

shoestring virus. Phytopathology 69:1087-1091.

R. W. Andrews, J. M. Gillett, and C. E. Morris.

1979. A comparison between enzyme-linked immunosorbent

assay (ELISA) and Chenopodium quinoa for detection of

peach rosette mosaic virus in 'Concord' grapes. Plant

Disease Reporter 63:74-78.

and J. M. Gillett. 1981. Peach rosette mosaic virus in

highbush blueberry. Plant Disease Reporter 65:757-758.

and R. L. Myers. 1974. Peach rosette mosaic virus.

symptomatology and nematodes associated with grapevine

"degeneration" in Michigan. Phytopathology 64:1174-1178.

and R. L. Myers. 1978. Epidemiology of peach

rosette mosaic virus in a Concord grape vineyard. Phytopathology 68:447-450.

and R. Stace-Smith. 1979a. Blueberry leaf mottle, a

new disease of high bush blueberry. Acta Horticulturae

95:37-45.

and R. Stace-Smith. 1979b. Blueberry shoestring

virus. Descriptions of Plant Viruses No. 204. Commonwealth Mycological Institute and the Association of Applied

Biologists. Kew, Surrey, England. Unpaged.

and R. Stace-Smith. 1981. Physical and chemical

properties of the particles and ribonucleic acid of blueberry

leaf mottle virus. Phytopathology 71:468-472.

Raniere, L. C. 1960. Responses of cultivated highbush

blueberry varieties to the known blueberry viruses. Proceedings of the Twenty-eighth Annual Blueberry Open House

28:18-20.

Shear, C. L. 1908. Cranberry diseases in Wisconsin.

Wisconsin State Cranberry Growers' Association Annual

Report 21:17-21.

Stace-Smith, R. 1970a. Tobacco ringspot virus. Descriptions

of plant viruses No. 17. Commonwealth Mycological

Institute and the Association of Applied Biologists. Kew,

Surrey, England. Unpaged.

1970b. Tomato ringspot virus. Descriptions of Plant

1964. Necrotic ringspot virus of blueberry, Vacci- 50241 [Abstract 1

Viruses No. 18. Commonwealth Mycological Institute and

the Association of Applied Biologists. Kew, Surrey,

England. Unpaged.

Stevens, N. E. 1931. The spread of cranberry false blossom

in the United States. U.S. Department of Agriculture

Circular No. 147, 19 p.

Stretch, A. W. 1964. Cranberry disease investigations —

1962. Proceedings of the American Cranberry Growers'

Association 1961-64:32-33.

and D. H. Scott. 1977. Production of highbush

blueberries free of red ringspot disease. Plant Disease

Reporter 61:605-607.

Téliz, D., R. G. Grogan, and B. F. Lownsbery. 1966.

Transmission of tomato ringspot, peach yellow-bud mosaic

and grape yellow-vein viruses by Xiphinema americanum.

Phytopathology 56:658-663.

Tjepkema, J. P., J. A. Knierim, and N. Knobloch. 1967.

The plant-parasitic nematodes associated with cultivated

blueberries in Michigan. Michigan Agricultural Experiment

Station Quarterly Bulletin 50:37-45.

Tomlinson, W. E., Jr., P. E. Marucci, and C. A. Doehlert.

1950. Leafhopper transmission of blueberry stunt disease.

Journal of Economic Entomology 43:658-662.

Uschdraweit, H. A. 1961. Eine für Deutschland neue Viróse

bei Vaccinium myrtillus. Phytopathologische Zeitschrift

40:416-419.

Uyemoto, J. K., E. F. Taschenberg, and D. K. Hummer.

1977. Isolation and identification of a strain of grapevine

Bulgarian latent virus in Concord grapevine in New York

State. Plant Disease Reporter 61:949-953.

Vamey, E. H. 1957. Mosaic and shoestring, virus diseases of

cultivated blueberry in New Jersey. Phytopathology 47:307-

309.

and L. C. Raniere. 1960. Necrotic ringspot, a new

virus disease of cultivated blueberry. Phytopathology

nium corymbosum L., and its identity. Ph.D. thesis, Rutgers

University, New Brunswick, New Jersey. 48 p. Wilcox, R. B. 1942. Blueberry stunt, a virus disease. Plant

Disease Reporter 26:211-213.

126
v^jSection 3.

yjVirus and Viruslike Diseases of Ribes

(Gooseberry and Black and Red Currant)/^

Introduction

By R.jCasper

During the last 10 yrs, no new major virus diseases of Ribes

crops have been detected. Some of the diseases of Ribes

crops are still restricted to certain areas or even single fields.

Others are widespread and common, but most of them do not

cause heavy losses in yield.

Black currant reversion is certainly the major disease of this

crop in Europe and is found in most areas growing black

currants. Many investigations on the cause of the disease

have been undertaken, but the causal agent is still not

defined. Reports about potato virus Y as the cause of black

currant reversion have not been confirmed despite careful

investigations in other laboratories. These reports are

probably based on an unnoticed virus transmission by aphids

in the greenhouse. Despite other assumptions published

during recent years, the causal agent of black currant

reversion remains unknown.

Since berry crops have received increasing attention in recent

years, interest in some of the poorly understood Ribes

diseases caused by viruses or viruslike agents may grow and

result in further useful research.

,v

^y Defection of Virus and Viruslike Diseases in RibeSjy

By A. N. JAdams and J. M.¿Thresh ^

Many of the viruses infecting Ribes crops cause latent

infection or slight symptoms that may be restricted to only a

small part of the plant. For detection and diagnosis, one

should either use serological techniques where possible or

inoculate indicator plants mechanically by vectors or by

grafts.

Graft transmission. Techniques that do not involve buds are

recommended to avoid transferring eriophyid mites (see

chapter in black currant section on "Viruslike Disorders," p.

142), which damage growth and cause viruslike symptoms.

Good results have been obtained by using patches of bark in

June, July, and August. The bark can be held in place with

polythene tape. Earlier in the season, or when working with

young seedlings, graft-transmissible diseases can be transferred in "chips" from unhardened green stem tissue. The

chips may be held in place with self-adhesive bandages.

Mechanical transmission. Several viruses infecting Ribes

can be inoculated to herbaceous plants, but extracts made

with buffer are usually only slightly infectious. The addition

to extraction buffers of either nicotine (1-2% v/v).

polyethylene glycol (mol. wt. 4000 or 6000), or polyvinyl

pyrrolidone (mol. wt. 24,000 or 44,000, 1-2% w/v) greatly

increases infectivity.

Ribes plants are very difficult to infect by mechanical

inoculation. Best results are obtained by using very young

seedlings grown from seeds extracted at harvest, sown in

trays of soil, and stored at 1°C. After several weeks, the trays

can be withdrawn as required and moved to higher

temperatures to provide a succession of seedlings.

Serology. Until recently, Ribes viruses could be diagnosed

reliably by serology only after transfer to herbaceous hosts.

Cucumber mosaic and arabis mosaic viruses, however, can

be detected in bud or leaf extracts of infected black currant by

enzyme-linked immunosorbent assay (ELISA). ELISA

testing of extracts from Ribes plants would probably be

successful with other viruses for which good quality antisera

are available. Such tests are likely to be at least as sensitive as

inoculation to herbaceous plants. Extracts from Ribes for

ELISA tests are best made with polyvinyl pyrrolidone, mol.

wt. 24,000 or 44,000 at 2% w/v in the buffer (Clark et al.

1976).

Before ELISA, or any other test, can be reliably used for

indexing, a detailed study should be made of the seasonal

distribution of the causal agent in the host. The sampling date

and tissue type can then be selected to maximize the chances

of collecting samples from infected bushes that contain

detectable amounts of this agent.

Indicator plants. These are shown in table 7.

127
Table 7.—Detection of virus and viruslike diseases of Ribes crops

Ribes host plant infected Indicator plants

Vectors and viruses

or viruslike agents Naturally Experimentally Herbaceousi Woody

VECTORS: APHIDS

Cucumber mosaic^

Vein banding

Black currant

Red currant

Ribes aureum

Black currant

Gooseberry

Red currant

VECTOR: ERIOPHYID MITE

Reversion Black currant

Red currant

R. alpinum

R. bracteosum

R. 'carrierei

R. rubrum

var. pubescens

R. spicatum

VECTORS: NEMATODES

Arabis mosaic^

Raspberry ringspot2

Strawberry latent

ringspot2

Tomato ringspot2

(American currant

mosaic)

Tobacco rattle2

VECTOR: UNKNOWN

Black currant

yellows

Gooseberry mosaic

Interveinal white

mosaic

Yellow leaf spot

(European currant

mosaic)

Black currant

Red currant

Gooseberry

Black currant

Red currant

Gooseberry

R. sanguineum

Black currant

Red currant

Black currant

Red currant

Red currant

Black currant

Gooseberry

Red currant

Red currant

Gooseberry

R. aureum

R. aureum

R. sanguineum

R. aureum

R. sanguineum

C. amaranticolor (L)

C. quinoa (L)

TV. tabacum (S)

Black currant

'Amos Black'

Black currant

*Amos Black'

Gooseberry seedlings

'Leveller'

Red currant seedlings

'Jonkheer van Tets'

Black currant

'Baldwin'

'Öjebyn'

C. amaranticolor (S)

C. quinoa (S)

N. tabacum (S)

C. amaranticolor (L)

C. quinoa (S)

N. tabacum (S)

C. amaranticolor (S)

C. quinoa (S)

N. tabacum (S)

C amaranticolor (S)

C. quinoa (S)

N. tabacum (S)

N. tabacum (S)

C. quinoa (L)

Black currant

Red currant

R. divaricatum

R. tenue

R. triste

Black currant

R. sanguineum

C. quinoa (S)

N. rustica (S)

Black currant

'Amos Black'

Black currant

'Amos Black'

Red currant

'Clemenceau'

Black currant

'Amos Black'

Gooseberry

'Whitesmith'

Black currant

'Blacksmith'

'Öjebyn'

Red currant

'Laxton's No. 1'

'Fay's Prolific'

1 Herbaceous plants susceptible to sap-inoculation become infected locally (L) or systemically (S). C

N. = species of Nicotiana.

^Antisera available.

species of Chenopodium,

128
Virus and Viruslike Diseases of Gooseberry

Aphid-Borne Diseases

^

Gooseberry Vein Banding.

By A. N.jAdams and A. F. jPosnette

Additional Common Names

Adembänderung der Stachelbeere; gooseberry mosaic; zilkova mosaiká angrestu.

History and Geograptiic Distribution

What seems to have been gooseberry vein banding disease

was first noted in Czechoslovakia (Blattny 1930), but it was

not shown to be graft and aphid transmissible until much later

(Posnette 1952). Infection is widespread in Europe but is not

reported from elsewhere. Tasmania is one of the few

countries where gooseberries have been grown extensively

without infection, probably because the original introductions were healthy and several of the known aphid vectors are

absent (Posnette 1970).

Economic Importance

The disease is obviously severe in cultivars such as 'Leveller'

but is usually mild in others such as 'Careless', which is the

most widely grown cultivar in England. Commercial

plantations of the older cultivars are almost totally infected in

England, and the disease is common in Europe (Kleinhempel

1968; Putz 1972; Thomsen 7970).

A meristem clone of cv. 'Careless' outyielded otherwise

comparable bushes infected with gooseberry vein banding

disease (GVBD) by approximately 15%, and cuttings from

uninfected bushes grew faster and survived better than those

from infected bushes (Adams 1979). The economic effects in

different regions will depend on the sensitivity of the

predominant cultivars.

Symptoms on Natural and Experimental Hosts

GVBD has been transmitted only within the genus Ribes

despite attempts to infect herbaceous plants, including

alternate hosts of the vectors (East Mailing Research Station

1970).

All cultivars of gooseberry, black currant, and red currant

appear to be susceptible. Many other Ribes species or hybrids

develop typical symptoms when inoculated with GVBD

including: Ribes x holosericeum Otto & Dietr. (R. petraeum

Wulf X R. rubrum L.), R. Koehneanum Jancz. (R.

muhiflorum Kit. ex R. & S. x R. sativum Syme), R.

midtiflorum Kit., R. leptanthum A. Gray, R. longeracemosum Franch., R. x robustum Jancz. (R. niveum Lindl. x R.

inerme Rydb.), R. x rusticum Jancz. (R. uva-crispa L. x R.

hirtellum Michx.), R. sativum Syme, and R. Watsonianum

Koehne. Symptoms have not been seen in R. divaricatum

Dougl. or in an F1 hybrid between R. sanguineum Pursh and

R. grossularia L. inoculated with GVBD. Some trial

selections with R. divaricatum or R. sanguineum ancestors

have remained symptomless for several years after inoculation, but it is not known whether this is due to resistance,

tolerance, or immunity (Knight and Manwell 1980; Knight

1981).

Figure 153. — Vein banding in gooseberry cv. 'Leveller'.

129
Symptoms in gooseberry: The main veins are banded with

translucent, pale-yellow areas. In the first leaves to expand in

the spring, the whole vein reticulum may be banded;

however, in leaves developing on extension growth, only

single veins or short lengths of the main veins may be

affected. Leaves with vein banding are often chlorotic and

distorted asymmetrically (fig. 153). Seedlings with severe

leaf symptoms are stunted; the rooting and vigor of cuttings

are depressed by this disease.

Symptoms in black currant: The first leaves to expand in the

spring show pale-yellow vein banding, usually restricted to

one side of the lamina. Later leaves develop a clearing and

yellow banding of the main veins which in some cultivars is

restricted to individual lobes. The graft-transmitted vein

banding is more precisely delineated than the more diffuse

mottle caused by aphid toxins. The two symptoms may also

be distinguished seasonally, since the former symptom

appears before large infestations of aphids.

Symptoms in red currant: Leaves formed early in the spring

show yellow banding of the main veins. Later, leaves

produced on extension shoots may have the vein reticulum

cleared or narrowly banded with translucent tissue.

Indicator hosts: Seedlings of sensitive gooseberry cultivars,

such as 'Leveller', can be used as indicators, but they are

slow growing, possess spines, and are prone to infection by

powdery mildew, Sphaerotheca mors-uvae (Schw.) Berk. &

Curt. Black currant cv. 'Amos Black' is without spines, but

it is susceptible to powdery mildew; the conspicuous

symptoms are transient. Two second backcross derivatives of

R. sanguineum x gooseberry East Mailing Research Station

selection numbers (1385/81 and 1385/90) with reduced

spines react with distinct symptoms lasting for several weeks

and may prove to be useful indicators, although they are

susceptible to powdery mildew (Knight 1981).

Natural and Experimental Transmission

GVBD is readily transmitted by chip budding or patch

grafting to other gooseberries and to black currant. This

disease has only occasionally been transmitted from

gooseberry to red currant (Karl and Kleinhempel 1969).

The causal agent has not been transmitted by sap inoculation

to Ribes test plants or herbaceous species.

The causal agent has been transmitted from gooseberry plants

by Aphis grossulariae Kalt., Aphis schneiden (Born.),

Hyperomyzus pallidus H.R.L., Nasonovia ribisnigri (Mosley) (Posnette 1952, 1964), Cryptomyzus ribis (L.),

Hyperomyzus lactucae (L.), and Myzus persicae (Sulz.)

(Karl and Kleinhempel 1969). Transmission was semipersistent, aphids requiring an acquisition access period of at least

30 min, the infection rates increasing with longer feeding

periods. Aphids were not inoculative after 3 hr of test feeding

(Posnette 796^).

Slow natural spread occurs in gooseberry in England. In a

field trial over a 5-yr period at East Mailing, only 2 out of 50

gooseberry seedlings became infected (Posnette 7964).

Reinfection of bushes of a meristem-derived clone of cv.

'Careless', at seven sites in Kent and Wisbech, Cambridgeshire, was also slow. Only 5 of 496 bushes became

infected in 6 yr, although they were adjacent to infected

commercial material at six of the seven sites (Adams 7979).

This contrasts with the almost total infection of most

commercial cultivars. Many of these are very old, as they

were raised in private gardens in the north of England for

exhibition at gooseberry-growing societies, which were

popular in the 18th and 19th centuries (Rake 7958). Slow

spread combined with indiscriminate vegetative propagation

may have resulted in the present situation.

Factors limiting spread are migratory habits of the most

prevalent aphid vectors and nonpersistence of the virus in the

vector. Alatae of only two vectors feed on Ribes during the

summer, those of the other species migrating to herbaceous

host plants in the Compositae.

Properties of the Causal Agent

Nothing is known of the morphology of the causal agent nor

of its properties in vitro.

Detection and Identification

The leaf symptoms of infection with GVBD are distinctive

and are unlikely to be confused with any other disorder

except the effects of aphid toxicity. Aphids, particularly

Hyperomyzus lactucae, produce a yellow, diffuse vein

banding, usually accompanied by interveinal mottling, in

contrast to the translucent clearing along the veins caused by

the graft-transmissible disease. Correct diagnosis is difficult

when bushes are infested with aphids and for some time after

aphids have flown away or been killed by sprays;

consequently, early spring is the best time for inspection.

Control Procedures

Gooseberry plants are heat sensitive, and the usual procedure

of propagating tip scions from heat-treated plants has been

unsuccessful. Plants of 'Careless' gooseberry free of

gooseberry vein banding disease were raised by meristem

culture (Jones and Vine 1968). Recent improvements to the

technique (Hedtrich and Feucht 7987) should facilitate

further application.

The very slow reinfection of plants with gooseberry vein

banding disease indicates that healthy plants will remain

virus-free with little isolation. The prospects of controlling

this disease by the issue of healthy planting material are

therefore good.

130
Nematode-Borne Diseases

<^

V

0¿

Gooseberry Deterioration,y

By F. A. van derJMeer

L- —

Additional Common Names

None, but it is caused by raspberry ringspot virus.

History and Geographic Distribution

Reported from The Netherlands by Houtman (1951). Van der

Meer (I960, 1965a) isolated raspberry ringspot virus (RRV)

from affected bushes, whereas this virus could not be

detected in healthy-looking bushes. The disease has not been

reported from other countries.

Economic Importance

Very little.

Symptoms on Natural and Experimental Hosts

Natural infection with RRV has been found in the gooseberry

cvs. 'Whitesmith' and 'Whynham's Industry', which are the

only ones grown in the area where the disease occurs.

Infected bushes of cv. 'Whynham's Industry' show an

indistinct mosaic of the leaves. Berries are small and

misshapen and ripen very late in summer (fig. 154). Affected

bushes usually die within a few years. RRV-infected bushes

of cv. 'Whitesmith' do not show symptoms.

Experimentally infected plants of Chenopodium quinoa

Willd. develop necrotic local lesions and systemic necrosis,

whereas C. amanmticolor Coste and Reyn. develops only

necrotic local lesions. The virus causes symptoms in several

other herbaceous hosts.

Natural and Experimental Transmission

The virus is assumed to be transmitted by Longidorus

elongatiis (de Man.). This nematode is common in the area

where the disease has been found and is known to infect red

currant with RRV. In comparison with red currant,

gooseberries are rather resistant to natural infection.

Experimentally, the virus can be transmitted to herbaceous

hosts by sap inoculation. Red currant seedlings inoculated

with sap from infected tobacco developed definite symptoms

of spoon leaf (van der Meer 1965a). (See "Spoon Leaf of Red

Currant," p. 146.)

Properties of the Causal Agent

Because RRV occurs only in deteriorating plants of cv.

'Whynham's Industry' and not in healthy plants of this

cultivar, RRV is believed to be the cause of gooseberry

deterioration. RRV isolates from red currant and gooseberry

are indistinguishable serologically from each other and from

Figure 154. — Gcx)seben7 deterioration: Top, healthy

shoot; below, shoot of deteriorated 'Whynham's

Industry'.

isolates obtained from other hosts in Scotland (Maat 1965).

(For additional information on properties of RRV, see the

Ruhus section, p. 214-219.)

Detection and Identification

Infection can be detected by sap inoculation to C. quinoa and

other herbaceous hosts. Identification is only possible by

serological tests.

Control Procedures

Tests on C. quinoa should be made when selecting healthy

gooseberry stocks. Sensitive cultivars like 'Whynham's

Industry' should not be grown on RRV-infested land. There

is no information on therapy of infected plants.

^ALatent Infection of Gooseberry with Arabis Mosaic

Virus// I

By F. A. van derJMeer

Additional Common Names

None.

History and Geographic Distribution

Latent infection of gooseberry with arabis mosaic virus

(AMV) has only been reported from East Germany

(Kleinhempel 1970, 1972).

Economic Importance

Very little.

131
Symptoms on Natural and Experimental Hosts

Naturally infected gooseberries (Kleinhempel 1972) and red

currants (Kleinhempel 7972; Thresh 1967) do not show

symptoms. On naturally infected black currants, AMV

causes chlorotic blotches of the first leaves. This is followed

by mottle and ringspot symptoms in May. Later developing

leaves are virtually symptomless (Thresh 1966b).

Experimentally infected Chenopodium quinoa Willd. and C.

amaranticolor Coste and Reyn. show many local lesions and

develop systemic mosaic and stunting. (For details on further

hosts and experimental hosts, see "European Nepoviruses in

Strawberry," p. 46.)

Natural and Experimental Transmission

AMV is transmitted by the nematode Xiphinema diversicaudatum (Micoletsky) to several crop hosts.

Experimentally, the virus can be transmitted from gooseberry

to herbaceous host by sap inoculation.

Properties of the Causal Agent

No details are reported about precise serological relationships

between AMV isolates from gooseberry and those obtained

from other hosts. (See the Ruhus section, p. 204, for further

details on properties of AMV.)

Detection and Identification

Detectable by sap inoculation to C. quinoa. Identification is

only possible by serological tests.

Control Procedures

Tests on C. quinoa should be made when selecting healthy

gooseberry stocks. There is no information on therapy of

AMV-infected gooseberry.

Viruslike Disorders

Gooseberry Mosaic and Leaf Malformation of Gooseberry

By A. N. Adams

Gooseberry Mosaic

A single gooseberry plant, cv. 'Lady Delamare,' was found

in Poland with a bright yellow mottle and vein yellowing that

was distinct from the normal symptoms of gooseberry vein

banding (Basak and Maskiewicz 1980). The disease was

graft-transmitted to gooseberry cvs. 'Whitesmith' and

'Resistenta', which showed similar symptoms to those on

'Lady Delamare', and to black currant cvs. 'Blacksmith',

'Öjebyn', and 'Roodknop', which reacted with symptoms of

localized, patchy yellowing that gradually spread to most of

the leaf area to resemble black currant yellows (Posnette

1952). Inoculated plants of Ribes divaricatum Dougl., R.

nigrum L. var. europaeum Jancz., R. tenue Jancz., and R.

triste Pall, also showed symptoms but not R. Gordonianum

Lem. {R. aureum Pursh. x R. sanguineum Pursh), R. x

nigrolaria (R. nigrum L. x R. uva-crispa L.), and R.

prostratum L'Her. The disease was apparently latent in red

currant cvs. 'Jonkheer van Tets' and 'Large Red Dutch'.

The host range and symptoms of the disease suggest that it

differs from gooseberry vein banding.

Leaf Malformation of Gooseberry

The 'claw leaf or 'hawthorn leaf condition in England

mentioned by Thresh {1970) was not graft-transmitted. Other

reports of similar malformations and of dieback in Scotland

(Gray 1949; and Gray and Everett 1956) could be records of

spoon leaf. (See "Spoon Leaf of Red Currant," p. 146.)

132
Virus and Viruslike Diseases of Black Currant

Mite-Borne Diseases

y

if.

Reversion of Black Currant v

By A. N.lAdams and J. M.ÎThresh

Additional Common Names

Atavismus; zvrátcemého rybízu.

History and Geographic Distribution

Reversion disease was first described in The Netherlands

(Ritzema Bos 1904) and later in England (Amos and Hatten

1927) where it was already common in gardens and

plantations, usually associated with infestations of the black

currant gall mite {Cecidophyopsis ribis (Westw.)), which had

long been known as a serious pest of black currant. The direct

damage caused by the mite was at first confused with the

effects of the disease agent that it transmits. This is because

reversion and its vector have a complex and unique

relationship with their black currant host (Thresh 1964a).

Reversion has been recorded in virtually all the countries

where black currants are grown. Infection is rare in New

Zealand and Australia, but widespread in most European

countries.

Economic Importance

Reversion is of major importance in Europe, and its effect on

crop yield is severe (Krczal 7976; Cropley et al. 1964). The

disease is less common in Great Britain now, compared with

10 to 15 yr ago because certified bushes have been planted

extensively and endosulfan has been widely used as an

effective acaricide (Thresh and Blandy 1979).

Symptoms on Natural and Experimental Hosts

Black currant is the usual natural host of reversion, but it has

also been recovered from naturally infected Ribes bracteosum Dougl. ex Hook., R. rubrum L. var. pubescens

Swartz and R. X Carrierei Schneid. (R. glutinosum Benth. x

R. nigrum L.) (Thresh 1970), R. alpinum L., R. spicatitm

Robson (a species of red currant growing wild in Finland),

and some commercial cultivars of red currant (Bremer and

Heikinheimo 1980, Rakús 1973). Several other species and

hybrids have been infected by graft inoculation, but none has

given more conspicuous symptoms than black currant.

Symptoms in black currant. All the main commercial black

currant cultivars in Western Europe are susceptible although

there are differences in tolerance to infection. Some Russian

cultivars, derived mostly from R. nigrum L. var. sibiricum

(E. WolO or R. dikuscha Fisch, ex Turcz., are reported as

resistant to infection (Saumjan 1964, Potapov and Grinenko

1968), and some may be immune (Knight and Manwell

1980).

Symptoms in black currant do not appear until the year after

inoculation, and they are at first restricted to one or a few

shoots. One-third to one-half of the bush is affected in the

second year, and infection is fully systemic by the third or

fourth year. The habit of growth is affected, together with

specific effects on the flowers and leaves.

Infection decreases the number and size of the primary leaves

that subtend flowers, and leaves produced during the blossom

period are chlorotic. There is little difference in the amount

of color of the later extension growth, although the shoots of

healthy bushes tend to be fewer and longer than those of

reverted bushes. These differences are not sufficiently great

or constant for routine diagnosis.

The common strains of black currant reversion agent

occurring in Britain and many other European countries

decrease the hairiness of the sepals, so that the flower buds

are almost glabrous and appear brightly colored, compared

with the gray, downy appearance of normal buds (fig. 155).

The difference is readily apparent unless the bushes are wet

or infected with an unusually avirulent strain (Thresh 1971).

Figure 155. —Left, healthy flower buds; right, glabrous flower buds of black currant with reversion.

In the U.S.S.R., Scandinavia, and some other areas, the

flowers of reverted bushes are often glabrous and severely

malformed, with the style elongated, stamens absent, and the

petals sepallike in appearance (fig. 156). The "double"

flowers seem to be caused by a particular strain of reversion

that is uncommon in Great Britain and Western Europe below

the Scandanavian Peninsula.

Infected bushes develop leaves that are flatter than usual and

have a smaller basal sinus. Infection also decreases the

number of main veins and marginal serrations (fig. 157).

After some experience, these differences can be used for

accurate diagnosis in May, June, or July, when attention

should be given only to leaves on undamaged shoots of the

133
Figure. 156. — A. malformed flowers of black currant

cv. "Rus' infected with reversion from Eastern Europe.

ß, malformed flowers of black currant infected with

reversion in Finland (left). Uninfected flowers on the

right are at the fruit swelling stage. (Courtesy O.

Heikinheimo.)

Figure 157. — Top row. left to right, healthy leaves of

black currant cvs. Baldwin'. 'Ben Lomond' and Ben

Nevis'; bottom row. leaves of the same cultivars

infected with reversion.

134
extension growth. Forked shoots and those damaged

mechanically or by mites, capsid bugs (Lygocoris pabulinus

(L.)), or other insects develop atypical leaves. A further

complication is the inherent differences between the leaves of

certain cultivars.

Leaves that are invaded by some strains of the reversion

agent develop a nonrecurring chlorotic vein pattern (fig.

158). This was originally thought to be a separate disease

(Posnette 1952). This reversion is of limited diagnostic

value, as symptoms are often slight and restricted to a few

leaves that may be concealed by later growth. Jacob (1976a)

reported an enhancement of chlorotic symptoms by holding

plants under continuous light at 23°C.

Symptoms of infectious variegation are particularly severe

when bushes are also affected by reversion.

Symptoms in red currant. Faint flower and leaf symptoms are

associated with infection in commercial cultivars of red

currants in Finland (Bremer and Heikinheimo 1980). Leaf

malformation and the transient vein pattern typical of the

disease in black currant were observed by Thresh (East

Mailing Research Station 796^) in red currant cultivars

inoculated with reversion from black currant.

Symptoms on indicator hosts. Numerous cultivars are

probably suitable as indicators, but 'Baldwin' (Thresh 1970)

and 'Öjebyn' (Bremer and Heikinheimo 1980) consistently

react with foliar symptoms the year after inoculation.

Natural and Experimental Transmission

Reversion is readily transmitted by various grafting methods,

but some are unsuitable because the mite vector could be

transferred in buds taken from the infected source. This risk

is avoided by using patch or chip grafts. Reversion has not

been transmitted by pollen or seed, and a report of sap

transmission (Jacob 1976a) has not been confirmed. (See

"Properties ofthe Causal Agent," p. 135-136.)

Reversion is transmitted by the gall mite Cecidophyopsis

ribis (Westw.). The disease is transmitted efficiently during

the late spring and early summer when mites disperse from

old galls to the buds of new growth. There is no further

spread until the following year, and mites remain within

infested buds, which become rounded galls and fail to

develop flowers or leaves (Thresh 1965). Disease symptoms

do not develop until the year after infestation. There is

generally a close correlation between the incidence of

reversion disease infection and the distribution of galls during

the previous winter.

There are up to 35,000 mites in a single gall, and several

hundred galls may occur on a heavily infested bush, from

which mites may crawl, leap, or be blown during the

Figure 158. — Black currant leaves showing the

chlorotic vein pattern of reversion. (Courtesy F. A. van

der Meer.)

dispersal period. Insects, said to act as carriers of the mites

(Massée 1928), may spread the disease to plants growing

considerable distances from large sources of infection

(Thresh 1966a). A feature of crucial importance in

epidemiology is that bushes infected with reversion are much

more susceptible to infestation by mites than healthy ones

(Thresh 1964a).

Some cultivars of black currant derived from R. nigrum var.

sibiricum are resistant to gall mites (Pavlova 1964, Anderson

1971) and react to infestation by forming necrotic tissues that

support few or no mites. Gooseberry has been used as a

donor for mite resistance in black currant, and progenies with

the single gene Ce for resistance appear to be virtually

immune (Knight et al. 1974), although a small proportion of

plants become reverted when exposed to very heavy

infestations (Knight 1981). A nongall-forming strain of C.

ribis has been found in England on Ribes, including

gooseberry and gooseberry x black currant hybrids. The mite

occurs in relatively low numbers and is not known to

transmit reversion (Easterbrook 1980).

There is little information on the transmission process owing

to the difficulty of transferring mites and their usual

requirement to feed within galls or buds. The disease has

been transmitted by single mites that were eradicated by

endrin 4 h after transfer from galls to healthy seedlings

(Thresh 1970). A minimum acquisition access time of 3 h

and retention in the mite for up to 25 days were reported by

Jacob {1976b).

Properties of the Causal Agent

Reversion has been associated with: mycoplasmalike organisms (Zirka et al. 1977), bacteria (Silvere and Remeikis

1973), and potato virus Y (Jacob 1976a), but evidence to

confirm that any of these agents cause the disease is lacking.

Although Jacob (1976a) appeared to have fulfilled Koch's

postulates for potato virus Y, this virus could not be detected

135
in other German reverted material either by ELISA or by

immunosorbent electron microscopy by R. Casper, H.

Krczal, and D. Lesemann (unpublished results). Furthermore, potato virus Y was not detected by sap inoculation or

by ELISA in reverted bushes in England (Thresh et al. 1978).

Detection and Identification

Diagnosis depends on the ability to recognize the characteristic effects of reversion on flowers or leaves. If growth is

damaged or malformed and the symptoms are indistinct,

suspect material should be graft-inoculated to 1 -yr-old bushes

of an indicator such as cv. 'Baldwin'.

Control Procedures

Stringent quarantine measures should be enforced to avoid

disseminating mites, additional infection, or further strains of

the disease to countries not already affected.

In countries where reversion occurs, new plantations should

be established with bushes or cuttings from stocks certified as

free from infection. Planting should be upwind, at least 90 m

from any contaminated holding, and routine acaricides

should be used (Ministry of Agriculture 1979). Plantations

should be inspected just before flowering begins, and again

later in the summer for leaf symptoms, to diagnose and

remove infected bushes. These measures are to a large extent

interdependent, and all must be adopted for full effectiveness.

Healthy clones are normally obtainable by selecting

disease-free plants; however, reversion-free plants can be

obtained from diseased bushes by heat therapy and top

grafting to seedlings (CampbeU 1965). Mites can be

eliminated from cuttings by warm water treatment (Savzdarg

1957, Thresh 1964b).

Although there are sources of resistance both to reversion and

to its vector, these characters have not yet been bred into

cultivars that are commercially viable in Western Europe

(Keep 1975). Considerable progress, however, has been

made towards the integration of agronomic qualities, disease

resistance, and gall mite resistance (Keep et al. 1982).

Aphid-Borne Diseases

\^'^.Green Mottle of Black Currant/;

By A. N. [Adams and J. M. Hresh

Additional Common Names

None, but the disease is caused by cucumber mosaic virus.

History and Geographic Distribution

Green mottle of black currant is caused by cucumber mosaic

virus (CMV), a cosmopolitan pathogen with an unusually

wide host range. Infection in black currant was reported in a

few bushes in each of several plantations or nurseries in

England and Wales (Thresh 1966b), in a single bush in

Germany (Kleinhempel 1970), and in cv. Trimorskij

Champion' in the Soviet Far East (Gordejchuk et al. 1977).

Economic Importance

Infected bushes are stunted and bear little crop. Infection

does not seem to spread rapidly between black currant

bushes, and the disease is not sufficiently widespread to be of

economic importance.

Symptoms on Natural and Experimental Hosts

All the main British commercial cultivars of black currant are

susceptible and develop similar symptoms, but there are

differences in tolerance. The cultivar 'Amos Black' is

particularly sensitive and is recommended as an indicator.

CMV causes green mottle disease of red currant and an "arc

mosaic" of the golden currant {Ribes aureum Pursh) in

Germany (Schmelzer 1963). Numerous other weed and

cultivated plants are susceptible, including many standard

indicator plants.

Small, rapidly growing black currant seedlings develop

symptoms 3 or 4 wk after graft inoculation. Established

bushes do not produce symptoms until the following year,

when they are often restricted to the inoculated shoots and

those nearby. Symptoms are very variable. They are seen

best as the leaves become fully expanded and tend to be

inconspicuous in young and senescing leaves. Large sectors

of some leaves become pale green (fig. 159A). At other

times, discoloration is restricted to broad bands along certain

main veins, sometimes giving a "watermark" effect that is

best seen by transmitted light (fig. 1595).

CMV is the only sap-transmissible virus of Ribes crops that

infects tobacco systemically and causes only local lesions in

both Chenopodium amaranticolor Coste & Reyn. and C

quinoa Willd. The latter hosts are particularly sensitive to sap

inoculation and develop necrotic local lesions from which the

virus may be transmitted to other herbaceous host plants.

136
Figure 159. — Green mottle of black currant: A, in

April; B, in June.

Natural and Experimental Transmission

Green mottle disease is readily transmitted by grafting. It is

easily transmitted by sap inoculation to herbaceous hosts but

only occasionally to black currant seedlings. Extracts of

leaves, flowers, roots, or dormant buds in buffer with

nicotine (10 g/L) or polyethylene glycol (mol. wt. 40{X) or

6000) or polyvinyl pyrrolidone (mol. wt. 24,000, 10 g/L) are

highly infectious to C. quinoa (Manwell et al. 1979).

CMV is transmitted in the non-persistent manner by the 60 or

more aphid species known to be vectors (Kennedy et al.

1962). An isolate of CMV from black currant has been

transmitted by Myzus persicae (Sulz.) and by five species that

spend all or part of their life cycles on Ribes crops: Aphis

grossulariae Kalt., A. schneiden (Born.), Cryptomyzus ribis

(L.), Hyperomyzus lactucae (L.), and Nasonovia ribisnigri

(Mosley) (Thresh 1970). The virus is readily transmitted

between herbaceous hosts and from black currant to

herbaceous hosts. Black currant seedlings are infrequently

infected either by aphids from black currant or from

herbaceous hosts.

There is little natural spread within plantations, and infection

seems to spread into or within the crop from weeds or

cultivated hosts, perhaps by aphids that visit black currant

temporarily.

Properties of the Causal Agent

Cucumber mosaic virus has been studied in detail. (See

"Cucumber Mosaic Virus in Raspberry," p. 191, in the

Rubus section of this handbook for some properties of

CMV.) The authoritative review by Francki et al. (7979)

should also be consulted.

Detection and Identification

Suspect bushes can be indexed by sap transmission to

Chenopodium quinoa and other herbaceous hosts or by graft

inoculation to cv. 'Amos Black'. Tests with buds provide an

opportunity to check the health of dormant bushes (Thresh

1970). Extracts from infected black currant leaves made in

June reacted strongly in ELISA tests using an antiserum to

CMV of unknown origin (A. N. Adams, unpublished data).

Control Procedures

Control measures are unnecessary, but care should be taken

to eliminate infected bushes from nursery stocks and those

used for propagation.

Vein Clearing and Vein Net Disease of Black Currant

By A. N. Adams and J. M. Thresh

Additional Common Names

None.

History and Geographic Distribution

Vein clearing and vein net disease was described by Thresh

(1966b) and attributed to infection with gooseberry vein

banding virus. Although this disease is widespread in

gooseberry and red currant, infected black currant bushes are

rare in Britain (Thresh 1966b) and in continental Europe

(Baumann 1974; Kleinhempel 1972; Putz 1972).

Economic Importance

Infection does not seem to be sufficiently widespread to cause

serious losses. Infected bushes are slightly stunted and carry

almost a full crop.

Symptoms on Natural and Experimental Hosts

The disease has only been transmitted within the genus

Ribes.

Gooseberry and red currant develop symptoms typical of vein

banding (Kari and Kleinhempel 7969,- Thresh 7970).

All the principal commercial cultivars of black currant in

Great Britain are susceptible to graft inoculation, but they

differ greatly in their tolerance to infection. 'Baldwin' and

'Wellington XXX' rarely develop symptoms in the field, but

137
'Wellington XXX' has been used as an indicator in Germany

(Baumann 1974). 'Amos Black' and 'Westwick Triumph'

are particularly sensitive, but the latter is not recommended

for use as an indicator because it grows slowly.

Sensitive black currant cultivars develop a broad yellow

banding and occasional clearing of the main veins of the

first-formed leaves that subtend flowers. Later leaves develop

a clearing and narrow yellow banding of the main veins (fig.

160/4). Entire leaves of cv. 'Mendip Cross' are affected in

May and June with a vein net pattern (fig. 160ß). Symptoms

in other cultivars, such as 'Amos Black', are often restricted

to individual lobes of occasional leaves that become slightly

distorted and asymmetrical (fig. 160C).

Natural and Experimental Transmission

The causal agent is readily transmitted by graft inoculation

but not by sap. Black currant seedlings have been infected by

aphids, Nasonovia ribisnigri (Mosley) transferred from

gooseberry with vein banding (Posnette 1964). The causal

agent has been transmitted between seedlings of the

following species by aphids (Karl and Kleinhempel 1969):

from gooseberry to black currant (Hyperomyzus lactucae

(L.)), from black currant to gooseberry and black currant to

black currant (Myzu.s persicae (Sulz.)), and from black

currant to red currant (Cryptomyzus ribi.'i (L.) and H.

lactucae).

Infection in black currant nurseries and plantations spreads

slowly, presumably by aphids.

Properties of the Causal Agent

There is no information on the morphology or properties in

vitro of the causal agent.

Detection and Identification

Infection in sensitive cultivars can be diagnosed in April,

May, or June, provided that aphids have not been allowed to

distort the growth and cause phytotoxicity. In tolerant

cultivars or late in the season, suspect bushes should be graft

inoculated to the sensitive cv. 'Amos Black'.

Control Procedures

Infected bushes should be removed during routine inspection.

Spread is likely to be slow if healthy stocks are planted and

aphids are controlled. No information is available on therapy

of infected cultivars.

Figure 160. — Vein clearing and vein net disease of

black currant: A, in early leaf; B. in cv. 'Mendip Cross'

in midsummer; C, in cv. 'Amos Black' in midsummer.

138
Nematode-Borne Diseases

r

á.

Yellow Mottle of Black Currant^/

By A. N. IAdams and J. M. [Thresh

Additional Common Names

None, caused by Arabis mosaic virus.

History and Geographic Distribution

Yellow mottle of black currant is caused by Arabis mosaic

virus (AMV). Yellow mottle has been reported in only one

English nursery and in a few plantations established with

bushes distributed from it (Thresh 1966b). The virus has been

isolated, once from black currant in France (Putz and Stocky

1971) and once from black currant in the Soviet Far East

(Gordejchuk et a!. 1977).

Economic Importance

Infected bushes produce little fruit and are less vigorous than

healthy ones, but infection does not seem to be sufficiently

widespread to cause serious economic losses.

Symptoms on Natural and Experimental Hosts

AMV has a wide host range in weeds, herbaceous test plants,

and cultivated crops, including gooseberry, red currant,

raspberry, and strawberry.

Isolates from black currant have been graft transmitted to

Ribes aureum Pursh, R. sanguineum Pursh, and all the black

and red currant cultivars tested. The black currant cultivars

reacted similarly with no great differences in sensitivity.

Black currant bushes graft-infected in July or August develop

symptoms the following year, when the first-formed leaves

show a conspicuous yellow mottle (fig. 161/1). This may be

irregularly distributed or may form yellow spots and rings.

Symptoms are less conspicuous on leaves of the extension

growth, and by midsummer the slight specks or flecks on the

leaves are barely detectable, so that diagnosis must be

confirmed by indexing (fig. 161ß).

R. sanguineum reacts similarly to black currant, whereas red

currant cultivars become infected without showing symptoms.

In herbaceous hosts, isolates from black currant behave like

the virulent strains obtained from raspberry. Chenopodium

amaranticolor Coste and Reyn. and C. quinoa Willd. are

particularly sensitive to infection by sap inoculation, and

within 2 wk develop local and systemic symptoms that

closely resemble those caused by strawberry latent ringspot

virus, that is, chlorotic local lesions and systemic chlorosis

and necrosis, particularly in the tip leaves. (See "Raspberry

Figure 161. — Lxaves of black currant with yellow

mottle caused by arabis mosaic virus: A. in an early leaf;

B. in midsuminer.

Yellow Dwarf and Associated Diseases of Rubus Caused by

Arabis Mosaic and Strawberry Latent Ringspot Viruses,"

p. 204.)

Natural and Experimental Transmission

AMV is readily transmitted between woody hosts by graft

inoculation. Extracts of dormant buds or leaves made with

nicotine, polyethylene glycol, or polyvinyl pyrrolidone

included in the buffer are highly infectious to herbaceous

hosts from which the virus is transmissible by sap inoculation

to black currant seedlings.

In Ribes. there have been no transmission experiments with

Xiphinema diversicaudatum (Micoletsky), the nematode

vector of AMV in other crops. X. diversicaudatum was

present in the soil of an infected nursery in England. It is

assumed to be the natural vector, although spread is also

caused by the indiscriminate propagation and sale of infected

cuttings (Thresh 1970).

139
Properties of the Causal Agent

See "Raspberry Yellow Dwarf and Associated Diseases of

Rubus Caused by Arabic Mosaic and Strawberry Latent

Ringspot Viruses," p. 104, for some properties of AMV.

The authoritative review of Murant (1970) should also be

consulted.

Detection and Identification

Black currant cv. 'Amos Black' is a suitable indicator for

graft-inoculation tests.

Infection is readily detected by sap inoculation to Chenopodium quinoa, but further tests are needed to distinguish AMV

from other nepoviruses. (See detailed discussion of nepoviruses in iht Rubus section, p. 204-228.)

AMV is easily detectable by ELISA in extracts of leaves or

buds (Clark et al. 1976).

Control Procedures

Black currant stock should not be placed at sites where virus

and vector are present. Special stocks destined for propagation should be checked to ensure that they are free of

infection. No information is available on the therapy of

infected black currant cultivars.

Vectors Unknown

ÁÍBlack Currant Yellows u

By J. M.JThresh

Additional Common Names

None.

History and Geographic Distribution

Black currant yellows was found in one English nursery

(Posnette 7952) and subsequently in several plantations

established with bushes distributed from it. The disease has

not been reported in other countries, although the term

"yellows" has been applied indiscriminately to other

symptoms not necessarily caused by infection by a

graft-transmissible agent.

Economic Importance

Infected bushes are stunted and their crop is greatly reduced

(Cropley et al. 1964), but infection is not sufficiently

widespread to cause serious economic losses.

Other Nepoviruses Isolated From Black Currant

By A. N. Adams and J. M. Thresh

Strawberry latent ringspot virus (SLRV) was isolated from a

single black currant bush cv. 'Baldwin' growing in Scotland.

The bush was also infected with reversion, and it was not

determined whether SLRV caused specific symptoms in

black currant (Lister 1964).

Two other nepoviruses were detected in black currant in

the Soviet Far East (Gordejchuk et al. 1977). Raspberry

ringspot virus was isolated from the leaves of cvs.

'Primorskij Champion', 'Likemaya', and 'Buraya'; infection

was associated with yellow ringspots in the early spring,

followed by a yellow mottle. Tomato ringspot virus was

isolated from the leaves of black currant plants cv.

'Primorskij Champion' that showed yellow spots and rings.

Tomato black ring virus was isolated from several bushes of

black currant cvs. 'Öjebyn,' 'Sunderby', and 'Brödtorp' at

one locality in Finland and was identified by serology (K.

Bremer, unpublished data).

Symptoms on Natural and Experimental Hosts

The disease has only been transmitted between black

currants, and the different cultivars react similarly to

infection.

Bushes graft infected in July or August develop symptoms

the following year. Slight, indistinct chlorotic flecks are

produced in April and May, followed in June and July by a

more distinct olive-green mosaic affecting large sectors of

leaves (fig. 162). There is a similar sequence in subsequent

years, and the most conspicuous symptoms follow periods of

warm, sunny weather.

Natural and Experimental Transmission

Slow spread in a field experiment at East Mailing in England

suggests that there is a rare or inefficient natural vector

although none has been found, and tests with the aphids

Hyperomyzus lactucae (L.),H. pallidus H. R. L.,Nasonovia

ribisnigri (Mosley), Aphis grossulariae Kalt., and A.

schneiden (Born.) were unsuccessful (Cropley et al. 1964).

Infection is readily transmitted by graft inoculation but not by

sap inoculation.

Properties of the Causal Agent

No information.

Detection and Identification

Yellows may be more widespread than present evidence

suggests because the symptoms are easily overlooked or

attributed to soil or nutritional disorders. Conspicuous

140
f\

>': f *~.TiK-«**,l

Figure 162. — Symptoms of black currant yellows.

symptoms are produced some weeks after those caused by

other virus and viruslike diseases of black currants, and

necessitate an additional late inspection at a time when

damage by the leaf spot fungus (Drepanopezzia ribis (Kleb.)

von Hohne!) may be prevalent. Preliminary diagnosis can be

confirmed by graft transmission to 'Amos Black' or other

black currant cultivars.

Control Procedures

No information.

Infectious Variegation// ,

By A. N. lAdams and J. M. Thresh

Additional Common Names

Gold dust (Campbell and Adam 1968).

History and Geographic Distribution

The symptoms of infectious variegation were described

(Posnette 1952) several years before transmission of the

disease was reported (EUenberger 1962). Infection occurs

throughout some little-grown British cultivars. A similar

condition has been noticed in other European countries

(Kristensen et al. 7962; Putz 1972).

Economic Importance

No information is available.

Symptoms on Natural and Experimental Hosts

Black currant is the only known host and cvs. 'Daniel's

September' and 'Laxton's Nigger' develop a bright chrome

or pale-yellow mosaic of the early leaves (ñg. 163A). This is

followed in summer by a broad yellow banding of the main

veins, forming a vein net pattern (ñg. Ï63B). Symptoms

differ greatly in severity between years.

Figure 163. — Infectious variegation in black currant;

A, In early leaf; B, in midsummer.

The common cvs. 'Baldwin' and 'Wellington XXX' develop

only very slight symptoms in occasional seasons.

Natural and Experimental Transmission

The disease was reported to be graft transmitted by

EUenberger (1962) and by Kristensen et al. (1962) but

confirmatory evidence is lacking. Similar diseases were not

graft transmitted by Posnette (1952), Campbell and Adam

(1968), or Putz (1972). Sap inoculation to herbaceous hosts

failed (EUenberger 1962), and no experiments on insect

transmission have been reported.

Properties of the Causal Agent

No information

141
Detection and Identification

Seedlings grown at East Mailing in England and Wageningen

in The Netherlands from certain black currant crosses have

developed symptoms exactly resembling those of infectious

variegation (Thresh 1970). Campbell and Adam (1968)

reported that gold dust symptoms appeared to a variable

extent in different cultivars and that this was reflected in the

seedling progeny; they concluded that the disorder was due to

an inherited factor. Graft transmission tests to seedlings must

therefore be suspect and, if the disease is transmissible, a

clonal indicator is essential.

Control Procedures

No information.

Remarks

Gold dust may be a nontransmissible syndrome similar to but

distinct from infectious variegation (Campbell and Adam

1968). In the absence of consistent evidence for a

graft-transmissible pathogen, however, these two apparently

identical syndromes are considered to be synonymous.

Viruslike Disorders

y

^^-

Viruslike Disorders// i

By A. N.ÍAdams and J. M.lThresh

Spring Vein Banding

In early spring, the first-formed leaves of fruiting bushes

sometimes develop a yellow banding of the main veins that

is very conspicuous in certain years. Affected leaves usually

subtend flowers and soon abscise. Symptoms rarely develop

on nursery bushes or on the leaves of the extension growth

and are missed unless the bushes are inspected as flowering

begins.

The symptoms have been seen in many cultivars. These

symptoms are distinct from those caused by gooseberry vein

banding virus, which are mild or absent on the first-formed

leaves of black currant and occur on leaves of extension

growth.

Transmission experiments have been hampered by the lack of

suitable indicators; young seedlings must be kept for at least

2 yr for flowers to develop. No symptoms occurred in

graft-transmission tests to red currant and gooseberry

seedlings (J. M. Thresh, unpublished data).

Aphid Damage

Several species of aphids that feed on black currant cause

downcurling of leaves and stunting. In addition, the feeding

of Hyperomyzus lactucae (L.) causes a yellow mottling and

vein banding (fig. 164), which may occur on uninfested

leaves. These symptoms tend to be confused with those of

gooseberry vein banding virus; however, the vein banding

caused by aphids is usually broader and more opaque than

that caused by virus. Other evidence of aphid colonization,

such as leaf curling and cast skins, is also likely to be present.

Damage of Leaves by Eriophyid Mites

Cecidophyopsis rihis (Westw.), the black currant gall-mite

vector of reversion, normally inhabits buds, which develop

into rounded galls and fail to produce flowers or leaves. The

leaves subtending infested axillary buds develop normally,

but leaves produced after an apical bud has become infested

are severely malformed. Ultimately, almost trifoliate leaves

appear (fig. 165).

Reverted bushes (that is, those infected with reversion

disease) are much more susceptible to mites than healthy

ones; and malformation tends to be associated with reversion

infection. This explains why distorted trifoliate leaves were

long considered the ultimate stage of reversion; however,

reversion disease affects the shape and venation of leaves

without affecting their bilateral symmetry.

142
Figure 164. — Vein banding in black currant caused by

Hyperomyzus lactucae.

Figure 165. — Leaf malformation in black currant

caused by the eriophyid mite, Cecidophyopsis ribis.

Sectorial Chimera

Occasionally, black currant bushes develop single leaves or a

sequence of leaves with abnormally distributed chlorophyll

that is entirely absent from certain lobes or restricted to the

palisade or mesophyll cells. There is no evidence that this

condition is transmissible, and it is assumed to be a sectorial

chimera. It is of no economic significance, although affected

shoots should be removed from nurseries to avoid perpetuating the disorder.

Virus and Viruslike Diseases of Red Currant

Aphid-Borne Diseases

Ái 7- Red Currant Vein Banding,^

By F. A. van derjMeer

Additional Common Names

Adernbänderung; Nerfbandmozaiek; Nervová mosaika.

History and Geographic Distribution

Symptoms of vein banding in red currants were first

described in Czechoslovakia (Blattny 1930) and Germany

(Winter 1940). Transmissibility of the disease was shown

first in The Netherlands (van der Meer 1961). Later on, the

disease was reported from Great Britain (Thresh 1967), East

and West Germany (Kleinhempel 1968; Baumann 1974),

France (Putz 1972), and Romania (Ghena and Botar 1974).

Red currant vein banding probably occurs wherever red

currants are grown.

Economic Importance

There is little exact information about the effect of vein

banding on growth and cropping of red currants. Growth

reduction of about 50%, probably partly due to shock effects,

has been reported for infected red currant seedlings

(Kleinhempel 1970). Cuttings of infected 'Jonkheer van

Tets' showed 28% growth reduction in their first growing

season, and vein banding-free bushes of 'Jonkheer van Tets'

consistently outyielded infected bushes of the same cultivar

(Adams 1979). Vein banding reduces the number of cuttings

produced in stool beds of red currant (van der Meer 1980).

Economically, vein banding is the most important virus

disease of red currant because of its general occurrence and

because symptoms are easily overlooked during field

inspections.

Symptoms on Natural and Experimental Hosts

In most red currant cultivars, symptoms are vein banding and

vein clearing, which are often restricted to parts of the leaves.

This uneven distribution of symptoms in leaves is very

characteristic and enables one to recognize the disease when

mild vein clearing is the only symptom, as happens quite

often (fig. 166). Symptoms are more pronounced by

transmitted than by reflected light (fig. 167). They are most

conspicuous in May and June and may disappear during July

and August. In sunny years, infected plants may not show

any symptoms, whereas symptoms may be very pronounced

when cloudy weather prevails during April and May.

Infected plants are somewhat stunted in comparison with

healthy ones.

143
Figure 166.—Vein banding and vein clearing in red

currant, cv. Rovada'.

Figure 167.—Vein banding and vein clearing in red

currant cv. Fay's Prolific'; healthy leaf is in the center.

Experimentally infected black currants show vein clearing in

the first-formed leaves of the fruiting wood and in some

leaves of the extension shoots. Symptoms are less conspicuous in black than in red currants. Very young seedlings of

red currants and gooseberry infected by aphids show severe

vein banding and stunting, which is sometimes accompanied

by small necrotic lesions in the leaves. Seedlings of cv.

'Jonkheer van Tets', used as indicators, may show a similar

shock reaction in May when kept in an unheated greenhouse

or when graft inoculation has been done in August of the year

before. Symptoms in black currant and gooseberry seedlings

resemble those caused by gooseberry vein banding virus.

Natural and Experimental Transmission

Red currant vein banding has been transmitted by aphids as

well as by patch grafting.

The following aphid species have been established as vectors:

Aphis schneidert (Born.), A. triglochinis Theob., Cryptomyzus galeopsides (Kalt.) subsp. citrinas H.R.L., C. ribis (L.),

Hyperomyzus lactucae (L.), and Nasonovia ribisnigri

(Mosley) (van der Meer 1965b, 1965c). These aphids

hibernate on currants, but most species migrate to summer

hosts in June. (See above references for details on the

seasonal host ranges of the aphids; also, Hille Ris Lambers

{1949, 1953.) In experiments of Kleinhempel (1968), Myzus

persicae (Sulz.) also transmitted red currant vein banding.

Transmission rates with all aphid vectors have been low.

Virus-vector relationships have been studied by F. A. van der

Meer (unpublished data) and Karl and Kleinhempel (1969).

Aphids can acquire the virus in 30 min, but the number of

infected plants is increased after an acquisition time of 24 hr.

The virus is transmitted less readily after an inoculation

access period of 30 min than after a longer period. Vectors

were observed to be infected 4 hr after leaving the infected

source, but not after 8 hr.

Natural spread of the disease has not been studied

extensively. The ease with which vein banding-free plants

can be found in very old plantations indicates that natural

spread in cropping bushes is very slow. Observations of

Adams (1979), however, show that natural spread in cv.

'Jonkheer van Tets' can be rather fast, although his

experiments were on a small scale. Natural spread has been

noticed in stool beds of red currant (van der Meer 1980).

Despite numerous attempts, no virus has ever been

transmitted in sap inoculations from diseased currants to

herbaceous plants. In experiments with several thousands of

red currant seedlings, seed transmission has never been

observed.

Properties of the Causal Agent

The assumption that red currant vein banding is caused by a

virus is based on its type of symptoms and on the observation

that it is transmitted by aphids and by grafting; however,

virus particles have not been detected so far.

Detection and Identification

This disease is detectable by its symptoms in the field,

although symptoms can be very inconspicuous in some years.

Symptom expression is promoted by growing potted plants in

an unheated and shaded greenhouse. Under such circumstances, infected plants of most cultivars show clear symptoms,

which offer the opportunity to select healthy stock material.

'Rondom' seldom shows symptoms, and infected plants can

only be detected with certainty by indexing them on seedlings

of cv. 'Jonkheer van Tets' (van der Meer 1965d).

Control Procedures

To ensure a good start of new plantations, planting material

should be free of vein banding. Such material can be

produced by using cuttings from isolated stool beds that have

144
been started with healthy material. Experience in The

Netherlands, however, has taught that even in isolated

propagation fields some cultivars, for instance cvs. 'Stanza'

and 'Rondom', may become reinfected to a rather high

degree within 8 to 10 yr. Propagation fields, therefore, have

to be renewed periodically. For this purpose, small amounts

of nuclear stock material have to be kept in insect-proof

screenhouses continually (van der Meer 7980).

Heat treatment experiments with red currant have almost

completely failed so far. Plants are rather sensitive to

temperatures of 35° to 37°C. They produce very little

extension growth during treatment, and they usually die

within 4 to 6 wk. With the exception of one tip of cv. 'Prince

Albert', all tips of many treated plants grafted to seedlings, or

rooted in a mixture of sand and peat, appeared still infected.

Remarks

In black currant and gooseberry seedlings, red currant vein

banding causes symptoms that resemble those of gooseberry

vein banding virus. However, attempts to induce vein

banding in red currants by grafting them with infected

gooseberry either failed (F. A. van der Meer, unpublished

data) or were partly successful (Karl and Kleinhempel ¡969).

Both red currant and gooseberry vein banding are transmitted

by the same aphid species and show the same virus-vector

relationships. Therefore, it seems reasonable, pending

further research, to consider them to be related strains.

V

Â

Green Mottle of Red Currant/y

By F. A. van derjMeer

Additional Common Names

None, but the disease is caused by cucumber mosaic virus.

History and Geographic Distribution

Green mottle of red currant has been noticed in The

Netherlands (van der Meer 1962) and tn England (Thresh

1967) as a very uncommon disease of red currant.

Economic Importance

Very little.

Symptoms on Natural and Experimental Hosts

In naturally infected bushes of cv, 'Maarses Prominent', the

virus causes a severe yellowing especially in the center part

of the leaf near the petiole (fig. 168). Affected leaves may be

deformed, and branches sometimes die back. In cv.

'Jonkheer van Tets', the virus causes green mottle, as well as

line patterns, which can be very clear in the spring (fig. 169).

The virus usually remains localized in the lower parts of only

some branches.

Figure 168.—Cv. 'Maarse's Prominent' with symptoms

of green mottle caused by cucumber mosaic virus.

Figure 169.—Leaf pattern in cv. 'Jonkheer van Tets'

infected with green mottle caused by cucumber mosaic

virus.

In Chenopodium quinoa Willd., necrotic local lesions appear

about 3 or 4 days after infection. Nicotiana tabacum L. cv.

'White Burley', N. glutinosa L., and A^. rustica L. react with a

mild systemic mottle, whereas cucumber develops a severe

mosaic.

Natural and Experimental Transmission

Natural spread in currants appears to be rare.

Experimentally, the virus can be transmitted mechanically to

many herbaceous hosts and can be transmitted between red

currant bushes by grafting. In greenhouse trials, the aphid

Myzus persicae (Sulz.) transmitted the virus from tobacco to

tobacco.

145
Properties of the Causal Agent

The virus has been identified serologically as a strain of

cucumber mosaic virus (CMV). An antiserum has been made

to one red currant isolate (Maat 1966). In agar-gel diffusion

tests, all six red currant isolates found in The Netherlands

reacted similarly. (See "Cucumber Mosaic Virus in Raspberry," p. 191, for details of particle morphology and properties

in vitro.)

CMV can be transmitted by many aphid species, including

some that live on Ribes species (Kennedy et al. 1962), and the

virus occurs commonly in many weed species. In view of the

nonpersistent character of the virus, red currant can probably

be infected by any aphid vector of CMV that feeds temporarily

or by chance on currant. A high resistance to infection and

the nonsystemic behavior of CMV in red currants may be the

reasons why infection occurs rarely.

Detection and Identification

The symptoms of green mottle may be confused with those of

other diseases. Preliminary diagnosis should be checked by

sap inoculation to C. quinoa and cucumber. The identification

must be confirmed by serological tests.

Control Procedures

The virus can easily be controlled by selection and propagation

of healthy planting material.

Remarks

CMV has also been found in black currants (Thresh 1966)

(see p. 136) and in Ribes aureum Pursh (Schmelzer 1963).

Nematode-Borne Diseases

Ai ^ Spoon Leaf of Red Currant ;y

By F. A. van derlMeer

Additional Common Names

Lepelblad; Löffelblättrigkeit.

History and Geographic Distribution

Spoon leaf disease was first reported from The Netherlands

by Maarse {1926, 1938b) who mentioned that the disease

occurred in patches and suggested that it could be caused

either by a virus or by soil conditions.

The infection was later found to be caused by a soil-borne

virus (van der Meer 1960, 1965a), subsequently shown to be

a strain of raspberry ringspot virus (RRV) (Harrison 1961;

Maat et al. 1962). The early symptoms of infection are

similar to those previously attributed to red currant ringspot

virus (Klesser 7957), now considered to be synonymous with

RRV.

Infection in red currant has been reported from The

Netherlands and from East (Richter et al. 1966) and West

Germany (Schuch 1963).

Economic Importance

The Bangert in The Netherlands is the only known area

where the disease is epidemic in red currants. Plants

becoming naturally infected in the first years after planting

often exhibit strong growth reduction. Cuttings from infected

bushes give rise to very weak young plants (Maarse 1938a).

Kleinhempel (1970) mentions a crop reduction of 32% for

artificially infected bushes of cv. 'Rote Spätlese'.

Symptoms on Natural and Experimental Hosts

Naturally infected red currants often show a bright yellow

mosaic and ringspots as shock symptoms in the first 1 or 2 yr

after infection (figs. 170 to 172). In later years, infected

plants show leaf deformation; whereas mosaic and ringspot

do not appear. Depending on the cultivar and the virus strain

involved, leaf deformations may differ very much in

severity. Leaves of some infected bushes only show a slightly

reduced dentation, whereas leaves of other infected bushes

become almost round with very little dentation (figs. 173 and

174). Margins of the leaves commonly curl down or up,

creating a spoon-shaped appearance.

Experimentally infected Chenopodium quinoa Willd. develops necrotic local lesions and systemic necrosis. C.

amaranticolor Coste & Reyn. shows only local lesions. The

virus causes a bright systemic yellowing in tomato and in

petunia. In this respect, RRV from red currant differs from

146
Figure 170.—Various shock symptoms of spoon leaf in

cv. 'Fay's Prolific'; that is, mosaic, rings, and leaf

pattern.

Figure 171.—Type of mosaic that is most common as a

shock symptom of spoon leaf in cv. 'Fay's Prolific'.

TT

Figure 173.—Typical symptoms of spoon leaf in cv.

'Fay's Prolific'. Leaves are almost round, with little

dentation.

Figure 172.—Sequence of shock symptoms and chronic

symptoms of spoon leaf in shoot of cv. 'Fay's Prolific'

after natural infection.

Figure 174.—Leaves of healthy 'Fay's Prolific'.

147
Scottish RRV strain (Harrison 7967; van der Meer 1965a).

(See the Rubus section, p. 211, for further details on

symptoms in other herbaceous hosts.)

Natural and Experimental Transmission

The virus is transmitted naturally by Longidorus elongatus

(de Man.) (van der Meer 1965a). This nematode transmits

the virus to red currants and to several weed species.

Gooseberries and black currants are rather resistant to natural

infection.

Experimentally, the virus can be transmitted to gooseberry

and black currant by grafting. By means of sap inoculation,

the virus can be transmitted from red currant to many

herbaceous hosts.

Properties of the Causal Agent

Red currant spoon leaf is caused by a strain of RRV that is

serologically indistinguishable from Scottish isolates

obtained from raspberry. The longevity of currant isolates in

vitro is 3 to 4 wk at 18°C., and the thermal inactivation point

is 70° to 75°C. (See "Raspberry Ringspot and Associated

Diseases of Rubus Caused by Raspberry Ringspot and

Tomato Black Ring Viruses," p. 211, for further properties

of RRV.)

Detection and Identification

The early symptoms of infection may resemble those of other

viruses and viruslike diseases, and the spoon leaf condition

may be difficult to distinguish from reversion or other leaf

abnormalities. Consequently, detection should be done by

sap transmission to herbaceous hosts, whereas identification

must be confirmed by serological tests.

Control Procedures

Stocks for propagation should be tested to ensure that they

are free of infection. Preplant treatment with dichloropropane-dichloropropene, and possibly other nematicides,

provides a good control of the disease when red currants have

to be planted in soil where the virus and its nematode vector

are present.

There is no information on therapy of infected plants;

however, there is as yet no need for therapy since no cultivars

are known to be universally infected.

Remarks

In testing procedures, transmission of the virus by sap

inoculation from currant to herbaceous hosts is greatly

facihtated by adding 2% nicotine solution to the inoculum.

4l 1

^ Infection of Red Currant With Arabis Mosaic and

Strawberry Latent Ringspot Viruses^/

By F. A. van derjMeer

Additional Common Names

No common names are justified,

information on symptomatology.

according to present

History and Geographic Distribution

Arabis mosaic virus (AMV) and strawberry latent ringspot

virus (SLRV) were first isolated from red currant while testing

an English collection of cultivars by sap inoculation to

herbaceous hosts (Thresh 1967). The same viruses were not

detected in many similar tests done over a period of 6 yr in The

Netherlands. AMV was isolated from material of French

bushes sent in by B. Lantin (F.A. van der Meer, unpublished

data). The infected bushes were part of a cultivar collection at

Angers and had been imported recently from elsewhere. Both

AMV and SLRV have been detected in red currant in East

Germany (Kleinhempel 1968).

Economic Importance

According to the present information, infection seems to

occur only incidentally. Kleinhempel (1970) found little or no

effectof SLRV on cropping ofred currant cv. 'Rote Spatlese'.

There is no further information on the effect of AMV and

SLRV on growth and cropping of red currants.

Symptoms on Natural and Experimental Hosts

Naturally infected red currants usually do not show symptoms

with either virus (Thresh 1967). One out of two SLRVinfected bushes found by Kleinhempel (1968) showed bright

yellow on only a few leaves, whereas 16 AMV-infected

bushes did not show any symptoms.

Young red currant seedlings, experimentally infected with

AMV by sap inoculation from herbaceous hosts, developed

slightly discolored leaves. Graft-inoculated black currant

bushes of the principal commercial cultivars reacted with

a yellow mottle of the leaves that becomes inconspicuous by

midsummer.

Experimentally infected Chenopodium quinoa Willd. and C.

amaranticolor Coste & Reyn. developed faint chlorotic local

lesions, followed by systemic mosaic and stunting, often

accompanied by collapse and death of the apex.

Natural and Experimental Transmissions

Both viruses are naturally transmitted, presumably by the

nematode Xiphinema diversicaudatum (Micoletsky), which

is known as a vector in other crops.

Experimentally, the virus can be transmitted from currant to

currant by grafting and from currantto herbaceous hosts by sap

inoculation. Addition of 2% nicotine solution to the inoculum

facilitates transmission from currants to herbaceous plants.

148
Properties of the Causal Agent

AMV and SLRV isolates from red currant closely resemble

those obtained from strawberry. (See the Rubus section, p.

204, for further details on properties of AMV and SLRV.)

Detection and Identification

The disease is detectable by sap inoculation to C.

Identification is only possible by serological tests.

quinoa.

Control Procedures

Selection, indexing, and propagation of healthy planting

material should be done in places where the nematode vector

does not occur.

There is no information on therapy of infected plants.

0'^.Tomato Ringspot Virus in Red Currant;/

By H. E. jWilliams, Q. L.JHoldemann, and R.ICasper

Additional Common Names

In red currant, the following names have been used: currant

mosaic (Hildebrand 1939); American currant mosaic (Hildebrand 1942); and tomato ringspot (Hildebrand 1942). Strains of

tomato ringspot virus (TomRSV) infecting various hosts cause

diseases known as tomato ringspot, peach yellow-bud mosaic,

and grape yellow vein.

History and Geograpliic Distribution

Naturally infected red currant is known in the United

States—where the disease has been reported from New York,

New Jersey (Hildebrand 1939, 1942), and California (H. E.

Williams and G. Nyland, unpublished data)—and the

U.S.S.R. (Eastern Siberia) (Gordejchuk et al. 1977).

TomRSV may have been disseminated in infected planting

material to other parts of the world. TomRSV has been found

in Yugoslavia in American cultivars of red raspberry

('Geneva' and 'Hilton') (Jordovic et al. 1972).

Economic Importance

Hildebrand (1939) reported

occasional killing of plants.

reduction in bearing and

Symptoms on Natural and Experimental Hosts

In red currant: At temperatures below 21 °C., TomRS V causes

symptoms consisting of varying degrees of chlorotic spotting

and vein banding (fig. 175). Chlorosis may vary from a few

spots or blotches, to a mild vein banding in a leaf, or to a

chlorotic leaf with only a few green spots. The chlorotic areas

may die and turn brown. On a single plant, the amount of

chlorosis may vary from mild symptoms on a single leaf to

conspicuous yellowing of the entire plant. In a critical

temperature range (21° to 27°C.), the symptoms on young

leaves are limited to chlorotic spots and rings. No symptoms

appear on new growth formed at temperatures above 27°C.

Figure 175.—Tomato ringspot virus in red currant.

(Courtesy of E. M. Hildebrand and The Botanical

Society of America.)

In herbaceous hosts: Experimental host range is wide; species

in more than 35 dicotyledonous and monocotyledonous

families are susceptible. In crops, the virus occurs mostly in

ornamentals and woody or semiwoody plants, but also occurs

naturally in many annual weed species. TomRSV is

transmissible by sap inoculation, readily to herbaceous hosts

but with difficulty to woody hosts (Stace-Smith 7970).

The host ranges of some TomRSV isolates differ, including

differences between the two red currant isolates.

Diagnostic species

Chenopodium amaranticolor Coste & Reyn. and C. quinoa

Willd. Small chlorotic local lesions; systemic apical necrosis.

Cucumis sativas L. (cucumber),

systemic chlorosis and mottle.

Local chlorotic spots;

Phaseolus vulgaris L. (bean). Chlorotic local lesions;

systemic rugosity and necrosis of tip leaves.

Nicotiana tabacum L. (tobacco). Necrotic local spots or

rings; systemic etched ring and line patterns. Leaves produced

later are symptomless but contain virus.

Petunia hybrida Vilm. (petunia). Local lesions; necrotic

collapse of young leaves.

Lycopersicon esculentum Mill, (tomato). Local necrotic

flecks; systemic mottle and necrosis.

Vigna unguiculata L. (Walp.) (cowpea). Chlorotic or

necrotic local lesions; most isolates cause systemic tip

necrosis.

149
Propagation species

Nicotiana tabacum or woody plants such as raspberry or

currant are suitable for maintaining cultures. Cucumber or

petunia are good sources of virus for purification.

Assay species

Vigna unguiculata, Nicotiana tabacum, Chenopodium

amaranticolor, and C. quinoa are useful local lesion hosts.

Cucumber is useful as a source and bait plant for nematode

transmission experiments (Téliz et al. 1966).

Natural and Experimental Transmission

No information is available on natural spread in currant. The

ncmaioátXiphinema americanum Cobb (and probably related

species), a known vector of TomRSV, has been observed

colonizing field soil under a monoculture of currant.

Presumably, TomRSV could be introduced into a new area in

infected plants, cuttings, scions, corms, and seed of cultivars

and weeds. If a nematode vector were present, the virus could

become established and perpetuated in weeds and other plants.

TomRSV has been transmitted from red currant to herbaceous

hosts by sap inoculation, but from currant to currant only by

grafting. Sap inoculation from herbaceous hosts back to red

currant has not been achieved. The incubation period in

currant is unknown but in herbaceous hosts, it is 3 to 7 days.

There is no evidence of transmission through the seed of red

currant, although this has been indicated or demonstrated for

TomRSV in other hosts (Price 1936\ Kahn 1956\ Mellor and

Stace-Smith 1963).

Properties of the Causal Agent

The disease is caused by TomRSV (Price 1936). For details,

see "Tomato Ringspot Virus in Rubus,'' p. 223, and StaceSmith (1970). The New York red currant isolate was demonstrated to be related to Price's original TomRSV isolate

by cross-protection tests (Hildebrand 1942). The California

isolate is assumed to be the same as, or related to, TomRSV.

Detection and Identification

Detection of TomRSV is made by sap inoculation from

young tips of currants to young, vigorous plants of several

herbaceous hosts, for example, cowpea, bean, cucumber,

Chenopodium amaranticolor, and tobacco. Identification is

made serologically with antisera to the type strain of

TomRSV by agar gel test or ELISA.

Control Procedures

Plants for propagation should be grown only from indexed,

certified, virus-tested sources. The results of Hildebrand and

Weber (1944) suggest the possibility of exploiting cultivar

resistance. No information is available on therapy of this

virus in red currant.

Remarks

Hildebrand's original hypothesis (1942) that TomRSV in red

currant and currant mosaic virus (CurMV) (Hildebrand 1939)

are distinct viruses was based on the following: (1) TomRSV

was not detected in two collections of plants showing currant

mosaic symptoms, and (2) symptoms attributed to TomRSV

in red currant were different from those attributed to CurMV.

In later unpublished works, however, E. M., Hildebrand

(personal communication) determined that only currant

mosaic symptoms appeared on plants at temperatures below

21°C. The two sets of symptoms could be induced

sequentially in a given plant by altering the temperature at

which the plant is grown. Based on this evidence, he

concluded that American currant mosaic is caused by

TomRSV.

Until the problem of mechanical transmission of TomRSV to

currant is resolved, we assume that the two distinct sets of

symptoms described by Hildebrand (1939, 1942) are caused

by TomRSV.

TomRSV has never been recovered from plants not showing

symptoms of currant mosaic, either in natural infections

(Hildebrand 1942; H. E. Williams and G. Nyland,

unpublished data) or in graft-infected plants (Hildebrand and

Weber 1944).

No relationship is known between American currant mosaic

caused by TomRSV and European currant mosaic. (See

"Yellow Leaf Spot of Red Currant," p. 152.)

^X

r Leaf Pattern of Red Currant//

By F. A. van der Meer

Additional Common Names

None, but the disease is caused by tobacco rattle virus

(TRV).

History and Geographic Distribution

The disease was first found in a single bush of cv. 'Fay's

Prolific' in The Netherlands. The virus isolate from this bush,

obtained by sap inoculation to herbaceous hosts, did not react

with antisera against known viruses of Ribes (van der Meer

1970), and no viruslike particles could be detected. Later on,

the disease was found in two bushes of cv. 'Jonkheer van

Tets'. Isolates, made from these bushes, contained long and

short particles, typical for TRV, and reacted positively with

TRV antisera (F. A. van der Meer, unpublished data).

Economic Importance

Because of its rare occurrence, the disease is of little

economic importance.

Symptoms on Natural and Experimental Hosts

Naturally infected red currants show sharply defined oak leaf

patterns on leaves of some branches (fig. 176). Symptoms

may remain restricted to certain branches for several years

150
Figure 176.—Symptoms of leaf pattern in cv. 'Fay's

Prolilic'. caused by tobacco rattle virus.

Figure 177.—Rings in leaf of Ribes sanguineum cv.

'King Edward VU', caused by tobacco rattle virus.

and often are only present in some of the first-formed leaves.

Oak leaf patterns are sometimes accompanied by light-green

mosaic (ñg.l77).

Experimentally infected Chenopodium quinoa Willd. always

reacts with sharply defined lesions after 2 or 3 days. The

isolate obtained from cv. 'Fay's Prolific' caused necrotic

local lesions in Nicotiana tabacum L. and no systemic

symptoms. Isolates obtained from cv. 'Jonkheer van Tets'

caused local and systemic necrosis in N. tabacum L. (fig.

178).

Natural and Experimental Transmission

TRV is known to be naturally transmitted by nematodes of

the genus Trichodorus to several crop hosts and many weeds

(Harrison 7970). Presumably, red currants are infected in the

same way.

Experimentally, the virus can be transmitted from red currant

to herbaceous hosts by sap inoculation. Such transmissions

Figure 178.—Necrotic lesions in lea! of tobacco, caused

by an incomplete strain of tobacco rattle virus from red

currant.

must be done in April and May, and the inoculum should be

prepared by macerating leaves in a 2% nicotine solution.

Properties of the Causa! Agent

Because TRV could only be detected in leaves showing

symptoms, we believe that TRV causes red currant leaf

pattern.

Complete TRV isolates produce long (about 190 nm) and

short (45-115 nm) particles. Long particles contain the

genetic information for the production of infectious RNA,

whereas the short particles contain the genetic information

for the production of the coat protein of the particles.

Incomplete isolates produce only infectious RNA. They can

be obtained from complete isolates by using inocula that

contain only long particles and have also been found in

naturally infected plants (Harrison 1970). Incomplete isolates

are less stable than complete isolates and often remain local

in infected plants. The isolate obtained from cv. 'Fay's

Prolific' was probably incomplete (fig. 178). Similar isolates

have been obtained from lilac (van der Meer 1976a). Two of

these have been converted to complete isolates by inoculating

them together with the short particles of a complete red

currant isolate (Huttinga 1976).

Detection and Identification

Because symptoms of leaf pattern disease of red currant are

easily confused with symptoms of other diseases, detection is

151
only possible by sap inoculation to herbaceous hosts.

Serological tests are necessary for identification of the virus;

however, incomplete isolates (short particles) do not respond

to such tests because they consist only of RNA without a

protein coat.

Control Procedures

Healthy stock material should be tested by sap inoculation on

C. quinoa and should not be propagated in soil where both

virus and vector occur.

There is no information on therapy of infected plants;

however, for practical purposes, therapy is not necessary

because very probably no cultivars are universally infected.

Remarks

Incomplete TRV isolates have been obtained from Ribes

sanguineum Pursh showing ringspot and leaf pattern

(Schmelzer 1970). Symptoms in R. sanguineum are often

restricted to a few leaves. In experiments of van der Meer

(1976b), TRV could be isolated only from leaves with

symptoms, which indicates that TRV indeed is the cause of

ringspot and leaf pattern in R. sanguineum (fig. 177).

Vectors Unknown

Yellow Leaf Spot of Red Currant y

By F. A. van derJMeer

Additional Common Names

Aucuba mosaic; European currant mosaic.

History and Geographic Distribution

Yellow leaf spot of red currant has been described and

referred to as aucuba mosaic in Czechoslovakia (Blattny

1930) and The Netherlands (Houtman 1951; van Katwijk

1953; van der Meer 1961), and as European currant mosaic

in Great Britain (Thresh 1967). Similar symptoms have also

been found in West Germany (Schuch 1957), East Germany

(Kleinhempel 1968), and France (Lantin 1968).

Economic Importance

The disease is of minor importance because it is quite

uncommon, and severe effects on growth and cropping have

not been reported.

Symptoms on Natural and Experimental Hosts

Naturally infected red currants cv. 'Fay's Prolific' and

several unnamed old Dutch cultivars develop small lightgreen or white spots that are scattered over the whole leaf

(fig. 179). Symptoms may vary in severity between years.

The outer margin of the leaves occasionally becomes light

yellow. Infected plants appear somewhat stunted.

Experimentally infected bushes of cvs. 'Laxton's No. 1'

(Thresh 7967) and 'Fay's Prolific' (Kleinhempel 1968) may

show pale-yellow patches or bands along the main veins.

Seedlings from cv. 'Jonkheer van Tets' show rather mild

symptoms, whereas infected black currant seedlings of cv.

'Baldwin' remained symptomless.

Natural and Experimental Transmission

There is no information on the way and rate of natural spread

in red currants. At one locality in The Netherlands, however,

a patch of diseased bushes occurred across the boundary

between two farms where bushes of different origins had

been planted on each farm, thus indicating natural spread of

the disease.

Experimentally, the disease can be transmitted between

currants by grafting.

Properties of the Causal Agent

Symptoms and graft transmissibility indicate that yellow leaf

spot of red currant is caused by a virus. Negative results of

sap inoculation experiments, reported by some authors (van

der Meer 1966; Thresh 1967; Kleinhempel 1968), suggest

152
y

A'í.

Figure 179.

currant.

-Yellow leaf spot in 'Fay's Prolific' red

that the causal virus is not mechanically transmissible. By

sap inoculation to Nicotiana glutinosa L., however, Jacob

(1976a) isolated potato virus (PVY) from five red currant

cultivars that showed yellow leaf spot. This virus occurred

latently in several other red and white currant cultivars (See

"Remarks," p. 153.)

Detection and Identification

This disease is detectable by its symptoms and by graft

transmission to the sensitive cvs. 'Laxton No. 1' and 'Fay's

Prolific'. Sap transmission to Chenopodium quinoa Willd.

should be attempted to check for the presence of interveinal

white mosaic, which can be confused with yellow leaf spot in

certain seasons. (See "Interveinal White Mosaic," p. 153.)

Sap transmission to A', glutinosa or Solanum demissum

Lindl. cv. ' A6' should be attempted to check for the possible

presence of PVY (De Bokx and Huttinga 1981).

Control Procedures

The disease has never been observed in plantations that had

been started with certified planting material. This suggests

that selection and propagation of healthy stocks give

adequate control.

Remarles

Jacob (1976a) also isolated PVY from reversion-infected

black currants and concluded from his further experiments

that PVY is the cause of black currant reversion. Other

workers, however, have not been able to confirm the

presence of PVY in reverted black currants (R. Casper, H.

Krczal, and D. Lesemann, unpublished results; Thresh et al.

1978). (See also "Reversion of Black Currant," p. 133.)

^ Interveinal White Mosaic

By F. A. van derJMeer

L—

Additional Common Names

Tussenervig wit mozaïek. Alfalfa mosaic virus (in Great

Britain) and an unidentified virus (in The Netherlands) have

been associated with this disease.

History and Geographic Distribution

The disease was first described in The Netherlands (van der

Meer 1961), where it had been found in five separate bushes

of cv. 'Fay's Prolific', each of which was situated in a

different area. In Great Britain, a similar disease has been

found in only one bush of 'Laxton's No. 1' (Thresh 1967).

Economic Importance

Infected bushes are somewhat stunted, but infection is not

sufficiently widespread to cause important economic losses.

Symptoms on Natural and Experimental Hosts

Naturally infected bushes of cv. 'Fay's Prolific' show

light-yellow or white patches that are often situated in the

angles between the main and secondary veins. Symptoms of

interveinal white mosaic in red currant seedlings are shown in

figures 180 and 181. Often, first-formed leaves are also

chlorotic. Later-formed leaves often show only a brightyellow or white margin.The late symptom is of limited

diagnostic value, for it may also occur in yellow leaf

spot-infected bushes. (See 'Yellow Leaf Spot of Red

Currant," p. 152.) Moreover, white leaf margins occasionally occur also in bushes that do not show other viruslike

symptoms and from which no sap-transmissible viruses can

be isolated.

Black currant and Ribes sanguineum Pursh graft inoculated

with Dutch sources develop symptoms that resemble those in

red currant. Black currant cultivars graft inoculated with the

English source, developed very mild symptoms that can be

easily overlooked.

Sap inoculations from 'Fay's Prolific' caused mosaic and

chlorosis on china aster (Callistephus chinensis (L.) Nees)

(fig. 182). On Nicotiana rustica L., symptoms may vary

greatly in severity. During winter and spring, local yellowing

and small gray rings may appear 7 to 10 days after

inoculation. These symptoms become systemic, and infected

plants are stunted. In summer, the symptoms are inconspicuous and may be hardly visible. No symptoms were obtained

on Phaseolus vulgaris L. A virus isolate obtained from the

English 'Laxton's No.l' source induced necrotic local

lesions and systemic mosaic in C. quinoa and was identified

serologically as a strain of alfalfa mosaic virus (ALMV).

Natural and Experimental Transmission

Natural spread has not been observed, and infection has only

been found in incidental bushes. With the Dutch isolates, no

experiments have been done with aphids or other potential

153
Figure 180.—Severe symptoms of imerveinal white

mosaic on first leaves of a red currant seedling in the

spring.

Figure 182.—Mosaic and chlorosis in Callisiephus

chinensis sap-inoculated from 'Fay's Prolific' showing

interveinal white mosaic.

vectors. ALMV is known to be transmitted by many aphid

species (Jaspars and Bos 1980) and occurs in many wild and

cultivated plant species, so the English source of interveinal

white mosaic may have resulted from aphid transmission.

Experimentally, the disease can be transmitted between

currants by grafting. Both ALMV and an unidentified virus

Figure 181.—Symptoms of interveinal white mosaic in a

red currant seedling.

found associated with this disease in The Netherlands can be

transmitted from currants to herbaceous hosts by sap

inoculation.

Properties of the Causal Agent

Two of the five sources found in The Netherlands were also

infected with raspberry ringspot virus and have not been

investigated further. Isolates from two other sources have

been studied more intensively. Serologically, they were not

related to nepoviruses or to ALMV, and no particles could be

found in crude sap by using negative staining methods. Both

isolates had a thermal inactivation point of about 45°C, and

tobacco sap remained infective for 8 h, but not for 24 h at

20°C (F. A. van der Meer, unpublished data).

The ALMV isolate from the English source of interveinal

white mosaic has not been studied intensively. ALMV has

bacilliform particles. The thermal inactivation point of the

virus ranges between 50° and 70°C and crude sap remains

infective from 1 to 4 days at 20°C. (For further information

on properties of ALMV, see Jaspars and Bos 1980.)

Circumstantial evidence obtained from extensive field

observations and indexing suggests that the Dutch isolates

that are not fully identified, as well as the English ALMV

isolate, are able to cause interveinal white mosaic in red

currant. This, however, has not been confirmed by

retransmission experiments from herbaceous hosts to red

currants.

Detection and Identification

Interveinal white mosaic can be detected by the obvious

chlorosis ofthe first leaves in spring and by the light-yellow or

white patches in later-developing leaves. Subsequent tests on

C. quinoa distinguish interveinal white mosaic from the

154
somewhat similar symptoms of yellow leaf, which is not

associated with a sap-transmissible virus causing symptoms in

C. quinoa. Viruses found associated with interveinal white

mosaic induce local and systemic symptoms in C. quinoa,

which distinguishes these viruses from cucumber mosaic virus

and tobacco rattle virus found also in Ribes but causing only

local symptoms in C. quinoa. (See chapters on these

respective viruses in Ribes, p. 145 and 150.) Virus isolates

should be further characterized by testing with antisera

against ALMV and nepoviruses known from Ribes.

Control Procedures

The limited occurrence suggests that the selection and

propagation of healthy stocks will give adequate control.

There is no information on therapy of infected plants.

Remarks

In host-range studies, Schmelzer (1963) transmitted ALMV

mechanically from Petunia to gooseberry. Infected plants

showed a yellowish mosaic. Red currant inoculated in the

same way in Schmelzer's experiments remained uninfected.

TAFull Blossom of Red Currant ^y

F. A. van derMeer

Additional Common Names

Plnokvetosti ribezle.

Symptoms of full blossom have been found in naturally

infected plants of the red currant cvs. 'Houghton Castle',

'Jonkheer van Tets', 'Erstling aus Vierlanden', and several

unnamed cultivars. Graft-inoculated plants of red currant cv.

'Heinemann's Rote Spätlese' and black currant cv. 'Baldwin'

became infected latently.

Natural and Experimental Transmission

There is no information on the way and degree of natural

spread. Experimentally, the disease can be transmitted by

patch grafting.

Properties of the Causal Agent

Full blossom has been found associated with MLO (Rakús et

al. 1974). Since MLO could not be detected in healthy red

currants, we believe these organisms cause full blossom;

however, like so many other so-called MLO diseases of

plants, Koch's postulates have not yet been fulfilled for this

disease agent.

Detection and Identification

The disease can be detected by the typical flower malformations. Nuclear stock material should be indexed by graft

inoculation to cv. 'Houghton Castle.'

Control Procedures

New plantations should be started with planting material

derived from disease-free stock.

History and Geographic Distribution

Described by Rakús (197}) as a disease of red currant cv.

'Houghton Castle' in Czechoslovakia. The disease has not

been reported from other countries.

Economic Importance

According to Rakús (1978), full blossom is an economically

important disease in Czechoslovakia. It has been found in

several red currant cultivars all over the country. Diseased

bushes are reduced in size and produce sparse crops of small

berries (Rakús 7975).

Symptoms on Natural and Experimental Hosts

Flower malformations are the most typical symptoms of

affected bushes (figs. 183 to 188). Stamens are often absent,

whereas several styles per flower may be present instead of

one. Ovaries on red currants infected with full-blossom disease are often half-inferior (fig. 187) or superior (fig. 188),

while those on normal plants are regularly inferior (fig. 186).

Petals may become sepallike in appearance, and petals as

well as sepals may enlarge and become leaflike (fig. 189).

Misshapen berries may take on a cauliflowerlike structure

(figs. I90-I9I) (Rakús ¡971). These flower malformations

suggest a relationship with yellows or witches'-broom diseases of plants, many of which are believed to be caused by

mycoplasmalike organisms (MLO). Affected red currants,

however, do not show witches'-broom symptoms or extreme yellowing.

There is no information on therapy of infected material. Since

hot water treatment is known to be effective for several MLO

diseases of woody hosts (Nyland and Goheen 1969, van der

Meer 1975), it would be interesting to see if full blossom can

be cured in this way.

Remarks

Full blossom of red currant shows some similarity to

descriptions of severely malformed blossoms of black currant

Figure 183.—Racemes with symptoms of full blossom

disease; healthy raceme (cv. 'Houghton Castle') at right.

155
Figure 184.—Normal red currant flower, x 29.

(Courtesy of D. Rakús.)

Figure 185.—Red currant flower affected by the full

blossom disease, X 14. (Courtesy df D. Rakus.)

(Ritzema Bos 7905,- Hatton and Amos 1917). According to

Adams and Thresh (see "Reversion of Black Currant," p.

133), this condition is not common in Great Britain and

Western Europe. During surveys in The Netherlands, it was

found very seldom and only in reverted black currant bushes.

Such malformations are generally assumed to be part of the

black currant reversion syndrome. Results of Rakús et al.

(1974), however, indicate that full blossom of red currant is

not related to reversion of black currant.

Figure 186.—Longitudinal section of normal red currant flower with inferior ovary, x 39. (Courtesy of D.

Rakús).

Figure 187.—longitudinal section of abnormal flower

with half inferior ovary from full blossom-diseased red

currant, x 32. (Courtesy of D. Rakiis.)

156
Figure 188.—Longitudinal section of abnormal flower

with superior ovary from full blossom-diseased red currant, X 38. (Courtesy of D. Rakús.)

Figure 190.—Abnormal flowers with cauliflowerlike

structures from full blossom-diseased red currant;

normal flower at right. (Courtesy of D. Rakús.)

Figure 191.—Extrusion of seeds from berries from a

full-blossom diseased red currant; normal berries at

top. (Courtesy of D. Rakiis.)

Figure 189.—Longitudinal section of abnormal flower

from a full-blossom diseased red currant with "leaflike" structures in the ovary, x 38. (Courtesy of D.

Rakijs.)

157
Viruslike Disorders

Vé'-

Leaf Malformation of Red Currant;y

By F. A. van derjMeer

Additional Common Names

Reversion of red currant.

History and Geographic Distribution

Red currant bushes with abnormally shaped leaves have been

reported from Germany (Winter 1940: Schuch 1957; Behrens

1964), The Netherlands (Dijksterhuis 1950: van Katwijk

1953), Czechoslovakia (Blattny and Paulechova 1964), Great

Britain (Thresh 7967), and France (Putz 1972). The

condition is sometimes referred to as reversion of red currant;

however, transmissibility of the disease has seldom been

reported, and few attempts have been made to infect black

currant.

Economic Importance

Natural spread of leaf malformation in red currants and serious

effects on cropping have been reported from certain localities

in The Netherlands, East Germany, Czechoslovakia. Elsewhere, certain cultivars have a tendency to produce

malformed leaves, but there is no evidence of spread, and

yields are little affected except in cvs. 'Fay's Prolific' and

'Rondom'.

Symptoms on Natural and Experimental Hosts

Naturally affected plants may show several apparently distinct

leaf abnormalities. For example, bushes of certain Czech

cultivars derived from Ribes petraeum Wulf, develop leaves

that closely resemble those of black currant with reversion.

The lobes and marginal serrations are fewer and more rounded

than usual, although the bilateral symmetry of the leaves is

unaffected.

At places in The Netherlands and East Germany where the

disease was reported to be epidemic, affected bushes

developed asymmetrical leaves with reduced numbers of lobes

and marginal serrations. In black currant, such symptoms are

known to be caused by gall mites. (See "Reversion of Black

Currant," p. 133.)

Bushes of cv. 'Rondom' are particularly liable to develop

abnormal leaves, and several different types occur. In the most

extreme instances, the leaves are rugose, distorted, and

asymmetrical (figs. 192 to 194).

A common leaf abnormality of 'Fay's Prolific' (fig. 195) may

resemble symptoms of spoon leaf, but is associated with an

unusual branching habit of this cultivar (See "Budlessness of

Red Currant," p. 160.)

Figure 192. — Leaf malformation of red currant cv.

'Rondom'.

Figure 193. — leal iiialloniiation together with reduced cropping of cv. 'Rondom'.

Natural and Experimental Transmission

There is no information on the method of natural spread of

the various types of red currant leaf malformation.

Experimentally, black currant reversion has been grafttransmitted from a naturally affected red currant clone to

black currant. Black currant reversion, however, could not be

detected in various other suspected sources in Great Britain

(Thresh 1967) nor in suspected bushes of cvs. 'Heros' and

'Rondom' in West Germany (Baumann 7974).

158
Figure 194. — Healthy red currant cv. Rondom'.

Figure 195. — Leaf malformation of red currant cv.

'Fay's Prolific'. Normal leaf in center.

1. Black currant reversion has been detected in a clone of

Ribes rubrum L. that was virtually sterile and showed

reversionlike symptoms. Black currant reversion is transmitted by the black currant gall mite Cecidophyopsis ribis

(Westw.). The disease is caused by a graft-transmissible

agent; however, properties of this agent are as yet unknown.

2. In East Germany and in The Netherlands, spread of leaf

malformation was found to be associated with C. selachodon

van Eyndhoven, an eriophyid mite that closely resembles the

black currant gall mite, yet is a morphologically distinct

species (van Eyndhoven 1967) that does not infest black

currant (van de Vrie 1967). It is not known whether the leaf

malformations involved were caused solely by mites or

whether a virus of viruslike agent was also involved.

3. The instability of cv. 'Rondom' has been attributed to its

labile genetic structure and complex origin from an

interspecific cross (Rietsema 1955). Seedlings of cv.

'Rondom' are heterogeneous and often exhibit the same leaf

abnormalities as the parent.

4. The common malformation in cv. 'Fay's Prolific' is

associated with a peculiar branching habit. Neither mites nor

graft-transmissible diseases have been implicated, and the

condition seems to be an inherent characteristic of the

cultivar.

Detection and Identification

The disease is only detectable by visual selection. To

distinguish between reversion infection and genetical malformations, graft inoculations should be done on sensitive

black currant cultivars.

Control Procedures

Stocks used for propagation should be carefully inspected to

avoid perpetuating the gross leaf abnormalities affecting

cultivars such as 'Fay's Prolific' and 'Rondom'.

Malformations caused by eriophyid mites can be avoided by

the use of an appropriate acaricide; however, additional

measures will be necessary if a graft-transmissible disease

agent is also involved. Further research will be necessary

before final recommendations can be made for localities

where a leaf malformation is spreading.

No information is available on therapy of affected plants.

None of the various types of leaf malformation in cv.

'Rondom' could be transmitted by grafting (van der Meer

1965b; Putz 7972).

Properties of the Causal Agent

Several apparently distinct causes of the various leaf

abnormalities have been reported as follows:

159
r^i

Budlessness of Red Currant .^

By F. A. van der ¡Meer

Additional Common Names

Blind bud; knoploosheid.

History apd Geographic Distribution

Typical symptoms were first described in The Netherlands

(Maarse 1936). They have since been reported from

Germany (Winter 1940), England (Thresh 1967), and France

(Lantin 1968; Putz 7972), and probably occur wherever

sensitive cultivars are grown.

Economic Importance

Considerable losses occur in nurseries and plantations where

sensitive cultivars such as 'Fay's Prolific' are grown. The

yield of cropping bushes is strongly reduced because of weak

growth and a reduced number of flower-producing buds.

Affected planting material is not suitable for sale because

growth is unsatisfactory.

Symptoms on Natural and Experimental Hosts

The condition is known only in red currant, especially in

cultivars derived from Ribes sativum Syme (also known as R.

vulgäre Lam.). 'Fay's Prolific' is by far the most sensitive,

although CVS. 'Versailles' and 'Rondom' are sometimes

affected.

Shoot extension growth of affected bushes stops in early

summer, often after leaves have been formed that are

abnormally dark green and rounded, with reduced dentation

(fig. 196). Axillary buds fail to develop or appear at some

distance from the nodes (fig. 197). This condition has been

termed "concaulescence" (Reinders 7957) and occurs also in

other plants such as Symphytum officinale L. (Boraginaceae).

Buds of affected growth are often small and may produce

weak laterals with terminal and axillary buds that die or fail

to develop (fig. 198).

In a survey during each of two winters, all observed bushes

of cv. 'Fay's Prolific' were affected to some extent. Some

were almost normal; whereas others were severely stunted

and almost entirely affected.

several cultivars (Putz 7972). Seedlings of cv. 'Fay's

Prolific' are unstable indicators because they often develop

budlessness by the time flowering commences.

Properties of the Causal Agent

The budless condition is assumed to be genetical.

Detection and Identification

In summer, diseased bushes can be recognized by their

unusual leaves and dwarfed appearance. The malformed

leaves alone are not sufficiently reliable for diagnosis because

they may resemble those affected by spoon leaf disease. (See

"Spoon Leaf of Red Currant," p. 146.) In winter, the very

short and budless shoots are diagnostic for this disorder.

Control Procedures

Maarse (1936) suggested that cuttings should be taken only

from stocks that are little affected. Any abnormal bushes that

appear in the nursery or in the early years of a bearing

plantation should be removed. Affected shoots that appear

subsequently should be pruned back to a normal lateral shoot

or bud.

Several unsuccessful attempts were made to produce normal

plants by growing bushes for several weeks at 37°C.

Figure 196. — Leaves of red currant affected with the

budlessness disorder and showing abnormal rounding

and reduced dentation, top row, compared with normal

leaves, bottom row.

There are indications that the budless condition is less severe

in bushes that are not infected with red currant vein banding

virus.

Natural and Experimental Transmission

Natural and experimental transmission in 'Fay's Prolific'

could never be established because no unaffected stocks of

this cultivar have been located.

Seedlings of cv. 'Jonkheer van Tets' grew normally after

grafting to affected shoots of cv. 'Fay's Prolific'. No

transmission has been obtained in grafting experiments with

160
W'k

íri

Figure 197. — Shoot of 'Fay's Prolific' red currant

affected with the budlessness disorder with buds

situated at some distance above the nodes.

Figure 198. — Two-year-old branch of 'Fay's Prolific'

red currant with one-year-old short, budless laterals.

161
Ribes Literature Cited Clark, M. F., A. N. Adams, J. M. Thresh, and R. Casper.

1976. The detection of plum pox and other viruses in woody

plants by enzyme-linked immunosorbent assay (ELISA).

Acta Horticulturae 67:51-57.

Adams, A. N. 1979. The effect of gooseberry vein banding

virus on the growth and yield of gooseberry and red currant.

Journal of Horticultural Science 54:23-25.

Amos, J., and R. G. Hatton. 1927. Reversion in black

currants. L Symptoms and diagnosis of the disease. Journal

of Pomology and Horticultlural Science 6:167-183.

Anderson, M. M. 1971. Resistance to gall mites in the

Eucoreosma section of Ribes. Euphytica 20:422-426.

Basak, W., and J. Maszkiewicz. 1980. Gooseberry mosaic.

Acta Horticulturae 95:49-52.

Baumann, G. 1974. Zur Gewinnung von virusgetesteten

Vermehrungsmaterial bei Johannisbeeren. Der Erwerbsobstbau 16:26-29.

Behrens, E. 1964. Zur Biologie und Ökologie der Johannisbeergallmilbe Eriophyes ribis Nal. sowie ihrer Bekämpfung

im Johannisbeeranbaugebiet Perleberg, Bezirk Schwerin.

Wissenschaftliche Zeitschrift, der Universität Rostock

13:279-288.

Blattny, C. 1930. Poznámky o virovych a pribuznych

chorobách rostlin. [Studies on virus and related diseases of

plants.] Ochrana Rostlin [Plant Protection] 10:130-138. [In

Czech.]

and K. Paulechova. 1964. Ochrana ovocnych stromù

kerù, a révy vinné proti virozám. [Protection of fruit trees,

small fruits, and grapevines against viruses.] Státni

Zemedelské Nakladatelství [State Agricultural Administration], Prague, p. 76-84. [In Czech.]

Bokx, J. A. de, and H. Huttinga. 1981. Potato virus Y.

Commonwealth Mycological Institute/Association of Applied Biologists, Descriptions of Plant Viruses No. 242, 6 p.

Bremer, K., and O. Heikinheimo. 1980. Problems of

reversion disease of Ribes in Finland. Acta Horticulturae

95:87-90.

Campbell, A. I. 1965. The inactivation of black currant

reversion by heat therapy. Long Ashton Research Station,

Report for 1964, p. 89-92.

and J. Adam. 1968. Transmission experiments with

"Gold Dust" disorder of black currant. Long Ashton

Research Station, Report for 1967, p. 104-109.

Cropley, R., A. F. Posnette, and J. M. Thresh. 1964. The

effects of black currant yellows virus and a strain of reversion

on yield. Annals of Applied Biology 54:177-182.

Dijksterhuis, H. P. 1950. Afwijkende verschijnselen in rode

bessen, welke aan virusaantasting doen denken. [Abnormalities in red currants reminiscent of virus.] Tuinbouwberichten

5:157. [In Dutch.]

Easterbrook, M. A. 1980. The host range of a 'non-gallforming' eriophyid mite living in buds on Ribes. Journal of

Horticultural Science 55:1-6.

East Mailing Research Station. 1968. Virus diseases of soft

fruit. East Mailing Research Station, Report for 1967, p. 42.

1970. Production of virus-free clones. East Mailing

Research Station, Report for 1969, p. 54.

Ellenberger, C. E. 1962. Transmission of variegation of

black currants. East Mailing Research Station, Report for

1961, p. 101.

Eyndhoven, G. L. van. 1967. The red currant gall mite,

Cecidophyopsis selachodon n. sp. Entomologische Berichte

27:149-151.

Francki, R. I. B., D. W. Mossop, and T. Hatta. 1979.

Cucumber mosaic virus. Commonwealth Mycological Institute/Association of Applied Biologists, Description of Plant

Viruses No. 213, 6 p.

Ghena, N., and A. Botar. 1974. Rezultate prelimiare privind

virusul clarifierii nervurilor la agris si la coacazul rosu.

[Preliminary data on the infection of gooseberry and red

currant with the vein clearing virus.] Analele Institutului de

Cercetari Pentru Protectia Plantelor 10:35-40. [In Romanian.]

Gorejdchuk, O. G., A. V. Krylov, N. V. Krylova, and I. N.

Samonina. 1977. [Virus diseases of berry crops in the Soviet

Far East.] Zentralblatt für Bakteriologie, Parasitenkunde,

Infektionskrankheiten und Hygiene, Abteilung 2, 132:686-

707.

Gray, E. G. 1949. An interesting disease of gooseberries.

Gardeners' Chronicle 125:198.

and H. F. Everett. 1956. Serious breakdown of

gooseberries. Gardeners' Chronicle 140:403.

162
Harrison, B. D. 1961. Identity of red currant spoon leaf

virus. Tijdschrift over Plantenziekten 67:562-565.

1970. Tobacco rattle virus. Commonwealth Mycological Institute/Association of Applied Biologists, Descriptions of Plant Viruses No. 12, 4 p.

Hatton, R. G., and J. Amos. 1917. Abnormal blossom on

black currant. Gardeners' Chronicle 61:180.

Jordovic, M., B. Dimitrijevic, and M. Rankovic. 1972

Identifikacija Virusa Prstenaste Pegavosti Paradajza Na

Malini U Jugoslaviji. [Identification of tomato ringspost virus

on red raspberry in Yugoslavia.]. Zastita Bilja 23:147-158.

[In Serbo-Croatian with English summary.]

Kahn, R. P. 1956. Seed transmission of the tomato ringspot

virus in the Lincoln variety of soybean. Phytopathology

46:295.

Hedtrich, C. M., and W. Feucht. 1981. Die Bedeutung der

Meristem-Vermehrung—der derzeitige Stand beim Beerenobst. Obstbau 6:82-86.

Hildebrand, E. M. 1939. Currant mosaic. Phytopathology

29:369-371.

1942. Tomato ringspot on currant. American Journal

of Botany 29:362-366.

and P. V. Weber. 1944. Varietal susceptibility of

currants to cane blight organisms and to currant mosaic virus.

Plant Disease Reporter 28:1031-1035.

Hille Ris Lambers, D. 1949. Contributions to a monograph

of the Aphididae of Europe. IV. Temminckia 8:182-323.

1953. Contributions to a monograph of the

Aphididae of Europe. V. Temminckia. 9:1-176.

Houtman, G. 1951. Het verlopen van kruisbessenstruiken.

[Deterioration of gooseberries.] Fruitteelt 41:720-721. [In

Dutch]

Huttinga, H. 1976. Biophysical characterization of viruses.

Annual Report 1975. Institute of Phytopathological Research, Wageningen: p.34.

Jacob, H. 1976a. Investigations on symptomatology,

transmission, etiology, and host specificity of black currant

reversion virus. Acta Horticulturae 66:99-104.

1976b. Untersuchungen zur Übertragung des virösen

Atavismus der Schwarzen Johannisbeere {Ribis nigrum L.)

durch die Gallmilbe Cecidophyopsis ribis. (Westw.). Zeitschrift für Pñanzenkrankheiten und Pflanzenschutz 83:448-

458.

Jaspars, E. M. J., and L. Bos. 1980. Alfalfa mosaic virus.

Commonwealth Mycological Institute/Association of Applied Biologists, Description of Plant Viruses No. 229, 7 p.

Jones, O. P., and S. J. Vine. 1968. The culture of gooseberry

shoot tips for eliminating virus. Journal of Horticultural

Science 43:289-292.

Karl, E., and H. Kleinhempel. 1969. Versuche zur

Blattlaus-und Pfropfübertragung verschiedener Herkünfte

des Adembänderungsvirus der Stachel-und Johannisbeere.

Acta Phytopathologica Academiae Scientiarum Hungaricae

4:19-28.

Katwijk, W. van. 1953. Virusziekten in de vruchtboomkwekerij. [Virus diseases in fruit tree nurseries.] Verslagen

en Mededelingen Plantenziektenkundige Dienst (Wageningen) 119:20-24. [In Dutch.]

Keep, E. 1975. Currants and gooseberries, p. 197-268. In J.

Janick, and J. N. Moore, editors. Advances in fruit breeding,

Purdue University Press, Lafayette, 623 p.

V. H. Knight, and J. H. Parker. 1982. Progress in

the integration of characters in gall mite resistant black

currants. Journal of Horticultural Science 57:189-196.

Kennedy, J. S., M. F. Day, and V. F. Eastop. 1962. A

conspectus of aphids as vectors of plant viruses. Commonwealth Institute of Entomology (London), 114 p.

Kleinhempel, H. 1968. Zur Analyse von Viren in Johannisund Stachelbeerbeständen der Deutschen Demokratischen

Republik. Archiv für Gartenbau 16:151-159.

1970. Verbreitung und Schadwirkung von Virosen

an Johannis-und Stachelbeere. Archiv für Gartenbau 18:319-

325.

1971. Mechanisch übertragbare Viren an Johannisund Stachelbeere in der Deutschen Demokratischen Republik. Zentralblatt für Bakteriologie, Parasitenkunde,

Infektionskrankheiten und Hygiene, Abteilung 2, 126:93-

109.

1972. Diagnose und Bekämpfung von Virusinfektionen an Johannis-und Stachelbeere. Archiv für Gartenbau

19:234-236.

Klesser, P. J. 1951. A virus disease of red currant {Ribes

rubrum L.). Annals of Applied Biology 38:707-772.

Knight, R. L., E. Keep, J. B. Briggs, and J. H. Parker.

1974. Transference of resistance to black-currant gall mites,

Cecidophyopsis ribis, from gooseberry to black currant.

Annals of Applied Biology 76:123-130.

163
Knight, V. H. 1981. Gooseberry veinbanding virus. East

Mailing Research Station, Report for 1980, p. 114.

1981. Screening black currants for resistance to the

gall mite Cecidophyopsis ribis (Westw.) In Breeding for

resistance to insects and mites. Bulletin of the International

Union for Biological Sciences, International Organization for

Biological Control of Noxious Animals and Plants. West

Palaearctic Regional Section, p. 89-93.

and W. E. Manwell. 1980. Gooseberry veinbanding

virus. East Mailing Research Station, Report for 1979, p.

142.

Krczal, H. 1976. Investigations on the effects of reversion

disease on crop and growth of black currant. Acta

Horticulturae 66:91-97.

Kristensen, H. R., H. A. Jorgensen, and J. Jorgensen. 1962.

New attacks of virus diseases, fungi and pests, 1960.

Tidsskrift for Planteavl 65:611-614.

Lantin, B. 1968. Les viroses des cassis et des grosseilliers a

grappes. Phytoma 200:25-29.

Lister, R. M. 1964. Strawberry latent ringspot: a new

nematode-bome virus. Annals of Applied Biology 54:167-

176.

Maarse, J. 1926. Een nieuwe afwijking in de Tay's Prolific'

en een raadgeving aan kwekers en telers. [A new deviation in

Tay's Prolific', and advice to nurserymen and growers.]

Floralia 41:473. [In Dutch.]

Manwell, W. E., M. Sykes, and J. M. Thresh. 1979.

Cucumber mosaic in black currant. East Mailing Research

Station, Report for 1978, p. 105

Massée, A. M. 1928. The life history of the black currant gall

mite. Bulletin of Entomological Research 18:297-310.

Meer, F. A. van der. 1960. Onderzoekingen betreffende

bessevirussen in Nederland. 1. Lepelblad van rode bes.

[Investigations of currant viruses in The Netherlands. I. Spoon

leaf of red currant.] Tijdschrift over Plantenziekkten 66:12-

23. [In Dutch.]

1961. Virusziekten bij rode bessen. [Virus disease of

red currants.] Fruitteelt 51:166-168. [In Dutch.]

1962. Een nieuw virus bij het rode-besseres

'Maarse's Prominent [A new virus in 'Maarse's Prominent'

red currant.] Jaarverslag 1961 (annual report). Institut für

Plantenziektenkundig Onderzoek, p. 93-94. [In Dutch.]

1965a. Investigations of currant viruses in The

Netherlands. II. Further observations on spoon leaf virus, a

soilborne virus transmitted by Longidorus elongatus. Netherlands Journal of Plant Pathology 71:33-46.

1965b. Virusziekten van bessen. [Virus diseases of

currants.] Jaarverslag 1964 (annual report). Institut für

Plantenziektenkundig Onderzoek, p. 85-87. [In Dutch.]

1965c. Nerfvergelingsmozaiek bij rode bessen.

[Vein banding in red currants.] Fruitteelt 55:268-270. [In

Dutch.]

1936. Hoe werken we knoploosheid zo veel mogelijk

uit de Fay's Prolific struiken? [How do we eradicate

budlessness from Fay's Prolific bushes?] Fruitteelt 26:5-6.

[In Dutch.]

1938a. Voor de rode bessen: attentiesein hoog!

[Concerning red currants: Be attentive!] Fruitteelt 28:187-

189. [In Dutch.]

1938b. Lepelblad bij rode bessen. [Spoon leaf in red

currants.] Fruitteelt 28:311-312. [In Dutch.]

Maat, D. Z. 1965. Serological differences between red

currant spoon leaf virus, virus isolates from Eckelraderdiseased cherry trees, and the Scottish raspberry ringspot

virus. Netherlands Journal of Plant Pathology 71:47-53.

1966. Jaarverslag 1965 (annual report). Institut für

Plantenziektenkundig Onderzoek, p. 80-81.

F. A. van der Meer, and H. J. Pfaeltzer. 1962.

Serological identification of some soil-borne viruses in The

Netherlands. Tijdschrift over Plantenziekten 68:120-122.

1965d. Nerfvergeling bij rode bes en kruisbes. [Vein

banding in red currant and gooseberry.] Jaarverslag 1964

(annual report). Institut für Plantenziektenkundig Onderzoek, p. 85-86. [In Dutch.]

1966. Virusziekten van bessen. [Virus diseases of

currants.] Jaarverslag 1965 (annual report). Institut für

Plantenziektenkundig Onderzoek, p. 85-88. [In Dutch.]

1970. Leaf pattern of red currant, p. 98-99. In N. W.

Frazier, editor. Virus diseases of small fruit and grapevines.

University of California Division of Agricultural Sciences,

Berkeley, 290 p.

1975. Heat therapy as a tool for the elimination of

plant viruses. Bulletin des Recherches Agronomiques de

Gembloux. Special volume, 109-117.

1976a. Observations on lilac ring spot. Acta

Horticulturae 59:105-111.

164
1976b. Ribes: Tobacco rattle virus. Annual Report

1975. Institute of Phytopathological Research, Wageningen,

p. 39.

1980. De bestrijding van virussen in bessen,

frambozen en bramen. [Control procedures of viruses in

currants, raspberries and blackberries.] Fruitteelt 70:342-

344. [In Dutch.]

Mellor, F. C, and R. Stace-Smith. 1963. Reaction of

strawberry to a ringspot virus from raspberry. Canadian

Journal of Botany 41:865-870.

Ministry of Agriculture. 1979. Reversion disease and gall mite

of black currant. Advisory Leaflet 277, Ministry of

Agriculture, Fisheries & Food, Northumberland, 7 p.

Murant, A. F. 1970. Arabis mosaic virus. Commonwealth

Mycological Institute/Association of Applied Biologists,

Descriptions of Plant Viruses No. 16.

Nyland, G., and A. C. Goheen. 1969. Heat therapy of virus

diseases of perennial plants. Annual Review of Phytopathology 7:331-354.

Pavlova, N. M. 1964. [Possibilities of breeding black currant

varieties resistant to the bud gall mite.] Trudy prikladnoi

Botanike, Genetike i Selektsii 36:94-102. [In Russian.]

Posnette, A. F. 1952. New virus diseases of Ribes. East

Mailing Research Station, Report for 1951, p. 133- 135.

1964. Transmission studies of gooseberry vein

banding virus. East Mailing Research Station, Report for

1963, p. 110-112.

1970. Gooseberry vein banding, p. 79-81. In N. W.

Frazier, editor, Virus diseases of small fruits and grapevines.

University of California Division of Agricultural Sciences,

Berkeley, 290 p.

Potapov, S., and A. Grinenko. 1968. [Reversion in black

currants and problems of breeding.] Vestnik selskochozyaistvennoi Nauki, Moskva 13:77-80. [In Russian.]

Price, W. C. 1936. Specificity of acquired immunity from

tobacco-ringspot diseases. Phytopathology 26:665-675.

Putz, C. 1972. Les viroses des petits fruits. II. Les viroses du

cassis et des groseilliers. Annales de Phytopathologie

4:59-75.

and G. Stocky. 1971. Identification du virus de la

mosaïque de l'Arabis chez le framboisier et le cassis en

France. Annales de Phytopathologie 3:503-507.

Rake, B. A. 1958. The history of gooseberries in England. In

The fruit year book No. 10, Royal Horticultural Society,

London, p. 84-87.

Rakús, D. 1971. Nova Choroba Cervenych ribezli. [A new

disease of red currant.] Biología (Bratislava) 26:355-358. [In

Czech.]

1973. Virus diseases and virus disease-suspected

phenomena on currant in Czechoslavakia. In Plant virology,

Proceedings of the Seventh Conference of Czechoslovak

Plant Virologists, High Tatras 1971:207-212.

1978. The incidence of currant full blossom in the

CSSR. Proceedings VII Czechoslovak Plant Protection Conference, Nitra, 6th-8th September, 1978:132.

O. Kralik, and J. Break. 1974. Mycoplazma V.

Ribes houghtonianum Jancz. nakazené "plnokvetosti"

[Mycoplasma-like organism in Ribes houghtonianum Jancz,

infected with a Yellows disease]. Sbomik Ustav Vedeckotechnickych Informad Ochrana Rostlin 10:307-309. [In

Czech.]

and V. Maliarciková. 1975. Studium skodlivosti

choroby "plokvetost ribezle," [Harmfulness of the currant full

blossom.] Sbomik Ustav Vedeckotechnickych InformaciZahradnictvi (Praha) 2:163-168. [In Czech.]

Reinders, E. 1957. Leerboek der algemene plantkunde.

[Textbook of general botany.] 1:258-264. Amsterdam. [In

Dutch.]

Richter, J., H. Kegler, and G. Zahn. 1966. Isolierung des

Himbeerringflecken Virus (raspberry ringspot virus) aus

Roter Johannisbeere (Ribes rubrum). Phytopathologische

Zeitschrift 57:259-266.

Rietsema, I. 1955. Hybrides interspécifiques des genres

Ribes et Rubus. Proceedings of the Fourteenth International

Horticultural Congress: 712-715.

Ritzema Bos, G. 1904. Eenige misvormingen of monstrositeiten. [Some malformations or monstrosities.] Tijdschrift

over Plantenziekten 10:135-144. [In Dutch.]

Saumjan, K. V. 1964. [Resistance of black currants to gall

mite and reversion.] Sadavodstvo 4:40-41. [In Russian.]

Savzdarg, E. E. 1957. [Methods of controlling mites on

berry plants, based on their biological and ecological

features.] Izvestiya Timiryazevskoi selsko chozyaistvennoi

akademii 14:19. [In Russian.]

Schmelzer, K. 1963. Untersuchungen an Viren der Zier- und

Wildgehölze. 1. Mitteilung: Virosen an Viburnum und Ribes.

Phytopathologische Zeitschrift 46:17-52.

165
1970. Untersuchungen an Viren der Zier- und

Wildgehölze. 7. Mitteilung: Weitere Befunde an Buddleja,

Viburnum, Caryopteris und Philadelphus sowie Viren an

Leycesteria, Chionanthus, Ribes, Hydrangea, Syringa,

Spiraea, und Catalpa. Phytopathologische Zeitschrift

67:285-326.

Schuch, K. 1957. Viruskrankheiten und ähnliche

Erscheinungen bei Obstgewächsen, p. 61-68. Mitteilungen

Biologische Bundesanstalt für Land- und Forstwirtschaft

Berlin-Dahlem 88: 96 p.

1963. Untersuchungen über den Nachweis des Raspberry Ringspot Virus bei der roten Johannisbeere in Deutschland. Nachrichtenblatt Deutschen Pflanzenschutzdienst

(Braunschweig) 15:105-107.

Silvere, A. F., and M. A. Romeikis. 1973. [Formation and

release of mesosome-like microbodies in the sporogenesis of

the endophytic currant reversion bacillus.] Eesti NSV

Teaduste Akadeemia Toimetised, Bioloogia 22:274-277. [In

Russian.]

Stace-Smith, R. 1970. Tomato ringspot virus. Commonwealth Mycological Institute/Association of Applied Biologists, Descriptions of Plant Viruses No. 18, 4 p.

Téliz, D., R. G. Grogan, and B. F. Lownsbery. 1966.

Transmission of tomato ringspot, peach yellow bud mosaic,

and grape yellow vein viruses by Xiphinema americanum.

Phytopathology 56:658-663.

Thomsen. A. 1970. Nervebandsklorose-virus hos Stikkelsbaer. [Veinbanding disease of gooseberry.] Tidsskrift

Plantavl 74:313- 317. [In Danish with English summary.]

Thresh, J. M. 1964a. Increased susceptibility to the mite

vector caused by infection with black currant reversion virus.

Nature, London 202:1028.

1964b. Warm water treatments to eliminate the gall

mite from black currant cuttings. East Mailing Research

Station, Report for 1963, p. 131-132.

1965. The effects of gall mite on the leaves and buds

of black currant bushes. Plant Pathology 14:26-30.

1966a. Field experiments on the spread of black

currant reversion virus and its gall mite vector. Annals of

Applied Biology 58:219-230.

1966b. Virus disease of black currant. East Mailing

Research Station, Report for 1965, p. 158-163.

1967. Virus diseases of red currant. East Mailing

1970. Virus and viruslike diseases of gooseberry and

currant, p. 75-104. In N. W. Frazier, editor. Virus diseases

of small fruits and grapevines. University of California

Division of Agricultural Sciences, Berkeley, 290 p.

1971. Some effects of reversion virus on the growth

and cropping of black currants. Journal of Horticultural

Science 46:499-509.

D. Bates, and W. Manwell, 1978. Black currant

reversion. East Mailing Research Station, Report for 1977,

p. 93.

and R. Blandy. 1979. Black currant reversion. East

Mailing Research Station, Report for 1978, p. 105.

Vrie, M. van de. 1967. De levenswijze en de bestrijding van

de rondknopmijt van zwarte bes, Cecidophyopsis ribis. [The

biology and control of the black currant gall mite,

Ceciophyopsis ribis.] Netherlands Journal of Plant Pathology

73:170-180. [In Dutch with English summary.]

Winter, A. G. 1940. Virusartige Erkrankungen der roten

Johannisbeeren (Ribis rubrum). Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz 1:512-520.

Zirka, T. I., I. G. Skrypal, and I. P. Alekseenko. 1977.

[Possible etiological factors of black currant reversion.]

Tagungsberichte Akademie der Landwirtschaftswissenschaften zu Berlin, DDR 152:101-105. [In Russian.]

Research Station, Report for 1966, p. 146-152.

166
(^Section 4.

l^ Virus and Viruslike Diseases ofRubus

(Raspberry and Blackberry)^^

Introduction

By R.jStace-Smith

In '*Virus Diseases of Small Fruits and Grapevines,"

Converse (1970c) discussed the occurrence, detection, and

control of Rubus viruses. Our understanding and knowledge

of these aspects of Rubus virus diseases has not altered

appreciably during the intervening years since the first edition

appeared. I will not attempt to update this introductory

chapter, although I will comment on a few significant

advancements. A marked improvement has been made in

virus detection with the introduction and widespread use of

the enzyme-linked immunosorbent assay (ELISA) technique

(Clark and Adams 1977). For those Rubus viruses for which

antiserum is available, this serological procedure has become

an important means of virus detection. Unfortunately, its use

is restricted to those viruses that can be purified in sufficient

quantity to inject into a laboratory animal and produce a

specific antibody. Virtually all of the true Rubus viruses, that

is, those viruses whose natural hosts are restricted to the

genus Rubus, either occur in low concentration or, for other

reasons, have defied purification attempts. However, where

some of the more damaging virus diseases affecting crops

belonging to the genus Rubus are not restricted to that genus

but infect a wide range of herbaceous and woody plants, and

since these viruses can be purified, serological techniques

such as ELISA can be usefully applied.

Advances in our basic knowledge of plant viruses in general

has been considerable in the past decade, but advances in our

knowledge and understanding of Rubus viruses has not

changed dramatically. In fact, one could justifiably question

whether there have been sufficient advances to warrant a

revised edition of the handbook. I have no doubts about the

value of the revised edition—although there has not been a

dramatic increase in the knowledge, there have been a few

major contributions and a number of minor contributions.

Cumulatively, these have resulted in a significant update in

the Rubus section of this as compared with the former

handbook.

There is good reason why there have been relatively few

major advances in our knowledge of Rubus viruses and virus

diseases in recent years. The cumulative research effort

devoted to Rubus viruses on a worldwide basis is relatively

modest. Precise figures are unavailable but I would estimate

that less than 10-person years are devoted to this field of

research. A bibliography covering the period 1973-78

includes 76 references to Rubus virus diseases (Stace-Smith

and Matsumoto 1979). A later compilation covering the

period 1979-81, contains only 29 references to Rubus viruses

(Stace-Smith and Matsumoto 1982), an average of about 10

citations per year.

One development that has had a positive influence on the

exchange of information on Rubus virus diseases was the

action of the Plant Protection Commission of the International Society for Horticultural Science in establishing a

working group, "Virus Diseases of Small Fruits," in 1974.

This working group was charged with the responsibility of

organizing international symposia on small fruit virus

diseases. To date, three symposia have been held, the first in

Heidelberg, Federal Republic of Germany, in 1976; the

second in Budapest, Hungary, in 1979; and the third in

Vancouver, Canada, in 1982. In these three symposia, 8, 5,

and 10 lectures, respectively, were on Rubus virus diseases.

The proceedings were published in Acta Horticulturae Nos.

66, 95, and 129. Judging by the response of the participants,

I anticipate that these international symposia will continue at

3-yr intervals for the foreseeable future. In addition to

facilitating an exchange of information on Rubus virus

diseases, the symposia provide a forum for keeping abreast of

developments in virus diseases affecting other small fruit

crops.

The ultimate objective of any research program on Rubus

virus diseases is directed towards minimizing the adverse

affects attributed to virus infections. In Western North

America, we have basically reached this objective with those

viruses that are transmitted by aphids. The raspberry mosaic

disease, which was once widespread along the Pacific Coast of

North America, is rarely a serious problem there today. The

absence of mosaic is attributed to the fact that the older

cultivars that supported populations of the aphid vector

Amphorophora agathonica Hottes have been replaced by

cultivars that are highly resistant to the aphid vector

(Daubeny and Stary 1982). With a reduction in the

importance of the aphid-borne viruses, we are experiencing

what appears to be an increase in the importance of the

pollen-borne viruses, particularly raspberry bushy dwarf

virus (RBDV). The pollen-borne viruses present a unique

problem in that there is no way to prevent their spread except

by eradicating infected sources and using immune parents

in breeding programs. Eradication of infected sources is not

readily achieved because infected plants often exhibit either

no obvious symptoms or symptoms that are so vague that

conclusive diagnosis cannot be made by visual examination

(Stace-Smith et al. 1982). Accurate diagnosis can be made by

serological tests or sap transmission to indicator plants but,

because of the time and expense involved, the extent of field

surveys is curtailed. The problem can be overcome by

concentrating the testing on nursery stock that is used to

establish new plantings, but there is still the concern that

these may become contaminated if planted near infected

stock. As noted by Daubeny et al. (1982), it is preferable not

to expose virus-tested stock of susceptible cultivars to pollen

from infected sources. There is no information as to what

167
constitutes safe geographic isolation, but we assume that this

distance would vary from cultivar to cultivar. In any event,

we suggest that it would be unwise to establish a new

planting of a susceptible cultivar adjacent to older plantings

of unknown virus content.

To supply healthy planting material, certification schemes are

now operating for several kinds of plants, including

raspberry, and the raising of stocks for propagation is often

separated from the growing of a crop for its main purpose.

Special stocks that form the basis of certification schemes are

built up by propagating from single virus-indexed plants.

Until recently, the production of virus-tested stocks of plants

that are grown as cultivars depended upon finding an

uninfected plant of the cultivar to start the stock. Fortunately,

this is no longer so, for methods have been devised whereby

plants can be freed from some or all of the viruses that infect

them. No useful clone need be abandoned because the whole

clone is virus infected. The method that has found the widest

application is meristem tip culture, usually taken from clonal

material that has been subjected to a prolonged period of

growth at a temperature that is considerably higher than

would normally be used for plant production. Virus-tested

raspberry clones are now available for all the newer cultivars,

but some of the older cultivars that appear to be totally

infected have not been revitalized by therapy procedures. It is

a tedious process to produce a clone free of known viruses

from a cultivar that is totally infected and, unless there is a

demonstrated need for such a clone, it is doubtful whether the

effort required is warranted. RBDV is of particular concern

because it is common in clones that may be useful to plant

breeders and a proportion of the progeny is infected. While

RBDV can be eliminated from clonal stock, the process

should not be necessary if the virus status of all clonal

material to be used in breeding programs is established and

selections that become infected are discarded.

What major advances will we see in Rubus virus disease

research over the next decade? This is a difficult question to

answer but, judging by current trends in plant virology, it is

at least possible to speculate on a few possibilities. First, we

will utilize advances that are being made in virus detection to

extend field indexing and obtain a more accurate picture of

precisely what viruses are present in the important Rubus

growing regions of the world. A precise understanding of the

problem is essential in devising control procedures and it is

anticipated that, in many areas where raspberries and

blackberries constitute a commercial crop, virus diseases will

cease to be an appreciable concern. Second, improvements

will be made in virus purification procedures to the point

where some of the Rubus viruses whose properties are little

understood will be purified, at least in minute quantities, and

antiserum will be prepared using the monoclonal antibody

technique. Finally, increased emphasis will be placed on

developing new cultivars that are resistant or immune to the

major Rubus virus diseases and their vectors.

Aphid-Borne Diseases

,1^^ ^ Raspberry Mosaic// .

By R. H.fconverse, R.|Stace-^mith, and A. T.[jones

Additional Common Names

Red raspberry mosaic (Bennett 7927); type b mosaic (Harris

1933); green mottle mosaic = green mosaic (Cooley 1936b);

raspberry Mosaic I (Harris 1939); veinbanding disease

(Cadman 1952b) and veinbanding mosaic (Murant 1974b).

Raspberry mosaic disease (RMD) is induced by infection

with a complex of viruses. In Canada, black raspberry

necrosis virus (BRNV) and rubus yellow net virus (RYNV)

are together reported to induce raspberry mosaic disease in

red raspberry (Stace-Smith 1956). In Europe, mosaicaffected plants usually contain, in addition, raspberry leaf

mottle virus (RLMV) and raspberry leaf spot virus (RLSV).

To what extent these two extra viruses are involved in the

disease is not clear. Infection with each of the four viruses

singly can induce symptoms in some Rubus species (see the

chapters dealing with these specific viruses for detailed

discussion on the common names associated with such

symptoms) and, in some sensitive red raspberry cultivars,

RLMV and RLSV induce a disease variously referred to as

Mosaic 2, type c mosaic symptoms, or leaf spot mosaic. This

disease is distinct from raspberry mosaic and is covered in

detail in the chapter dealing with these two viruses.

History and Geographic Distribution

Wilcox and Smith (1924) first demonstrated a mosaic disease

of raspberry that was induced by an agent(s) transmissible by

the aphid Amphorophora agathonica Hottes, formerly

designated A. rubi (Kalt.). The early literature on RMD was

reviewed by Bennet (7927), Harris {1933, 1939), StaceSmith (1956), and Cadman (1961b). Graft transmission was

first demonstrated by Harris (1939) in Great Britain. Other

papers that review RMD have been published by Converse

(1966a, 1977), Converse et al. (1970a), Jones (1981b),

Murant (1974b, 1976b), and Stace-Smith (1960a, 1968).

Stace-Smith (1956) demonstrated that RMD in British

Columbia was caused by dual infection with viruses

transmitted by the aphid vector, Amphorophora agathonica

Hottes. He named these black raspberry necrosis virus

(BRNV) and rubus yellow net virus (RYNV). As already

indicated, in Europe a second and distinct type of mosaic,

described initially as type c symptoms (Harris 1933) and later

as Mosaic 2 (Harris 1939) or leaf spot mosaic (Murant

1974b), is induced in sensitive raspberry cultivars by

infection with either of the two distinct aphid-borne viruses

RLMV and RLSV (Cadman 1951, 1952d). This chapter does

not consider this second type of mosaic but does discuss the

possible involvement of RLMV and RLSV in RMD.

168
RMD is worldwide in distribution, occurring virtually

wherever red, black, or purple raspberries are grown. Crops

in some regions are less severely affected than those in others,

either because healthy planting material or specific cultivars

are used, or because aphid vectors do not occur there. This

disease was not observed in New Zealand, probably because

symptomless plants were introduced and aphids of the genus

Amphorophora do not occur (Jones and Wood 1979). In

California, Oregon, and Washington, the climate and Riihiis

hosts appear to be unfavorable for the maintenance and

development of large colonies of A. agathomca. and

although RMD has been found in wild and cultivated Riihiis.

it is rare. In Great Britain, because healthy planting material

is used and the acreage of cultivars that resist colonization by

aphid vectors is increasing, RMD is a decreasing problem

(Jones 1981c). RMD can be expected to decrease in

prevalence in North America too as the acreage of

aphid-resistant cultivars increases (Daubeny 1982). In parts

of northern Europe and eastern North America, however,

where older cultivars are still widely grown and Amphorophora vectors occur in large numbers, RMD is still

widespread in cultivated and wild Riihiis.

Economic Importance

A range of symptoms is associated with RMD. from mild to

severe mottling or veinbanding, dwarfing, and crumbly fruit,

depending on the cultivar and the growing conditions. Yield

losses due to RMD in some red raspberry cultivars were 11 to

14% in British Columbia (Freeman and Stace-Smith 1970)

and 39% in Maryland (Converse 1963). Pollen abortion in

affected plants of some red raspberry cultivars was twice that

found in healthy plants (Freeman and Stace-Smith 1970). but

drupelet set was unaffected (Daubeny et al. 1970). In

Scotland, RMD was thought to decrease red raspberry yields

by 28% (Wood and Anderson 1959). The effects on growth

and yield of infection with the individual component viruses

of the RMD complex are presented in the chapters dealing

with these viruses. Strain differences within the individual

viruses are possibly an additional source of variation in the

severity of the disease complex, but this has not been

quantified.

Symptoms on Natural and Experimental Hosts

In cultivated black raspberry, RMD delayed foliation in the

spring (Cooley 1936a). In affected plants, leaves produced

during cool weather are mottled and blistered (fig. 199). but

leaves formed during hot weather may be symptomless;

young shoot tips are often necrotic and brittle. Canes are

short and rosetted. Fruit yield is reduced and fruit is small,

seedy, and of inferior flavor. Plants infected for a few years

often fail to survive the winter.

Figure 199. — Young shoot of black raspberry infected

with raspberry mosaic disease, showing mottled,

blistered leaves after leaf grafting with black raspberry

necrosis virus- and rubus yellow net virus-infected red

raspberry.

Figure 200. — Red raspberry cv. Mailing Jewel"

naturally infected in Scotland with raspberry mosaic

disease and showing leaf puckering and veinbanding

symptoms. (Copyright Scottish Crop Research Institute.)

prevailing temperature. Leaf symptoms often fade in hot

weather. Pollen production, fruit yield, and quality are

decreased in affected raspberry plants.

In cultivated blackberry, RMD has not been described as

such, but some of the component viruses of RMD have been

identified. Critical studies of their effects on growth and yield

have not been made. In general, blackberry cultivars appear

to be more tolerant of infection than raspberries, but plant

vigor, fruit yield, and fruit quality are probably decreased by

such infections.

In cultivated red raspberry, affected plants may show

decreased vigor and may remain symptomless or exhibit mild

to severe leaf mottling, blistering, and vein clearing or

veinbanding, depending on the cultivars (fig. 200) and the

169
Natural hosts of the four viruses associated with the RMD

complex are all in the genus Rubus and are listed below.

Natural host list and RMD prevalence, where known:

Rubus, subgenus Idaeobatus

R. idaeus L. Widespread

R. idaeus L. var. strigosus (Michx.) Maxim. Widespread

R. innominatus S. Moore (Wilcox 1926)

R. leucodermis Dougl. (Zeller 1923; Huber and Johnson

1952)

R. occidentalis L. and hybrids with red raspberries.

Widespread

R, odoratus L. (Zeller 1923)

R. parviflorus Nutt. (Zeller 1923)

R. phoenicolasius Maxim., a common wild host locally

(Zeller 1923; Converse 1960)

R. spectabilis Pursh (Zeller 1923)

Rubus, subgenus Eubatus

R. allegheniensis Porter cv. 'Darrow'. Eastern U.S. (R.

H. Converse, unpublished data)

R. fruticosus L. (aggregate species)

R. gracilis Roxb. (also known as R. niveus Wall.)

(Jones 1975b)

R. laciniatus Willd. (Zeller 1923; Converse et al. 1970a)

R. lasiocarpus Thumb, var. rosifolius (Hook. F.) (Jones

and Roberts 7977)

R. loganobaccus Bailey cv. 'Logan'. (Jones and

Jennings 1980b)

R. procerus P. J. Muell. (Stace-Smith 1955a)

Rubus ursinus Cham, and Schlecht. (Converse and

Bartlett 1979)

R. ursinus Cham, and Schlecht, var. macropetalus

Dougl. (Zeller 1923)

Rubus species. Various named and unnamed, cultivated

and wild, erect and trailing blackberries (Bennett

1927; Converse 1981; Converse et al. 1970a; Jones

and Roberts 7977; Jones and Jennings 1980b)

Additional rosaceous hosts infected experimentally either by

aphids or by graft inoculation:

Fragaria vesca L. (RYNV only) (Stace-Smith and Mellor

7957)

Rubus albescens Roxb. (Stace-Smith 1955a)

R. ellipticus Smith (Converse et al. 1970)

R. henryi Hemsl. and Kuntze (Cadman 7957)

R. molaccanus L. (Jones and Roberts 7977)

R. saxatilis L. (Cadman 7957)

For additional experimental herbaceous hosts of BRNV, see

p. 179.

RMD has only once been reproduced experimentally.

Stace-Smith (1956) found that leaves of 'Cuthbert' red

raspberry remained symptomless when they were experimentally infected with BRNV, developed a fine vein

chlorosis when infected with RYNV, and showed symptoms

of RMD only when infected with the complex of BRNV and

RYNV (fig. 201 a, b, c). Converse (1966b) found that all of

the 20 'Latham' red raspberry clones collected from

commercial fields in Eastern U.S. were infected with

heat-labile mosaic components of the BRNV type, but that

only 35% of them were additionally infected with heat-stable

virus of the RYNV type.

For symptoms caused by the individual viruses of the RMD

complex on various Rubus and non-Rubus hosts, see the three

following chapters.

Natural and Experimental Transmission

RMD occurs either because diseased material has been

planted or because the viruses inducing RMD have been

transmitted to healthy plants. None of the viruses associated

with RMD are transmitted through soil or seed, but all are

transmitted, probably in a semipersistent manner (Cadman

7957, 1954; Murant 1974b), by aphids of the genus

Amphorophora. A few aphid species other than Amphorophora have been found to transmit some of the component

viruses experimentally, but their role in nature is uncertain.

(See chapters on the individual component viruses.) The

major vector in Europe is Amphorophora idaei Borner [also

known as A. rubi (Kalt.) ssp. idaei (Borner)] and in North

America, Amphorophora agathonica (also known as A. rubi

(Kalt.) ) (fig. 202).

The biology of A. idaei was investigated by Dicker (1940)

and by Rautapää (1967). Four biotypes of this aphid have

been recognized in Great Britain by their different abilities to

colonize certain red raspberry genotypes (Briggs 1965). The

biology of A. agathonica was studied in Michigan,

Minnesota, and New York (Giles 7966; Winter 7929;

Kennedy and Schaefers 1974c). Only one biotype of A.

agathonica is recognized in North America (Converse et al.

7977).

These two Amphorophora species complete their life cycles

on Rubus (that is, they are monophagous) and produce alates

involved in the long-distance spread (500 m or more) of

RMD-causing viruses. In Great Britain, A. idaei is present in

crops from June to August (Jones 1976d; Converse et al.

1970a; Dicker 1940), and, in New York State, A. agathonica

occurs from mid-June to mid-August (Kennedy and Schaefers 1974c). Apterae are active, drop to the ground when

disturbed, and probably are involved in local RMD spread by

their own movements and by passive movements caused by

wind, rain, and passage of machinery through the crop. Virus

spread is usually along rows more than across rows (Rankin

1931; Cooley 1936b). In Great Britain and The Netherlands,

peak populations of A. idaei occur in mid-summer and early

autumn (Dicker 1940; Kronenberg and de Fluiter 7957 ; Jones

1976d). For A. agathonica, peak populations occur in late

June in British Columbia (Stace-Smith 1960b) and in July

170
Figure 201. — 'Latham' red raspberry leaves chronically infected by grafting with, left, black raspberry

necrosis virus (BRNV); center, Rubus yellow net virus

(RYNV) plus BRNV; right, RYNV. This illustration

shows the loss of vigor characteristic of infection by

BRNV plus RYNV.

Figure 202. — Amphorophora agathonica on Rubus.

and August in the United States (Bennett 1932; Huber and

Schwartze 1938; Converse et al. 1970a). Natural rates of

transmission of the component viruses by aphids vary with

the virus, cultivar, season, and region, but annual infection

rates of 60% or more have been measured (Converse et al.

1970a; Jones 1976d, 1979a). The three following chapters

give specific details for the individual viruses of the RMD

complex.

The component viruses of the RMD complex have been

experimentally transmitted by one or more of the following

methods: (1) aphids; (2) graft inoculation; and (3)

inoculation of sap.

1. Aphids. The three following chapters give the details of

transmission of individual viruses by specific aphids. The

aphids listed below have been found to be vectors of one or

more viruses associated with RMD:

Amphorophora agathonica Hottes [also known as A. rubi.

(Kalt.)) (Bennett 1927)

A. idaei Borner [also known as A. rubi. ssp. idaei

(Borner)] (Cadman and Hill 1947)

A. sensoriata Mason (Bennett 1932)

A. rubicumberlandi Knowlton and Allen (Huber 1939)

Aulacorthum solani (Kalt.) (Jones and Murant 1972)

Macrosiphum euphorbiae (Thos.) (Cadman 1954; Jones

1976d)

Macrosiphum fragariae (Wlk.) (also known as Sitobion

fragariae (Wlk.) (Jones 1976d)

lllinoia rubicola (Oestlund) (also known as Masonaphis

rubicela and Oestlundia rubicola) (Bennett 1932)

Myzus ornatus Laing (A. T. Jones, unpublished data)

The following aphids have been found to be nonvectors of

one or more of the viruses associated with RMD.

Amphorophora rubito.xica Knowlton (Stace-Smith 1954)

A. ruborum Borner (also known as A. rubi. ssp. ruborum

Borner) (Cadman 1954) A. ruborum is common on

blackberry in Europe (Hille Ris Lambers 1950;

Blackman et al. 1977)

Aphis rubicola Oestlund (Bennett 1927)

Aphis idaei van der Goot (Cadman 1952b)

Chaetosiphon fragaefolii (Cock.) (Stace-Smith and Mellor

1957)

Note: C. fragaefolii is able to acquire RYNV from

graft-inoculated strawberry and infect Rubus but not

vice-versa.

In North America, A. agathonica can be used in a reliable

system to detect viruses of the RMD complex by infecting

small, vigorous R. occidentalis seedlings. (See "Detection

and Identification" as well as the following chapter on

BRNV.)

2. Graft inoculation. All viruses involved in RMD can be

graft transmitted to Rubus. Techniques used are cleft

grafting, patch grafting, cane inarching, a modification of

cane inarching in which cut scions are maintained in small

bottles of water during the incubation period (bottle grafting),

and leaf grafting (Cadman 1951 ; Harris 1939; van der Meer

1958). Bottle grafting is the current standard graft indexing

technique in Great Britain, whereas leaf grafting is the

current standard method in the United States.

Susceptible cultivars of R. occidentalis like 'Plum Farmer'

or 'Munger' or their open-pollinated seedlings and R. henryi

have been widely used to detect viruses of the RMD complex

occurring singly or in mixtures in Rubus (Cadman 1951;

Converse 1979; Jones 1976d; Jones and Roberts 1977).

Detection of pure cultures of BRNV and RYNV was 95%

reliable in R. henryi if three scion leaflet grafts survived for

14 days (Converse 1965).

BRNV, RLMV, and RLSV all produce similar symptoms in

graft-inoculated R. henryi and R. occidentalis, and further

graft inoculations are needed to specific red raspberry

indicator cultivars to distinguish these viruses. (See detailed

discussion of this separation in "Raspberry Leaf Mottle and

171
Table 8.—Particle morphologies of viruses probably involved in the raspberry mosaic disease complex

Virus Morphology Dimensions Reference

RYNV Unenveloped

bacilliform particle

with rounded ends.

80-150 X :

BRNV Isometric 25-30 nm

RLMV Possibly isometric 30 nm

RLSV No particles seen

Stace-Smith and

Leung 1976\ Jones

and Roberts 1976.

Jones and Murant 1972\

Murant et al. 1976,

Jones 1976h.

Jones I98la.

Raspberry Leaf Spot," p. 183.) Additionally, R. henryi

develops necrotic shoot tips following graft inoculation with

many isolates of tobacco streak virus. This necrosis could

easily be confused with that caused by BRNV, RLMV, or

RLSV (Frazier 1966; Converse and Kowalczyk 1980; Jones

and Jennings 1980b). (See "Tobacco Streak Virus in Rubus/'

p. 235.)

3. Sap inoculation. Among the four viruses associated with

the RMD complex, only BRNV has so far been successfully

transmitted in sap to herbaceous plants (Cadman 1960a,

1961a; Jones and Murant 1972; Richter 7962, 1964c), but it

is transmitted only with difficulty. In Chenopodium quinoa

Willd., BRNV typically induces small, chlorotic, local

lesions within a week and systemic chlorotic mottle or

necrosis a week later. (For further discussion of details, see

"Black Raspberry Necrosis," p. 178.)

Properties of the Causal Agents

Particle morphologies of the viruses of the RMD complex are

listed in table 8. (See the respective chapters on these viruses

for further details.)

Detection and Identification

In some Rubus cultivars, RMD produces characteristic

symptoms; however, identification of the causal viruses

associated with RMD in a given infected Rubus plant from

the field is not possible by study of the symptoms produced

on that plant. Although BRNV can be transmitted to

Chenopodium quinoa test plants by inoculation of sap, this is

often erratic and therefore not reliable for routine testing

(Jones and Murant 7972; Jones and Roberts 7977). No

antisera have been produced against any of the causal viruses

of the RMD complex so that their detection depends on

assays either by (1) aphid transmission, (2) grafting, or (3)

graft indexing following heat treatment. Such assays are best

done in the spring when vigorous, new, succulent growth is

formed on both source and indicator plants grown at about

18° to 25°C.

1. Aphid transmission. In North America, where the

efficient vector Amphorophora agathonica is available and

will feed on R. occidentalis, the use of aphids for indexing is

recommended by some workers (Mellor and Stace-Smith

1979). Several A. agathonica are allowed to feed on the

source plant for 1 day and are then transferred to young,

vigorous Rubus occidentalis seedlings (like 'Munger' op,

from open-pollinated seed) for 1 day in the greenhouse. The

insects are then killed with an insecticide, and the test plants

are observed for up to 6 wk for symptom development. (See

separate chapters on the specific viruses of the RMD complex

for details.) By sequentially feeding aphids on a series of

black raspberry seedlings, component viruses can be

separated from mixtures (Stace-Smith 7956). In Europe, the

vector A. idaei does not readily feed on R. occidentalis and

aphid transmission is not used for detecting infection.

2. Grafting. Various grafting procedures have been used.

Leaf grafting is preferred in North America and bottle

grafting in Europe. Young, vigorous, susceptible R.

occidentalis seedlings (like 'Munger' op) are stripped of all

mature leaves except those used to accept leaflet grafts.

Donor leaflets from vigorous, recently matured leaves are

cut, and their petioles are sharpened to a long, thin point.

These are then inserted into split debladed petioles of the test

seedlings and are tightly wrapped with tape. Self-cohering

tape is often used. (See the introductory chapter of the

strawberry section of this handbook, fig. 1, for detailed

illustrations of the leaf graft technique.) The grafted plants

are placed in a humid environment for 1 wk to allow the

grafts to become attached and are then placed on the

greenhouse bench for 6 wk or more to observe symptom

development. (See detailed symptom descriptions of the

specific viruses.) Speed in handling the cut petioles, keeping

them moist at all times during the grafting procedure, and

tight binding of the graft unions are essential for successful

development of the leaflet graft unions. When carefully done,

wide interspecific and even intergeneric leaf grafts can be

made with Rubus leaflet sources (Converse 7965, 1979).

172
In Europe, R. henryi and R. occidentalis are vegetatively

propagated, and small, potted plants are bottle-grafted

(inarched with a cleft graft to a donor shoot, which is

maintained in a container of water fixed to a supporting

stick). The graft is tightly wrapped and the donor shoot is

well supported to prevent separation of the tissues (fig. 203).

Successful union of such grafts may be determined by

removing the donor shoot from water after about 3 to 4 wk

and noting its survival. Test plants are observed for symptom

development for up to several months. (See chapters on

individual viruses for discussion of symptoms.)

In Scotland, bottle grafting to 'Mailing Landmark' is used to

detect RLMV and to 'Norfolk Giant' to detect RLSV. (See p.

185-186 for fuller details.) Leaflet grafting is also satisfactory for inoculating 'Mailing Landmark' and 'Norfolk Giant'

red raspberry with viruses (Converse 1981); however, separation of component viruses is not possible by grafting to

Rubus.

In addition to separation by serial aphid transfers, RYNV can

be separated from BRNV in mixed infections by leaf grafting

to Fragaria vesca var. semperflorens cv. 'Alpine'. This

cultivar is susceptible to RYNV but not to BRNV

(Stace-Smith and Mellor 1957). Separation of RYNV and

BRNV may also be achieved by leaf grafting to healthy

'Fairview' red raspberry and, after 6 mo which must include

a dormancy period, selecting root propagants that show

mottling (indicating the presence of only heat-labile

components like BRNV) but not mosaic symptoms (BRNV

plus RYNV) (Freeman and Stace-Smith 1965). The probable

movement of RLMV and RLSV into roots under these

conditions is unknown.

3. Graft indexing following heat treatment. RYNV is not

eradicated from plants kept at 37°C for several weeks, but

BRNV, RLMV, and RLSV usually are eradicated (Jones and

Roberts 1976); however, Mellor and Stace-Smith (1979)

reported an isolate of BRNV that was resistant to heat

treatment.

Control Procedures

There is no known immunity in Rubus to any of the viruses

associated with RMD; however, control of the incidence and

effects of RMD can be attempted in five ways:

1. Use of Rubus material free of the viruses inducing

RMD.

2. Use of management methods to restrict virus spread.

3. Use of insecticides to control populations of aphid

vectors.

4. Use of Rubus cultivars resistant to vector aphids.

5. Use of virus-tolerant Rubus cultivars.

1. Use of Rubus material free of the viruses inducing

RMD. With the finding of suitable indicator plants, the

development of indexing methods, and the application of

heat treatment, it became possible in the 1950's to produce

Figure 203. — Transmission of raspberry mosaic component viruses by bottle grafting to Rubu\ sp (Copyright

Scottish Crop Research Institute.)

virus-tested clones of Rubus cultivars, increase them in

vector-free enclosures (screenhouses and gauzehouses or

isolated sites), and distribute stocks to nurseries. Various

certification schemes have been established to monitor the

health of such stocks prior to their release to growers [United

Kingdom (1965); Ontario Horticultural Experiment Station

(1966): California Department of Agriculture (1973)\.

Chambers (1954. 1961) developed Rubus heat treatment

techniques and helped to originate a virus-tested Rubus stock

program in Great Britain. Similar systems were developed in

Canada (Bolton and Turner 7962), the United States

(Converse 1964. 1966b), the Federal Republic of Germany

(Baumann 1980. 1981), and France (Morand 1963). Tissue

culture expiant techniques were successful in eliminating the

component viruses of RMD (Putz 1971) and have been

combined with heat treatment to produce virus-tested Rubus

stocks (Pyott and Converse 1981).

2. Use of management methods to restrict virus spread. In

the past, roguing out RMD-affected plants was used in

attempts to control RMD. However, single infections with

viruses associated with RMD induce no symptoms in most

red raspberrry cultivars, so that roguing is of little value in

controlling the spread of these viruses.

173
The desirability of planting healthy Rubus plants at a distance

from diseased Rubus has long been known. Because black

raspberries are more severely damaged by RMD than most red

raspberries, growers in the past were advised not to plant the

two crops next to each other. This can now be done safely,

however, if virus-tested stocks are used. Isolation distances

of 100 m or more from RMD-infected wild or cultivated

Rubus have been recommended in the United States (Cooley

1936c). In northwestern United States, however, the general

rarity of A. agathonica in cultivated Rubus (presumably

because of unfavorable hosts and environmental conditions),

results in only a low incidence of RMD in certified black and

red raspberry plantings planted next to uncertified plants

(Converse 7975; and R. H. Converse, unpubHshed data).

In cultivars that have some resistance to colonization by A.

idaei, the size of the planting influences the amount of virus

infection in Scotland (Jones and Murant 7975; Jones 7979a).

The larger the planting, the smaller the proportion of plants

that are peripheral and that are particularly vulnerable to

primary infection by viruliferous alate A. idaei.

As a general rule, growers should not keep Rubus plantings

beyond the time when viruses, uncontrolled fungus diseases

or insects, or adverse environmental conditions decrease fruit

yield and quality below an economic level. The use of

virus-tested stocks ofresistant cultivars, planted as far away as

possible from sources of inoculum, and treated to decrease

the population of vector aphids when they are found, are

useful aids in the protection of Rubus crops from losses

caused by RMD.

3. Use of insecticides to control populations of aphid

vectors. Although many insecticides are available that give

excellent control of Amphorophora species on Rubus, none

can kill viruliferous aphids before they can probe and

transmit virus to plants. Thus Cadman [in Converse et al.

{1970a)], Taylor and Chambers (1969), and Freeman and

Stace-Smith (1970) were not able to decrease the incidence of

RMD by the use of insecticides applied at an economically

acceptable rate; however, insecticides that prevent the

buildup of Amphorophora colonies within a field may be

useful in decreasing secondary spread. Schaefers (1967)

found that the systemic insecticides oxydemeton methyl,

dimethoate, and aldicarb provided satisfactory aphid control

for 30 to 100 days in New York tests, and he recommended

"maintenance of a total chemical aphid control program" in

Rubus nurseries as an important element in the production of

virus-tested stock.

4. Use of Rubus cultivars resistant to vector aphids. The

development of red raspberry cultivars resistant to

colonization by Amphorophora agathonica and A. idaei is

often used as a classical example of successful breeding for

insect resistance. This work has been reviewed by Briggs

(7965;, Daubeny (7972, 1982), and Baumeister (7967,

7962). Schwartze and Huber (1937) were the first to

demonstrate heritable resistance in Rubus to feeding and

colonization by Amphorophora. Subsequently, several North

American workers evaluated Rubus species and cultivars for

this resistance (Huber and Schwartze 1938; Schwartze and

Huber 7959; Converse and Bailey 7967; Daubeny and

Stace-Smith 1963; Daubeny 7966; Kennedy et al. 1973).

Rapid and effective screening procedures have detected

independent sources of dominant genes for immunity to

colonization by A. agathonica (Brodel and Schaefers 1980;

Daubeny 7972; Daubeny and Stary 1982; Kennedy and

Schaefers 1974a, b). Several raspberry plant breeding

programs in North America, particularly at Vancouver,

B.C., are using these techniques to select resistant genotypes

(Daubeny 1982).

In Great Britain, Briggs (7965) and Knight et al. (7959)

identified four strains of A. idaei and developed a simple

technique for the evaluation of resistance to colonization on

Rubus seedlings. In this test, three aphids are placed on a

seedling shoot tip and observed. If they walk off, the seedling

is immune; if they remain and colonize, it is susceptible.

Jones (1976d, 1979a) demonstrated the value of such

resistance in restricting the spread of viruses transmitted by

A. idaei and showed that even moderate resistance to A. idaei

colonization was effective in some situations. The

incorporation of resistance to A. idaei colonization is

therefore an important aspect of British red raspberry

breeding programs at the East Mailing Research Station

(Keep et al. 7972) and the Scottish Crop Research Institute

(Jennings 1963; Jones 7976úí, 1981b; Jones and Jennings

1980b). Although early selections of red raspberries in Great

Britain contained the resistance gene Aj, which does not

provide resistance to A. idaei strains 2 or 4 (Knight et al.

7959), current breeding programs are using the resistance

gene Ajo and AK49, which confers resistance to the four

British strains of A. idaei (Keep and Knight 7967).

Stace-Smith (1960b) found that when A. agathonica

colonized certain red raspberry cultivars infected with some

of the viruses associated with RMD, the aphids were unable

to transmit these viruses to other susceptible raspberries. In

other instances, viruliferous aphids are able to colonize but

not infect cultivars that can be graft-inoculated with these

viruses (Converse et al. 1970a). Although the genetics of

these host responses have not been studied, they may provide

additional sources of resistance to infection by RMD.

5. Use of virus-tolerant Rubus cultivars. Growers have

long known that differences in the amount of damage by

RMD occur among red raspberry cultivars. Furthermore, red

raspberries are more tolerant to RMD than black raspberries,

and purple raspberries (red x black raspberry hybrids) are

intermediate in reaction. Jones and Jennings (1980b)

presented quantitative data on the relative sensitivity of these

three groups to infection with BRNV and concluded that the

genetic control of the differences was complex, though the

absence of symptoms in the purple hybrids indicated the

174
presence in the red raspberry of dominant genes. They also

showed that the symptoms induced by infection with RLMV

and RLSV in sensitive red raspberry cultivars were

determined by the single dominant genes Lm and Ls,

respectively.

Red raspberry cultivars like 'Glen Clova' and 'Norfolk

Giant' in Great Britain and 'Willamette' in North America

support low populations of vector aphids but do not readily

become affected by RMD (Cadman and Fisken 1958;

Stace-Smith 7955; A. T. Jones, unpublished data). Jennings

(1963) suggested that in 'Norfolk Giant' this might be due to

tolerance to RMD and that such tolerance should be

incorporated into Rubus cultivars. Jones (1976d, 1979a) felt

that the field performance of 'Glen Clova' and 'Norfolk Giant'

could be explained by their moderate levels of resistance to

A. idaei colonization. The nature and inheritance of tolerance

to infection by RMD require more study before tolerance to

the disease can be incorporated into new cultivars.

Remarks

Symptoms resembling RMD can also have other causes, such

as (1) feeding damage caused by the aphid Amphorophora

rubitoxica Knowlton (Stace-Smith 1954); (2) late spring

frosts (Bennett 1927); (3) powdery mildew {Sphaerotheca

humuli DC), although the powdery white growth of this

fungus and the water-soaked lesions it causes on the

undersides of leaves help to distinguish its symptoms from

RMD (Converse 1966a); (4) leaf speckling and blotching

caused by feeding of spider mites such as Tetranychus

urticae (Koch) and of Eriophyes gracilis (Nal.); (5) certain

chemicals (see "Viruslike Disease Symptoms in Rubus in

Great Britain," p. 251); and (6) deficiency of soil boron

(Maryland Agricultural Experiment Station 1942).

Despite the great amount of research that has been devoted to

RMD in many countries for many years, a number of

problems still await solution, including:

• Characterization of the component viruses and determination of their relationships to each other and to other plant

viruses.

• Rapid and precise methods of identifying the component

viruses in plants and vectors.

• Surveys for the occurence of the viruses associated with

RMD in the main Rubus growing areas of the world.

• Influence of these viruses singly and in combination on

growth and yield of the main Rubus cultivars.

^ 'Ruhus Yellow Net . By R.lStace-Smith and A. T./Jones

Additional Common Names

Raspberry yellow mosaic virus (Bennett 7927, 1932) is

considered a probable synonym, but unequivocal evidence is

lacking. Although rubus yellow net virus (RYNV) was

characterized under controlled conditions and clearly distinguished from other aphid-transmitted viruses, yellow mosaic

was a field disease and in most instances a virus complex was

probably involved.

History and Geographic Distribution

RYNV was first isolated and described from naturally

infected Himalaya blackberry {Rubus procerus P. J. Muell.)

in British Columbia. Although it was rarely observed in

Himalaya blackberry, it was later found in raspberry as a

component virus of the raspberry mosaic disease complex

(Stace-Smith 1956) that is common and has been known for

many years in North America and Europe (Cadman 1961b;

Jones et al. 1974; Jones and Roberts 1976).

This disease complex has been recorded from virtually every

major raspberry growing area in the world, so that RYNV

can be considered to have a worldwide distribution. With the

widespread use of virus-free planting material, however, and

the increased use of cultivars that are either aphid-immune or

aphid-resistant, the incidence of the disease is decreasing in

North America and Europe.

Economic Importance

Limited observations have been made on the economic

importance of RYNV. A single plant of the red raspberry

cv.'Washington' that was graft inoculated with RYNV

showed no evidence of degeneration after 3 yr in a field plot

(Stace-Smith 1955a). In a field trial in Canada, the yield of

plants infected with RYNV and black raspberry necrosis

virus (BRNV) was decreased by 43 to 78% in the first

cropping year compared with 0 to 30% for plants infected

with BRNV alone. Losses in dually infected plants in

subsequent years, however, was 0 to 15% (Freeman and

Stace-Smith 1970). In Western North America, the economic

importance of RYNV is minimal because widespread use of

raspberry cultivars with genes for immunity to the aphid

vector has virtually precluded its spread into commercial

plantations. In Great Britain and most of Europe, where a

different aphid species is the vector, such cultivars have

become available only recently and most plantations,

therefore, still contain a large proportion of the older

aphid-susceptible cultivars.

Symptoms on Natural and Experimental Hosts

Natural hosts of RYNV are restricted to the genus Rubus,

primarily red raspberry {R. idaeus L.) and black raspberry

{R. occidentalis L.). RYNV is occasionally found in

Himalaya blackberry (/?. procerus) and other wild or

cultivated species.

Symptoms on red raspberry. Symptoms are evident about 4

to 8 wk after inoculation by grafting or 3 to 4 wk after

inoculation by aphids. Leaves of infected plants develop a

netlike chlorosis of the tissue along the veins, giving the

plant a pale green appearance (fig. 204). Some of the leaves

are slightly cupped downward, but there is no distortion or

stunting and no obvious decrease in vigor (Stace-Smith

1955a).

175
Symptoms on black raspberry. Young seedlings of black

raspberry show a diagnostic netlike chlorosis 3 to 4 wk after

inoculation by viruliferous aphids. The initial symptom is

flecks of netlike chlorosis on the fourth or fifth leaf from the

tip of the infected seedling, followed by progressive veinal

chlorosis on the younger leaves. This chlorosis is typically

unilateral, involving one of the basal leaflets and the lower

edge of the terminal leaflet (ñg. 205).

As the affected leaf expands, that portion showing netlike

chlorosis develops at a slower rate, causing the affected

leaflet to bend towards the chlorotic side. Beneath the first

affected leaf, the older leaves remain normal, but the netlike

chlorosis spreads upward towards the tip of the shoot,

becoming more severe and extensive, until all affected leaves

are chlorotic, stunted, and cupped downward. RYNV can

also be detected in grafted black raspberry, but the

chronology of disease development, so distinctive in

aphid-inoculated seedlings, is less distinctive in graftinoculated plants (Stace-Smith 1955a and unpublished data).

Symptoms on Himalaya blackberry. Himalaya blackberry

shows considerable variations in its response to RYNV. A

naturally infected clone exhibits a distinctive yellow

chlorosis on some of the mature leaves but no symptoms on

others or on younger leaves (Stace-Smith 1955a). Seedlings

of Himalaya blackberry vary in their response; some showing

no obvious symptoms and others different intensities of

netlike chlorisis (R. Stace-Smith, unpublished data). The

growth and vigor of infected plants is not apparently affected

(Stace-Smith 1955a).

Experimental hosts. Tropical black raspberry (Rubus

albescens Roxb.). Symptoms in seedlings of tropical black

raspberry are essentially the same as those in seedlings oí R.

occidentalis. Symptoms develop about 18 days after aphid

inoculation on the third or fourth leaf from the tip of the

inoculated plant. The netlike chlorosis is often more severe

on one side of the petiole, resulting in a stunting of the

affected R. albescens leaf and a bending of the petiole

(Stace-Smith 1955a).

Rubus henryi. Although Converse (1965) attributed symptoms of vein clearing, mottling, distortion, and necrosis of

the leaves and shoots of R. henryi to RYNV, there is now

doubt as to whether these were caused by RYNV alone or

RYNV combined with a heat-stable strain of black raspberry

necrosis virus. (See section on "Black Raspberry Necrosis

Virus," p. 178.)

Strawberry {Fragaria vesca L.). Symptoms on 'Alpine'

strawberry (F. vesca var. semperflorens (Duch.) Ser.) appear

about 3 wk after graft inoculation, when the young leaves

begin to bend downward and necrotic lesions appear at the

base of the petioles. Affected leaves die within a few weeks,

and lesions develop at the base of petioles of older unaffected

leaves, which ultimately wilt and die. The plant is usually

killed within 2 mo of graft inoculation (Stace-Smith and

1-

Figure 204. — Symptoms of rubus yellow net virus in

a systemically infected leaf of "Washington' red

raspbeiry.

Figure 205. — Unilateral development of rubus yellow

net virus symptoms in a leaf of black raspberry.

176
Mellor 1957). In other clones of F.vesca symptoms develop

more slowly than on 'Alpine', and they are not as severely

affected. Although some of the graft-inoculated plants may

die, others persist with only the older leaves alive

(Stace-Smith and Mellor 1957).

Natural and Experimental Transmission

RYNV is transmitted by the raspberry aphids Amphorophora

agathonica Hottes in North America and A. idaei Borner in

Europe. Other Rubus-inftcting species of Amphorophora

may serve as vectors, but, because of the widespread

occurrence of A. agathonica and A. idaei on raspberry,

transmission by any other species is probably relatively

unimportant. Aphids can transmit the virus after an

acquisition access feed of 1 hr, but frequency oftransmission is

greater after 4 hr. There is no latent period in the vector, but

aphids require a minimum of 15 min feeding to transmit.

Aphids maintain the ability to transmit the virus after feeding

for 2 to 3 hr on healthy plants (Stace-Smith 1955a), but if

they are starved, they may retain the virus for 1 day at 20°C

and up to 4 days at 3°C (Stace-Smith 1960a).

In controlled experiments, A. agathonica did not transmit

RYNV from raspberry to strawberry but was capable of

acquiring the virus from graft-inoculated strawberry plants

and transferring it to black raspberry seedlings (Stace-Smith

and Mellor 1957). Efficiency of transmission is not as high as

when raspberry is used as a virus source, but, using five

aphids per plant, 22 of 34 test plants were infected.

Under similar test conditions, the strawberry aphid Chaetosiphon fragaefolii (Cock.) did not acquire and transmit

RYNV from infected raspberry or strawberry plants to black

raspberry (Stace-Smith and Mellor 1957).

Properties of the Causal Agent

RYNV is readily transmitted by the aphid vectors A.

agathonica and A. idaei, but it has not been transmitted

mechanically (Converse et al. 1970a; Stace-Smith and Jones

1978). Unlike other viruses transmitted by Amphorophora

species, RYNV is usually not inactivated by exposure to an

air temperature of 37°C for several weeks (Stace-Smith

1960a; Converse 1966b; Jones and Roberts 1976), but it can

be eradicated from small meristem tip cuttings following

treatments at 37° to 39°C for 4 to 14 wk (Mellor and

Stace-Smith 1979).

Particles of RYNV are bacilliform (fig. 206) and in thin

sections of infected raspberry leaves are 80 to 150 nm long

and 25 to 31 nm wide (Jones and Roberts 1976; Stace-Smith

and Leung 1976). Both ends are rounded (figs. 206 and 207)

and, in cross section, particles show an electron-translucent

core about 17 nm in diameter (fig. 208). In the early stages of

infection, the particles appear to be confined to the sieve

tubes, but in later stages of infection the particles are found in

xylem parenchyma, mesophyll, and epidermal cells. Particles occur singly or in clusters, often in degenerate

Ù

Figure 206. — Electron micrograph of sap of R.

macraei A. Gray stained with 29c ammonium molybdate (pH 6.5). showing bacilliform particles of rubus

yellow net virus. Bar represents 100 nm.

: -V •k'tfrxáv.^'rK.' <«^'-J« >»^i».i

Figure 207. — Electron micrograph ul iliin section of

R. occidenialis infected with rubus yellow net virus,

showing longitudinal section of particles. Bar represents

200 nm.

Figure 208. — Electron micrograph of thin section of

R. occidenialis infected with rubus yellow net virus,

showing transverse section of particles and electrontranslucent core. Bar represents 40 nm.

177
endoplasmic reticulum. Within each cluster, the particles

lack orientation; some appear in cross section, others in

oblique or longitudinal section.

Detection and Identification

Other aphid-borne viruses such as black raspberry necrosis,

raspberry leaf mottle, and raspberry leaf spot (see chapters on

these viruses in this section, p. 178 and 183) are prevalent in

raspberry and are transmitted by Amphorophora species, so

that RYNV rarely occurs on its own in red raspberry. In

combination with some of these viruses, RYNV induces veinbanding mosaic disease in North America known as

rapsberry mosaic disease (Cadman 1952b, 1961; StaceSmith 1956). A plant showing veinbanding mosaic

symptoms might therefore be assumed to be infected with

RYNV; however, this assumption is difficult to justify because RYNV does not induce distinctive symptoms in complex infections. Moreover, graft and aphid inoculations to R.

occidentalis will transmit the complex of viruses, and some

of these will induce severe necrotic symptoms that mask

those induced by RYNV. However, if aphids are fed on a

source containing a virus complex and then transferred individually to test plants for short inoculation access feeds, a

few of the inoculated plants will become infected with

RYNV only (Stace-Smith 1955a). Additionally, heat treatment of plants or roots of plants infected with the complex

will inactivate most of the viruses (Chambers 1961) but not

RYNV (Stace-Smith and Mellor 1957). Such treatment has

provided sources of RYNV free from other contaminating

aphid-borne viruses (Stace-Smith and Mellor 1957; Converse

1965\ Jones and Roberts 1976). While this technique has

been useful, some mosaic sources may contain other aphidborne viruses that are heat stable (Mellor and Stace-Smith

1979). A third method is to graft the mosaic-affected plant to

strawberry (F. vesca), which is susceptible to RYNV but immune to most aphid-borne viruses oiRubus (Stace-Smith and

Mellor 7957).

Although the small bacilliform particles associated with

RYNV infection are unlike those of any other virus known to

infect Rubus spp., use of electron microscopy for detection

and identification is difficult because such particles are rarely

seen in leaf dip preparations, and electron microscopy of thin

sections of infected tissue is too laborious to be useful for

routine identification.

Control Procedures

The most effective control for RYNV is obtained by planting

cultivars that are either immune or resistant to the aphid

vector. (See "Black Raspberry Necrosis," p. 178, for a full

discussion of control using aphid-resistant cultivars.)

RYNV is classified as a heat-stable virus (Stace-Smith

1960a); a term applied to those viruses that persist in plants

held for several weeks at an air temperature that approaches

the maximum at which plants can survive. The heat stability

of RYNV was first reported by Stace-Smith and Mellor

r

{1957) and later confirmed by other workers (Chambers

1961; Converse 1965). Mellor and Stace-Smith (7979),

however, showed that most small shoot tips or stem segments

that were excised from plants during heat treatment and

induced to root were free from RYNV.

ok

Black Raspberry Necrosis/; .

By. R.]Stace-Smith and A. T.¿Jones

Additional Common Names

Mild mosaic (Bennett 7927); a component of red raspberry

mosaic (Stace-Smith 795^); 52V virus (Jones and Murant

7972; Jones and Roberts 7977); heat labile mosaic

components (Converse 1963).

History and Geographic Distribution

The name "black raspberry necrosis virus" (BRNV) was

coined for an aphid-transmitted entity that was latent or mild

in red raspberry cultivars but which induced severe tip

necrosis on black raspberry seedlings (Stace-Smith 1955b).

This virus, together with rubus yellow net virus (RYNV; see

"Rubus Yellow Net," p. 175), was consistently associated

with the raspberry mosaic disease in North America (StaceSmith 1956). Similar entities had been observed previously

but had not been clearly distinguished from other viruses associated with the mosaic disease complex. Of the aphidborne viruses that have been isolated and described in

Europe, the one initially designated "52V virus" (Jones and

Murant 7972) is now equated with black raspberry necrosis

(Jones and Roberts 7977). Raspberry leaf mottle and

raspberry leaf spot viruses also induce a systemic necrosis in

black raspberry, but they are distinguished from BRNV by

inducing distinct symptoms while BRNV is usually latent in

red raspberry indicators. (See "Raspberry Leaf Mottle and

Raspberry Leaf Spot," p. 183.)

At one time, all clones of some of the older red raspberry

cultivars were infected with BRNV and, as a consequence,

the virus was introduced by farmers to many regions in the

world where raspberries were grown. In Western North

America, the replacement of these old cultivars with new

ones immune to the main aphid vector has greatly decreased

the incidence of BRNV in red raspberry, and this will

probably also happen in other major raspberry growing areas

where aphid-resistant or aphid-immune cultivars have

recently become available.

Economic Importance

Black raspberry cultivars vary in their response to infection,

but even the most tolerant cultivars are seriously affected.

Although all red raspberry cultivars tested are susceptible to

BRNV (Jones and Jennings 1980b), the economic importance of the virus depends on the cultivar and the duration of

the infection. Thus, in North America, the yield of some

cultivars was unaffected by infection, whereas that of others

was decreased by up to 30% in the initial cropping years but

lessened to stabilize at about 14% in subsequent years. The

178
sensitive cultivars produced smaller fruits and shorter,

thinner cane than virus-free controls (Converse 1963\

Freeman and Stace-Smith 1970). Freeman et al. {1969) also

showed that infection with BRNV increased pollen abortion

in some raspberry cultivars and that this was further increased

by additional infection with RYNV.

In Great Britain, BRNV is one of the first aphid-borne viruses

to infect new plantings of healthy red raspberry, and the main

cv. 'Mailing Jewel' may become 100% infected with BRNV

by the end of its first fruiting year (Jones and Murant 7972;

Jones 1976dy 1979a). In Scotland, infection of red raspberry

by BRNV alone decreased the mean length of canes and mean

berry weight in cvs. 'Glen Prosen' and 'Mailing Leo'. This

effect increased with the age of infection (Jones 1980b and

unpublished data). Furthermore, in Great Britain, BRNV

infection of cultivars such as 'Mailing Jewel' is commonly

accompanied by infection with several other viruses, and such

multiple infections are believed to contribute to the

degeneration ofplantations (Cadman 1961b;Jones 1981b). For

example, BRNV is found together with raspberry bushy dwarf

virus in plants of cv. 'Lloyd George' affected by the

degenerative disease, raspberry bushy dwarf. (See "Raspberry

Bushy Dwarf," p. 229.) In controlled experiments, infection

of 'Lloyd George' plants with BRNV alone induced many

features of the disease, but plants inoculated with both viruses were the most obviously diseased (Jones 1967b). In

combination with RYNV, BRNV induces raspberry mosaic

disease in North America (Stace-Smith 1955b) and veinbanding mosaic disease in Europe (Cadman 1952b, 1961b).

(See "Raspberry Mosaic," p. 168.)

Symptoms on Natural and Experimental Hosts

Natural hosts. The natural hosts of BRNV are restricted to

the genus Rubus. Natural hosts include cultivated and wild

Rubus fruticosus Hort, R. idaeus L. and R. idaeus var.

strigosus (Michx.) Maxim, (red raspberry), R. occidentalis

L. (black raspberry) and R. leucodermis Dougl. (western

black raspberry), R. proceras P. J. Muell. (Himalaya

blackberry), 'Thomless Young' derivative of/?, ursinas Cham.

and Schlect., R. ursinas var. macropetalus Dougl., R.

lasiocarpus Thumb, var. rosifolius (Hook. F.) Hara, R.

allegheniensis Porter cv. 'Darrow'; R. phoenicolasius

Maxim., and R. loganobaccus Bailey (Stace-Smith 1955b;

Jones and Murant 7972; Jones and Wood 7979; Jones and

Roberts 7977; Converse and Bartlett 7979; Jones and

Jennings 1980b; Converse, unpublished data). Other wild

and cultivated Rubus spp. are reported to be naturally

affected by raspberry mosaic (Zeller 1923), but tests to

identify the virus or viruses involved were not done.

Experimental hosts. In addition to red raspberry and black

raspberry, BRNV has been transmitted by grafting or by

aphid vectors to 'Boysen', 'Tayberry', Rubus albescens

Roxb., R. henryi Hemsl. and Kuntze, R. laciniatus Willd.,

R. loganobaccus y R. molaccanus L., and R. phoenicolasius

Maxim. (Jones and Roberts 1977). The virus has also been

transmitted to the following herbaceous plants by mechanical

innoculation of raspberry sap: Chenopodium amaranticolor

Coste and Reyn., C. quinoa Willd., C. murale L., Petunia

hybrida Vilm., Spinacia olerácea L., Gomphrena globosa

L., and Nicotiana debneyi Domin (Jones and Murant 7972;

Murant et al. 7976).

Symptoms. Black raspberry. Distinctive symptoms of

BRNV are based on the reaction of succulent, young test

plants grown in a protected greenhouse environment.

Symptoms on field-grown plants are similar but are not

diagnostic. Symptoms are first evident 5 to 7 days after aphid

inoculation, when the shoot tip appears bent. Within a day or

two of the initial bending, the tip is distinctly downcurled and

brittle and the partially expanded leaves beneath the tip

appear wilted. The wilting is followed by necrosis of the

petiole, midribs, unfolding leaves, and the stem tip. Wilting

and necrosis is a shock reaction, and, if the plant survives,

later shoots produce leaves showing varying intensities of

mottle. Symptoms after graft inoculations (fig. 209) are

similar.

When BRNV is transmitted to black raspberry by grafting,

the symptomatology is similar except that the period between

grafting and the appearance of initial symptoms is 3 to 8 wk.

The reaction oí R. henryi to graft-inoculation with BRNV is

similar to that of 7^. occidentalis (fig. 210) (Stace-Smith

1955b\ Jones and Roberts 7977).

Red raspberry. Most cultivars infected with BRNV exhibit

no visible symptoms but some, such as 'Mailing Admiral',

'Mailing Orion', 'Taylor', and 'Washington', show small

chlorotic spots and mottling adjacent to leaf veins (fig. 211)

(Stace-Smith 1955b; Jones and Roberts 7977; Jones and

Jennings 1980b).

Other Rubus species. In a heated greenhouse, leaves of

'Himalaya' blackberry and tropical black raspberry {R.

albescens) may show a mild chlorotic spotting or mottling

(Stace-Smith 7955^?; Jones and Jennings 1980b) and R.

henryi and R. molaccanus develop apical necrosis accompanied by leaf deformity and/or epinasty 4 to 8 wk after

grafting; young leaves oíR. molaccanus often show necrotic

flecking (Jones and Roberts 1977). Infected R. phoenicolasius seedlings are less vigorous than normal but do not show

obvious leaf symptoms (Jones and Roberts 1977). Under

cooler conditions, infected plants of 'Boysen' and 'Tayberry'

may show a chlorotic mottle (Jones and Jennings 1980b).

C. quinoa and C. amaranticolor. Small chlorotic/necrotic

local lesions sometimes develop about 6 to 10 days after

mechanical inoculation; such plants usually show systemic

chlorotic necking and/or necrosis within 2 wk (fig. 212). C.

murale develop large necrotic local lesions but no systemic

infection. S. olerácea plants may develop systemic chlorosis

or necrosis under winter conditions (Jones and Murant 7972;

Murant et al. 1976).

179
Figure 209. — Tip necrosis in R. occidentalis cv.

'Plum Farmer' graft inoculated with black raspberry

necrosis virus.

Figure 210. —Tip curling prior to tip death in R.

henryi graft inoculated with black raspberry necrosis

virus.

Figure 211. — Veinal chlorotic mottle in a leaf of the

red raspberry cv. 'Mailing Orion' infected with black

raspberry necrosis virus.

Figure 212.—Systemic chlorotic flecking and mottle in

a leaf (lefi) and plant (right) of C. quinoa mechanically

inoculated with the 52V isolate of black raspberry necrosis virus.

180
Natural and Experimental Transmission

The natural vectors of BRNV are aphids belonging to the

genus Amphorophora, primarily A. agathonica Hottes in

North America and A. idaei Borner in Europe. Other species

that may serve as minor vectors in North America include A.

sensoriata Mason, A. rubicumberlandii Knowlton and Allen,

and Illinoia (also known as Masonaphis) rubicola (Oestlund). In Europe, species other than A. idaei are infrequently

observed in red raspberry but small populations of

Macrosiphum euphorbiae (Thos.), M. (Sitobion)fragariae

(Wlk.), and Myzm ornatus Laing have been recorded (Jones

1976d and unpublished data). While there is no evidence in

Europe of field transmission by any species other than A.

idaei, under test conditions Aulacorthum solani (Kalt.) and

M. euphorbiae as well as A. idaei have transmitted BRNV

from red raspberry to C. quinoa seedlings (Jones and Murant

1972; Murant et al. 7976; Jones ¡976d). Attempts to transmit

the virus from C. quinoa using these aphid species failed.

Partially purified preparations contain a few viruslike

particles about 25 to 30 nm in diameter (fig. 213) (Jones and

Murant 1972; Murant et al. 7976). Similar particles have

been detected by electron microscopy of ultrathin sections of

BRNV-infected R. henryi, R. occidentalis, and C. quinoa.

Particles occurred in the cytoplasm in many kinds of cells and

were often found arranged in single file and in plasmodesmata (fig. 214) (Murant et al. 7976; Jones and Roberts 1977).

During winter, sap of C. quinoa containing BRNV lost

infectivity after diluting 10"' to 10"^ heating for 10 min at 50

to 52°C, and storage at 18°C for 6 to 24 h (Jones and Murant

7972).

BRNV is transmitted by aphids in a semipersistent manner.

In North America, all instars of A. agathonica can transmit

BRNV, requiring minimum acquisition and transmission

access feeds of 15 to 30 min and 2 min, respectively.

Viruliferous aphids can continue to transmit for up to 3 to 4 h

after acquisition while feeding and, depending on the

temperature, up to 4 days if starved (Stace-Smith 1955b).

BRNV is readily graft transmissible from Rubus to Rubus but

not from herbaceous plants such as C. quinoa to Rubus

(Murant et al. 7976); BRNV is not seed-borne in red

raspberry (Jones and Murant 1972).

BRNV is transmitted manually with difficulty by grinding

young red or black raspberry leaves with alumina, Celite (a

diatomaceous product), and 2% nicotine solution, and

rubbing the inocula on leaves of C. quinoa. Transmission is

achieved more readily from field-grown raspberry plants in

spring and autumn than in summer, and from infected black

raspberry than from infected red raspberry. Transmission

from raspberry plants grown in the greenhouse is difficult at

all times of the year (Jones and Murant 7972; Jones and

Roberts 7977; Jones and Jennings 1980b).

Properties of the Causal Agent

BRNV is difficult to maintain in greenhouse-grown C.

quinoa, and this is especially so in summer. The virus,

however, can be continuously maintained in culture by

keeping inoculated C. quinoa plants in growth cabinets

(18°C, 8000 lux, 8 h photoperiod). Systemically infected

leaves from such plants are suitable for purification (Murant

et al. 1976). The virus is present in very low concentration in

infected raspberry and C. quinoa plants, with the result that

only very small amounts of inadequately purified virus have

been obtained. Attempts to produce an antiserum to the virus

using such material were unsuccessful.

Figure 213. — Electron micrograph of a partially

purified preparation of the 52V isolate of black

raspberry necrosis virus showing a few viruslike

particles among numerous particles of phytoferritin. Bar

represents 20() nm.

i'.^T «ifr. jv.-

Figuri; 214, — HlcclrDii microgruph ol a thin section of

R. occidentalis infected with black raspberry necrosis

virus showing viruslike particles aligned in a row in the

cytoplasm of a vascular cell. It also shows the particles

within a tubule, which is continuous with a plasmodesma. Bar represents 200 nm.

Detection and Identification

BRNV can occasionally be detected in sensitive red raspberry

cultivars under field conditions in the spring and early

summer by the appearance of veinal chlorotic spots.

However, as most currently grown cultivars show no foliar

symptoms or develop only very faint symptoms, this is of

little value in detecting field infections. Consequently, insect

or graft transmission to a sensitive indicator host is

necessary.

181
The technique of choice in North America is transmission by

the aphid A, agathonica to seedlings of black raspberry. If

the plant being tested is naturally infested with this aphid, 5

to 10 aphids are transferred to black raspberry seedlings for

inoculation access feeds of at least 30 min. If the plants being

indexed are not already colonized by this aphid, those from a

laboratory colony can be given an overnight acquisition

access feed on test material before being transferred to black

raspberry seedhngs (Huber and Johnson 7952; Stace-Smith

1955b, Converse 1961). The technique is reliable for

detecting the virus in most cultivars that can be colonized by

this aphid but is unreliable for detecting virus in those not

colonized by this aphid (Stace-Smith 1960b).

While A. agathonica readily transmits BRNV to healthy R.

occidentalis, the European vector, A. idaei, does not readily

feed on it and transmission of virus from diseased raspberry

to R. occidentalis is difficult (Cadman 1961b). Detection of

BRNV in Europe is therefore done by graft inoculation to

Rubus indicator hosts and/or by inoculation of sap to C.

quinoa plants. Inarch bottle grafting to R. henryi or R.

occidentalis is usually used (Jones and Roberts 7977; Jones

1976d). Manual transmission of BRNV may be done by

grinding young raspberry leaves with alumina, Celite, and

2% nicotine and rubbing the inocula on leaves of C. quinoa.

A disadvantage of both aphid and graft transmission is that

many raspberry plants are naturally infected with several

unrelated aphid-vectored viruses and the virus complex may

be transmitted. Thus, BRNV frequently occurs with RYNV,

the complex inducing mosaic disease. The two viruses have

similar vector relations, and they are not readily separated by

routine aphid transmissions. However, they may be separated

by transferring individual aphids from doubly infected plants

to a series of black raspberry seedlings, permitting the aphid

to feed for only a short time on each seedling (Stace-Smith

1956). Another technique is to graft inoculate the complex to

a healthy red raspberry plant and subdivide the grafted plant

into root cuttings before the viruses have had time to invade it

completely. BRNV becomes systemic sooner than RYNV,

with the result that a proportion of the root cuttings are

infected only with BRNV (Freeman and Stace-Smith 1965).

In Europe, BRNV is commonly found in red raspberry with

two other latent viruses, raspberry leaf mottle (RLMV) and

raspberry leaf spot (RLSV). All three viruses are transmitted

by A. idaei and induce apical necrosis in R. occidentalis and

R. henryi. RLMV and RLSV can be distinguished on the

basis of symptom response in the red raspberry indicator cvs.

'Mailing Landmark' and 'Norfolk Giant', respectively. (See

"Raspberry Leaf Mottle and Raspberry Leaf Spot", p. 183.)

Because BRNV induces few if any symptoms in red

raspberry, however, it cannot be identified by graft indexing

when in mixed infections with RLMV and/or RLSV. In these

situations, successful mechanical transmission to C. quinoa

is the only means of identifying BRNV.

Control Procedures

The most effective control measure is to plant cultivars that

are not susceptible to colonization by vector aphids. Several

current raspberry breeding programs emphasize selection for

resistance to these vectors and, as a result, older cultivars that

lack this character are gradually being replaced (Jones and

Jennings 1980b; Daubeny 1982). Immunity to A. agathonica

is controlled by a single dominant gene derived from the cv.

'Lloyd George'. In North America, where some cultivars

immune to this aphid have been grown for many years, there

is no evidence of resistance-breaking A. agathonica biotypes

(Converse et al. 7977). In Great Britain, four biotypes of A.

idaei exist, and breeding programs have attempted to

incorporate resistance to each. To be fully effective in

preventing virus spread, resistance to the aphid must be

extreme; however, even low levels of resistance have been

shown to decrease the rate of virus spread (Jones, 1976d,

1979a, 1981b).

While resistance to A. idaei in Great Britain appears to

prevent the spread of BRNV in red raspberry, one of the best

sources of gene(s) for this character is black raspberry.

Because of the severe reaction of black raspberry to BRNV

infection and the possibility of transferring this sensitivity to

infection to red raspberry in breeding programs, Jones and

Jennings {1980b) surveyed the response to BRNV infection

in more than 30 Rubus species and hybrids. None was

immune from infection, and the study considerably expanded

the number of Rubus species that are now known to be

susceptible. There seems little prospect, therefore, of

breeding raspberries immune from BRNV; however, the

absence of foliar symptoms in BRNV-infected red raspberry

was found to be a dominant character and the inheritance of

the necrosis reaction in R. occidentalis was found to be

complex.

Most isolates of BRNV are readily eradicated from Rubus

spp. by heat treatment at 32° to 37°C for 1 to 4 wk (Chambers

795^; Stace-Smith and Mellor 7957; Converse 1963) or by

excising and rooting tip cuttings from plants during heat

treatment (Bolton and Turner 7962). Clones free of BRNV

are available for virtually all commercial cultivars. Some

virus isolates, however, may be more difficult to eradicate

than others because Mellor and Stace-Smith (7979) reported

that a virus isolate, thought to be BRNV, survived heat

treatment at 39° to 42°C for 8 wk.

Remarks

Although BRNV, raspberry leaf mottle, and raspberry leaf

spot viruses seem to be separate entities, their similarity in

several properties suggests that they may be related. The

features that suggest that they are distinct are: (1) differences

in reaction of red raspberry indicator plants; (2) frequent

occurrence of the three viruses together in the same plant; (3)

mechanical transmissibility of BRNV but not of RLMV or

RLSV; (4) 30-nm particles, presumably those of BRNV, are

readily found in thin sections of BRNV-infected black

182
raspberry and C. quinoa, but no such particles have been

found in RLMV- and RLSV-infected plants; and (5) the

genetic bases for reaction to the three viruses are different

(Jones and Jennings 1980b). (See also "Raspberry Leaf

Mottle" and "Raspberry Leaf Spot," p. 183.)

^^\Raspberry Leaf Mottle and Raspberry Leaf Spotty

By A. T.lJones

Raspberry leaf mottle virus (RLMV, Cadman 1951) and

raspberry leaf spot virus (RLSV, Cadman 1952d) are

aphid-borne viruses that are latent in most red raspberry

cultivars but produce symptoms in a few red raspberry

indicator cultivars. Their similarity in symptoms induced in

indicators, vector relations, and response to thermotherapy

suggests that they may be related though distinct viruses.

Because of this and the fact that in many published reports it

is not clear which of the two viruses is involved in the

diseases described, the two viruses will be considered

together.

Additional Common Names

The following are names used to describe the characteristic

disease symptoms induced by infection with either RLMV or

RLSV in sensitive cultivars: Type c symptom (Harris 1933),

raspberry Mosaic 2 (Harris 1939), Flekkmosaikk (Bj0rnstad

1953), spot mosaic (Fleckenmosaik) (Richter 1964a, b),

raspberry chlorotic spot (Jordovic 1963), and leaf spot

mosaic (Murant 1974b).

History and Geographic Distribution

Harris (1933) was probably the first to describe leaf spot

mosaic disease in detail. He classified the many viruslike

symptoms occurring in certain red raspberry cultivars in

Great Britain into several kinds. One of these, termed type c,

was characterized in cv. 'Baumforth B' by sharply defined

chlorotic spots scattered randomly over the leaves. Later,

Harris (1939) simplified the symptom categories into two

major kinds which he termed Mosaic 1 and Mosaic 2; Mosaic

2 included the symptom previously referred to as type c

(Harris 1933).

Cadman (1951, 1952d) showed that at least two distinct

aphid-borne viruses could induce Mosaic 2 in some red

raspberry cultivars but that they were symptomless in many

others. Subsequently, Mosaic 2 symptoms have been

reported in raspberry from Scandinavia (Bj0mstad 1953;

Tapio 1961), Germany (Richter 1962a, b), Jugoslavia

(Jordovic 1963), U.S.S.R. (Kuznetsova and Pomazkov

7977) and France (Bouchery and Putz 1972). However,

although some of these reports refer to the causal agent of the

disease as "spot" or "leaf mottle," most do not distinguish

between infection with RLMV and RLSV. Nevertheless,

RLMV and RLSV probably occur in each of these countries.

The two viruses have also been identified in New Zealand

where they were probably introduced from Europe (Jones and

Wood 7979). There is also some circumstantial evidence that

they were introduced into Australia and North America

(Cadman 7957, 1952d; Converse 1981).

Economic Importance

RLMV and RLSV are widespread in raspberry in Great

Britain and possibly many European countries. In Great

Britain, they rapidly infect newly planted stocks of the main

commercial cv. 'Mailing Jewel' but infect the other main cv.

'Glen Clova' less rapidly (Jones and Murant 7975; Jones

1976d, 1979a). Most red raspberry cultivars are infected

symptomlessly, but a few are sensitive to infection and show

severe symptoms frequently resulting in plant death (Cadman

7957, 1952d; Jones and Murant 7975; Jones and Jennings

1980b). Latent infections with these and other viruses are

also believed to be involved in the degeneration of vigor of

some cultivars (Cadman 7957, 1952d; Jones 1980b, 1981b).

Thus, in some cultivars single infections with RLMV and

RLSV impaired cane quality and decreased berry weight,

and, in cv. 'Glen Prosen', RLSV infection decreased total

fruit yield (Jones 1980b). It is likely that in mixed infections

with other viruses, a situation which commonly prevails,

latent infections with RLMV and RLSV significantly

decrease plant growth and yield. The effects of either of these

two viruses in mixed infections with rubus yellow net virus

are not known. (See "Rubus Yellow Net," p. 175, and

"Raspberry Mosaic," p. 168.)

Symptoms on Natural and Experimental Hosts

RLMV and RLSV can occur singly but are often found

together in naturally infected wild European raspberry,

cultivated red raspberry, and some cultivated blackberries

(Cadman 7957, 1952d; Jones and Murant 7975; Jones and

Jennings 1980b; A. T. Jones, unpublished data); RLMV and

RLSV have also been detected in R. gracilis Roxb. and

RLMV in R. occidentalis L. (Jones 1975b). Each virus has

been experimentally transmitted to several Rubus species,

and all Rubus species and cultivars tested have been found

susceptible (Jones and Jennings 1980b). Most are infected

symptomlessly, but a few species show pronounced

symptoms. The symptoms produced in sensitive plants by

infections with RLMV and/or with RLSV generally are very

similar.

Symptoms on sensitive red raspberry cultivars. Leaves of

primocanes show sharply defined angular, chlorotic yellow

spots about 1 to 2 mm or larger, which are randomly

distributed over the leaf; leaves are often distorted (fig. 215).

Leaves on fruiting canes are usually small and deformed and

often show a more intense spotting than those on primocanes;

some spots may merge to form large interveinal chlorotic

areas (fig. 216); fruiting laterals of such affected canes are

poorly developed (fig. 217). Plants become stunted and often

die within 2 to 3 yr of infection (fig. 218).

Table 9 lists 13 red raspberry cultivars known to be sensitive

to infection with either RLMV or RLSV. In addition, the

183
^^^Huri^';-.V^HMip^^H

^^^^^^^^B '"M^^l 4r ' '^^ " '*',"'i^^^^^B

^^^^f"\ \'9!^ ' ^sl^^^^^^l

^^^ . ..^'^w^^^H

O3H

^^^^^^1 1 5cms

Figure 215. — Angular chlorotic leaf spots and distortion in a leaf of a primocane of 'Glen Clova" red

raspberry infected with raspberry leaf spot virus.

(Copyright Scottish Crop Research Institute.)

Figure 216. — Angular chlorotic leaf spots in leaves of

'Norfolk Giant' red raspberry infected with raspberry

leaf spot virus. Left: leaf from a primocane. Right: leaf

from a fruiting cane. (Copyright Scottish Crop Research

Institute.)

following cultivars are reported to show symptoms characteristic of those induced by RLMV or RLSV, but no

information is available on which of the viruses is involved in

the disease: 'Andenken an Paul Camenzind', 'Bois Blanc',

'Deutschland', 'Frommes Erfolg', 'Frommes Vollendung',

'Hailsham', 'Harzjuwel', 'Magnum bonum', 'Norwich

Market', 'Novost'kuz'mina', 'Preussen', 'Rode Radboud',

'Romy', 'Turks Frühe Rote', and 'Zeva F (Bj0mstad 1953:

Bouchery and Putz 1972; Harris 1933. 1940: Jordovic 1963:

Kuznetsova and Pomazkov 1971 : Richter 1964a, b).

Symptoms on blackberries. Plants of R. laciniatus Willd..

R. proceras P. J. Muell cv. 'Himalaya Giant', 'Boysen".

'Logan', and 'Tayberry' that are graft inoculated with RLMV

or RLSV are often infected symptomlessly when kept in a

heated greenhouse. R. laciniatus and R. procerus, however.

Figure 217. — Distortion and chlorotic mottling in

leaves of fruiting canes of 'Glen Clova' red raspberry

Held infected with raspberry leaf spot virus. Notice

poorly developed fruiting laterals and dead nodes.

(Copyright Scottish Crop Research Institute.)

Figure 218. — Plants of 'Glen Clova' red raspberry

killed by field infection with raspberry leaf spot virus.

(Copyright Scottish Crop Research Institute.)

184
Table 9.—Red raspberry cultivars sensitive to infection

with raspberry leaf mottle

or raspberry leaf spot viruses

Reaction to infection v^^ith —

Cultivar

Raspberry leaf

mottle virus

Raspberry leaf

spot virus

Baumforth B + S

Burnetholm + S

Chartham S •

Gertrudis S +

Glen Clova + S

Mailing Delight S +

Mailing Landmark s +

Norfolk Giant + s

Phyllis King + s

St. Walfried s +

Seedling K s -fVeten s +

Zeva Herbsternte s +

+ = Susceptible but shows no symptoms, S = pronounced

chlorotic angular spots in leaves, and • = not tested.

Data from Cadman {1951, 1952) and Jones and Jennings {1980).

sometimes develop a transient, faint chlorotic mottle a few

weeks after grafting (Jones and Jennings 1980b). Under the

cooler conditions of an unheated gauze house, and

particularly after pruning, new growth of 'Boysen' and

Tayberry' infected with RLMV, but not with RLSV,

showed faint transient line patterns in leaves of fruiting

laterals (Jones and Jennings 1980b; A. T. Jones, unpublished

data).

Symptoms on other Rubus species. R. henryi Hemsl. and

Kuntze and R. occidentalis develop apical necrosis and

mosaic symptoms 4 to 8 wk after graft inoculation with either

RLMV or RLSV (Cadman 1951, 1952d; Jones and Jennings

1980b). R. molaccanus L. also shows tip necrosis, but this is

generally slower to develop than in R. henryi or R.

occidentalis (A. T. Jones, unpublished data). R. saxatilis L.

inoculated with RLMV, either by grafting or by aphids,

develops conspicuous interveinal chlorotic patches (Cadman

1951). RLMV and RLSV symptomlessly infect/?, phoenicolasius Maxim. (Jones and Jennings 1980b).

Natural and Experimental Transmission

RLMV and RLSV are each transmitted in nature by

Amphorophora idaei Borner (also known as A. rubi (Kalt.))

but not by Aphis idaei van der Goot (also known as Dorsalis

{Aphis) idaei van der Goot) (Cadman 7957, 1952d; Jordovic

1963). RLMV was not transmitted by Amphorophora rubi

Borner (bramble aphid), A. ruborum Borner, or Macrosiphum frageriae (Wlk.) [also known as Sitobion fragariae

(Wlk.)]; a single transmission by M. euphorbiae (Thos.) was

unconfirmed (Cadman 1954). Each virus is transmitted by

grafting to Rubus (Cadman 7957, 1952d; Jordovic 1963;

Jones and Jennings 1980b). Raspberry chlorotic spot virus

(probably RLSV) studied by Jordovic {1963) was not

transmitted through soil or seed to raspberry, nor was it

mechanically transmitted to herbaceous test plants. In

Scotland, neither RLMV nor RLSV have been transmitted to

herbaceous plants by mechanical inoculation with sap

(Cadman 7957; A. T. Jones, unpublished data). The

properties of the virus transmitted mechanically by Richter

{1964a) from raspberry plants with Mosaic 2 symptoms,

suggest that it is raspberry bushy dwarf virus (See "Raspberry

Bushy Dwarf," p. 229.)

Experimental transmissions using Amphorophora idaei,

although possible, are beset by difficulties, the chief of which

is the inherent resistance of many Rubus species and

raspberry cultivars either to the aphid vector or to the viruses

themselves (Cadman 7954, 1961b; A. T. Jones, unpubUshed

data). In transmissions from infected red raspberry to R.

idaeus L., R. saxatalis, and R. occidentalis, the minimum

acquisition and inoculation access times required by

Amphorophora idaei to transmit RLMV were less than 30

min and less than 60 min, respectively. The frequency of

transmission was increased by extending acquisition and

inoculation access times (Cadman 7954; Converse et al.

1970a). Much less precise studies have been done with

RLSV (Cadman 1952d); however, both viruses were

regarded as having similar vector relations (Cadman 1961b)

(probably semipersistent), but further work is necessary to

confirm this.

Properties of the Causal Agents

No information is available on the particle morphology of

RLMV and RLSV. No viruslike particles were observed by

electron microscopy of thin sections of infected raspberry

plants (A. T. Jones and I. M. Roberts, unpubUshed data). A

few isometric viruslike particles about 30 nm in diameter

were observed in partially purified preparations obtained

from raspberry plants infected with RLMV (Jones 1976b).

These were not infective to Chenopodium quinoa Willd.

plants, suggesting that they were not those of black raspberry

necrosis virus, (BRNV, see p. 178), but it is not known if

these particles represent those of RLMV.

Both RLMV and RLSV are heat-labile viruses and infected

raspberry plants can be freed from infection with these

viruses by thermotherapy (Chambers 7967; Jordovic 1963;

Richter 1964b).

Detection and Identification

In raspberry cultivars sensitive to infection with RLMV^or

RLSV (table 9), infection can be detected by the presence of

characteristic angular chlorotic spots on the leaves (figs. 215

and 216). However, in plants with pronounced symptoms of

raspberry vein chlorosis virus (see "Raspberry Vein Chlor185
osis," p. 194) or veinbanding disease (see "Raspberry

Mosaic," p. 168 ), diagnosis may be difficult. Detection of

RLMV and RLSV in cultivars of unknown response to infection or in which the viruses are latent depends on graft transmission to Rubus species and cultivars sensitive to either

virus. The standard Rubus indicators, R. henryi and R. occidentalism react similarly to RLMV and RLSV and also to

BRNV (see "Black Raspberry Necrosis," p. 178) (Jones

and Jennings 1980b). These viruses induce few if any

symptoms in most raspberry cultivars. BRNV, however, induces few if any symptoms in most red raspberry cultivars.

Thus, specific detection of LRMV and RLSV can be made

by graft transmission ot the raspberry cultivars sensitive to

these viruses listed in table 9. Of these cultivars, 'Mailing

Delight', 'Mailing Landmark', and 'St. Walfried' have been

used to detect RLMV; and 'Bumetholm', and 'Glen Clova',

and 'Norfolk Giant' to detect RLSV (Cadman 1951, 1952d;

Jones and Murant 1975; Jones and Wood 7979; Jones and

Jennings 1980b).

Control Procedures

Raspberry plants infected with these viruses can be freed

from infection by heat treatment at 32° to 3TC for 10 to 20

days (Chambers 1961; Jordovic 1963, Richter 1964b;

Baumann 1980; A. T. Jones, unpublished data) to produce

virus-tested elite mother material. A combination of heat

treatment and meristem tip culture appears to be more

successful than heat treatment alone (Baumann 1981). In

Great Britain, most plants of the cv. 'Mailing Jewel' (the

main cultivar grown) derived from elite stock are reinfected

with these and other aphid-borne viruses 2 to 3 yr after

planting in the field (Jones and Murant 1975; Jones 1976d).

Attempts to prevent reinfection using insecticides have not

been successful (Taylor and Chambers 7969).

Cadman and Fisken {1958) observed that raspberry cultivars

differed in the rate at which they became infected with RLSV

in the field and found cvs. 'Mailing Landmark' and 'Norfolk

Giant' the most resistant. As cv. 'Mailing Landmark'

appeared very resistant to colonization by the aphid vector

Amphorophora idaei and 'Norfolk Giant' did not (Cadman

1961b), they postulated two kinds of resistance mechanisms;

that in cv. 'Mailing Landmark' was effective against the

vector, that in cv. 'Norfolk Giant' was effective against the

virus. It is now known that cv. 'Norfolk Giant' also has some

resistance to Amphorophora idaei (Knight et al. 7959;

Jennings 1963; Jones 1976d, 1979a) and that much of its

ability to escape infection is proably due to this.

Nevertheless, the two kinds of resistance postulated by

Cadman and Fisken (1958) are currently being exploited by

plant breeders to protect cultivars from the effects of

infection with RLMV, RLSV, and other aphid-borne viruses

(Jones 1981b).

Jones and Murant {1975) showed that the weak resistance

(minor gene resistance) to Amphorophora idaei in the cv.

'Glen Clova', which is sensitive to RLSV infection, was very

effective in restricting infection with RLSV, but only when

grown in large plots. Under such conditions, the incidence of

infection increased less than 1 % per year and infected plants

were largely confined to the periphery of the crop, and

especially where this was adjacent to sources of the virus and

its vector. In small plots and in areas of high inoculum

pressure, the incidence of infection was much greater.

Later studies (Jones 1976d, 1979a), showed that major gene

resistance to Amphorophora idaei was much more effective

in restricting spread of aphid-borne viruses even under high

inoculum pressure. Observations of commercial plantings of

such material confirm these experimental results (Jones

1981c). Current raspberry breeding programs in Great

Britain emphasize selection for resistance to this vector, and

the planting of cultivars containing this resistance promises to

be a major factor in decreasing the incidence and spread of

RLMV and RLSV in commercial raspberry crops.

The severity of symptoms induced by infection with RLMV

and RLSV in sensitive cultivars poses a serious threat should

strains of Amphorophora idaei arise that can overcome the

resistance currently being used in raspberry breeding

programs. Jones and Jennings {1980b) found no source of

immunity to either virus in many Rubus species and cultivars

tested but showed that most were tolerant of infection. They

found that inheritance of sensitivity to RLJVIV and RLSV

infection was determined by single dominant genes designed

Lm and Ls, respectively. Plant breeders should therefore be

able to avoid introducing this sensitivity to infection with

these viruses into future cultivars, although they have

unwittingly allowed this to happen in the pas't.

Remarks

The viruses have been detected only in Europe, New

Zealand, and the U.S.S.R; however, tests to detect virus

infection in raspberry in most countries are made by graft

inoculation oí R. henryi and R. occidentalis. Infection with

these viruses in many other countries may have gone

unnoticed because, as noted earlier in this chapter, these

indicators will not distinguish between infection with

RLMV, RLSV, and BRNV and because most red raspberry

cultivars are" symptomless when infected with RLMV and

RLSV. RLMV and RLSV can be distinguished from BRNV

in pure culture by inducing symptoms in red raspberry

cultivars in which BRNV is symptomless (Jones and

Jennings 1980b).

RLMV and RLSV differ from the agent of yellow spot

disease of raspberry described from Poland (Basak 7974; see

"Rubus Virus Diseases of Minor or Undetermined Significance," p. 248) by infecting R. henryi and by inducing apical necrosis in this species and in R. occidentalis. Furthermore, yellow spot disease affects red raspberry cultivars that

are symptomless when infected by RLMV or RLSV.

186
Further information is needed on the relationship of RLMV

and RLSV to one another and to BRNV, and on their vector

relations.

¿r Raspberry Leaf Curl;/ .

By R.[Stace-^mith and R. H. [Converse

Additional Common Names

Curl; raspberry curl; yellows. The term "yellows" was used

in the early, descriptive literature (Rankin and Hockey 1922)

to refer to a disease complex that included raspberry leaf curl.

In Europe and the U.S.S.R., the name "leaf curl" is used to

refer to a disease caused by raspberry ringspot and tomato

black ring viruses (Murant 1974b). (See "Nematode-Bome

Diseases," p. 211.)

History and Geographic Distribution

Raspberry leaf curl virus (RLCV) was one of the first virus

diseases of Rubus recognized in North America. The early

literature on the disease was reviewed by Rankin and Hockey

(7922), who believed that it was transmitted by the aphid

Aphis ruhiphila Patch (now known as A. rubicola Oestlund).

Confirmation of A. rubicola as a vector was provided by

Smith (7925) and by Bennett (7927) who also established the

existence of two types of RLCV which he called alpha and

beta. Both types are restricted to North America and can

infect blackberry (Bennett 1930). Otherwise, in cultivated

/?w¿?M5,alpha curl is limited to red and purple raspberries,

whereas beta curl also infects black raspberries.

Raspberry leaf curl disease occurs almost everywhere

raspberries are grown in the United States and Canada. In a

survey in Quebec, raspberry leaf curl disease was found in

8% of the red raspberry fields surveyed (Caron et al. 7977).

Raspberry leaf curl disease is rare along the eastern seaboard

south of New York and is not known on the Pacific slope.

The absence of A. rubicola on Rubus on the Pacific slope

explains the absence of the disease there.

Economic Importance

Where it occurs in North America, raspberry leaf curl has the

potential of being an important raspberry disease problem.

Yield reductions in red raspberries of 20 to 40% and

reduction in fruit quality have been reported, and infected

plants may fail to survive the winter after a few seasons

(Bennett 7927; Bolton 7970).

Symptoms on Natural and Experimental Hosts

RLCV has been transmitted only to the genera Rubus and

Fragaria. In the subgenus Idaeobatus (raspberries), natural

Rubus hosts mcXnát Rubus idaeus L. and R. idaeus var.

strigosus (Michx.) Maxim, (red raspberry), R. occidentalis

L. (black raspberry), R. neglectus Peck (purple raspberry),

R. phoenicolasius Maxim (wineberry); subgenus Eubatus

hosts (blackberries, which are minor hosts) include R.

allegheniensis Porter (wild blackberry and cv. 'Eldorado'),

R. procerus P. J. Muell. (Himalaya blackberry), and R.

ursinus Cham. & Schlect. (Pacific coast trailing blackberry).

Symptoms on red raspberry. Plants show no symptoms or,

at most, a mild downcurling of the tip leaves in the current

year of infection (fig. 219). The following spring, leaves on

both fruiting canes and primocanes are curled and slightly

yellow (fig. 220). The fruiting laterals are shortened, and

there may be proliferation of the shoots, producing a rosette.

New canes are stunted, numerous, and branched at the leaf

axils. The plants remain stunted and are often killed in a

succeeding winter. Fruit in diseased plants is small and

crumbly. All red raspberry cultivars tested are susceptible to

infection (Stace-Smith 1962a), although there are marked

differences among cultivars in their resistance to colonization

by the vector aphid. Aphis rubicola. (See "Natural and

Experimental Transmission.")

Symptoms on purple raspberry. Symptoms are milder than

on other raspberries, and the cv. 'Columbian' was found to

recover spontaneously from infection by the alpha strain of

RLCV, a rare phenomenon in plant virology (Bennett 1930).

Ameson and Braun (1975) felt that purple raspberry cultivars

grown at that time were resistant to both alpha and beta

strains of RLCV.

Symptoms on black raspberries. The symptoms are similar

to those on red raspberry. Leaves are arched, firm, and

remain small and nearly circular in outline, developing a dark

greasy-green cast (fig. 221). In a chronic infection, the young

canes are stiff and brittle, and frequently do not branch.

Symptoms on blackberries. Some blackberry cultivars

show symptoms similar to those on red raspberry, whereas

other cultivars remain symptomless.

Experimental hosts include: Fragaria vesca L. var. semperflorens (Duch.) Ser. cv. 'Alpine' (Alpine strawberry)

(Stace-Smith 1962a); Rubus albescens Roxb. (tropical black

raspberry, with the beta strain (R. H. Converse, unpublished)); R. baileyanus Britton x R. argutus Link cv.

'Lucretia' ('Lucretia' dewberry) (Bennett 1930); R. henryi

Hemsl. and Kuntze (alpha and beta strains) (R. Stace-Smith

1962a; R. H. Converse, unpublished).

Symptoms on indicator hosts. Symptoms on wineberry (R.

phoenicolasius): Symptoms are usually evident 7 to 10 days

after aphid inoculation. The syndrome is essentially the same

as on raspberry, but is considerably more pronounced, rapid,

and reliable in development. The petiole of the tip leaf is

recurved downward. The leaf blade does not expand

normally, and the interveinal tissue of the unexpanded

portion is chlorotic. Succeeding leaves are curled and

stunted, resulting in a rosette at the tip of the plant (fig. 222).

187
Symptoms on R. henryi. The first symptoms are evident 10

to 14 days after inoculation. The young leaves are chlorotic

and develop an asymmetric twist (fig. 223). Within a month

after inoculation, the shoot tips and axillary buds become

necrotic.

Symptoms on 'Alpine' strawberry. Interveinal chlorosis is

evident about 3 wk after graft inoculation. This chlorosis is

visible on two or three succeeding leaves; later, infected

plants tend to recover and cannot be distinguished from

control plants. The presence of the latent A strain of

strawberry crinkle virus does not intensify the symptoms, as

it does with some of the strawberry viruses. (See "Strawberry

Crinkle," p. 20.)

Natural and Experimental Transmission

RLCV has been transmitted by aphids as well as by patch and

petiole-insert grafting (Harris 1935; Stace-Smith 1962a;

Smith 1925).

Aphis rubicola is the only known natural vector of RLCV

(Smith 1925: Bennett ¡927. 1930; Converse 1962; StaceSmith 1962a; Brodel et al. 1979) (fig. 224). A. rubicola

transmitted alpha and beta strains of RLCV (Bennett 1930).

The alpha strain was acquired after 2 hr of feeding and

persisted in the aphid several days (Bennett 7927). Table 10

summarizes the known vector relationships of RLCV. The

aphid is sluggish and is thought to be a rather inefficient

vector (Bolton 1970). The influence of time, temperature,

and light on the production of sexual forms of A. rubicola

have been studied (Brodel and Schaefers 1979; Brodel and

Schaefers 1980a).

In studies in New York, populations of A. rubicola reached a

minor peak in late July and a major peak in early October

(Schaefers 1967). RLCV transmission patterns appeared to

follow the direction of prevailing winds and to be more

influenced by local populations of viruliferous A. rubicola in

a given field than by more distant occurrences (Bolton 1970).

Differences exist in the resistance of red raspberry cultivars

to supporting colonies of A. rubicola. No immunity to

colonization has been found. However, significant and

repeatable differences in resistance to colonization (10-30%

below susceptibles) have been identified in red raspberry.

Selections and cultivars like NY 632, 'Canby', 'Latham',

and 'Willamette' are being used in the New York raspberry

breeding program (Brodel et al. 1979; Kennedy et al. 1973).

Aphis idaei van der Goot is an experimental vector of RLCV

(Stace-Smith 1962a). The relationships of RLCV with this

aphid vector are summarized in Table 10. The aphid occurs

in Eurasia but is known in the Western Hemisphere only in

coastal British Columbia, where RLCV does not occur.

RLCV might become a problem in red raspberry in Europe if

introduced because of the widespread occurrence of A. idaei

there.

Figure 219. — Early symptoms of alpha strain of

raspberry leaf curl virus on 'Lloyd George' red

raspberry.

Figure 220. — Chronic symptoms ol alpha strain of

raspberry leaf curl virus on 'Lloyd George' red

raspberry.

Aphis rubifolii (Thos.), a small blackberry aphid, may be a

vector of RLCV on blackberry since the disease is reported

on 'Eldorado' blackberry, which is not a host of A. rubicola

(Bennett 1930); however, in greenhouse tests, A. rubifolii

failed to transmit RLCV (Converse 1962).
Figure 221. — Chronic symptoms of beta strain of

raspberry leaf curl virus on 'New Logan' black

raspberry.

Figure 222. — Symptoms of alpha strain of raspberry

leaf curl virus on wineberry seedling (Rubus phoenicolasius).

Figure 223. — Raspberry leaf curl disease symptoms

on Ruhus henni.

Figure 224. — Aphis rubicola on red raspberry shoot.

Amphorophora agathonica Hottes (referred to in older

literature as A. rubi), A. sensoriata Mason, Illinoia rubicola

(Oestlund) [also known as Macrosiphum rubicola (Oestlund)], and Aphis spiraecola Patch, all aphids that feed on

red raspberry, have been found to be nonvectors of RLCV

(Bennett 1930; Converse ¡962; Stace-Smith 1962a).

Properties of the Causal Agent

The alpha strain of the RLCV will not crossprotect against

the beta strain (Bennett 1930); therefore, the notion that alpha

and beta are strains of one virus remains unconfirmed.

Movement of the alpha strain in raspberry is relatively slow

and is limited to phloem tissues (Bennett 1927). Both strains

of RLCV behave like circulative viruses in A. rubicola.

Stace-Smith and Lo (1973) speculated that RLCV might be a

bacilliform virus like raspberry vein chlorosis virus (see

"Raspberry Vein Chlorosis," p. 194) because of the similar

vector relationships of the two viruses, but subsequent

examination of thin sections of RLCV-infected raspberry

tissue failed to demonstrate the occurrence of such particles

(R. Stace-Smith, unpublished). Matthews (7979) included

RLCV as a possible member of the luteovirus group because

of its vector relationships. Direct information is lacking on

morphology, properties, and serological relationships of

RLCV.

189
Table 10.—Some vector-virus-host plant relationships of raspberry leaf-curl virus

Vector

Vector

host

range

Virus

strain

Transmitting

stages of

aphids

Minimum

acquisition

feed time

Inoculation

threshold

Maximum

retention

Transmission

efficiency

of aphids References

Aphis rubicola Red, black,

purple

raspberry;

wineberry.

Alpha All but egg 2hr — Life Single =19% Bennett U927.

1930); Smith (1925).

Beta All but egg — — — — Bennett (1930).

Aphis rubifolii Blackberry ('.') Field

population.

— — — — Bennett (¡927).

Aphis idaei Red

raspberry.

Alpha — 24 hr 20 min 11 + days Groups of

10 = 80%.

Stace-Smith

(1962).

Detection and Identification

Raspberry leaf curl disease can be readily detected in the field

in raspberries by the tightly curled foliage of infected plants

(fig. 225). False symptoms resembling raspberry leaf curl

disease can be caused by infestations of A. rubifolii on

blackberries (Hottes and Frison 1931), by heavy infestations

of nonviruliferous A. rubicola on young black raspberry

foliage, and by two European nepoviruses, raspberry ringspot

virus and tomato black ring virus (see "NematodeBome Diseases" p. 211). Chronically infected raspberries

are always severely dwarfed, produce few main stems, and

have curled foliage. Wineberry is a rapid indicator host (by

leaf grafting or by transmission with A. rubicola) for latent

or presumptive infections, but both red and black raspberry

must be inoculated to distinguish between alpha and beta curl

viruses.

Control Procedures

Control procedures include the use of certified planting stock

free of this disease, avoidance of planting new fields near

infected wild or cultivated raspberries, periodic inspection

and roguing of infected plants, use of aphicides to limit

populations oí A. rubicola, and use of cultivars resistant to

colonization by A. rubicola. Since the apterae of A. rubicola

are relatively sluggish and do not readily drop off disturbed

foliage, inspections and roguing programs are useful for

control of raspberry leaf curl disease. A few new infected

plants can be expected each year in raspberry fields in areas

where the disease is prevalent, even though the above control

procedures are practiced, because of the movement of

viruliferous alate A. rubicola.

Immunity exists in 'Plum Farmer' black raspberry against

both alpha and beta strains of RLCV (Converse 1962), but

has not yet been used to develop immune, horticulturally

desirable types of red, purple, or black raspberry. Red

raspberry cultivars resistant to colonization by A. rubicola,

Figure 225. — Raspben7 leaf curl disease symptoms

on a naturally field-infected red raspberry.

however, are being developed by the New York Agricultural

Experiment Station (Brodel et al. 1979; Kennedy et al.

1973).

The alpha strain of RLCV was not eliminated from infected

plants held at an air temperature of 37°C for periods up to 4

wk (Stace-Smith 1962a). Heat therapy is academic,

however, since cultivars are not universally infected.

Remarks

A number of gaps exist in the basic information about both

strains of RLCV. Nothing is known about the properties of

the virus particles. Electron microscopy of thin sections of

infected raspberry phloem tissue should provide some

evidence of the morphology of the virus(es) causing this

disease. Several of the basic virus-vector properties have not

yet been reported, especially those for the beta strain and the

inoculation threshold periods.

190
4^h Cucumber Mosaic Virus In Raspberry

By A. T.Jones "

Additional Common Names

None.

History and Geographic Distribution

First reported from a few plants of Rubus idaeus L. cv.

'Lloyd George' in Scotland (Harrison 1958a). Later records

of infection come from Scotland (Jones 1976a. 1980c) and

the Soviet Far East (Gordejchuk et al. ¡977). Fern-leaf

symptoms in 'Cumberland' black raspberry plants growing

adjacent to cucurbits in Pennsylvania were suggested by

Zundel (1931) to be due to cucumber mosaic virus (CMV)

infection because of the similarity of the symptoms to those

produced by CMV in tomato. However, experimentally

infected R. occidentalis L. showed only a mild foliar mottle

(Harrison 1958a) quite unlike the symptoms observed by

Zundel (1931). CMV occurs worldwide in many different

crops and weed species (Francki et al. 1979), and it is likely

that it occurs very occasionally in Rubus species worldwide.

Economic Importance

The virus appears to be lethal in R. phoenicolasius Maxim.

(Jones 1976a) but induces only mild foliar symptoms in red

raspberry (Gordejchuk et al. 1977; Harrison 1958a; Jones

1980c) and is symptomless in cultivated brambles (Jones

1976a. 1980c). Infections are rare in Rubus in Scotland and

are of no importance economically.

Symptoms on Natural and Experimental Hosts

Rubus species. The few cultivated bramble plants found

infected with CMV in Scotland were symptomless (Jones

1976a). Pale green blotching of the leaves occurs in the red

raspberry cv. 'Lloyd George' with no apparent effect on plant

vigor or fruiting (Harrison 1958a). A single CMV-infected

plant of an unnamed red raspberry selection showed foliar

chlorotic ringspot symptoms but no obvious degeneration in

vigor (fig. 226^4) (Jones 1980a). In the Soviet Far East,

infected raspberry plants of the cultivar 'Visluha' were

characterized by small leaves with bright chlorotic mottling

(Gordejchuk et al. 1977). In contrast, leaves of field-infected

plants of R. phoenicolasius were misshapen and showed

areas of chlorotic blotching and line pattern, which often

became bright yellow in summer (fig. 226B); plants showed a

marked decline in vigor, and some plants died within 3 to 4

yr (Jones 1976a). Experimentally infected plants of R.

occidentalis developed a green mosaic (Harrison 1958a).

Herbaceous species. CMV infects a wide range of

herbaceous plants (Francki et al. 1979). Isolates obtained

from Rubus species infected and induced symptoms in the

following hosts: Chenopodium amaranticolor Coste and

Reyn., C. murale L., C. quinoa Willd., and Phaseolus

vulgaris L. — necrotic local lesions in a few days, not

systemic. Cucumis sativus L.. Nicotiana clevelandii Gray,

A', glutinosa L., and N. tabacum L. cvs. 'White Burley' and

'Xanthi-nc' — systemic mosaic.

Natural and Experimental Transmission

Natural transmission occurs by many aphid species and is in

the nonpersistent manner (Kennedy et al. 1962). Rubus

isolates have been transmitted between herbaceous hosts by

Amphorophora idaei (Born.) (formerly A. rubi (Kalt.)),

Macrosiphum euphorbiae (Thos.), and Myzus persicae

(Sulz.) (Harrison 1958a; Jones 1976a). Only A. idaei,

however, has been shown to transmit CMV to raspberry.

Although CMV is transmitted through the seed of several of

its hosts (Francki et al. 1979), it was not detected in seedlings

derived from CMV-infected R. phoenicolasius (Jones

1976a).

The virus is readily transmissible by inoculation of sap from

most hosts, but transmission from Rubus species is

sometimes difficult even when extracts are made in

2% nicotine solution. Mechanical transmission of CMV to

Rubus. even with purified preparations, was not successful in

Scotland (Harrison 1958a; Jones 1976a), but is reported from

the U.S.S.R. (Gordejchuk et al. 1977).

Figure 226. — Chlorotic blotches and line pattern in

leaves of Rubus infected with cucumber mosaic virus:

A. Unnamed red raspberry selection; B. Ruhu.s

phoenicolasius. (Copyright Scottish Crop Research

Institute.)

191
An isolate in R. phoenicolasius was readily graft transmissible to R. phoenicolasius but did not infect R. henryi Hemsl.

and Kuntze, R. ¡oganobaccus Bailey, R. procerus P. J.

Muell, or several red raspberry cultivars including cv. 'Lloyd

George' — a cultivar found naturally infected with CMV.

This suggests either that this isolate is restricted in its Rubus

host range or that graft transmission of CMV to certain Rubus

species is difficult.

Properties of the Causal Agent

For a detailed description of the virus see Francki et al.

(1979). All isolates of CMV are relatively unstable. In sap of

Nicotiana species, Rubus isolates lost infectivity after

diluting to 10-' to lO-", heating for 10 min at 65° to 70°C, or

storage at 20°C for 3 to 5 days (Harrison 1958a; Jones

1976a).

Most strains, but not all (Francki et al. 1979), can be purified

by clarification with organic solvents, followed by precipitation with 10% polyethylene glycol (mol. wt. 6000) or

acidification to pH 5.0 and differential centrifugation.

Further purification can be achieved by sucrose density

gradient centrifugation (for further details see Francki et al.

1979). The only Rubus isolate to be purified and examined in

any detail is that from R. phoenicolasius (Jones 1976a). Like

other CMV isolates, it has icosahedral particles about 28 nm

in diameter (fig. 227), which sediment as a single component

with a sedimentation coefficient of about 92 S (Jones 1976a).

Strains of CMV that have been examined in more detail are

known to contain a single polypeptide of about 24,500 mol.

wt. and four ssRNA species; some isolates contain an

additional satellite RNA species of about 100,000 mol. wt.

At least one of these satellite RNA species is known to

modify the symptoms induced by the satellite-free CMV

strain in some hosts (Francki et al. 1979).

There are several serotypes of CMV but all Rubus isolates

tested by Jones (1976a and unpublished) were serologically

indistinguishable from the W strain, which is found

commonly in British crop and weed plants (Tomlinson et al.

1973).

Detection and Identification

Detection of infection is by inoculation of sap from Rubus in

2% nicotine solution to C. quinoa, C. amaranticolor, or N.

clevelandii test plants. Identification of isolates can be made

by testing the ability of sap from infected test plants to react

with CMV antiserum. In agar gel double diffusion tests,

particles of many CMV isolates are degraded in the absence

of ethylene diamine tetra-acetate (EDTA) (Tomlinson et al.

1973; Jones 1976a); extracts from plants and the agar gel

should therefore contain 0.001 M EDTA.

Figure 227. — Electron micrograph of a purilied

preparation of cucumber mosaic virus particles stained

in 2% ammonium molybdate, pH 6.5. Bar represents

100 nm. (Copyright Scottish Crop Research Institute.)

Control Procedures

Infection with CMV is rare in Rubus; consequently,

elimination of the virus from Rubus has not been attempted.

The possibility of propagation from CMV-infected plants

should easily be avoided by indexing mother plants for virus

infection.

Remarks

CMV is not systemic in C. quinoa and can therefore be

readily distinguished in this host from black raspberry

necrosis virus (see "Black Raspberry Necrosis," p. 178),

nepoviruses (see the chapters in this section dealing with

nematode-bome viruses), raspberry bushy dwarf virus (see

"Raspberry Bushy Dwarf," p. 229), and isolates of tobacco

streak virus (see "Tobacco Streak Virus in Rubus," p. 235).

It is also distinguishable from wineberry latent virus (WLV;

see "Wineberry Latent Virus," p. 239) in C. quinoa as local

lesions induced by WLV, although initially small, expand to

2 to 3 mm, whereas those induced by CMV remain the size

of pinpoints; furthermore, the particles of WLV are filamentous and easily distinguished from CMV.

^

,*^Thimbleberry Ringspot >/

By R.[Stace-Smith

Additional Common Names

None.

History and Geographic Distribution

The virus was described from naturally infected thimbleberry

(Rubus parviflorus Nutt.) in British Columbia. Thimbleberry

is a native understory plant widespread in the Pacific

Northwest. It grows in patches under closed forest canopy or

in the open, but characteristically along the edges of forest

clearings and along forest creeks. The viruslike symptoms

were first observed on a few plants near Vancouver, British

Columbia, in 1953. The symptoms were later shown to be

caused by a virus to which the name thimbleberry ringspot

was applied (Stace-Smith 1958). In the intervening years,

192
many patches of thimbleberry have been examined for

virusHke symptoms, but no additional infections have been

observed (R. Stace-Smith, unpublished).

Economic Importance

The virus is of no economic importance in thimbleberry. It

was initially investigated because wild Rubus hosts could

serve as a potential reservoir of viruses in commercial

plantings. The fact that the virus has never been detected in

cultivated Rubus spp. suggests that it is unlikely to constitute

a potential problem.

Symptoms on Natural and Experimental Hosts

Thimbleberry is the only natural host that is known. Diseased

plants exhibit irregular ringspot and oakleaf markings on the

leaves. The rings are faint and small as the young leaves

unfold in the spring, but as the leaves expand the markings

become more pronounced (fig. 228). Some leaves do not

show line patterns and symptoms are restricted to patches of

netlike vein chlorosis (fig. 229), varying in intensity of

symptoms. Some show no or only slight mottling, whereas

other leaves on the same plant show severe mottling and leaf

distortion. Those plants with mild foliar symptoms show no

stunting; those with severe mottling bear canes that are

stunted.

Experimental hosts. The virus has been transmitted from

thimbleberry to three Rubus spp., each of which was

susceptible. Red raspberry {R. idaeus L. cv. 'Washington')

developed faint chlorotic markings that took the form of

ringspot or oak leaf patterns. Symptoms were not as striking

as on thimbleberry. Markings could be detected readily on

the leaves produced in the spring but were faint on leaves

produced during the summer. The virus had no obvious effect

on plant vigor or fruit yield. Black raspberry (R. occidentalis

L. cv. 'Munger') developed a distinct mottling on some

leaves (fig. 230), but more often there was a diffuse mottling

rather than a definite pattern. Within a few weeks of the

initial appearance of leaf symptoms, the tips of affected

plants became necrotic and the axillary buds near the base of

the cane sprouted, giving the plant a rosette type of growth.

R. henryi Hemsl. and Kuntze developed symptoms about 7

wk after grafting, when chlorotic spots appeared on the

young expanding leaves near the tip of the plant. Terminal

buds on affected canes failed to develop and became

necrotic. The chlorosis and necrosis of the first few canes to

show symptoms could be considered a shock reaction since

the plant recovered, and leaves on subsequent canes either

showed no symptoms or at most a few chlorotic spots.

Natural and Experimental Transmission

No direct evidence is available as to the source of the few

virus-infected plants that have been found or whether the

virus is spreading in nature. Although thimbleberry plants

produce seed, most of the canes arise from underground

rhizomes and a single infected plant may produce several

canes. The outbreaks near Vancouver have been monitored

Figure 228. — Chlorotic line patterns and rings that

develop on leaves of thimbleberry plants infected with

thimbleberry ringspot virus.

Figure 229. — Mild symptoms of thimbleberry ringspot virus, consisting of patches of diffuse vein

chlorosis, on some leaves of an infected thimbleberry

plant.

for nearly three decades, and the virus has not spread to

adjacent healthy plants. Further, the infected plants that have

been found are confined to forested areas, well isolated from

agricultural areas, suggesting that the virus had its origin in

wild plants and is rarely transmitted in nature.

Despite the fact that there is no evidence of natural spread,

should any natural transmission occur it could probably be

attributed to one of the thimbleberry inhabiting aphids. The

aphid Illinoia (also known as Masonaphis) maxima (Mason)

is prevalent in the area, appears to be confined to the young

leaves and terminal shoots of thimbleberry (Frazer and

Forbes /96S),and is capable of transmitting the virus from

thimbleberry to thimbleberry and from thimbleberry to black

raspberry (Stace-Smith 1958). Two other aphid species,

Illinoia davidsoni (Mason) and Amphorophora parviflori

Hill, are occasionally found on thimbleberry and are also

experimental vectors. All three species are inefficient

vectors; when aphids were transferred from an infected

source plant to thimbleberry seedlings, 10 aphids per test

plant, a low percentage of the exposed seedlings became

infected (Stace-Smith ¡958).

193
Figure 230. — Diffuse mottle symptoms on blaclc

raspbeiry (Riihii.s occidenialis) cv. "Munger' following

aphid inoculation with thimbleben7 ringspot virus.

Properties of the Causal Agent

Thimbleberry ringspot virus has not been transmitted

mechanically despite repeated attempts using a variety of

buffers and a range of herbaceous test plants (R. StaceSmith, unpublished). It is assumed that the virus, like most

aphid-transmitted viruses affecting Rubus spp., is not

mechanically transmissible.

The virus can be transmitted by each of the three aphid

species that occur on thimbleberry in British Columbia,

namely Illionia maxima, I. davidsonii, and Amphorophora

parviflori but not by the large raspberry aphid A. agathonica

Hottes (Stace-Smith 1958). Transmission efficiency is low,

and infective aphids retain the virus for less than 1 day.

In thin section electron microscopy of infected thimbleberry

leaf tissue, virus-like particles were detected. The particles

were spherical, about 25 nm in diameter, and confined to

single rows enclosed in tubules. Such tubules were only

detected in cell walls or invaginations in cell walls between

the leaf mesophyll cells (R. Stace-Smith, unpublished).

Detection and Identification

The virus can be detected by visual examination of

thimbleberry plants, particularly in the spring of the year,

where the characteristic ringspot or oak leaf markings are

readily seen. As the season progresses, the symptoms are less

obvious, and many plants that are free of this virus develop

chlorotic blotches on the upper leaf surface as a result of

powdery mildew {Sphaerotheca humuli (DC.) Burr.) infection on the lower surface. In a superficial examination, such

blotches might be confused with symptoms of viral origin.

Surveys in British Columbia on the incidence of virus in the

native thimbleberry have revealed no viruses other than

thimbleberry ringspot, and even this virus appears to be

confined to a limited area. Thimbleberry is widely distributed

in western North America, and additional infections may be

detected in the future. Should plants suspected of being

infected with thimbleberry ringspot be found, tentative

identification could be made on the basis of the symptoms

induced on the natural host. Positive identification would

require graft or aphid transmission tests to R. occidentalis

and R. henryi.

Control Procedures

Thimbleberry ringspot is an unusual Rubus virus in that it

appears to be confined in nature to the wild host. The facts

that it is transmitted inefficiently by the thimbleberryinhabiting aphids and that these aphids rarely feed on other

Rubus spp. suggest that there is little likelihood of the virus

ever being introduced into any of the commercial Rubus

species. For the above reasons, control measures may never

be required.

A^ Raspberry Vein Chlorosis;/

By A. T.jjones, A. F.lMurrant, and R. iStace-Smith

Additional Common Names

Vein chlorosis mosaic (Cadman and Harris 1951); raspberry

chlorotic net (Jordovic 1963)\ Ademchlorose (Richter 1964a,

b).

History and Geographic Distribution

The disease, which occurs naturally only in red raspberry,

was first described from Scotland by Cadman (¡952a) who

showed that it was caused by a graft-transmissible agent,

which he called raspberry vein chlorosis virus (RVCV). The

disease was later found in Canada (Stace-Smith 1961),

Europe (Bj0mstad 1958; Helebrant 1958; Jordovic 1963;

Richter 1964a; Szilágyi 1980; Tapio 1961), U.S.S.R.

(Kuznetsova and Pomazkov 1971; Tiits 1962), and New

Zealand (Cadman and Stace-Smith ¡970; Jones and Wood

1979). The disease is widespread in Great Britain and

continental Europe, common in some areas of New Zealand,

but rare in Canada. It has not been reported from other

raspberry growing areas such as Australia and the United

States.

The virus is transmitted by the aphid Aphis idaei van der

Goot (Cadman 1952a), which is widespread in Europe. The

aphid appears not to be present in Australia and is found

only infrequently in British Columbia; infection and spread

of the disease in New Zealand and Canada are probably due

to introduction and propagation of infected plants from

Europe (Cadman and Stace-Smith 1970; Jones and Wood

1979).

Economic Importance

Vein chlorosis is one of the commonest diseases in raspberry

in continental Europe and the U.S.S.R. This high incidence

is largely caused by propagation from infected stock. Almost

all stocks of some cultivars, such as 'Baumforth B', are

infected with the virus. Although on its own the virus is not

194
lethal to raspberry, it undoubtedly affects plant vigor,

especially in combination with other viruses. In some

cultivars, the virus causes significant decrease of berry

weight (Daubeny et al. 7970; Jones 1980d)\ infected plants of

cv. 'Mailing Leo' produced thinner canes and earher ripening

fruit than did virus-free controls (Jones 1980b). Infection of

some cultivars was associated with increased pollen abortion

(Freeman et al. 1969) and retarded embryo sac development

(Eaton and Turner 1971).

Symptoms on Natural and Experimental Hosts

In nature, the virus has been found only in red raspberry (R.

idaeus L. and R. idaeus var. strigosus (Michx.) Maxim.);

only two other species {R. loganohaccus Bailey and Fragaria

vesca L.) have been infected experimentally.

The following red raspberry cultivars have been reported to

be infected with RVCV either naturally or by graft

inoculation in Great Britain, Canada, continental Europe,

and New Zealand: 'Asker', 'Badenia', 'Baumforth B',

'Burnetholm', 'Canby', 'Deutschland', 'Devon', 'Fairview',

'Gertrudis', 'Glen Clova', 'Glen Prosen', 'Golden Queen',

'Great American', 'Hailsham', 'Herbert', 'Joy', 'LaFrance',

'Lloyd George', 'Mailing Admiral', 'Mailing Delight',

'Mailing Exploit', 'Mailing Leo', 'Mailing Jewel', 'Mailing

Landmark', 'Mailing Notable', 'Mailing Orion', 'Mailing

Promise', 'Marcy', 'Newburgh', 'Norfolk Giant', 'Noma',

'Norwich Market', 'Park Lane', 'Preussen', 'Pyne's Royal',

'Romy', 'St. Walfried', 'Schönemann', 'Schopska alena',

'Seedling M', 'Seedling K', 'Seedling Z', 'Sumner',

'Taylor', 'Valjevka', 'Washington', 'Willamette', and

'Winkler's Seedling' (Bj0mstad 1953; Cadman 1952a;

Freeman et al. 1969; Jones 1981b; Jones and Wood 1979;

Jordovic 1963; Richter 1964a, b; Stace-Smith 1961; Tapio

7967; A. T. Jones, unpublished data). A few North

American cultivars (for example, 'Cuthbert', 'Latham', and

'Viking') seem immune to field infection and graft

inoculation (Cadman 1952a; A. T. Jones, unpublished data).

'Boysen', 'Logan', 'Tayberry', R. henryi Hemsl. and

Kuntze, R. molaccanus L., R. occidentalis L. cvs. 'Munger'

and 'Plum Farmer', R. phoenicolasius Maxim, and R.

procerus P. J. Muell cv. 'Bedford Giant' failed to become

infected after graft inoculation (A. T. Jones, unpublished

data). Stace-Smith (7967) also found R. henryi and R.

occidentalis resistant to infection by graft inoculation, but

found 'Logan' susceptible.

Symptoms on red raspberry. After graft inoculation, plants

may not show symptoms until the following year, but plants

grafted early in the year or inoculated by aphids may develop

symptoms in 4 to 12 wk. The extent and severity of

symptoms depends on host genotype, virus strain (Cadman

1952a), and growing conditions. The cvs. 'Lloyd George',

'Mailing Delight', 'Norfolk Giant', and 'Washington' are

good indicators (Jones et al. 7977).

Symptoms are usually less intense in the greenhouse than in

the field. The most obvious symptoms appear on leaves of

first-year canes as a chlorosis of the minor veins, either in

patches (fig. 231) or throughout the leaf (fig. 232). When

symptoms are severe, the leaf blade may become distorted by

uneven growth as the leaf expands. In cv. 'Mailing Delight',

infected leaves may show epinasty (Jones et al. 7977).

Symptoms on 'Logan'. Plants graft-inoculated with a

Canadian or a German isolate of RVCV developed symptoms

similar to those in raspberry (Stace-Smith 7967; Richter

1964a).

Symptoms on 'Alpine' strawberry. Plants inoculated by

Aphis idaei developed symptoms after 3 to 4 wk, similar to

those in raspberry. In addition, veinal necrosis often

developed along one of the secondary leaf veins (Jones et al.

7977).

Natural and Experimental Transmission

RVCV is transmitted in nature by Aphis idaei, but not by the

aphids Amphorophora agathonica Hottes or Amphorophora

idaei Borner (also known as A. rubi (Kalt.)) (Cadman 1952a;

Stace-Smith 7967; Jordovic 1963). The virus is also

transmitted experimentally by grafting but not by mechanical

inoculation with sap. It is not seed-transmitted in red

raspberry (Jordovic 7965).

Aphis idaei require at least 1 day to acquire RVCV, and they

retain it for at least 1 day (Cadman 1952a; Stace-Smith 7967)

and probably for life. Efficiency of transmission is increased

after 7-day acquisition access feeds (Cadman 1952a), the

greatest recorded frequency of transmission (46%) being

obtained after acquisition and inoculation access periods of 7

and 30 days, respectively (Jordovic 796i).

Properties of the Causal Agent

RVCV is not transmissible by inoculation of sap, nor has it

been purified; however, electron microscopy of thin sections

of raspberry leaves infected with RVCV alone showed large

bacilliform particles, some about 430 to 560 x 65 to 91 nm

and rounded at both ends and others shorter and rounded at

only one end (fig. 233 A) (Stace-Smith and Lo 7975; Jones et

al. 797^). The particles have a densely staining nucleocapsid

about 50 to 70 nm in diameter surrounded by an

electron-lucent zone and a unit membrane, which, in some

sections, appears continuous with the endoplasmic reticulum.

The nucleocapsid shows some crossbanding with a periodicity of 4 to 5 nm (fig. 233 B) (Stace-Smith and Lo 797J; Jones

et al. 1974). Similar particles have been found in thin

sections of viruliferous Aphis idaei (Murant and Roberts

1980).

In raspberry, virus particles were detected in only a small

proportion of parenchyma cells of the vascular bundles and

occurred singly or in groups (often within a membranous sac)

in the cytoplasm and perinuclear space but not in the nucleus

195
Figure 231. — Patches of vcinal chlorosis in a leaf of

'Lloyd George' red raspberry Infected with raspberry

vein chlorosis virus. (After Jones et al. 1977.)

Figure 232. — Chlorosis of the fine veins of a leaf of

'Glen Prosen' red raspberry infected with raspberry vein

chlorosis virus. (After Jones et al. 1977.)

(Stace-Smith and Lo 7975/Jones et al. 1974). In Aphis idaei,

virus particles were found in the brain and salivary glands, in

the connective tissue surrounding the sucking pump and

esophagus, and in the muscle cells of the sucking pump; they

occurred only in the cytoplasm, not in the nuclei or

perinuclear space (Murant and Roberts 1980).

The particles of RVCV closely resemble those of plant

rhabdoviruses (Peters 1981), several of which are aphidborne. By analogy with other plant rhabdoviruses, RVCV

probably multiplies in its aphid vector but may have a long

latent period after which the insect transmits it for life. The

observations of Jordovic (1963) that RVCV is transmitted

most efficiently when allowed very long acquisition and

inoculation feeds are consistent with this expectation.

Detection and Identification

The characteristic clearing of the fine veins is evident in most

susceptible cultivars of red raspberry. Confirmation of

infection can be obtained by graft-inoculation to sensitive

cultivars such as 'Lloyd George', 'Mailing Delight', or

'Washington', although the presence of other viruses may

make diagnosis difficult. Transmission to indicators by Aphis

idaei is also possible, but the aphid is difficult to handle and

maintain in culture. In some raspberry cultivars, the

symptoms induced by rubus yellow net virus on its own (see

'Rubus Yellow Net,"p. 175) may be confused with those of

RVCV, but the former are usually much less conspicuous.

Pure cultures of the two viruses may be distinguished by

graft-inoculation to R. occidentalism which is immune to

RVCV but develops a faint yellow net symptom on infection

with rubus yellow net virus. Symptoms induced by either of

these viruses alone are quite distinct from those of

veinbanding mosaic disease. (See "Raspberry Mosaic," p.

168.)

Control Procedures

In Scotland, the aphid vector Aphis idaei is usually

uncommon, and roguing infected plants has helped to restrict

spread (Cadman and Stace-Smith 1970). The aphid is much

more common in continental Europe, but here the virus is

widely disseminated in infected planting material because

many stocks of the older and most popular cultivars are

totally infected. They have not been freed from infection

because RVCV is not inactivated in raspberry plants grown at

37°C for several weeks or months (Stace-Smith 1960;

Chambers 1961; Jordovic 1963). Van der Meer (7975),

however, obtained plants free of RVCV by rooting excised

tips from infected plants that had been kept at 35°C for 4 wk.

More recently. Baumann {1982) eradicated RVCV from

infected plants by a combination of thermotherapy and

meristem tip culture.

Control of the aphid vector by the use of insecticides may

decrease the rate of reinfection of healthy planting material,

but there are no reports of the benefits of such treatment.

Although red raspberry cultivars differ in susceptibility to A.

idaei, there are no good sources of resistance to this aphid.

196
Leafhopper-Borne Diseases

V^

Figure 233. — Particles of raspberry vein chlorosis

virus in thin sections of infected raspberry cells. Bars

represent 100 nm: A. Particles rounded at one or both

ends; B. cross-banding of the nucleocapsid. (Jones et al.

1977.)

The alternative approach, to breed plants with resistance to

RVCV itself, is being made in Scotland. Crosses between the

CVS. 'Viking' (believed to be resistant or immune to RVCV)

and 'Mailing Delight' (susceptible) indicate that resistance in

cv. 'Viking' is due to a single recessive gene (Jones and

Jennings 1980a). However, genetic control of RVCV

resistance in other cultivars may be complex (A. T. Jones and

D. L. Jennings, unpublished data). Nevertheless, researchers

using this source of RVCV resistance, and possibly that in

other Rubus species, may be able to incorporate resistance to

RVCV into future raspberry cultivars.

Remarks

Viruslike particles and ultrastructural effects resembling

those of RVCV were first found by Putz and Meignoz (¡972)

in raspberry showing symptoms of veinbanding mosaic disease. Such particles were not found in veinbanding mosaicdiseased raspberry examined by Jones et al. (1974).

Furthermore, it is now known that of the two viruses believed

to be responsible for raspberry mosaic disease, black

raspberry necrosis virus has isometric particles about 25 nm

in diameter (see "Black Raspberry Necrosis," p. 178) and

rubus yellow net virus has small bacilliform particles about

80 to 150 X 25 to 31 nm (see "Rubus Yellow Net," p. 175).

It therefore seems very probable that the plants examined by

Putz and Meignoz (¡972) were also infected with RVCV.

Rubus Stunt , By F. A. van der¿Meer

Additional Common Names

Witches'-broom; Heksenbezen, dwergziekte; Rubus Stauche;

Verzwergungskrankheit.

History and Geographic Distribution

Although his description of the disease is very short and

undetailed, a small epidemic of Rubus stunt was very

probably mentioned first by de Vries (¡896). In a very old

raspberry area in The Netherlands, Rietsema (¡954) observed

the disease as early as 1920. Wormald and Harris (¡932)

reported an epidemic of the disease in cultivated blackberries

in Great Britain, and Prentice (¡950) mentioned severe

outbreaks in raspberry X blackberry hybrids (that is,

'Phenomenalberry' and 'Logan') in the same country. As

cited by Ryschkow (¡946), Rubus stunt was described by

Vertogradova (¡938) as a serious and widespread disease of

raspberry in the U.S.S.R. After the First World War, the

disease became disastrous in the old raspberry area in the

southern parts of The Netherlands (De Fluiter and Thung

1951), and many young plantations, started with healthy

planting material, were found to contain 60 to 90% infected

plants in the second year after planting (van der Meer 1954).

Small epidemics of the disease have been seen and reported

in Bulgaria (Trifonov ¡96¡), East Germany (Richter ¡963),

and Denmark (Kristensen ¡962). Incidental occurrences of

Rubus stunt have been reported from several other European

countries such as West Germany, Hungary, Czechoslovakia,

Norway (Ramsfjell ¡952), and Italy (Marani et al. ¡977).

Recently, a disease similar to Rubus stunt has been found in

black raspberries (Rubus occidentalis L.) in the western part

of the United States (Converse et al. ¡982); however, further

host range studies must be done to determine if this disease is

identical with Rubus stunt.

Economic Importance

Rubus stunt is of great potential economic importance,

because crop losses can be very severe in places where the

disease becomes epidemic.

Symptoms on Natural and Experimental Hosts

Natural infection has been found in all principal European

cultivars of raspberries and in many species of wild blackberries. In all species and cultivars of Rubus, symptoms are

basically the same, that is, numerous, small, thin, and erect

canes (figs. 234 to 236) and an excessive lateral branching of

the whole plant, together with phyllody and proliferations of

the flowers (figs. 237 to 240). Except for cv. "Mailing

Promise', which is rather tolerant and seldom shows flower

malformations, all tested raspberry cultivars are equally

197
Figure 234. — First symptoms of Rubus stunt in red

raspberry. Numerous weak and erect shoots develop

from the root buds.

Ï '9 '

• .> <l

Figure 235. — Floricane of RUDUS Mum-inietied

blackberry cv. Thomless Evergreen', showing witches"-broom growth and yellowing.

sensitive. In cultivated raspberry plantations, many diseased

plants in the shock stage of infection die because they are

overgrown by healthy ones. However, raspberries grown

from root cuttings of infected plants and planted at a proper

distance from each other seldom die and, on the contrary,

may show a certain degree of regeneration. Among the great

number of shoots formed, some become larger than the

others and bear normal but small berries which are difficult to

harvest. Fruiting laterals of such regenerated plants are

always much shorter than those of healthy plants.

Plants that are already badly affected by raspberry mosaic

and raspberry leaf mottle are much more sensitive to Rubus

stunt, and often die within a year after infection. (See

"Raspberry Mosaic," p. 168, and "Raspberry Leaf Mottle

and Raspberry Leaf Spot," p. 183.)

Experimentally infected Fragaria vesca and strawberry

cultivars show witches'-broom, phyllody of flowers, and a

severe growth reduction (figs. 241 and 242). Infected plants

always die within 1 or 2 yr.

Figure 236.

blackberry.

Rubus stunt in naturally infected wild

198
i

à'

Figure 237. — Various forms and stages of flower and

fruit deformation in red raspberry cv. 'Radboud'

affected by Rubus stunt. Normal flowers and fruits are

in upper right row.

Figure 238. — Phyllody of flowers of red raspberry cv.

'Norfolii Giant'. Sepals, petals, and pistils become

leaflike structures. Stamens usually remain normal.

f f i # #

\

^^ty-f•

^

^^^ y^^

Figure 239. — Phyllody in Rubus stunt-infected wild

blackberry.

199
Figure 240. — ftoliferated flower of Rubus stuntinfected wild blackberry.

Natural and Experimental Transmission

From results of transmission experiments and field observations, de Fluiter and van der Meer {1953) assumed that Rubus

stunt is naturally transmitted, mainly by leafhoppers of the

genus Macropsis Lewis. The species M.fuscula Zett. was the

only common and abundantly present leafhopper in raspberry

plantations during the last epidemic in The Netherlands.

In transmission experiments, M.fuscula was able to transmit

Rubus stunt from raspberry to strawberry (van der Meer and

de Fluiter 1970). The froghopper Philaenus spumarius L.

and the leafhopper Allygus mayri Kbm. transmitted the

Rubus stunt agent to celery (Jenser et al. 1981), whereas the

leafhopper Euscelis plebeja Fallen transmitted the agent to

white clover and Chrysanthemum carinatum (Lehman 1973).

Experimentally, Rubus stunt can be transmitted between

Rubus species by graft inoculation.

Depending on the time of the growing season in which the

plants are infected, the incubation time varies from 4 to 11

mo (van der Meer 1954).

Biology of Macropsis species. The eggs of M. fuscula

overwinter in the bark of Rubus canes. When large numbers

are present in artificial cultures, the eggs are easily

detectable, but they are very difficult to find in naturally

affected canes (fig. 243). Therefore, it is difficult to prevent

distribution of the vector by means of planting material.

Figure 241. — Strawberry cv. 'Climax' graft-infected

by Rubus stunt. Healthy plant at left.

Figure 242. — Flower of Fragaria vesca affected by

Rubus stunt after graft inoculation .

M. fuscula has been reported from several European

countries and from parts of western Canada (Beime 1954;

Tonks 7960) and the United States (Converse et al. 1982).

On cultivated raspberries in The Netherlands, it was found in

the heavily infested area but not in other raspberry-growing

areas that were free of Rubus stunt. On wild blackberries,

however, the insect occurred all over the country, and Rubus

stunt was found in these vines in many places.

These observations have led to the opinion that infected wild

blackberries do not play an important role in the severe

outbreak of Rubus stunt in raspberries in The Netherlands. In

laboratory experiments, however, M. fuscula from several

wild blackberry species developed well on raspberries.

Another Macropsis species was found on R. caesius L., a

trailing wild blackberry that is very common on wet soils.

This species has been described by Wagner (1964) as M.

200
Figure 243. — Macropsis fuscula. vector of Rubus

stunt: Left, adult male; righl. adult female.

brabantica. It was not found on other blackberry species, and

in laboratory experiments it was not able to develop on

raspberries. M. brabantica probably is also able to transmit

Rubus stunt because severe outbreaks of the disease in R.

caesius have been observed in several places.

A third Macropsis species, M. scotti Edw., has been found

very commonly on cultivated Himalaya blackberries (R.

procerus P. J. Muell.) in the province of Zeeland in the

southwestern part of The Netherlands. In this area,

leafhoppers of the genus Macropsis were never found on

raspberry, even where they were planted next to heavily

infested 'Himalaya' blackberries, and the inability of M.

scotti to develop on raspberries has been confirmed in

laboratory experiments. According to J. T. Legg, as cited by

Cadman (1961b), M. scotti is also able to transmit Rubus

stunt. In the Netherlands, however, the disease has never

been observed in 'Himalaya' blackberries whereas in

England this cultivar was found infected commonly (Wormald and Harris 1932).

All three Macropsis species known from Rubus have one

generation a year, and there are few morphological

differences between species (Wagner 1964). All live

monophagously on Rubus species and hibernate in the egg

stage in the bark of Rubus canes. In The Netherlands, the first

larvae appear in the middle of May, whereas the first adults

appear at the end of June (de Fluiter and van der Meer 1958).

Adults may be observed until the first week of October.

To establish if Macropsis species do occur in Rubus

plantations, a sample of canes should be forced in a heated

greenhouse at the end of April. Larvae, hatching after about 3

wk, can more readily be found on such canes than on canes in

the field because of the small size and the often dark brown

color of the larvae, and their tendency to hide in dark and

moist places along the basal part of the canes. Larvae are

immobile and can easily be handled with a small paint brush.

Adults, on the contrary, are mobile and can easily be missed

in plantations, even when sampling is done with nets,

especially if populations are low and plantings exist of

heavily thorned cultivars.

Natural spread in raspberry. During the last epidemic in

The Netherlands, infection in raspberry plantations mainly

took place in August and September of the first growing

season (de Fluiter and van der Meer 1955). The first

symptoms, numerous weak shoots developing from the root

buds, showed up in August and September of the following

year (fig. 234). In the third summer after planting, typical

witches'-broom symptoms appeared; bunches of 5 to 10

fruiting laterals arising from single buds and showing

abnormal flowers together with the development of numerous

weak and thin young canes at the base of the plants (figs. 236

and 237). Symptoms never developed in the first growing

season, provided that healthy planting material was used (van

der Meer 1954).

During surveys in 1953 and 1954, plants in older plantations

were found to be much more resistant than those in young

plantations. On a number of farms, where 8- to 10-yr-old

plantings were situated next to 2-yr-old plantings, the older

plantings contained about 10% infected plants, whereas the

young plantings contained 50 to 80% infected plants. A

possible explanation for this phenomenon could be that

newly planted raspberries start their growth later than do

older plants and thus are physiologically younger in August

and September, at which time the leafhoppers are able to

transmit the Rubus stunt agent. Young shoots in such

plantings keep their leaves until November, but leaves of

shoots in older plantings begin to drop in July. Observations

actually showed that the population on older healthy plants

decreased very rapidly after the end of July, whereas on

maiden plants, which were free of leafhoppers when planted,

M. fuscula could be found until October. Diseased plants in

older plantations are good host plants for the leafhoppers,

probably because they keep their leaves until very late in

autumn; however, they seem to be of minor importance for

further spread within such old plantations.

Although M. fuscula is not able to develop on strawberry, it

appeared able to transmit Rubus stunt from raspberry to

strawberry in laboratory experiments. Infection of Rubus

stunt in strawberries, however, has never been observed in

the field, although in the heavily infested area strawberries

and raspberries usually were grown side by side on the same

farms.

201
Natural spread between different Ruhus species. There

is little exact information on the influence of infected wild

blackberry species during epidemics in cultivated raspberries

and blackberries; neither is there any such knowledge about

the ease with which Rubus stunt is transmitted naturally

between different cultivated species and cultivars of Rubus.

During the last epidemic in The Netheriands, infected wild

blackberries appeared of little importance in the infection of

cultivated raspberries (van der Meer and de Fluiter 1962).

There are reports from two areas where cv. 'Thomless

Evergreen' {R. laciniatus Willd.) became infected, while cv.

'Himalaya' on the same farms remained healthy (Schambach

1972; Dijkstra 1973). The latter cultivar, however, was

found to be susceptible during an epidemic in England

(Prentice 1950).

Converse et al. {1982) found Rubus stuntlike symptoms

common in 'Munger' black raspberries (/?. occidentalis

L.), but not at all in adjoining plantings of 'Willamette' red

raspberries. Transmission of Rubus stunt between different

cultivated Rubus species and between wild and cultivated

Rubus species may be influenced by the host plant

preferences of the Macropsis species occurring in certain

areas and by the physiological condition of the hosts, which

induce the leafhoppers to migrate on a large scale or may

determine whether plants visited by migrating leafhoppers

become infected.

It seems unlikely that the other^ reported vectors, P.

spumarius, A. mayri, and E. plebeja, play an important role

in transmission between Rubus species because they do not

live specifically on Rubus. By chance feeding, however, they

may be able to transmit the disease agent occasionally

between Rubus and other plant species and vice versa. The

very polyphagous character of P. spumarius marks this

species as a likely vector between different plant species and

families; however, froghoppers do not seem to be common

vectors of witches'-broom diseases. By our best knowledge,

Jenser et al. (1981) were the first to report such transmission.

Properties of the Causal Agent

Like many witches'-broom or "yellows" diseases of plants,

Rubus stunt was formerly attributed to a virus; however,

since Doi et al. (1967) discovered mycoplasmalike organisms

(MLO) in several witches'-broom diseased plant species,

many other workers have found such diseases to be

associated with MLO (Nienhaus and Sikora 7979; Davis and

Whitcomb 1971). MLO have also been found in stuntinfected Rubus species, that is, in red raspberries (Murant

and Roberts 1971; Müller et al. 7977), blackberries (Marani

et al. 7977; van der Meer 1980; Klein et al. 1976), and black

raspberries (Converse et al. 7952). Presently, it is assumed

that MLO are the direct cause of Rubus stunt and other

witches'-broom diseases of plants, although Koch's postulates are fulfilled in only a few cases (Bos 1981).

There is little information on the relationship between MLO

that cause diseases in different crops. Results of Lehman

(7975) and Jenser et al. (1981) show that the infective

agent(s) causing Rubus stunt can be experimentally inoculated into non-Rubus test plants. In these inoculated test

plants, symptoms develop that show much similarity to other

MLO diseases, such as aster yellows, strawberry green

petal, and clover phyllody. (See discussion, on leafhopper-bome diseases in the strawberry section of this

handbook, p. 31^6.) Information is lacking, however, on

the serological relationships of these MLO diseases.

Like many other MLO diseases (Whitcomb and Davis 7970),

Rubus stunt is persistently transmitted by its vectors, which

means that there is a latent period between the moment of

acquisition and the moment at which the vector is able to

transmit the disease agent. After this latent period, vectors

usually remain infective throughout their lives.

Larvae of M.fuscula, bom on diseased plants in the second

half of May and raised on diseased plants until they became

adults in the second half of July, were only able to transmit

Rubus stunt after the fifth of August (de Fluiter and van der

Meer 7955). Young larvae, from 5 to 7 days old, collected

from diseased plants and subsequently raised on healthy

plants, did not transmit Rubus stunt after they became adults,

but third- and fourth-instar larvae, sampled from diseased

plants in June, transmitted the disease in August, after

becoming adults in the middle of July. From this, it can be

estimated that the latent period of Rubus stunt in M. fuscula

is about 8 wk. Once infected, M. fuscula remains infective

until it dies. Transmission of Rubus stunt through the eggs

has not been detected.

According to Jenser et al. (7957), the latent period of Rubus

stunt MLO in P. spumarius and A. mayri is between 28 and

35 days, and both species remain infective during the rest of

their lives.

Detection and Identification

Rubus stunt is detectable by its symptoms: the development

of numerous thin erect shoots together with abundant lateral

branching. Phyllody of ñowers is the most typical symptom.

Some raspberry and blackberry cultivars may regenerate to a

high degree. Such regenerated plants generally do not show

flower deformation and for the that reason should be indexed

by grafting to sensitive raspberry cultivars, such as cvs

'Radboud' and 'Mailing Landmark' or to the sensitive

blackberry cv. 'Thomless Evergreen'. Attempts should be

made to detect MLO in diseased plant by electron

microscopy.

Control Procedures

According to de Fluiter and van der Meer (1958), the eggs of

M. fuscula can easily be killed by a tar oil spray in winter.

According to Reitzel (1971), however, such treatment killed

only half the population of the insect. Nymphs can be

202
controlled by spraying with parathion or other insecticides in

spring. A campaign, organized by The Netherlands'

Advisory Board, during which every grower was urged to

spray his raspberry plantation with tar oil in winter and with

parathion in spring (Slits 1954, 1955; van der Meer 7957),

resulted in a good control of the disease in the heavily

infested area (van der Meer and de Fluiter 1962).

Thanks to the long latent period of the disease agent in the

vector, raspberries can be protected against infection by

spray applications after harvest in August and September, the

period in which infection takes place. Because the time of

harvest is much later, such applications are usually not

possible in blackberry plantations.

Blackberries must not be sprayed with tar oil because they are

softer and less woody than raspberries in winter and will be

damaged by this spray.

Infected plants can easily be cured by hot water treatment of

dormant root cuttings or rooted shoots (Thung 7952).

Treatment for 2 or 3 hr in water at 45°C appeared sufficient to

inactivate the Rubus stunt agent.

Remarks

To the author's knowledge, Rubus stunt is the only known

disease of economic consequence in the genus Rubus that has

been proved to be caused by a leafhopper-bome agent.

Pierce's disease, however, probably caused by leafhopperbome rickettsialike organisms (Mollenhauer and Hopkins

7974), appears to occur latently in Rubus vitifolius Cham,

and Schlecht (Freitag 7957). Nichols et al. (7957) reported

shoot proliferation of 'Olallie' blackberry in California. The

symptoms resemble those of some leafhopper-bome diseases, but further studies have failed to associate a

transmissible agent with this disorder. Witches'-broom

symptoms in black raspberry have been observed in the

United States by Zundel {1931) in Pennsylvania, by R. H.

Converse (personal communication) in Michigan in 1963,

and, again by Converse in 1980 in Oregon. With respect to

the first two observations in black raspberries, no further

research was done. During their last observations in Oregon,

Converse et al. {1982) noticed a rapid spread of the disease in

a plot of 'Munger' black raspberries, and MLO appeared to

be common in sieve tubes of infected plants. Although

further research is needed to confirm this, it seems likely that

witches'-broom of black raspberry is a leafhopper-bome

disease related to or identical with Rubus stunt.

203
Nematode-Borne Diseases

.4

¿^ Raspberry Yellow Dwarf and Associated Diseases of

Rubus Caused by Arabis Mosaic and Strawberry Latent

Ringspot Viruses

By A. F.jMurant

Additional Common Names

None.

History and Geographic Distribution

The name "raspberry yellow dwarf was given by Harrison

{1958c) to a disease of 'Mailing Exploit' red raspberry

(Rubus idaeus L.) in Great Britain. This disease was caused

by a sap-transmissible soil-borne virus. Cadman {1960b)

showed that the virus was closely related to arabis mosaic

virus (AMV) described by Smith and Markham {1944).

AMV has since been reported throughout Great Britain in

several other red raspberry cultivars (Taylor et al. 1966; Dale

and Brown 1973; Cotton et al. 7978).

Another sap-transmissible soil-borne virus, strawberry latent

ringspot virus (SLRV) (Lister 1964), causes a similar

stunting disease in some raspberry cultivars (Taylor and

Thomas 1968; Putz and Stocky 1970) and often occurs in

mixed infections with AMV (Lister 1964; Dale and Brown

1973), Both viruses are transmitted by nematodes of the

genus Xiphinema, principally X. diversicaudatum

Micoletzky (Harrison and Cadman 1959; Jha and Posnette

7959; Lister 1964), and therefore commonly occur together

in the same soils.

Both AMV and SLRV have wide natural host ranges and

occur locally throughout the British Isles and continental

Europe. In addition, AMV is reported from the U.S.S.R.,

including the Soviet Far East (Gordejchuk et al. 7977), Japan

(Iwaki and Komuro 797^), New Zealand (Thomas and

Procter 7972, 7977), and the United States (Waterworth

1975); SLRV is reported from New Zealand (Fry and Wood

1973), Canada (Allen et al. 7970), and the United States

(Hanson and Campbell 7979). X. diversicaudatum occurs in

Europe, U.S.S.R., Canada, the United States, Australia, and

New Zealand (Pitcher et al. 7974). However, the nematode

was not associated with any of the reported occurrences of

these viruses in North America, all of which resulted from

the importation of infected plant material.

In raspberry, both viruses have been reported from several

countries outside the British Isles: AMV in France (Putz and

Stocky 7977), East Germany (Richter 1964c), and the Soviet

Far East (Gordejchuk et al. 7977); SLRV in France (Putz and

Stocky 1970) and Italy (Vegetti et al. 7979).

Economic Importance

Diseases of raspberry caused by AMV and/or SLRV are

locally important in England but rare in Scotland, where most

of the British raspberry crop is grown; they also seem rare in

continental Europe. If the outbreak is large, crop losses may

be considerable because infected plants yield little or no fruit

and may die. Because few or no symptoms appear in the

early stages of infection, the viruses may be distributed in

infected propagating materials; this can result not only in

losses of crop but also in the viruses becoming established in

the soil if vector nematodes are already present. It is also a

potential problem in the international exchange of planting

material.

Symptoms on Natural Hosts

Both AMV and SLRV occur naturally in red raspberry

{Rubus idaeus L.). AMV has also been found in blackberry

{Rubus procerus P. J. Muell.) cv. 'Himalaya Giant'

(Harrison 1958c). Both viruses also infect plants in the small

fruit genera Fragaria and Ribes. (See these sections of this

handbook.)

Many other cultivated and wild plants have been found

naturally infected with both viruses. The following is a

selection of plants found infected with AMV; those in which

SLRV has also been found are marked with an asterisk.

Cultivated Plants

Apium graveolens L. var. dulce (celery)*, Armoracia

rusticana Gaertn., Mey., and Scherb. (horse-radish),

Asparagus officinalis L. (asparagus)*, Cucumis sativus L.

(cucumber), Cucúrbita pepo L. (marrow), Cyphomandra

betacea Sendt. (tamarillo, tree-tomato), Daucus carota L.

(carrot). Delphinium sp.*, Dianthus caryophyllus L. (carnation), Euonymus europaea L. (spindle tree)*, Forsythia sp.,

Fraxinus excelsior L. (ash), Humulus lupulus L. (hop),

Jasminum officinale L., Lactuca sativa L. (lettuce),

Ligustrum vulgäre L. (privet), Melilotus officinalis Lam.

(sweet clover), Narcissus spp.*, Phaseolus multiflorus

Willd. (scarlet runner bean). Prunus avium L. (sweet

cherry)*, P. domestica L. (plum)*, P. pérsica Batsch

(peach)*. Rheum rhaponticum L. (rhubarb)*, Rosa spp.

(rose)*, Syringa vulgaris L. (lilac), Trifolium repens L.

(white clover)*. Tulipa spp. (tulip), Vitis vinifera L.

(grapevine)*.

Wild Plants

Anagallis arvensis L., Arabis hirsuta (L.) Scop., Bellis

perennis L., Capsella bursa-pastoris (L.) Medic.*, Lamium

amplexicaule L.*, Mentha arvensis L.*, Plantago lanceolata

L., Polygonum aviculare L., P. persicaria L., Ranunculus

repens L., Sambucus nigra L.*, Senecio vulgaris L.*,

Stellaria media (L.) Vill.*, Taraxacum officinale Weber*,

Urtica dioica L.*, U. urens L.

204
Table 11.—Susceptibility of red raspberry and blackberry cultivars to British isolates of raspberry

ringspot virus, tomato black ring virus, arabis mosaic virus, and strawberry latent

ringspot virusi

RRV RRV TBRV

(common (yellow (common AMV SLRV

Scottish blotch Scottish (common (common

Cultivar strain) strain) strain) strain) strain)

Red raspberry:

Baumforth's Seedling B + • • • •

Burnetholm - + + -

•

Cuthbert - + • • •

Glen Clova + • + + -

Glen Isla + + + + +

Lloyd George - + - -( + ) -

Mailing Admiral + - - + +

Mailing Delight + + + + -

Mailing Enterprise + + - - +

Mailing Exploit + + + + +

Mailing Jewel + (E) + - -( + ) +

Mailing Landmark - + -

• -

Mailing Leo - - + - -

Mailing Notable + • - -

•

Mailing Orion + + - - -h

Mailing Promise + (E) + - + +

Norfolk Giant + + + -( + ) -

Preussen -f • • • •

St. Walfried + + • • •

Seedling M - + -

• •

Seedling V - + + • •

Blackberry:

Himalaya Giant •(E) • • • +

Tayberry + - -

• —

^Data are based on graft-transmission tests supplemented by data on field infection.

Note: + = susceptible; ( + ) = susceptible to some strains; (E) found infected with isolates of the English serotype;

- = considered immune; »^not tested.

Symptoms on red raspberry. Table 11 lists the susceptibility of red raspberry cultivars to British isolates of AMV and

SLRV. There is evidence that AMV strains differ in ability to

infect some raspberry cultivars. Thus, 'Lloyd George' and

'Norfolk Giant' seem immune to common isolates of AMV,

but AMV-infected plants of these cultivars were found in

Scotland by Taylor et al. (1966), Subsequent grafttransmission tests by J. Chambers and A. F. Murant

(unpublished data) showed that this AMV isolate infected not

only 'Lloyd George' and 'Norfolk Giant' but also 'Mailing

Jewel', a cultivar that has consistently failed to become

infected with AMV at other sites (Taylor and Thomas 1968;

Dale and Brown 1973), although becoming infected with

SLRV. By contrast, the cv. 'Glen Clova' is susceptible to

AMV but does not become infected with SLRV.

As with other nematode-borne virus diseases, outbreaks of

AMV and SLRV occur in patches (fig. 244), reflecting the

horizontal distribution of vector nematodes in the soil.

However, if the disease results from the planting of infected

stocks, the infected plants are of course distributed randomly

throughout the crop. AMV-infected 'Mailing Exploit' plants

show symptoms 2 to 3 yr after planting; the young canes are

stunted, and produce little or no fruit, and yellow speckling

appears on the leaves (fig. 245A); conspicuous veinyellowing or yellow net symptoms (fig. 2455) may appear on

the lower leaves. AMV induces similar symptoms in the

cultivars 'Mailing Promise' and 'Mailing Admiral', but

causes leaf mottling in infected plants of 'Glen Clova' (fig.

246).

205
Figure 244. — An outbreak of strawberry latent

ringspol virus in 'Mailing Jewel' raspberry in Scotland.

(After Taylor and Thomas 1968: copyright Scottish

Crop Research Institute.)

I B

Figure 245. — Leaves of arabis mosaic virus-Infected

'Mailing Exploit' raspberry showing; A, yellow speckling; B. vein-yellowing. (After Harrison 1958: copyright Scottish Crop Research Institute.)

206
Figure 246. — Leaf of arabis mosaic virus-infected

'Glen Clova' raspberry, showing mottle symptoms.

(After Murant 1981b: copyrigiit Scottish Crop Research

Institute.)

It is not known what symptoms SLRV induces in most red

raspberry cultivars because it is usually found together with

AMV. Lister (1964) reported that the few 'Mailing Exploit'

plants found infected with SLRV alone were symptomless,

and plants containing both viruses looked similar to plants

infected with AMV alone. However, Taylor and Thomas

(1968) found that 'Mailing Jewel' raspberry infected with

SLRV alone were severely stunted (fig. 244) and showed

foliar symptoms closely resembling those induced by AMV

in 'Mailing Exploit', except that vein-yellowing was not

observed. Lateral shoots on the fruiting canes were poorly

developed or dead, and the leaves were down-curled and

yellow-blotched; leaves on primocanes showed yellow

speckling (fig. 247).

Symptoms on blackberry. Leaves of 'Himalaya Giant'

blackberry infected with AMV showed yellow mosaic

(Harrison 1958c).

Symptoms on other cultivated plants. For the symptoms

induced by AMV and SLRV in Fragaria and Ribes. see those

sections of this handbook, p. 46, 131, 139 and 148.

In association with viruses of the prunus necrotic ringspot

type, AMV induces rasp-leaf symptoms in cherry (Cropley

796/; East Mailing Research Station 1963). In mixed

infections with prune dwarf virus, SLRV induces a severe

decline disease of peach (Scotto la Massese et al. 1973).

Symptoms induced by AMV in some other crops are

Figure 247. — Leaf of strawberry latent ringspot

virus-infected 'Mailing Jewel' raspberry, showing

yellow speckling. (After Taylor and Thomas J968;

copyright Scottish Crop Research Institute.)

described by the following authors: scarlet runner bean,

celery, white clover, and marrow (Harrison and Winslow

1961); cherry (Cropley 1961); cucumber (Hollings 1963);

hop (Bock 7966); lettuce (Walkey 1967a). Symptoms

induced by SLRV were described by the following: celery

(Walkey and Mitchell 1969); rose (Harrison 7967; Ikin and

Frost 7976).

Symptoms on Experimental Hosts

Both AMV and SLRV have wide experimental host ranges

and infect nearly all commonly used herbaceous test plants.

In detailed investigations of host range, AMV infected 93

species in 28 families (Schmelzer 7962) and SLRV infected

126 species in 27 families, most of them symtomlessly

(Schmelzer 7969).

The following are some useful diagnostic hosts:

Chenopodium amaranticolor Coste and Reyn., C. murale L.,

and C. quinoa Willd.

AMV and SLRV: Chlorotic or necrotic local lesions (figs.

248 and 249); systemic chlorotic mottle (fig. 250) or

necrosis.

Citcimiis sativas L.

AMV: Chlorotic local lesions; systemic yellow spots or

vein-banding, subsequently fading. The plants then stop

growing.

SLRV: Chlorotic local lesions or none, systemic interveinal

chlorosis or necrosis (fig. 251). In summer, subsequent

leaves are symptomless but contain virus; in winter,

symptoms may persist.

207
Figure 248. — Local lesions induced by arabis mosaic

virus in Chenopodhim amaranlicolor. (After Harrison

¡958: copyright Scottish Crop Research Institute.)

Figure 250. — Systemic symptoms induced by arabis

mosaic virus in Chenopodium amaranlicolor. (After

Murant 1970: copyright Scottish Crop Research Institute.)

Figure 249. — Local lesions induced by strawberry

latent ringspot virus in Chenopodium murale. (After

Murant 1970: copyright Scottish Crop Research Institute.)

Nicotiana tabacum L. cv. 'White Burley'

AMV: Chlorotic or necrotic local lesions. Some isolates give

systemic yellow spots and rings (fig. 252) and line patterns.

Leaves produced later appear almost normal but contain

virus.

SLRV: Symptomless systemic infection.

Petunia hybrida Vilm.

AMV: Local chlorotic lesions or necrotic rings. Systemic

vein-clearing or chlorotic rings and line patterns. Leaves

produced later are symptomless but contain virus.

SLRV: Symptomless systemic infection.

Figure 251. — Systemic irucrveinal chlorosis induced

by strawberry latent ringspot virus in Cucumis sativus.

(After Murant 1974: copyright Scottish Crop Research

Institute.)

208
Figure 252. — Yellow spots and rings in a systemically

infected ieaf oí Nicoliana labacum cv. 'White Burley'.

(After Harrison I951Í: copyright Scottish Crop Research

Institute.)

Isolates of both viruses differ in virulence, and symptoms in

most hosts are milder in summer than in winter.

Petunia hybrida and Nicotiana clevelandii Gray are good

hosts in which to propagate AMV. Local lesions on

Chenopodium amaranticolor can be used to assay virulent

isolates of AMV, but local lesions caused by mild isolates are

too indistinct to count. For SLRV, Cucumis sativus is the

best host for propagation and Chenopodium murale the most

reliable local lesion host. Cucumis sativus and Petunia

hybrida are useful "bait" plants for use in nematode

transmission experiments with both viruses. These plants

rarely become systemically infected or show symptoms

following inoculation of the roots by nematodes, but the

viruses may be detected in the roots or hypocotyls by

inoculation of sap to Chenopodium quinoa.

Natural and Experimental Transmission

Both viruses are transmissible by grafting, by inoculation

with sap, and through seed. Their natural vectors are

nematodes in the genus Xiphinema.

Transmission of AMV and SLRV to herbaceous plants by

inoculation with sap from rosaceous plants is greatly

facilitated if inocula are prepared at pH 8 with 2% nicotine or

1% polyethylene glycol (mol. wt. 6000), or if powdered

alumina is added to the inoculum; these additives prevent

tannins from inhibiting infection.

Transmission through seed has been shown for AMV in at

least 16 species in 12 plant families (Lister 7960; Lister and

Murant 1967: Walkey 1967b) and for SLRV in at least 6

species (Taylor and Thomas 1968: Murant and Goold 1969:

Schmelzer 1969: Allen et al. 1970: Walkey and Whittingham-Jones 1970). In many host species, more than 10%, and

in some nearly 100%, of progeny seedlings are infected,

commonly without showing symptoms.

The main vector of both viruses is the nematode Xiphinema

diversicaudatum (Harrison and Cadman 1959: Jha and

Posnette 1959: Lister 1964). Consequently, they often occur

together in soils. In addition, there are unconfirmed reports of

transmission of AMV by X. coxi (Fritzsche 1964) and X.

bakeri (Iwaki and Komuro 1974) and of SLRV by X. coxi

(Putz and Stocky 1970). Both larvae and adults of X.

diversicaudatum transmit both viruses (Harrison and Cadman

1959: Harrison 1967: Taylor and Thomas 1968: Putz and

Stocky 1970), but moulted nematodes do not retain AMV

(Harrison and Winslow 1961) or, probably, SLRV. Jha and

Posnette (1961) found that X. diversicaudatum acquired

ability to transmit AMV after access to infected plants for 1

day, could inoculate bait plants in 3 days, and continued to

transmit AMV after 31 days in fallow soil. Harrison and

Winslow (¡961) found that X. diversicaudatum was still able

to transmit AMV after 8 mo on the virus-immune raspberry

cultivar 'Mailing Jewel'. SLRV and AMV were retained for

up to 84 and 112 days, respectively, in X. diversicaudatum

kept in fallow soil (Taylor and Thomas 1968). By analogy

with other nematode-transmitted viruses, the viruses can

probably be acquired within a few minutes, can be inoculated

in a single brief feed, and do not multiply in the vector or

circulate within it (Taylor 1980). Particles of both viruses are

associated in a monolayer with the cuticle lining of the lumen

of the odontophore, esophagus and esophageal bulb (Taylor

and Robertson 1970: Taylor 1980).

Little comparative work has been done on the transmissibility

of serological forms of AMV by nematodes, but serological

variants of SLRV from peach and raspberry in Italy were not

transmitted by a Scottish population of X. diversicaudatum

that transmitted the type strain efficiently; moreover,

nematodes of an Italian population of X. diversicaudatum

were only inefficient vectors of the three SLRV isolates and

of the type strain of AMV (Brown and Taylor 1981).

Within an outbreak area, AMV and SLRV are spread by X.

diversicaudatum, but because the nematodes do not withstand airdrying of soil they do not carry the viruses efficiently

over a distance. There is also little lateral migration of the

vector, and outbreaks extend only slowly. The viruses are

probably disseminated in nature in infected seeds, as are

raspberry ringspot and tomato black ring viruses (Lister and

Murant 1967: Murant and Lister 1967). (See "Raspberry

Ringspot and Associated Diseases of Rubus. . .," p. 211.) The

presence of infected seeds in soils, however, is less important

for the survival of AMV and SLRV through periods of fallow

than for raspberry ringspot and tomato black ring viruses,

which persist for only 8 to 9 wk in their vector, Longidorus

elongatus. Soils from outbreaks of AMV and SLRV seem, in

fact, to contain relatively few infected weed seeds (Murant

and Lister 7967; Taylor and Thomas 796S). The role of wild

plants in the ecology of these and other nematode-borne

viruses was discussed by Murant (1970b, 1981b).

209
Properties of the Causal Agent

AMV is a definitive member of the nepovirus group; SLRV

has many similar properties and has long been regarded as a

nepovirus but is now considered only a tentative member of

the group because of its anomalous protein composition

(Harrison and Murant 1977b; Murant 1981a).

AMV. For a detailed description of the virus, see Murant

(1970a). In Petunia hybrida sap, the virus loses infectivity

after dilution to I0-' to 10', after 10 min at 55° to 61°C, or

after 1 to 2 wk at room temperature (Harrison 1958c); some

workers report longer survival at room temperature (Hollings

1963; Schmelzer 1962). Infectivity survives for many years

at -15°C. The virus may be purified by the butanol/

chloroform method (Harrison and Nixon 7960) or by the

procedure described on p. 218 for raspberry ringspot virus

(Murant et al. 1972; Murant 1978). The virus particles are

isometric, about 28 nm in diameter, with hexagonal outlines

(fig. 253A); some of them are penetrated or partially

penetrated by negative stain, others are not penetrated. The

particles form three sedimenting components, T, M and B,

with sedimentation coefficients (s^o, w) of 53, 93, and 126 S,

respectively (R. Stace-Smith, personal communication). The

coat protein is a single species of mol. wt. 54,000 (Mayo et

al. 1971), and the genome consists of two species of

single-stranded RNA with mol. wt. ( x 10") of 2.8 and 1.3

(Murant et al. 1981).

Although serological variability exists in AMV (Bock 7966;

Bercks et al. 7976), most isolates are not greatly dissimilar;

however, grapevine fanleaf virus is a distantly related

serotype.

SLRV. For a detailed description of the virus, see Murant

(1974a). In Chenopodium quinoa sap, the virus isolates

studied by Lister (1964) lost infectivity after dilution to 10"'

to 10' or after 10 min at 52° to 58°C but were still infective

after 50 days at room temperature. Some other isolates

survived less well in vitro (Tomlinson and Walkey 7967;

Richter and Kegler 7967). The virus may be purified by

various methods: clarification with butanol/chloroform

(Lister 7964), or ether/carbon tetrachloride (Richter and Proll

1970), or clarification with chloroform followed by precipitation with ammonium sulphate (Allen et al. 7970), or use of

Mg-activated bentonite (Savino et al. 7979). The virus

particles are isometric, about 30 nm in diameter, with

hexagonal outlines. Some are penetrated by negative stain

and others are not (fig. 253ß). Purified preparations often

contain three components, bottom (B), middle (M), and top

(T). The major component (B), sediments at 126 to 130 5;

sometimes components sedimenting at about 58 5 (T) and 94

S (M) are also present. There are two coat protein species of

mol. wt. 44 000 and 29 000 (Mayo et al. 7974), and the

genome consists of two species of single-stranded RNA with

mol. wt. ( X 10") of 2.9 and 1.4 (Mayo et al. 1974; Murant

et al. 1981). Particles of some isolates contain a third RNA

species with a molecular weight of about 0.5 x 10', which

may be a "satellite" (Mayo et al. 7974).

ligure 2.Ï.Î. — Virus particles in phospholungstate, pH

6: A. Particles of arabis mosaic virus; B. particles of

strawberry latent ringspot virus. The smaller particles in

both pictures are phytoferritin. Bars represent 100 nm.

(Copyright Scottish Crop Research Institute.)

All isolates of SLRV studied until recently were serologically

very similar, but isolates from olive and peach in Italy

(Savino et al. 7979) and an isolate from raspberry, also in

Italy (A. F. Murant, unpublished data), were distinguishable

from type strain by spur formation in gel diffusion tests.

Detection and Identification

The patchy distribution of the disease, stunted plants, and

characteristic leaf symptoms enable the presence of a

nematode-bome virus to be readily diagnosed. To discover

which of several possible viruses is present, the plants must

be tested by inoculation of sap to herbaceous indicators. Any

viruses transmitted must be identified by serological tests (for

example, by gel diffusion tests with sap from infected

Chenopodium quinoa) because the reactions of test plants are

not sufficiently distinctive to enable the viruses to be

distinguished from each other or from mild strains of other

nepoviruses.

Control Procedures

Use of certified virus-tested planting material. Both viruses

may be distributed in infected planting material especially

because few or no symptoms are visible in tolerant cultivars

or in the eariy stages of infection in sensitive cultivars. This

source of infection can be eliminated by introducing adequate

certification schemes for the production of virus-tested stock.

Such schemes should require that stocks for certification are

not established in soil containing vector nematodes.

Use of immune cultivars. If the outbreak in a sensitive

cultivar is small, only affected plants need to be removed and

replaced with plants of an immune cultivar (see table 11).

Immunity to AMV in red raspberry is inherited as a dominant

210
character, but at least two genes are concerned (Jennings

1964). No studies on the inheritance of immunity to SLRV

have been made.

Chemical control ofvector nematodes. Treatment ofsoil with

the fumigants D-D (dichloropropene-dichloropropane) or

methyl bromide prevented Xiphinema diversicaudatum from

transmitting AMV in strawberry (Harrison et al. 1963; Dale

and Hendy 1967). Similar fumigant nematicides, such as

dazomet or dichloropropene (the active constituent of D-D),

are now used commercially.

Thermotherapy. No information is available on the response

of AMV or SLRV to thermotherapy in Rubus.

Remarks

The symptoms induced by isolates of AMV and SLRV in

herbaceous indicators are similar to those induced by many

other Rubus-inítcúng viruses, especially by members of the

nepovirus group such as cherry leaf roll, raspberry ringspot,

tomato black ring, tomato ringspot, and tobacco ringspot

viruses. (See papers in the Rubus section devoted to these

viruses, p. 211-228.) Moreover, all these viruses have very

wide host ranges and naturally infect many other wild and

cultivated plants. Serological tests are the only satisfactory

method of identification.

1^i4Raspberry Ringspot and Associated Diseases of Rubus

Caused by Raspberry Ringspot and Tomato Black Ring

Viruses//

By A. F.JMurant

Additional Common Names

Raspberry leaf curl (Harris et al. 1943); raspberry Scottish

leaf curl (Review of Applied Mycology 7957); Lloyd

George yellow blotch (Cadman and Harris 7952).

History and Geographic Distribution

The name "leaf curl" was applied by Harris et al. (1943) to a

graft-transmissible disease of 'Norfolk Giant' red raspberry

(Rubus idaeus L.) occurring in Scotland. It seemed the same

as a disease first noticed in 1922 in 'Baumforth's Seedling

B'. A sap-transmissible, soil-borne virus named raspberry

ringspot virus (RRV) (Cadman 1956; Harrison 1956, 1958a)

was found to cause this disease and also to occur in many

other red raspberry cultivars showing ringspots, leaf

blotches, stunting, and decline symptoms. The "yellow

blotch" disease of the cv. 'Lloyd George' (Cadman and

Harris 7952) is also caused by a strain of RRV (Murant et al.

1968). Another soil-borne virus, tomato black ring virus

(TBRV) (Smith 1946), was found to cause a similar disease

in 'Mailing Exploit' and 'Seedling V (Harrison 1958b) and

later in many other cultivars, including 'Norfolk Giant'. Both

viruses proved to be transmitted by nematodes in the genus

Longidorus. Strains of the viruses occurring in Scotland

share the same vector, L. elongatus de Man (Harrison et al.

7967; Taylor 1962) and therefore usually occur together in

the same outbreak areas.

In most red raspberry cultivars, RRV and TBRV cause

ringspots on the leaves rather than leaf-curl symptoms.

Because of this, and also because the disease caused by

TBRV is very similar to that caused by RRV in some

cultivars and has never been separately named, Cadman

(1961b) suggested that "raspberry ringspot" was a better

name than "leaf curl" for the disease caused by either or both

viruses. Raspberry ringspot is, however, etiologically

distinct from American red raspberry ringspot disease,

caused by tomato ringspot virus (also nematode-bome) (see

"Tomato Ringspot Virus in Rubus,'' p. 223) and from

American raspberry leaf curl disease, caused by an aphidborne virus (see "Raspberry Leaf Curl," p. 187).

RRV and TBRV are widespread in eastern Scotland,

although of local occurrence, and are also reported in other

parts of Great Britain and in continental Europe and

U.S.S.R. RRV is also reported in Turkey, and TBRV in

Japan. In raspberry, RRV is reported in Great Britain and

The Netherlands, is widespread in the U.S.S.R. (GordejcLuk

et al. 7977; M. A. Keldysh, personal communication), rnd

has also been found in Hungary (E. Pocsai, personal

communication); infection of raspberry with TBRV is

reported in Great Britain and occurs rarely in the U.S.S.R.

(M. A. Keldysh, personal communication). Vector nematodes (Longidorus spp.) occur in all these countries (Hooper

1973; Brown and Boag 7975, 7977); L. elongatus is also

reported locally in Canada, United States and New Zealand

(Hooper 1973), but the viruses are not reported there.

Economic Importance

RRV causes a lethal disease in some raspberry cultivars, and

economic losses may be considerable if the outbreak is large.

TBRV is usually less damaging, but both viruses may

decrease the yield of "tolerant" cultivars, as happens with

TBRV in 'Mailing Exploit' (Taylor et al. 7965). In

Scotland, diseases caused by both viruses are now effectively

controlled and are of much less economic importance than

formerly.

The viruses cause few or no symptoms in the early stages of

infection and may therefore be inadvertently distributed in

infected planting material. This can result not only in losses

of crop but also in the viruses becoming established in soils

already containing vector nematodes. These viruses are also a

potential problem in the international exchange of planting

material.

Symptoms on Natural Hosts

Both RRV and TBRV occur naturally in red raspberry (Rubus

idaeus L.); RRV is also reported from blackberry (R.

procerus P. J. Muell cv. 'Himalaya Giant') (Cadman 1960b)

211
Figure 254. — An uuibicak ol raspberry ringspol in a

plantation of 'Mailing Jewel' raspberry in eastern

Scotland. (After Harrison 1958b: copyright Scottish

Crop Research Institute.)

and Ruhus sachalinensis Léveillé (Gordejchuk et al. 1977).

Both viruses also infect plants in the small fruit genera

Fraaciria and Ribes. (See these sections of this handbook, p.

46, 131, 140, and 146.)

Many other cultivated and wild plants have been found

naturally infected with both viruses. A selection of plants

found infected with TBRV is listed below; those in which

RRV has also been found are indicated by an asterisk.

Cultivated Plants

Alliiim ascalonicum L. (shallot), A. cepa L. (onion), A.

porrum L. (leek), A. schoenoprasum L. (chives), Apiiim

graveolens L. var. dulce Mill, (celery). Asparagus officinalis L. (asparagus), Beta vulgaris L. subsp. saccharifera

(sugarbeet)*, Brassica olerácea L. (cabbage), B. napus L.

(rape), B. napobrassica DC. (swede), B. rapa L. (turnip),

Cucumis sativus L. (cucumber). Daucus carota L. (carrot).

Lactuca sativa L. (lettuce), Lolium perenne L. (ryegrass),

Lycopersicon esculentum Mill, (tomato), Medicago sativa L.

(lucerne, alfalfa). Narcissus pseudo-narcissus L. (daffodil)*.

Pastinaca sativa L. (parsnip), Petroselinum crispum (Mill.)

Nym. (parsley). Prunus amygdalus Batsch (almond), P.

avium L. (cherry)*, P. pérsica Batsch (peach), Solanum

tuberosum L. (potato), Trifolium repens L. (white clover).

Tulipa gesneriana L. (tulip), Vitis vinifera L. (grapevine)*.

Wild Plants

Capsella bursa-pastoris (L.) Medic.*, Cerastium vulgatum

L.*, Geranium dissectum L., Lamium amplexicaule L.,

Myosotis arvensis (L.) Hill*, Polygonum aviculare L.,

P. convolvulus L.*, Spergula arvensis L.*, Stellaria media

(L.) Vill.*, Veronica agrestis L.*, V. pérsica Poir*.

Symptoms on red raspberry. Table 11 (p. 205) lists the

susceptibility of red raspberry cultivars to British isolates of

RRV and TBRV. In soils containing both RRV and TBRV,

some raspberry cultivars may become infected with only one

of the viruses because they are immune to the other. Thus,

the widely grown cv. "Mailing Jewel' is immune to TBRV.

Several cultivars, notably 'Lloyd George", "Mailing Landmark', and "Seedling M', are immune both to TBRV and to

common strains of RRV; however, a resistance-breaking

strain of RRV is known and is the cause of '"yellow blotch"

disease (Cadman and Harris 1952; Murant et al. 1968).

212
Outbreaks of disease caused by RRV and TBRV occur in

patches, whicii may vary from a few square meters to a few

hectares in extent, reflecting the horizontal distribution of the

vector in the soil (fig. 254). However, if the disease results

from the planting of infected stocks, the infected plants are of

course scattered randomly throughout the crop. In Great

Britain, because spread of the viruses is now effectively

controlled, the field reaction of some newer cultivars is

unknown. The symptoms in long-established cultivars are as

follows:

RRV. Conspicuous chlorotic ringspots appear on the

leaves (fig. 255), usually in the spring following the year of

infection, but they may become less distinct or disappear

altogether in midsummer, often to return in the autumn. In

addition, some cultivars, notably "Baumforth's Seedling B"

and 'Norfolk Giant', show typical leaf-curl symptoms (fig.

256): the leaves exhibit a pronounced downward curling, and

are crisp and brittle to the touch. Plants of "Baumforth's

Seedling B', 'Glen Clova', 'Mailing Enterprise', "Mailing

Jewel', 'Mailing Notable', 'Norfolk Giant', and 'Preussen'

produce stunted, brittle canes, and may die within 2 to 3 yr of

the first appearance of leaf symptoms. Infected plants of

other cultivars are usually less vigorous than healthy ones,

but are not killed, and often show few or no leaf symptoms.

T3RV. This virus causes a severe disease in the old cv.

'Seedling V (Harrison 1958b), affected plants producing

many short, spindly, and brittle young shoots with ill-defined

chlorotic markings on the leaves. However, it causes

relatively mild symptoms in most other cultivars. 'Mailing

Exploit' develops faint chlorotic mottling or ringspots (fig.

257) on the leaves but is otherwise little affected in the first

few years after infection. Later, the canes are somewhat

stunted, yield is decreased, and the fruit is deformed

(""crumbly": fig. 258) due to abortion of some of the drupelets

(Taylor et al. 1965). 'Norfolk Giant' develops leaf-curling

symptoms similar to those induced by RRV but is otherwise

little affected by TBRV. whereas plants infected by RRV are

killed.

Symptoms on blackberry. RRV-infected plants of 'Himalaya Giant' blackberry {Rubus procerus P. J. Muell.) were

stunted (Cadman 1960b), but a detailed description of

symptoms was not given.

Symptoms on R. sachalinensis. Symptoms were similar to

those in cultivated raspberry (Gordejchuk et al. 1977).

Symptoms on other cultivated plants. For the symptoms

induced by RRV and TBRV in Fragaria and Ribes, see these

sections of this handbook, p. 46 and 131. RRV, in association

with viruses of the prunus necrotic ringspot type, causes raspleaf symptoms in cherry (Cropley 1961; East Mailing Research

Station 1963). Symptoms produced by TBRV in some other

crops are described by the following authors: sugarbeet

Figure 255. — Chlorotic ringspot symptoms in leaf of

Mailing Jewel" raspberry Infected with raspberry

ringspot virus. (After Cadman 1956: copyright Scottish

Crop Research Institute.)

Figure 256. — Leaf curl symptom in "Norfolk Giant'

raspberry infected with raspberry ringspot virus. (After

Murant 1981b: copyright Scottish Crop Research

Institute.)

213
Figure 257. — Diffuse chiorotic ringspots in leaf of

'Mailing Exploit' raspberry infected with tomato black

ring virus. (After Taylor et al. 1965: copyright Scottish

Crop Research Institute.)

'»Jo,'

Figure 258. — Fruit of 'Mailing Exploit' raspberry,

(left) healthy, (right) infected with tomato black ring

virus showing "crumbly fruit" symptoms. (After Taylor

et al. 1965: copyright Scottish Crop Research Institute.)

Figure 259. — Lesions induced by raspberry ringspot

virus in inoculated \cdf oí Chenopodiiim amaranticolor.

(After Murant 19Hlh: copyright Scottish Crop Research

Institute.)

(Harrison 7957); celery (Hollings 1965); grapevine (Stelimach 7970); lettuce (Smith and Short 1959); leek and onion

(Calvert and Harrison 1963); potato (Gehring and Bercks

¡956; Harrison 1959); swede and turnip (Harrison 1957);

tomato (Smith 1946).

Symptoms on Experimental Hosts

Both RRV and TBRV have very wide experimental host

ranges and infect nearly all commonly used herbaceous test

plants. RRV infected species in more than 14 dicotyledonous

families (Murant 1978) and TBRV infected species in more

than 29 dicotyledonous families (Schmelzer 1963). The

following are some useful diagnostic hosts:

Chenopodium amaranticolor Coste and Reyn.

RRV: Chiorotic or necrotic local lesions (fig. 259); no

systemic infection.

TBRV: Chiorotic or necrotic local lesions; systemic necrosis

or chiorotic mottle (fig. 260).

Chenopodium quinoa Willd.

RRV and TBRV: Chiorotic or necrotic local lesions; systemic

chiorotic mottle or necrosis (fig. 261).

Nicotiana clevelandii Gray

RRV and TBRV: Local necrotic spots and rings; systemic

veinal necrosis (fig. 262). Leaves produced later appear to

"recover," that is, they look normal but contain virus.

214
Figure 260. — Local and systemic symptoms induced

by tomato black ring virus in C. amaranticolor. (After

Murant 1981b; copyright Scottish Crop Research

Institute.)

Figure 261. — Systemic symptoms induced by raspberry ringspot virus in C. quinoa. (After Murant 1978;

copyright Scottish Crop Research Institute.)

Figure 262. — Local necrotic rings and systemic veinal

necrosis in Nicoliana clevelandii infected with tomato

black ring virus. (After Murant 1981b: copyright

Scottish Crop Research Institute.)

Figure 263. — Systemic symptoms induced by raspberry ringspot virus in N. rustica. (After Murant J978;

copyright Scottish Crop Research Institute.)

Nicotiana rustica L.

RRV and TBRV: Local chlorotic or necrotic spots or rings;

systemic rings and line patterns with variable amounts of

necrosis (fig. 263). Leaves produced later appear to

"recover," that is, they look normal but contain virus. The

'Lloyd George' yellow blotch strain of RRV gives

symptomless local and systemic infection.

215
Figure 264. — Systemic symptoms induced by tomato

black ling vims in N. tabacum cv. 'Xanthi'. (After

Murant 198lh: copyright Scottish Crop Research

Institute.)

Nicotiana tabacum L. cvs. 'White Burley' or 'Xanthi'.

RRV: Chlorotic local lesions; scattered systemic chlorotic

spots and rings. Not infected by the 'Lloyd George" yellow

blotch strain (table 11).

TBRV: Local necrotic spots and rings; systemic chlorotic and

necrotic spots, rings, and line-patterns (fig. 264). Leaves

produced later appear to "recover," that is, they look normal

but contain virus (fig. 265).

Phaseolus vulgaris L. cv. 'The Prince'.

RRV: In winter in Great Britain, dark-brown necrotic local

lesions 0.5 mm in diameter (fig. 266); in summer, chlorotic

lesions or symptomless. Systemic symptoms are chlorotic

mottle with variable amounts of necrosis and distortion (fig.

267). The 'Lloyd George" yellow blotch strain gives

symptomless local infection and does not invade the plants

systemically.

TBRV; In winter in Great Britain, dark-brown local lesions 2

mm in diameter (fig. 268); in summer, chlorotic lesions or

symptomless. Systemic symptoms are chlorotic mottle with

variable amounts of necrosis and distortion.

Petunia hybrida Vilm.

RRV and TBRV: Chlorotic local lesions, sometimes with

brown necrotic margins; systemic veinal chlorosis or

necrosis, or line-patterns. With TBRV, leaves produced later

are symptomless but contain virus ("recovery"). RRV tends

to produce persistent yellow rings and line-patterns (fig. 269)

in addition to symptomless leaves; some strains of RRV

induce a prominent overall yellowing or bleaching (Harrison

et al. 1972b, 1974). The 'Lloyd George' yellow blotch strain

of RRV gives symptomless local and systemic infection.

Isolates of both viruses differ considerably in virulence, but

Chenopodium amaranticolor and C. quinoa develop symptoms with all isolates. Most hosts show milder symptoms in

summer than in winter.

Figure 265. — Systemic symptoms (lower leaves)

followed by apparent recovery (upper leaves) in N.

tabacum cv. 'Xanthi' infected with tomato black ring

virus. (After Murant 1981b: copyright Scottish Crop

Research Institute.)

- ' * '*.

Figure 266. — Lesions induced by raspberry ringspot

virus in inoculated leaf of/"/IU.çPO/H.V vulgaris cv. 'The

Prince'. (After Harrison ¡958a: copyright Scottish Crop

Research Institute.)

216
i^l^

'^jéL ïFigure 267. — Systemic symptoms induced by raspberry ringspot virus in P. vulgaris cv. 'The Prince'. (After

Murant I98lh: copyright Scottish Crop Research

Institute.)

^^ <>5

* <

Figure 268. — Lesions induced by tomato black ring

virus in inoculated leaf of P. vulgaris cv. 'The Prince'.

(After Harrison 1957: copyright Scottish Crop Research

Institute.)

Figure 269. — Systemic symptoms induced by raspberry ringspot virus in Peliiniii hyhrida. (After Harrison

l95Hii: copyright Scottish Crop Research Institute.)

Both viruses may be propagated in Nicotiuna clevelandii or

Petunia hybrida and may be assayed by counting local

lesions in Chenopodium amaranticolor. C. qidnoa and P.

hyhrida are convenient "bait" plants for use in nematodetransmission experiments; these plants rarely become systemically infected or show symptoms following inoculation of

the roots by nematodes, but the viruses may be detected in

the roots or hypocotyls by sap inoculation to the leaves of

further C. qidnoa test plants.

Natural and Experimental Transmission

Both viruses are transmissible by grafting, by sap inoculation, and through seed. Their natural vectors are nematodes

in the genus Longidorus.

Transmission of the viruses to herbaceous plants by

inoculation with sap from rosaceous plants is greatly

facilitated if inocula are prepared at pH 8 with 29c nicotine or

1% polyethylene glycol (mol. wt. 6000), or if powdered

alumina is added to the inoculum. These additives prevent

tannins from inhibiting infection. Transmission by inoculation with sap from herbaceous plants to rosaceous plants is

extremely difficult.

Lister (I960) and Lister and Murant [1967) showed that both

viruses are seed-borne in a wide range of host plants,

including raspberry, strawberry, and many weed species.

There are usually no symptoms in infected progeny

seedlings. The viruses are transmitted through seed to up to

20% of raspberry progeny and up to 40% of strawberry

progeny via either gamete; however, the presence of

competing virus-free pollen greatly decreases the ability of

pollen from infected plants to fertilize ovules. Transmission

through pollen may therefore be of little importance in

nature. Healthy plants pollinated with pollen from infected

plants do not become infected.

Scottish strains of RRV and TBRV share a common vector,

Longidorus elongatus de Man (Taylor 1962; Harrison et al.

1961) and therefore often occur together in the same outbreak

217
area. In contrast, English and Continental European strains

of RRV and TBRV, which are serologically distinguishable

from Scottish strains, are transmitted only inefficiently by L.

elongciius; their natural vectors are, respectively, L.

macrosoma Hooper and L. attematus Hooper (Harrison

¡964: Taylor and Murant 1969). Because these nematodes

have different soil-type preferences, English strains of RRV

and TBRV tend to occur in separate sites.

L. elongatus kept in fallow soil retains infectivity with RRV

and TBRV as long as 8 or 9 wk (Murant and Lister

7967; Taylor 7970). L. macrosoma retains the English strain

of RRV for at least 34 days (Debrot 1964). Both viruses are

transmitted by larvae and adults of L. elongatus (Harrison et

al. 7967,- Taylor 7962; Yassin 796S), but they do not pass

through the egg, nor are they retained by the nematode after

moulting (C. E. Taylor, unpublished data). By analogy with

other nematode-bome viruses, it seems unlikely that RRV or

TBRV multiply in their vectors or circulate within them

(Taylor ¡980). Particles of both viruses are associated in a

specific manner with the stylet lumen or guiding sheath of

Longidorus spp. (Taylor and Robertson 7969). The vector

specificity of the viruses is determined by the composition of

their coat proteins (Harrison et al. 1974: Harrison and Murant

7977a).

Within an outbreak area, the viruses are spread by the vector

nematodes, but because the nematodes do not withstand

airdrying of soil they do not carry the viruses efficiently over

a distance. Since there is little lateral migration of the vector,

outbreaks extend only slowly. The viruses are probably

disseminated in nature in infected seeds, and these are also

important as a continuing reservoir of the viruses in the soil,

enabling them to survive periods of fallow or fasting of the

vector (Murant and Taylor 7965; Murant and Lister 7967).

The role of wild plants in the ecology of these and other

nematode-borne viruses was discussed by Murant (1970b,

1981b).

Properties of the Causal Agents

Both viruses are members of the nepovirus group (Harrison

and Murant 1977b: Murant 1981a) and have many similar

properties.

RRV. For a detailed description of the virus, see Murant

(1978). In Nicotiana rustica sap, the virus loses infectivity

after dilution to 10^' to lO"*, or after 10 min at 65 to 70°C or 2

to 3 wk at room temperature (Harrison 1958b). It survives for

many years in sap at -15°C. The virus may be purified

(Murant et al. 7972; Murant 1978) from A', clevelandü

extracts by adding «-butanol to 8.5% (v/v) and centrifuging

at low speed. The virus is then precipitated from the

supernatant fluid by adding polyethylene glycol (mol. wt.

6000) to 10% (w/v) and NaCl to 1% (w/v) and concentrated

further by differential centrifugation. The virus particles are

isometric, about 28 nm in diameter, with hexagonal outlines

(fig. 2*70). Some are completely or partially penetrated by

Figure 270. — Particles of raspberry ringspol virus

showing some completely, some partially, and some not

penetrated by phosphotungstate. Bar represents 50 nm.

(After Murant 1978: copyright Scottish Crop Research

Institute.)

negative stain; others are not penetrated. The particles form

three sedimenting components, T, M and B, with sedimentation coefficients (s 2o.w) of 50, 92, and 130 S, respectively,

and A26()/A28o of 0.68 (T), 1.48 (M), and 1.69 (B),

respectively (Murant et al. 7972). The coat protein is a single

species with a mol. wt. about 54000 (Mayo et al. 7977), and

the genome consists of two species of single-stranded RNA

with mol. wts. of 2.8 and 1.4 X 10" daltons (Murant et al.

7972, 1981). Both RNA species are necessary for infectivity

(Harrison et al. 7972), each carrying different genetic

information. For example, the larger RNA carries the

determinant for ability to infect 'Lloyd George' raspberry and

the smaller RNA carries determinants for nematode transmissibility and serological specificity, that is, it contains the coat

protein cistron (Harrison et al. 1972b, 1974).

Scottish isolates of RRV, both those of the common strain

and those of the 'Lloyd George' yellow blotch strain, are

serologically very similar to each other and to a strain causing

spoon leaf disease of red currant (Ribes rubrum L.) in The

Netherlands (Harrison 7967; Maat et al. 7962). However,

these strains differ serologically from some found in England

and Germany (Cadman 1960b), and this difference is

correlated with a difference in transmissibility by Longidorus

spp. (See "Natural and Experimental Transmission," p. 217).

An isolate from grapevine in Germany (Vuittenez et al. 1970)

was serologically very distantly related to the Scottish strain.

TBRV. For a detailed description of the virus, see Murant

(1970a). In tobacco sap, the virus loses infectivity after

dilution to 10 ' to 10-*. or after 10 min at 60° to 65°C, or 2 to 3

wk at room temperature (Harrison 1957). The virus may be

purified by the method described above for RRV. The

particles are similar to those of RRV and, like it, sediment as

three components, called T, M, and B, but with sedimentation coefficients (s 20.,,) of 55, 97, and 121 S. respectively

(Murant 1970c). M and B components have AIôQ/A^SO of

1.62 and 1.78, respectively (Forster 1980). The coat protein

is a single species with a molecular weight of about 57000

218
(Murant et al. 1972), and the genome consists of two species

of single-stranded RNA with mol. wts. of 2.7 and 1.7

X 10' daltons (Murant et al. 1973, 1981). Both RNA species

are necessary for infectivity (Murant et al. 1973), each

carrying different genetic information (Randies et al. 7977;

Harrison and Murant 7977fl; Hanada and Harrison 7977). For

example, the smaller RNA carries the information for

nematode transmissibility and serological specificity, that is,

it contains the coat protein cistron. Some isolates of TBRV

also contain a "satellite" RNA, of mol. wt. 0.5 x 10^ which

appears to depend on TBRV for its replication (Murant et al.

1973).

Strains of TBRV that have been studied serologically fall into

two groups, one group containing the English lettuce ringspot

isolate and the German potato bouquet and grapevine strains

(Harrison 1958d; Stellmach and Bercks, 7965; Vuittenez et

al. 7970), the other containing the Scottish beet ringspot

isolate and the German potato pseudoaucuba strain (Bercks

7962). This serological difference is correlated with a

difference in specific nematode vector. (See "Natural and

Experimental Transmission," p. 217.) TBRV is very distantly related to cocao necrosis and grapevine chrome mosaic

viruses.

Detection and Identification

The patchy appearance of a disease outbreak, ringspot lesions

on leaves tending to fade in midsummer and, in cultivars

highly sensitive to RRV, the stunted, dead, and dying plants

are characteristic features; however, similar symptoms are

induced by other nematode-bome viruses. Moreover, some

raspberry cultivars show only mild symptoms, and even

sensitive cultivars may show few or no symptoms in early

stages of infection. The virus(es) present are detected by

inoculation of sap to a suitable indicator, preferably

Chenopodium quinoa, and are identified by serological tests,

preferably by double diffusion in agar or agarose gel.

Serological tests are essential because, although RRV and

TBRV may be distinguished from each other by the reaction

of C. amaranticolor, they cannot be reliably identified and

distinguished from other nepoviruses by their effects on test

plants.

Control Procedures

Use of certified virus-tested planting material. Both

viruses may be distributed in infected planting material,

which may present a hazard because few or no symptoms are

visible in tolerant cultivars or in the early stages of infection

in sensitive cultivars. This source of infection can be

eliminated by introducing adequate certification schemes for

the production of virus-tested stock. Such schemes should

include the requirement that stocks for certification are not

established in soil containing vector nematodes.

Use of immune cultivars. If the outbreak in a sensitive

cultivar is small, only affected plants need be removed to be

replaced with plants of an immune cultivar (see table 11).

Immunity to RRV and TBRV in red raspberry appears to be

inherited as a dominant character, but for each virus at least

two genes are concerned (Jennings 7964). Although in some

Scottish plantations, the 'Lloyd George' yellow blotch strain

of RRV infects cultivars that are immune to the common

strain, this resistance-breaking strain has not become

prevalent, probably because it is poorly transmitted through

seed of common weeds and therefore does not survive well in

soils (Murant et al. 7968; Hanada and Harrison 7977).

Cultivars immune to RRV have therefore given good control,

although they are not preferred agronomically. Fortunately,

the major cultivar in Scotland, 'Mailing Jewel', is immune to

TBRV and has never been found infected with this virus after

some 30 yr in cultivation.

Cultural methods. The wide host ranges of the viruses and

their vectors among wild and cultivated plants preclude crop

rotation as the sole control measure, but not all plants are

equally good hosts of vector nematodes. L. elongatus

populations increase rapidly on strawberry, ryegrass, clovers, and many weeds such as Stellaria media, but decrease on

barley plants, raspberry, and many vegetable crops (Taylor

7967; Thomas 7969). Therefore, in areas where RRV and

TBRV are known to be troublesome, infection can be

minimized by not planting raspberry after strawberry or

grass/clover pasture, and by adopting good long-term weed

control measures. The latter also prevent the accumulation in

the soil of infected weed seeds, which act as virus sources.

Chemical control of vector nematodes. Treatment ofthe soil

with D-D (dichloropropene-dichloropropane), dazomet, or

pentachloronitrobenzene gave good control of L. elongatus

and prevented spread of RRV and TBRV in strawberry and

raspberry (Murant and Taylor 7965; Taylor and Murant

7965, 1968; Trudgill and Alphey 7976). Although side

effects were noticed with pentachloronitrobenzene in plantings of 'Lloyd George' raspberry and sugarbeet (Taylor and

Murant 7968), this chemical has been widely used and

effective in Scotland. However, fumigant nematicides such

as dazomet or dichloropropene (the active constituent of

D-D) are now the preferred treatments in commerce.

Chemical treatments are most effective and most necessary

after the land has carried crops, such as strawberry, that lead

to an increase in numbers of L. elongatus. The practice of

pulverizing old raspberry canes and returning them to the soil

is also effective in decreasing the numbers of L. elongatus

(Taylor and Murant 7966).

Thermotherapy. Little information is available on the

response of RRV and TBRV to heat treatment. In one

experiment, RRV was not eliminated from 'Mailing Promise'

raspberry held for 3 wk at 3TC (J. Chambers, unpublished

data).

Remarks

The symptoms produced by isolates of RRV and TBRV in

standard herbaceous indicators are similar to those induced

219
by many other viruses infecting small fruits, particularly

members of the nepovirus group such as arabis mosaic,

cherry leaf roll, strawberry latent ringspot, tomato ringspot,

and tobacco ringspot viruses. (See papers on these viruses

in the Rubus section.) Moreover, all these viruses have very

wide host ranges and infect naturally many other wild and

cultivated plants. Serological tests are the only satisfactory

method of identification.

'VACherry Leaf Roll Virus in Rubus „

By A. T.jJones ' *

Additional Common Names

None.

History and Geograpliic Distribution

Cherry leaf roll virus (CLRV) was first reported from

blackberry plants in England (East Mailing Research Station

1970. Ormerod 1972a) and later in red raspberry in New

Zealand where it was found in several plantations (Jones and

Wood 1978). CLRV is common in several species of trees

and shrubs in Europe, North America, and the U.S.S.R.

(Cropley and Tomlinson 1971: Bubaker and Pomazkov

1978). but no other reports of infection in Ruhiis are known.

Economic Importance

The virus is common in some red raspberry plantations in

New Zealand, but the incidence of infection within

plantations varies from only one or two plants to over 70%

(Jones and Wood 1978). Fruiting canes of infected plants

usually show severe leaf symptoms and decreased vigor. The

virus is thus a potentially serious disease problem; however,

the precise extent of infection in New Zealand is not yet

known.

Ormerod (1972a and East Mailing Research Station 1970).

reported three separate outbreaks of CLRV in 'Himalaya

Giant' blackberry in Great Britain. The disease associated

with CLRV infection was lethal in some plants (Cropley and

Tomlinson 1971). but the incidence of infection is not

known.

Symptoms on Natural and Experimental Hosts

Rubus hosts. In naturally infected R. procerus P.J. Muell. cv.

'Himalaya Giant', CLRV is reported to cause chlorotic

mottling and line-pattern leaf symptoms, stunting, and

sometimes death (Cropley and Tomlinson 1971). Natural

infection in red raspberry in New Zealand was associated

with stunted fruiting canes, which were characterized by poor

and distorted leaf development. Some leaves showed

line-pattern symptoms, severe chlorotic mottle, and/or

ringspot symptoms late in the season (figs. 271 and 272)

(Jones and Wood 1978, 1979). No symptoms were evident

on primocanes. The red raspberry cultivars found naturally

infected were 'Marcy', 'Lloyd George', and 'Taylor'.

Figure 271. — Chlorotic mottling in leaves oía Iruiting

cane of 'Marcy' red raspberry infected with cherry leaf

roll virus. (Copyright Scottish Crop Research Institute.)

Herbaceous hosts. After mechanical inoculation with a

raspberry isolate, the following herbaceous species showed

symptoms:

Chenopodium amaranticolor Coste and Reyn., C. foetidum

Schrad., C. quinoa Willd., and Phaseolus vulgahs L. cv.

'Market Wonder' developed chlorotic or necrotic local

lesions within 6 days followed by systemic apical necrosis.

Cucuinis sativus L. (fig. 273), Nicotiana clevelandii Gray,

and A', tabacum L. cvs. 'Samsun', 'White Burley', and

'Xanthi-nc' developed large chlorotic or necrotic local

lesions within 4 to 5 days followed by a systemic mosaic.

Local infection in A', tabacum was frequently characterized

by the development of necrotic rings (fig. 274). Nicotiana

glutinosa L. was often symptomlessly infected. Strains of

CLRV from different natural hosts differed somewhat in host

range and symptomatology (Jones 1973. 1976c).

Natural and Experimental Transmission

Natural transmission by nematode vectors, particularly

species of Xiphinema, was reported by Fritzsche and Kegler

(1964). However, when Jones et al. (1981) reinvestigated the

possibility of transmission of three strains of CLRV by 10

species of potential vector nematodes, they rarely recovered

CLRV from bait plants and then only when these were

220
Figure 272. — Range of chlorotic mottling symptoms

in leaves of 'Marcy' red raspberry infected with cherry

leaf roll virus. (Copyright DSIR, New Zealand.)

Figure 273. — Cucumber seedlings mechanically inoculated with cherry leaf roll virus showing large

chlorotic-necrotic local lesions and systemic mosiac.

(Copyright DSIR, New Zealand.)

Figure 274. — Leaf of N. tabacum cv. 'Xanthi-nc'

mechanically inoculated with cherry leaf roll virus and

showing necrotic rings. (Copyright Scottish Crop

Research Institute.)

221
growing concurrently in pots containing CLRV-infector

plants. They attributed these few infections to contamination

and concluded that nematode transmission was unlikely to

account for the widespread occurrence of CLRV in woody

hosts. For more detailed discussion on this subject, see Jones

et al. (1981).

Recent information on the spread of CLRV in walnut

orchards in California confirms that nematodes are not

involved but provides good circumstantial evidence that

CLRV is transmitted via pollen to the plant pollinated

(Mircetich et al. 1980). Further experimental work is needed

to prove that this is so and to determine if this method of

transmission also occurs in Rubus and other natural hosts.

CLRV is seed-borne, often to a large proportion of seedlings,

in many natural (Callahan 1957a; Schimanski and Schmelzer

1972; Cooper 1976) and experimental (Lister and Murant

1967; Tomlinson and Walkey 1967) hosts and can infect seed

of some species via both ovule and pollen (Callahan 1957a,

b). However, no information is available on seed transmission in Rubus.

CLRV is transmitted experimentally by mechanical inoculation, readily to herbaceous hosts, and less readily to natural

host species of Betula, Prunus, Rheum, and Sambucus

(Tomlinson and Walkey 1967; Hansen and Stace-Smith

1971; Jones 1973; Cooper and Atkinson 1975).

CLRV is graft transmissible in many woody hosts, but there

are no reports of this in Rubus.

Properties of the Causal Agent

For a detailed description of the virus, see Cropley and

Tomlinson (1971), Jones and Mayo (1972), and Walkey et

al. (1973). Many isolates of CLRV have been described, and

most are relatively stable in sap of herbaceous hosts.

Infectivity in sap of C. quinoa or A', clevelandii usually

survives diluting 10 ' to lO"*, heating for 10 min at 55 to

60°C, and storing for 4 to 8 days at room temperature

(Cropley and Tomlinson 1971). Virus preparations free from

most contaminating host components can be prepared in the

following way: Extract sap of CLRV-infected C. quinoa or

A^. clevelandii in 0.1 M phosphate buffer (pH 7) and clarify

either by freeze/thawing, or treatment with organic solvents,

or ammonium sulphate, or combinations of these.

Further clarification and concentration is by differential

centrifugation and sucrose density gradient centrifugation.

Purified preparations of CLRV contain isometric particles

about 28 nm in diameter, some of which are penetrated by

negative stain (fig. 275). Particles sediment as two

nucleoprotein components with sedimentation coefficients of

about 115 5 and 128 5, and in some preparations a nucleic

acid-free component of about 54 S is detectable. The A260/280

value of mixtures of the 2 nucleoprotein components is about

1.6. Particles of several different strains of CLRV have been

Figure 275. — Electron micrograph of a purified

preparation of cherry leaf roll virus stained in 2%

phosphotungstate, pH 6.5. Some particles are penetrated by the stain. Bar represents 150 nm. (Copyright

Scottish Crop Research Institute.)

shown to contain a single polypeptide species of 54000 mol.

wt. and 2 RNA species of estimated mol. wt. 2.1 x 10" and

2.4 X 10", which are contained in the 115 S and 128 S

particles, respectively (Jones and Mayo 1972; Walkey et al.

1973).

Many serotypes of CLRV are known (Jones and Murant

1971; Jones 1976c; Cooper and Edwards 1980); indeed,

isolates from different plant genera tend to be serologically

distinct (Jones 1976c; Cooper and Edwards 1980). Ormerod

(1975), however, reported that one isolate from blackberry

was serologically identical to the type strain of CLRV from

cherry but that this blackberry isolate differed in symptomatology in herbaceous hosts from two other isolates from

blackberry. Raspberry isolates of CLRV tested from various

parts of New Zealand were serologically indistinguishable

from one another when tested against antiserum to CLRV

from American dogwood (Cornus nuttallii Aud.) (Jones and

Wood 1978).

Detection and Identification

Although disease symptoms were associated with CLRV

infection of blackberry and raspberry (East Mailing Research

Station 1970; Jones and Wood 1978), the virus is best

detected by mechanical inoculation of herbaceous test plants,

such as Chenopodium spp. or cucumber, and is then best

identified by serological tests. Because of the antigenic

differences among CLRV isolates, some may fail to react

with diluted antiserum to a given isolate.

Control Procedures

In the absence of firm evidence on the mode of transmission

of CLRV in Rubus, control measures are difficult to prescribe

in detail. Much of the incidence in raspberry in New Zealand

was attributed by Jones and Wood (1978) to propagation

from infected material. The planting of material derived from

222
virus-tested elite stock should restrict further unwitting

spread of this virus; however, if CLRV is pollen transmitted

in Rubus, as it is suspected to be in walnut (see "Natural and

Experimental Transmission"), much of the incidence

observed in raspberry plantations in New Zealand could be

the result of natural spread. If this is so, eradication of

affected plants in the only known means of controlling

spread. Resistant or immune cultivars have not been

reported.

No attempts have been made to cure infected Rubus plants

from CLRV, but the virus was eliminated from rhubarb by

meristem-tip culture (Walkey 1968).

Remarks

Although CLRV appears not to be spread readily if at all by

nematodes (Jones et al. 1981), it is regarded as a nepovirus

because of the properties of its particles (Jones and Mayo

1972; Harrison and Murant 1977b). It induces symptoms in

Chenopodium and Nicotiana species similar to those caused

by many nepoviruses (see the nematode-bome diseases

papers of the Rubus section of this handbook, p. 204-228)

and by some isolates of tobacco streak virus (see "Tobacco

Streak Virus in Rubus,'' p. 235) and can only be identified

with certainty by serological tests.

/^i ñornato Ringspot Virus in Rubus^^

By R.jStace-Smith and R. ifiConverse

Additional Common Names

Raspberry yellow blotch curl (Chamberlain 1938); raspberry

decline (Zeller and Braun 1943); Himalaya blackberry

mosaic (Alcom et al. 7955); raspberry ringspot (Vaughan et

al. 1951).

History and Geographic Distribution

The symptoms now attributed to infection with tomato

ringspot virus (TomRSV) were not recorded in the early

raspberry virus literature in North America. In retrospect, the

virus was probably in those plantings where the mosaic

complex (see "Raspbery Mosaic," p. 168) and raspberry

leaf curl (see "Raspberry Leaf Curl," p. 187) were first

observed, but the symptoms were probably attributed to one

of those viruses. The first description of TomRSV in

raspberry was from Ontario, Canada (Chamberlain 1938).

The new disease was named "yellow blotch-curl" and,

although conclusive evidence on the identity of the causal

virus was not obtained, there is little doubt that the virus

involved was TomRSV.

The next record of the disease was from Oregon, where

Zeller and Braun (1943) proposed the name "raspberry

decline" for a disease that lacked leaf or cane symptoms but

was characterized by crumbly fruit and a decline in plant

growth and productivity. Raspberry decline was shown to be

graft transmissible and the pattern of spread in the field led

the authors to speculate that spread of infection involved

some underground factor. Although raspberry decline was

not shown to be caused by TomRSV, the evidence today

leaves little doubt that the virus involved was TomRSV.

Vaughan et al. (7957) used the term "ringspot" to describe a

disease that was generally found in red raspberry throughout

Oregon and Washington. This disease was later found in

British Columbia (Stace-Smith 1962b) and was shown for the

first time to be caused by TomRSV. This virus is now known

to occur throughout the raspberry growing areas of the United

States and Canada. Field spread is restricted to those areas

where certain vectors of the genus nematode Xiphinema

occur.

The geographic distribution of TomRSV in Rubus is confined

to the temperate regions of North and South America. To a

very limited extent, the virus has been distributed in infected

clones to other parts of the world. Reports to date indicate

that the virus has been isolated from cultivars originating in

North America, Yugoslavia (Jordovic et al. 1972a), and the

U.S.S.R. (Gordejchuketal. 7977).

Economic Importance

TomRSV is considered to be one of the most widespread and

economically important virus diseases of Rubus in North

America. Loss is difficult to assess because variability in

symptoms depends on the cultivar and duration of infection.

The ringspot disease, caused by TomRSV, is the most

common virus disease seen in field-grown red raspberries in

Oregon and Washington (Converse et al. 1970). The virus is

also prevalent in Eastern United States, where it is associated

with a crumbly berry condition in red raspberry (Keplinger et

al. 1968).

Symptoms on Natural and Experimental Hosts

TomRSV has a wide experimental and natural host range;

species in more than 35 dicotyledonous and monocotyledonous families are susceptible (Stace-Smith 1970b). In nature,

the virus occurs mostly in ornamentals and woody or

semiwoody plants. Transmission by sap inoculation is readily

achieved to herbaceous hosts but with difficulty to woody

hosts.

Symptoms on red raspberry. Symptoms of TomRSV in red

raspberry are variable, depending to a large extent on the

cultivar and the duration of the infection. Plants develop

symptoms associated with a shock reaction in the year

following infection. As new foliage is produced in the spring,

leaves may show yellow rings, line-patterns, or a fine yellow

vein chlorosis (figs. 276 and 277). Symptoms that develop

remain visible throughout the growing season, but leaves that

develop during hot weather usually show no symptoms.

Those plants that have been infected for more than one year

either develop no symptoms on the new foliage or show ring

and line-patterns on only one or two leaves.

223
Figure 276. — Leaf of red raspberry, cv. 'Willamette', naturally infected with tomato ringspot virus,

showing ringspot markings.

The pattern of spread of TomRSV is characteristic of

nematode-borne viruses. Patches of infected plants form a

circular pattern with the chronically infected plants in the

center of the patch and the recently infected plants, showing

shock symptoms, at the margin. In such infections, the

chronically infected plants of some cultivars are dwarfed in

the spring, foliage is slower to develop (fig. 278), and the

primocanes have a distinctly bronze cast in comparison with

healthy plants (Converse and Stace-Smith 1971). Cultivars

that are severely affected by TomRSV (for example,

'Fairview') show cane death in the spring, and those canes

that do survive produce small downcurled leaves that mature

early and abscise early in the fall (Freeman and Stace-Smith

1968).

The effect of TomRSV infection on plant yield depends to a

large extent on the cultivar. In a study involving 10 cvs.,

'Lloyd George', 'Avon', 'Latham', 'Glen Clova', and

'Meeker' showed a reduction in yield in the third cropping

year, whereas 'Canby', 'Carnival', 'Mailing Jewel', 'Matsqui', and 'Puyallup' showed no significant yield reduction

(Freeman et al. ¡975). Drupelet set also varied with the

cultivar. 'Avon', 'Fairview' and 'Lloyd George' showed a

particularly adverse affect (fig. 279); 'Matsqui', 'Puyallup,'

and 'Newburgh' were affected to a lesser extent, and

TomRSV infection did not affect drupelet set in 'Canby',

'Carnival', 'Glen Clova', 'Latham', 'Mailing Jewel', and

'Meeker' (Daubeny et al. 1975).

Figure 277. — Leaf of red raspberry, cv. •Willamette', naturally infected with tomato ringspot virus,

showing netlike chlorosis along leaf veins.

Figure 278. — Red raspberry plant, cv. 'Puyallup'.

infected with tomato ringspot virus showing delayed

foliation associated with chronic infection (left) as

compared with healthy plant (right).

Symptoms on blackberry. The effects of TomRSV on

blackberry cultivars have not been investigated, but transmission experiments have been done with a 'Himalaya'

blackberry plant with what is thought to be TomRSV plus a

virus causing feather vein symptoms (Alcorn et al. 1955).

These experiments indicate that TomRSV may cause a

variety of leaf symptoms, including small chlorotic spots

scattered over the leaf blade, large yellow blotches at the base

of the leaflets, conspicuous veinal chlorosis, and oak leaf

patterns in 'Himalaya' blackberry. The absence of these

224
Figure 279. — Fruit from red raspberry, cv. "Fairview", infected witii tomato ringspot virus, sliowing

reduced drupelet set. abnormal shapes, and small size

(left and right) as compared with fruit from a healthy

plant (center).

symptoms in grafted plants of 'Boysen', 'Nectar', 'Youngberry", and seedlings of 'Chehalem', 'Logan', and the native

trailing blackberry (R. ursinas Cham, and Schlecht.)

suggests that these cultivars are either mildy affected or

immune.

Symptoms on indicator hosts. Since TomRSV affects a

wide range of herbaceous hosts, many species have been

utilized for detection and diagnosis. The host reactions are

valuable for detecting virus infections, but for identification

of the virus, confirmatory tests (see "Detection and

Identification," p. 226) must be employed (Stace-Smith

1970b). The most useful indicator hosts are as follows:

Chenopodium quinoa Willd. (fig. 280) and C. amaranticolor

Coste and Reyn. (fig. 281).

Small chlorotic local lesions; systemic apical necrosis.

Cucumis sativus L. (cucumber)

Local chlorotic lesions; systemic chlorosis and mottle.

Nicotiana tabacum L. (tobacco)

Necrotic local spots or rings; systemic etched ring or

line-patterns on a few leaves; later leaves symptomless (fig.

282).

Phaseolus vulgaris L. (bean)

Chlorotic local lesions; systemic rugosity and necrosis of tip

leaves.

Prunus pérsica (L.) Batsch (peach)

Seedlings show no symptoms on inoculated leaves; systemically infected leaves show netlike chlorosis, and tip leaves

are distorted and stunted (fig. 283).

Natural and Experimental Transmission

Natural transmission: Natural transmission in Rubus spp. is

thought to be exclusively by means of nematode vectors

belonging to the genus Xiphinema, particularly X. americanum Cobb and X. rivesi Dalmasso. These nematodes can be

found in raspberry plantings where TomRSV spread is

occurring (McElroy 1977; Forer and Stouffer 1982). The

Figure 280. — Local lesions on Chenopodium quinoa

caused by inoculation with tomato ringspot virusinfected Rubus ssp.

Figure 281. — Systemic symptoms on C. amaranticolor. Photograph taken 15 days after sap inoculation from

a tomato ringspot virus infected red raspberry plant.

virus moves more rapidly from plant to plant along the rows

than it moves between rows, producing oblong patches.

Where active spread is occurring, the virus moves from plant

to plant along rows at an annual rate of about 2 m (Converse

and Stace-Smith 1971). Most new infections occur in plants

adjoining infected plants. New infections in raspberry may

also arise from the feeding of viruliferous nematodes that

have acquired the virus by feeding on an infected weed host.

Infected chickweed (Stellaria media (L.) Cyrillo) as well as

225
Figure 282.—Tobacco, cv. Haranova', showing

lesions on inoculated leaf 7 days after sap inoculation

from a tomato ringspot virus infected raspberry plant.

Figure 283. — Peach seedling showing systemic chlorosis and tip distortion. Photograph taken 18 days after

sap inoculation from a tomato ringspot virus-infected

red raspberry plant.

many other weed species can harbor the virus in a

symptomless condition (Converse and Stace-Smith 1971;

Forer and Stouffer 1982).

The virus is transmissible through a small percentage of seed

from an infected raspberry plant (Braun and Keplinger 1973).

The possibility exists that a healthy plant could be infected by

pollen from an infected source, but there is no experimental

evidence of pollen transmission.

Experimental transmission: Transmission from raspberry

to raspberry can be achieved by grafting, Experimental

transmission to raspberry by means of viruliferous nematodes

has not been demonstrated, but it is assumed that techniques

similar to those used with other host plants (Téliz et al. 1966)

would succeed with Rubus spp.

Sap transmissions from infected raspberry to herbaceous host

plants are readily achieved, provided succulent leaf tissue is

used as the source of inoculum. A phosphate buffer (0.02M,

pH. 7.5) containing 2% nicotine is satisfactory, as is 0.05 M

phosphate, pH 7.0, containing 2% polyvinylpyrrolidone

(mol. wt. 10,000) (Martin and Converse 1982). The most

useful indicator hosts are Chenopodium quinoa or Cucumis

sativus.

Properties of the Causal Agent

TomRSV is a member of the nepovirus group (Harrison and

Murant 1977b). It has three types of isometric particles about

28 nm in diameter, sedimenting at 53, 119, and 1275, and

containing respectively 0, 40, and 43% single-stranded

RNA. The two RNA species, mol. wt. 2.4 x 10" and 2.8 x

10", are both required for infection. Each particle contains 60

molecules of a single coat polypeptide, mol. wt. 55000. The

virus has a wide natural host range, primarily woody or

semiwoody cultivated species and herbaceous and perennial

weed species, and may cause ringspot or mottle shock

symptoms followed by recovery. Natural transmission is by

means of the nematode vectors X. americanum andX. rivesi.

Detection and Identification

Infection in raspberry may be detected by field examinations,

particularly if surveys are conducted in the spring when foliar

symptoms are most pronounced (Vaughan et al. 1951;

Converse et al. 1970). Field surveys detect a high proportion

of new infections (that is, plants infected during the previous

growing season) but a low proportion of chronically infected

plants. Some sensitive cultivars (for example, 'Washington'

and 'Fairview') show foliar markings on at least a few canes

in most years; other cultivars show no symptoms.

Since the absence of symptoms does not necessarily mean

absence of infection, visual examinations must be supplemented with tests capable of detecting latent infections.

Two tests are useful, namely sap transmissions from Rubus

to herbaceous hosts or direct serological tests on Rubus sap.

Bioassay and agar gel serology can be effectively used with

foliage produced in the spring, but as summer progresses, it

becomes difficult to detect infections (Converse 1976). The

enzyme-linked immunosorbent assay (ELISA) technique is

more reliable and can be used to detect TomRSV in leaf,

stem, bud, and root samples from infected plants even late in

the autumn (Converse 1978). Serological tests have the

added advantage that the virus is identified. Bioassays may

detect the virus, but it is only tentatively identified on the

basis of the symptoms induced on a range of herbaceous

indicator hosts.

Control Procedures

TomRSV infections are usually not detected at an early stage

of development in field plantings. Infections are not detected

until the virus has spread to produce circular patches of

unthrifty plants. At this stage, control of the virus is difficult.

Plants showing symptoms could be removed and replaced

226
with healthy plants; but, unless measures were taken to

destroy the viruliferous nematodes by soil fumigation, the

virus would soon spread into the healthy plants in the

replanted area.

A more effective course would be to delay action until yield

loss resulting from infection was sufficient to warrant

complete removal of both healthy and diseased plants from

problem fields. The soil would have to be fumigated with a

nematicide before being replanted to a susceptible host.

Treatment of established red raspberry plants with the

nematicide phenamiphos (58 kg/ha) or dibromochloropropene (64 kg/ha) reduced existing populations of X.

americanum by half but did not reduce the spread of

TomRSV in the field. If roguing is practiced in an attempt to

reduce spread of this disease, removing a band at least five

red raspberry plants wide together with weeds and suckers

beyond those exhibiting symptoms may be helpful in limiting

spread of TomRSV in an established field (R. H. Converse,

unpublished data).

Precautions should be taken to avoid TomRSV problems

when new raspberry plantings are established. These are

particularly important if nematode surveys have detected

populations of A", americanum in the area to be planted. The

vector nematodes themselves cause little damage to red

raspberry unless the virus is also present (McElroy 1977).

The source of inoculum may be excluded from the new

planting if planting stock that is certified as free from

TomRSV (and other recognized Ruhus viruses) is used to

established the new planting. If previous history suggests

there is a possibility of TomRSV becoming a problem,

growers should avoid those cultivars (for example, 'Avon',

'Canby', "Fairview", Lloyd George', and 'Puyallup") that are

known to be particularly damaged by the virus.

^Tobacco Â Ringspot Virus in Rubus

By R.!Stace-Smith ' ''''

Additional Common Names

None.

History and Geographic Distribution

Tobacco ringspot virus (TRSV), a member of the nepovirus

group, was first isolated from a wild erect blackberry plant in

North Carolina in 1965 (Rush et al. 1968). It was later (Rush

and Gooding 7970) found in four native Rubus species — R.

allegheniensis Porter, R. argutu.s Link, and R. flagellari.'i

Willd. plus an unidentified Ruhus sp. in North Carolina. The

only record of the virus being isolated from a cultivated

blackberry is from British Columbia (Stace-Smith and

Hansen 1974).

Economic Importance

None, primarily because there are essentially no commercial

raspberry or blackberry plantings in those areas of North

America where TRSV and its nematode vector are endemic.

Symptoms on Natural and Experimental Hosts

TRSV has a wide natural and experimental host range. The

virus causes a ringspot disease of tobacco, cucumber, Easter

lily, hydrangea, iris, and Pelargonium. It also causes

blueberry necrotic ringspot (see "Necrotic Ringspot of

Blueberry," p. 114), soybean bud blight, and chlorotic or

necrotic spotting in many other annual and perennial crops

(Stace-Smith 1970a).

Infected native Rubus spp. in North Carolina showed faint to

severe ringspots, mottling and mosaic, yellow line patterns,

leaf distortion, and stunting of infected foliage (fig. 284).

An unidentified blackberry cultivar growing in a backyard at

Kamloops, British Columbia, exhibited rasp leaf symptoms

similar to those induced on cherry by cherry rasp leaf virus.

Figure 284. — Symptoms in wild blackberrj' (Ruhus

sp.) associated with tobacco ringspot virus infection: A,

Ringspots; B. mottling and leaf distortion. (Courtesy G.

V. Gooding, Jr., North Carolina State University.)

227
(See "Cherry Rasp Leaf Virus in Rubus,'" p. 241.) Two

infected plants were found, and most of the leaves in these

plants showed some symptoms. The only virus that was

isolated from these plants was TRSV which was assumed

responsible for the rasp leaf symptoms (R. Stace-Smith,

unpublished data).

TRSV has a wide experimental host range, but the following

species have been used for assay, propagation, or diagnostic

purposes:

Cucumis sativus L. Chlorotic local lesions, systemic

mottling, or dwarfing, severe apical distortion.

Nicotiana tabacum h., N. glutinosa L., and A^. clevelandii

Gray. Necrotic local lesions that frequently develop into

rings or ringspots; systemic ring or line-patterns; leaves

produced later show no symptoms.

Chenopodium amaranticolor Coste and Reyn. and C. quinoa

Willd. Local necrotic dots; usually no systemic reaction.

Vigna unguiculata L. Walp. Necrotic local lesions, systemic

necrosis, apical necrosis, and wilt.

Phaseolus vulgaris L. Necrotic spots on inoculated leaves;

systemically infected leaves show spots and rings, and the

growing tip becomes necrotic.

Natural and Experimental Transmission

The virus was isolated from 17 plant species indigenous to

North Carolina, including 4 Rubus spp. All naturally infected

plants were collected from areas near fields containing TRSV

infected tobacco plants. It is assumed that weed hosts such as

Rubus spp. serve as reservoirs of the virus and as acquisition

sources for vectors. Mites {Tetranychus sp.) have been

reported to be inefficient vectors (Thomas 1969), but the

American dagger nematode Xiphinema americanum Cobb

was reported as an efficient vector (McGuire 1964), and it is

assumed that most field spread is attributable to this

nematode. The taxonomy of the complex species, X.

americanum, is in question and the true species is thought to

be limited in its distribution to the eastern part of the U.S.A.

and Canada (Lamberti 1980).

Experimental transmission can be achieved by screening

American dagger nematodes from soil collected from the root

area of infected plants, adding the nematodes to cucumber

seedlings, and, after a few weeks, assaying the cucumber

roots by mechanical inoculation or serology. However, this

technique is cumbersome and would not be used in routine

assay. Sap transmission can be achieved by triturating a small

piece of leaf tissue from infected Rubus spp. with buffer

(0.01 M phosphate buffer, pH 7.5 containing 2% nicotine)

and inoculating to cucumber or any of several other

herbaceous test plants.

Properties of the Causal Agent

TRSV is a member of the nepovirus group (Harrison and

Murant 1977b). It has three types of isometric particles

sedimenting at 51, 91, and 1265 and containing 0, 35, and

43% RNA, respectively. The two RNA species, mol. wt. 1.4

X 10' and 2.4 x 10', are both required for infection. The 91

S particle contains one strand of the smaller RNA; the 126 S

particle contains either one strand of the larger or two strands

of the smaller RNA. Natural transmission is primarily by

means of the nematode vector X. americanum or, in some

species, by seed (Stace-Smith 1970a).

Detection and Identification

The virus can be detected by mechanical inoculation from

infected Rubus spp. to one of many herbaceous test plants

(see "Symptoms on Natural and Experimental Hosts," p.

227); however, since the geographical distribution, natural

host range, and vector relationships of the virus are similar to

those of tomato ringspot virus (see "Tomato Ringspot Virus

in Rubus,'' p. 223) serological tests are essential for positive

identification. Evidence to date suggests that most isolates

that may be found in Rubus are serologically indistinguishable from the "common strains" of TRSV (Rush and Gooding

7970; Stace-Smith and Hansen 7974) based upon the absence

of spur formation in agar gel diffusion tests. Although the

ELISA technique has not been used for detection of TRSV in

Rubus, the technique would undoubtedly be effective if

extensive indexing or mass screening were being considered.

Control Procedures

No problem requiring control procedures has been detected to

date. A problem would only arise if plantings were made in

soils having a history of TRSV in cultivated crops such as

tobacco. Since Rubus spp. are not grown to any extent in

those regions where TRSV is prevalent, it is unlikely that this

virus will become a problem in cultivated raspberry or

blackberry. No information is available on the therapy of

TRSV-infected Rubus plants.

228
Pollen-Borne Diseases

AÍ

/ 'Raspberry Bushy Dwarf.

By A. F.lMurant

Additional Common Names

Loganberry degeneration virus (Legg 1960)\ raspberry

yellows virus (Cadman 1952c); probably raspberry linepattern virus (Basak 7977).

History and Geographic Distribution

A widespread decline disease of the red raspberry cv. 'Lloyd

George' in Great Britain was called "bushy dwarf by

Cadman and Harris (7957) and "symptomless decline" by

Cadman (7952c). A sap-transmissible virus consistently

associated with this disease was called raspberry bushy dwarf

virus (RBDV) by Cadman {1961b) and reported (Cadman

1963) to be serologically related to apple chlorotic leaf spot

virus, which has flexuous filamentous particles. Barnett and

Murant (7970), however, disproved this relationship and

showed that RBDV has quasi-isometric particles about 33 nm

in diameter. Cadman (1961b) found no evidence for

transmission of RBDV by aphids or through soils, although it

appeared to spread rapidly in the field. Later, he reported that

RBDV is transmitted through seed and pollen and infects the

pollinated plant (Cadman 7965); this was confirmed by

Murant et al. (7974) who concluded that transmission in

pollen is probably the only means by which RBDV spreads in

the field.

Confusingly, red raspberry plants infected with RBDV alone,

either by manual inoculation (Barnett and Murant 1970) or by

pollination (Murant et al. 1974), do not show bushy dwarf

disease. Jones (1979b) showed that this disease is probably

caused by mixed infection with RBDV and black raspberry

necrosis virus (BRNV) or even by infection with BRNV

alone. (See "Black Raspberry Necrosis Virus," p. 178.) As a

further complication, recent evidence (Jones et al. 1982)

shows that RBDV is, under some conditions, associated with

the raspberry yellows disease of Cadman (1952c) and is

therefore synonymous with raspberry yellows virus; however, other yellowing diseases of raspberry may have other

causes. (See "Blackberry Calico," p. 245.)

RBDV also has other effects. It induces drupelet abortion

("crumbly fruit") (Murant et al. 7974; Daubeny et al. 1978), a

condition that can also be induced by other viruses and other

factors. Jones and Murant (7972) noted a similarity between

RBDV and raspberry line-pattern virus reported from Poland

(Basak 7977), but no serological studies on the relationship

between these viruses have been reported. Daubeny et al.

(7978), however, found an association between RBDV

infection and presence of chlorotic line-pattern or interveinal

chlorosis in the leaves of some red raspberry cultivars in

North America. In addition, Barnett and Murant (7970)

showed that RBDV is serologically identical to loganberry

degeneration virus, which is associated with loganberry

degeneration disease (Legg 1960; Ormerod 797Ö; 1972b).

RBDV probably occurs throughout the world wherever

susceptible cultivars are grown. In red raspberry and 'Logan'

('Loganberry'), it is reported from western Europe (Cadman

1961b; Barnett and Murant 797Ö; Desvignes and Savio 7975;

Converse and Casper 7977), North America (Converse 1973;

Daubeny et al. 1978); New Zealand (Fry and Wood 1978),

Australia (Guy et al. 1982), U.S.S.R. (M. A. Keldysh,

personal communication; Knight and Barbara 7957; Jones et

al. 1982), South Africa (Kooyman et al. 7982), and Chile

(Auger and Converse 1982). A strain of the virus also occurs

in black raspberry in the United States (Converse 1973;

Murant and Jones 1976).

Economic Importance

In Great Britain, RBDV rarely occurs alone in raspberry

plants in the field. It is therefore important mainly as a

component of mixed infections with viruses, most of them

aphid-borne. It is undoubtedly a major factor in the

virus-induced decline of the red raspberry cv. 'Lloyd George'

after its heyday in the 1930s.

In pot experiments Jones (1979b) found that cane height,

cane diameter, and fruit size of 'Lloyd George' raspberry

were decreased significantly by infection with RBDV but

especially by joint infection with RBDV and BRNV, which

induced symptoms resembling the classical bushy dwarf

disease. Most red raspberry cultivars now grown commercially in Great Britain (notably 'Mailing Jewel', 'Glen

Clova', and 'Mailing Admiral') do not become infected with

RBDV, so that the virus is at present of little economic

importance there; however, it could become important with

the planting of new, susceptible cultivars (for example,

'Mailing Leo' and 'Glen Prosen') or if a newly detected

resistance-breaking strain (Knight and Barbara 1981, D. J.

Barbara and A. T. Jones, unpublished data) becomes

prevalent. Its effects on fruit quality (crumbly fruit) could be

of particular importance; however, not all susceptible

cultivars are as sensitive as 'Lloyd George' to mixed

infection with RBDV and BRNV.

In North America and New Zealand, bushy dwarf disease is

not reported, although RBDV occurs in many cultivars of red

raspberry, including 'Lloyd George' (Converse 7975;

Daubeny et al. 7978; Jones and Wood 7979). Perhaps this is

because the RBDV-infected plants do not also contain

BRNV. The two main vectors of BRNV, Amphorophora

agathonica Hottes and A. idaei Borner (also known as A.

rubi (Kalt.), are not found in New Zealand, and the cv.

'Lloyd George' is not colonized by A. agathonica, the only

one of these aphids that occurs in North America. In New

Zealand, yellows disease caused by RBDV is prevalent in

most years and, in the main cv. 'Marcy', is accompanied by

crumbly fruit (Wood and Todd 7976; Fry and Wood 797S;

229
Jones and Wood ¡979)\ it is regarded as a serious disease,

althougti there are no estimates of yield loss (G. A. Wood,

personal communication).

In Western North America, the prevailing cv. 'Willamette'

is immune, but newer cultivars (for example, "Meeker' and

'Skeena') are susceptible (Daubeny et a!. 1978, Daubeny

1982). Daubeny et al. (1978) found that RBDV caused

significant decreases in yield and in percentage drupelet set in

a breeder's selection although it did not significantly affect

cane height or cane diameter.

In a more recent experiment (Daubeny et al. 1982),

significant reductions in cane height and diameter, as well as

in fruit yield, were observed in the cvs. 'Canby', 'Lloyd

George', and 'Meeker'; 'Crestón' appeared relatively

tolerant. In black raspberry, in contrast to red raspberry,

RBDV caused a nonsignificant increase in fruit yield

although it significantly impaired vegetative growth (Converse 1973).

Symptoms on Natural Hosts

In nature, RBDV has been found only in species of Rubus:

Subgenus Idaeobatus (raspberries)

Natural hosts reported are Rubus idaeus L. (red raspberry),

R. occidentalis L. (black raspberry), R. phoenicolasius

Maxim, (wineberry), R. sachalinensis Léveillé, and R.

vulgatus ssp. buschii Roz.

Subgenus Eubatus (blackberries)

Not found occurring naturally in any species in this subgenus

except in Rubus macropetalus Dougl. and also in five

blackberry-raspberry hybrids: 'Boysen', 'Cascade', 'Logan',

'Marion', 'Merton', and 'Olallie'.

Symptoms on red raspberry. Table 12 lists a selection of

modern cultivars that are susceptible to RBDV. together with

some that have never been found infected in the field. A

complete list of published records is given by Jones et al.

(1982). When infected with RBDV alone, either naturally or

experimentally (by manual inoculation, grafting or pollination), plants of many susceptible cultivars are symptomless.

Under some circumstances, however, symptoms may be

expressed, as follows:

1. In the cv. 'Lloyd George,' RBDV usually causes no

symptoms on its own in Great Britain (Barnett and Murant

1970; Murant et al. 1974), but Jones (1979b) showed that in

mixed infection with BRNV it causes "bushy dwarf disease

(Cadman and Harris 1951). Canes of affected plants are

shorter than normal, are prone to autumn fruiting, and

produce leaves that are downcurled and greasy-looking (fig.

285). Young canes are slow to appear in spring and the

shoots are chlorotic and red-tinged.

The "bushy drawf" syndrome is difficult to recognize unless

uninfected "control" plants are available for comparison. A

mild form of the disease may be caused by BRNV on its own

Figure 285. — Plant of 'Lloyd George' red raspberry

showing bushy dwarf disease. (Copyright Scottish Crop

Research Institute.)

(Jones 1979b). No other red raspberry cultivar is reported to

show this symptom, although many are susceptible to infection with both RBDV and BRNV. In North America, RBDV

was found to cause stunting and reduction in yield of

'Canby', 'Lloyd George', and, especially, 'Meeker'

(Daubeny et al. 1982).

2. Infected plants of at least some cultivars may show

"crumbly fruit" symptoms due to drupelet abortion (Murant

et al. 1974; Wood and Todd 1976; Daubeny et al. 1978).

Expression of this symptom seems to depend on environmental factors because not all infected plants produce crumbly

fruit, and those that do so in one season may not do so in

another.

3. Infected plants of cultivars given in italics in table 12 may

develop "yellows" (Cadman 1952c). The etiology of this

disease has long remained obscure, but recent evidence

summarized by Jones et al. (1982) shows that it is associated

with infection by RBDV. In the field, symptoms occur in late

spring in the lower leaves as a vivid chlorosis of the veins; the

chlorosis later extends into the leaf lamina (vein-banding)

and broadens until the whole interveinal area is chlorotic (fig.

286). The whole or part of a leaf may be affected.

In some cultivars, particularly in Canada and New Zealand,

the chlorosis may take the form of line-patterns or interveinal

chlorosis (Daubeny et al. 1978; Jones and Wood 1979).

Symptoms may gradually progress to affect leaves throughout the plant but tend to become less prominent in

midsummer. Most leaves produced late in the season show

no symptoms. Expression of symptoms seems to depend on

environmental factors because plants of even the most

sensitive cultivars may show symptoms in some years but not

in others. The disease is now uncommon in Great Britain but

seems prevalent in New Zealand (Jones and Wood 1979).

RBDV may not be associated with all types of yellowing in

Rubus. For example, neither the "calico" disease of the cv.

'Puyallup' (Johnson 1972), the symptoms of which closely

230
Table 12.—Susceptibility of some red raspberry and black raspberry cultivars to RBDVi

Red raspberry:

'Canby' + * Mailing Admiral' -t 'Nootka' (-)t

^Chilcotin' (-)t ^Mailing Delight' - 'Norfolk Giant' +

'Crestón ' + 'Mailing Exploit' - 'Red Antwerp' +

^Glen Clova' -t * Mailing Jewel' -t 'Rode Radboud' +

*Glen Isla' -t 'Mailing Joy' -t 'Schönemann' (-)t

*Glen Moy' - 'Mailing

Landmark'

+ 'September' (-)

*Glen Prosen' + 'Mailing Orion' -t 'Skeena' +

'Great + 'Mailing -t 'Taylor' +

American' Promise'

*Haida' - 'Marcy' + 'Veten' +

*Leo' + *Matsqui' (-) 'Willamette' (-)

'Lloyd George* f 'Meeker' + 'Zeva

Herbsternte'

(-)t

Black raspberry:

^Cumberland' (-) 'Bristol' (-) 'New Logan' +

^Black Hawk' (-) 'Munger' + 'Plum Farmer' +

^A more complete list of published records is given by Jones et al. {1982).

+ = susceptible; cultivars given in italics are those in which yellows symptoms have been recorded.

(-) = cultivars not found infected in the field.

- = cultivars not infected in the field or by graft inoculation with a Scottish isolate.

t = cultivars recently found to be infected by graft inoculation with a Russian isolate (Knight and

Barbara 1981 and unpublished data). These workers also found 'Mailing Delight' and 'Zeva

Herbsternte' infected in the field in southern England. These results are contrary to previous

experience in Canada, New Zealand, and Great Britain. Recent tests (D. J. Barbara and A. T.

Jones, unpublished data) indicate that the Russian isolate is a resistance-breaking strain.

resemble yellows disease, nor the calico diseases of

'Chehalem', 'Logan', and 'Marion' blackberry (Converse

and Kowalczyk 1980) seem to be associated with RBDV

infection.

Symptoms on black raspberry. Table 12 gives details of

cultivar susceptibility; field-infected plants of cvs. 'Munger',

'New Logan', and 'Plum Farmer', and graft-inoculated

plants of cv. 'Munger' were symptomless (Converse 1973).

Seedlings infected through seed show no symptoms.

Symptoms on wineberry {R, phoenicolasius). No symptoms were observed in a field-infected plant, but faint

transient line-patterns were observed in grafted plants soon

after inoculation (Jones 1977).

Symptoms on R, sachalinensis and R, vulgatus ssp.

buschii. Most plants were symptomless, but some showed

"yellows" (Jones et al. 1982).

Symptoms on 'Marion' berry. Plants showing "yellows" in

New Zealand contained RBDV (Jones et al. 1982).

Symptoms on 'Boysen' berry. Field-infected plants were

symptomless (Converse 1973).

Symptoms on 'Logan' berry. Affected plants were

symptomless but "weak" and gave decreased cane weights

and fruit yields (Legg 1960).

Symptoms on 'Merton' berry. Affected plants showed

chlorotic mottle (Jones et al. 1982).

Symptoms on experimental hosts. Bamett and Murant

{1970, 1971) obtained experimental infection in 55 species in

12 dicotyledonous families. Experimental hosts include:

Fragaria vesea L. (Bamett and Murant 1970)\ Rubus bartoni

Newton cv. 'Ashton Cross' (Jones et al. 1982); R. henryi

Hemsl. and Kuntze (Bamett and Murant 1970); R. laciniatus

Willd. (Jones 1977)\ R. molaccanus L., R. parviflorus Nutt.,

and R.parvifolius L. (Jones et al. 1982)\ R. proceras P. J.

Muell. cv. 'Himalaya Giant' (Jones 1977); Cydonia oblonga

Mill. cv. 'C7/r (Desvignes and Savio 7975; Jones et al.

1982); Chenopodium amaranticolor Coste and Reyn.

(Cadman 1961b); C. murale L. (Bamett and Murant 1970);

231
Figure 286. — Leaves of raspberry bushy dwarf

virus-infected 'Norfolk Giant" red raspberry showing

(upper left to lower right) progressive stages in

development of yellows symptoms. (After Jones et al.

I9H2: copyright Scottish Crop Research Institute.)

C. quinoa Willd. (Cadman 1961b); Cucumis sativus L.

(Cadman 196Ib)\ Nicotiana clevelandii Gray (Bamett and

Murant 1970); and Phaseolus vulgaris L. cv. 'The Prince'

(Bamett and Murant 1970).

Symptoms on indicator hosts, (a) Graft-inoculated plants

Rubus henryi: transient chlorotic mottle, easily overlooked;

this distinguishes RBDV from BRNV, raspberry leaf spot,

and raspberry leaf mottle viruses, which induce severe tip

necrosis in this indicator. (See "Black Raspberry Necrosis,"

p. 178, and "Raspberry Leaf Mottle and Raspberry Leaf

Spot," p. 183).

R. molaccanus: prominent chlorotic line-patterns, interveinal

yellowing (fig. 287).

Cydonia oblonga cv. 'C7-1': yellow line-patterns; leaves

produced later display prominent yellow vein-banding (fig.

288) or are entirely yellow.

(b) Manually inoculated plants

Chenopodium amaranticolor: transient chlorotic local lesions

may appear in 4 days, especially in spring and autumn;

systemic chlorotic rings and line-patterns develop after 7

days (fig. 289).

C. murale: inoculated leaves show sunken necrotic rings; no

systemic infection.

C. quinoa: transient chlorotic local lesions may appear in 4 to

7 days, especially in spring and autumn; systemic chlorotic

Figure 287. — Prominent interveinal yellowing induced

by raspberry bushy dwarf virus in Rubus molaccanus.

(After Jones et al. 1982: copyright Sottish Crop

Research Institute.)

Figure 288. — Raspberry bushy dwarf virus-infected

leaves of Cydonia oblonga cv. 'Cl/W showing

prominent yellow vein banding. (After Jones et al.

1982: copyright Scottish Crop Research Institute.)

Figure 289. — Chlorotic rings and line-patterns induced

by raspberry bushy dwarf virus in systemically infected

leaf of Chenopodium amaranticolor. (After Bamett and

Murant 1970: copyright Scottish Crop Research Institute.)

232
Figure 290. — Chlorotic rings and line-patterns induced

by raspberry bushy dwarf virus in systemically infected

leaf of C. quinoa. (After Bamett and Murant ¡970:

copyright Scottish Crop Research Institute.)

spots develop after 7 days followed by light- and dark-green

mosaic and ring patterns (fig. 290). This plant is useful for

propagating the virus.

Cucumis sativus: transient chlorotic lesions in inoculated

leaves; transient systemic mottling.

Nicotiana clevelandii: symptomless systemic infection.

Phaseolus vulgaris cv. 'The Prince': In winter, minute brown

local lesions (fig. 291) develop after 3 days; no systemic

infection. This plant is useful for quantitative assays in winter

or when grown in controlled environment chambers (20°C,

5000 lux, 16-h photoperiod). Lesion numbers are increased

by keeping the plants in darkness for 1 day before inoculation

and by using phosphate buffer in the inoculum. Lesion

development is inhibited by a component of C. quinoa sap,

which occurs in increased concentration in plants grown in

long days and high light intensities (Bamett and Murant

1970).

Figure 291. — Minute local lesions induced by raspberry bushy drawf virus in leaf of Phaseolus vulgaris cv.

'The Prince'. (After Bamett and Murant 1970;

copyright Scottish Crop Research Institute.)

Natural and Experimental Transmission

Experimentally, RBDV is transmissible by grafting and by

mechanical inoculation. Sap from raspberry is more infective

in spring and autumn than in summer, and inocula are best

prepared at pH 8 with 2% nicotine or 1 % polyethylene glycol

(mol. wt. 6000). Chenopodium quinoa is the most sensitive

test plant. RBDV is detectable in leaves, flower parts, pollen,

and seed of infected raspberry.

RBDV is transmitted through raspberry seed (Cadman 1965;

Converse 1973; Murant et al. 1974). The virus may enter

seed via either gamete, although less readily via pollen, and

transmission was greatest (77%) when both parents were

infected (Murant et al. 1974); only 1 to 2% seed transmission

was found in Fragaria vesca and none in Chenopodium

quinoa. Jones (1977) found 15% seed transmission in Rubus

phoenicolasius. Pollination of healthy or infected raspberry

flowers with infected pollen may result in the production of

crumbly fruit (Murant et al. 1974).

In raspberry and 'Logan', the virus carried in pollen

infects not only the progeny seedlings but also the pollinated

plant (Cadman 1965; Ormerod 7970). Murant et al. (1974)

found that the virus did not spread to plants that were

prevented from flowering for 3 yr and concluded that

transmission in pollen is probably the only means of spread in

the field; most plants that were near to RBDV sources

became infected in the first two or three flowering seasons.

Properties of the Causal Agent

For a detailed description of the virus, see Murant (1976b).

In Chenopodium quinoa sap, typical isolates from Rubus

idaeus lose infectivity when diluted 10^, heated for 10 min at

65°C, or stored for 4 days at 22°C (Bamett and Murant

1970). An isolate from R. occidentalis lost infectivity when

diluted \Qr- or after storage for 2 to 3 hr at room temperature

(Murant and Jones 1976). Isolates of both types were still

infective in lyophilized leaf tissue after 6 yr (A. F. Murant,

unpublished data). The vims is purified (Bamett and Murant

1970; Murant 1976b) by acidifying C. quinoa extracts to pH

4.8 and concentrating the vims from pellet or supematant

fractions by precipitation from 8% polyethylene glycol,

(mol. wt. 6000) + 0.8% NaCl, and differential centrifugation.

In the electron microscope, the vims particles are stable in

uranyl acetate or uranyl formate negative stain but dismpt in

phosphotungstate; they are isometric, about 33 nm in

diameter (fig. 292), but appear somewhat pleiomorphic

because they partially collapse on the grid. They form a

single sedimenting component with a sedimentation coefficient (í2o,w) of 115 5 in 0.05 M citrate buffer, pH 6 or 7.

Fractions from this zone have A26C/A280 of 1.62. The

particles contain a single major protein of mol. wt. about

29,000 daltons and three species of single-stranded RNA

with mol. wt. of 2.2, 0.9, and 0.4 x 10*.

233
Iigiirc 292. — Particles ol raspberry bushy dwart virus

in uranyl formale. Bar represents 100 nm. (After

Bamett and Murant 1970: copyright Scottish Crop

Research Institute.)

All tested isolates from red raspberry (from Great Britain.

France, Canada, New Zealand, and U.S.S.R.) were

serologically indistinguishable (A. F. Murant, unpublished

data), but two isolates from R. occidentalis differed slightly

from R. idaeiis isolates in gel double-diffusion serological

tests as well as in properties in vitro (Murant and Jones

1976). It was suggested that species-specific strains could

have arisen as a result of transmission exclusively through

pollination.

The particle morphology of RBDV and its transmission

through pollination suggest that it may have affiinities with

ilarviruses, but it differs from them in the number and size of

its RNA molecules and in the sedimentation behavior of its

particles.

Detection and Identification

Although under some conditions RBDV may be associated

with symptoms of decline, yellowing, line-patterns, or

crumbly fruit, it more often infects plants without inducing

obvious symptoms. Presence of the virus is detected by one

or more of the following methods:

1. Manual inoculation to Chenopodium quinoa. Identity of

the virus is confirmed serologically by double diffusion tests

in agarose gels.

2. Grafting to Rubiis molaccanus and/or Cydonia oblonga

cv. -Cl-V.

3. Enzyme-linked immunosorbent assay (ELISA).

some control may be achieved by planting virus-free stocks

and siting fruiting plantations at a distance from infected wild

or cultivated Riibiis: plants in cane nurseries must not be

allowed to flower.

RBDV is somewhat resistant to thermotherapy but it has been

eliminated from red raspberry (Murant et al. 1974; Mellor

and Stace-Smith 7976) and from black raspberry (Converse

1973) by keeping infected plants at or above 36°C for several

weeks and propagating from the shoot tips that appears

subsequently. 'Canby' red raspberry, all stocks of which

were infected with RBDV, was freed from infection in this

way.

Remarks

The characteristic symptoms in Chenopodium quinoa and

symptomless infection of Nicotiana clevelandii distinguish

RBDV from most nepoviruses found in Rubus (see

"Nematode-Bome Viruses" in this section, p. 204-228),

except perhaps strawberry latent ringspot virus; the nepoviruses also differ from RBDV in particle morphology (regular

isometric particles with hexagonal outlines, some penetrated

by negative stain). The type of symptom in C. quinoa also

distinguishes RBDV from black raspberry latent virus (see

"Tobacco Streak Virus in Rubus,"' p. 235), which is more

difficult to transmit by manual inoculation and has regular

isometric particles. Black raspberry latent virus (see

"Tobacco Streak Virus in Rubus," p. 235) resembles

RBDV in particle morphology and transmission through

pollination but causes severe systemic necrosis in C. quinoa

and Phaseolus vulgaris.

The economic importance of RBDV is difficult to assess, but

some loss in yield and fruit quality is certainly caused.

RBDV assumes greater importance in mixed infections with

other viruses. Because the planting of resistant cultivars is the

only method of control, breeders should, if possible, not

release new cultivars that are susceptible to RBDV.

Control Procedures

The only method of controlling RBDV is by planting

resistant cultivars (table 12). In red raspberry, a single

dominant gene confers resistance or immunity to the Scottish

type strain of RBDV (Jones et al. 1982), but Knight and

Barbara {1981) found a more complex situation in tests with a

Russian isolate. They suggested that resistance is controlled

by dominant complementary genes. In susceptible cultivars.

234
Vectors Unknown

Át Tobacco Streak Virus in ^ubus j

By R.jStace-Smith

Additional Common Names

Strawberry necrotic shock virus (Frazier et al. 1962); black

raspberry latent virus (Converse and Lister 1969).

History and Geographic Distribution

The history of our understanding of the occurrence of tobacco

streak virus (TSV) in Rubus spp. is difficult to trace with any

degree of certainty. The reason for this is that at the time the

work was done and reported there was no indication that the

virus involved was either distantly or closely related to TSV.

The first virus involved, strawberry necrotic shock virus

(SNSV), had not even been transmitted mechanically from

strawberry to herbaceous hosts at the time it was shown to

occur in Rubus spp. (Frazier 1966). Later, a virus isolated

from strawberry plants infected with strawberry necrotic

shock was identified as TSV (Stace-Smith and Frazier 1971).

In this review, therefore, I am equating SNSV with TSV.

The second virus that features in the history of TSV in Rubus

spp. is black raspberry latent virus (BRLV), a virus isolated

from clones of black raspberry and red raspberry in Eastern

United States (Converse and Lister 1969). At the point this

work was reported, the authors had not succeeded in

producing an antiserum and, since there were no characteristic properties that suggested that it might be a strain of TSV,

they concluded that it was a new virus. Later, when an

antiserum was available against BRLV, a serological

relationship to some strains of TSV was demonstrated (Jones

and Mayo 7975; Brunt and Stace-Smith 1976). Therefore 1

am equating BRLV with TSV.

The first indication of the natural occurrence of TSV in Rubus

spp. was obtained when Frazier (1966) grafted leaves from

'Boysen' and 'Logan' plants into strawberry, producing

necrotic shock symptoms. Several plants of 'Olallie', a

trailing blackberry cultivar, 'Himalaya' blackberry (R.

procerus P. J. Meull), and the Pacific coast trailing

blackberry {R. ursinus Cham, and Schlecht.) indexed

negative. Converse and Lister (79(59) found the virus to be

widely distributed in most cultivars of black raspberry in

Eastern United States but rare in red raspberry. Converse

(7972) found a strain of tobacco streak virus to be prevalent

in black raspberry cultivars in Oregon and Washington. In all

instances, affected plants were symptomless. Stace-Smith

and Brunt (1974) and Converse and Bartlett (7979) found the

virus to be widespread in wild Pacific coast trailing

blackberry (R. ursinus). The virus was equally prevalent in

agricultural and nonagricultural areas, indicating a long

association between the virus and its host.

TSV is prevalent in black raspberry in both Eastern and

Western United States (Converse and Lister 7969; Converse

7972). The virus has been detected in some blackberry

cultivars in California (Frazier 1966) and has been isolated

from a number of blackberry cultivars originating in the

United States and imported into Scotland (Jones and Mayo

7975), Canada (Brunt and Stace-Smith 7976), Australia (Guy

et al. 1982), and possibly Yugoslavia (Perisic and Babovic

7978). It has also been isolated from a blackberry selection

originating in Australia and imported into New Zealand

(Jones and Wood 7979). The virus rarely infects red

raspberry, and the reports of its occurrence are confined to

the United States and Canada (Converse and Lister 7969;

Peterson and Corbett 1980; Stace-Smith et al. 7982).

The occurrence of the virus in wild Rubus appears to be

confined to a single species, R. ursinus (Stace-Smith and

Brunt 7974; Converse and Bartlett 7979). This species occurs

in a narrow zone along the Pacific coast, extending from

California to British Columbia. The high level of TSV

infection encountered in virus surveys done in British

Columbia and Oregon suggests that the virus is generally

prevalent in 7?. ursinus throughout its geographical range.

Although the natural geographical distribution of TSV in

Rubus appears to be restricted to United States, Canada, and

Australia, the virus has been recovered from other plants in

many areas of the world (Fulton 7977).

Economic Importance

No information is available on the economic importance of

TSV in Rubus spp. The fact that the virus appears to be

symptomless in several black raspberry, red raspberry, and

blackberry cultivars suggests that the damage is negligible.

Some infected red raspberry plants were slower to break

dormancy in the spring than virus-free plants (Jones and

Mayo 7975), and infected 'Santiam' blackberry plants

produced significantly fewer primocanes than virus-free

plants (Converse 7978). These two observations provide

evidence that the virus is not completely symptomless in

Rubus hosts, and it must be recognized that, even though

TSV is mild or symptomless in commercial cultivars, it may

contribute to a decline in productivity of field plantings,

alone or acting synergistically with other viruses (Fulton

7987).

Symptoms on Natural and Experimental Hosts

The natural host range of TSV is very wide, including

monocotyledonous and dicotyledonous hosts and both woody

and herbaceous hosts. The symptoms induced in these hosts

are so variable as to be of little diagnostic value. The virus is

known to cause necrotic symptoms in tobacco, pea, bean,

and potato; mottling symptoms in cotton and dahlia; and

ringspot symptoms in tomato. Most of the herbaceous hosts

recover from the virus and produce foliage that is

systemically infected but exhibits no symptoms of infection.

In contrast, woody hosts generally exhibit no symptoms

235
when initially infected and remain symptomless following

systemic invasion of the virus. Infections can therefore only

be detected by graft or sap transmissions to a sensitive host or

by serological indexing.

As would be expected, a virus with a wide natural host range

also has a wide experimental host range. In one extensive

test, Fulton (1948) inoculated 169 species with TSV and

succeeded in recovering the virus from 87 of the inoculated

species. Even this test underestimates the experimental host

range of the virus since virus preparations are unstable. With

improvements in techniques in inoculation and in stabilizing

the virus, many of the species that did not become infected in

earlier tests are known to be hosts of the virus (Fulton 1981).

Symptoms are as variable on the experimental hosts as they

are on the natural hosts. For this reason, it is virtually

impossible to identify the virus with any degree of certainty

on the basis of symptoms induced on a variety of

experimental hosts. Symptoms on Nicotiana tabacum L.

(most cultivars) (fig. 293) include necrotic rings and,

sometimes, solid necrotic spots on the inoculated leaves,

which usually appear within 4 days of inoculation. Systemic

symptoms appear on the younger leaves a few days later and

consist of necrotic lines that follow the small leaf veins.

Succeeding leaves are free of necrotic symptoms and appear

healthy, although virus can be recovered from such leaves.

Other commonly used virus indicator hosts, such as

cucumber, bean, and Chenopodium quinoa Willd.. develop

necrotic or chlorotic local lesions followed by systemic

necrosis or chlorosis. The variability in host reaction is

extreme because there is a high degree of strain variation in

TSV. None of the indicator hosts is entirely reliable in

identifying all strains, although the symptom sequence in N.

tabacum is helpful in at least providing a tentative diagnosis.

Symptoms on Rubus hosts. As a generalization, symptoms

of TSV infections cannot be detected in field plantings of red

raspberries, black raspberries, or blackberries, although there

is some question in the literature with respect to the symptom

response in infected blackberry clones. Frazier (1966) first

detected TSV in degenerate-appearing 'Boysen' plants but,

since he later detected the virus in vigorous plants with a

strong chlorotic leaf pattern, he concluded that none of the

symptoms on the 'Boysen' plants could be ascribed to the

virus. Jones and Wood (1979) isolated TSV from 'Scoresby

Selection' bramble, which showed chlorotic ringspot and

line-pattern symptoms. These symptoms may have been

induced by TSV, and the fact that several symptomless

clones of 'Scoresby Selection' have indexed negative for

TSV (Guy et al. 1982 and R. Stace-Smith, unpublished

results) leaves this possibility open.

The virus is prevalent in blackberry cultivars in British

Columbia, and some of the infected plants show strong

mosaic symptoms, whereas others are symptomless. Similarly, all commercial 'Logan' plantings that have been indexed

Figure 293. — Local lesions in Nicoliana tabacum cv.

'Haranova' 5 days after inoculation with a Rubus isolate

of tobacco streak virus.

in British Columbia have proven to be infected with TSV, yet

none of these plants show viruslike symptoms (R. StaceSmith, unpublished results). The conclusions from these

observations are that TSV does not induce foliar symptoms in

blackberry cultivars but that cultivars infected with TSV

often contain other viruses that do induce foliar symptoms.

In contrast to the absence of symptoms in naturally infected

commercial cultivars, some Rubus hosts develop a severe

necrotic reaction following graft inoculation. Frazier (1966)

reported that several seedling clones of 'Himalaya' blackberry, seedling clones of 'Logan', 'Ollalie', wineberry (R.

phoenicolasius Maxim), and R. henryi Hemsl. and Kuntze

react by becoming necrotic at the side of the graft union. The

necrosis spreads basally or distally through one or more

internodes, usually causing wilting and death of the grafted

shoot. The virus did not become systemic in these plants.

Jones and Mayo (1975), using a different isolate of TSV,

observed the same necrotic reaction in R. henryi, R.

phoenicolasius and R. procerus (fig. 294) as did Converse

and Kowalczyk (1980) in R. ursinus cv. 'Marion'. Other

Rubus hosts, such as black raspberry, red raspberry, 'Logan',

and 'Boysen', are invaded systemically following graft

inoculation but remain symptomless (Frazier 7966,- Jones and

Mayo 7975).

Natural and Experimental Transmission

TSV, like many other members of the ilarvirus group

(Matthews 1981), is known to be transmitted through the

seed of many of its natural and experimental hosts (Mandahar

7987; Kaiser et al. 1982). The evidence is too sparse to

speculate as to whether seed and pollen transmission are the

major means of natural spread of the virus, but these

mechanisms are undoubtedly important in the dissemination

and survival of the virus. Occurrence of TSV is usually low

and erratic, and this has led to speculation that insect vectors

may be involved. In tobacco, infections are more prevalent

near the periphery of the field, suggesting that the source of

236
Figure 294. — Shock reaction (necrosis below the

graft) in Rubus proceras ("Himalaya' blackberry)

graft-inoculated with a Rubus isolate of tobacco streak

virus. (Copyright Scottish Crop Research Institute.)

the virus is infected perennial weed species and that

transmission is by some insect vector. Although a number of

attempts have been made to demonstrate insect transmission,

the only vectors implicated to date are species of thrips.

Evidence that thrips {Frankliniella sp.) may serve as a vector

was first obtained in Brazil (Costa and da Costa Lima Neto

¡976). More recently, two species of thrips [Thrips tabaci

Lindeman and Frankliniella occidentalis (Pergande)l have

been implicated as vectors in the United States (Kaiser et al.

1982).

There is considerable evidence for seed and pollen

transmission in Rubus spp. Converse and Lister (1969)

reported about 6% infection in seedlings arising from seed of

infected black raspberry plants. They also transmitted the

virus to healthy black raspberry plants by hand pollinating

with infected pollen. Converse (1980) found that TSV spread

more rapidly into black raspberry and 'Boysen' plantings that

were permitted to flower as compared with those that were

deflowered. He concluded that virus transmission could have

taken place by flower-visiting vectors or by viruliferous

pollen moved by wind or insects. An alternate explanation

was proposed by Kaiser et al. (1982), namely that thrips

could have been responsible for TSV spread to both

flowering and deflowered Rubus hosts.

Experimental transmission to or from Rubus hosts can be

achieved either by grafting or by sap inoculation. Leaf or

approach grafts were first used by Frazier (1966) to transmit

the virus from 'Boysen' to Fragaria and Rubus indicator

plants. Sap transmission from Rubus to Rubus has not been

achieved, but Jones and Mayo (1975) succeeded in infecting

black raspberry seedlings by inoculating them with purified

virus preparations. The virus is readily transmitted from

infected Rubus hosts to herbaceous hosts, provided appropriate buffers are used. Buffers that have been used include 2%

nicotine (Jones and Mayo 1975), 2% nicotine plus aluminum

oxide powder (Converse and Lister 1969), or 1% nicotine

plus 1% polyvinylpyrolidone (Brunt and Stace-Smith 1976).

Properties of the Causal Agent

TSV has been designated as the type member of the ilarvirus

group (Matthews 1981). The particles are quasi-isometric,

averaging about 28 nm in diameter (fig. 295). Three particle

types are normally separated upon sucrose density gradient

centrifugation, with S20, «, values of approximately 90, 98,

and 113 S. Differences in sedimentation rates are due to

different size groups of the virus particles. Those

sedimenting most rapidly averaging 35 nm in diameter, the

middle group averages 30 nm, and the slowest group

averages 27 nm. Particles are fragile and deform readily;

hence fixation in glutaraldehyde or formaldehyde is recommended for good electron micrographs (Fulton 1981;

Matthews 1981). All three components contain nucleoproteins with maximum absorption at 260 nm and minimum

absorption at 242 nm. Unfractionated preparations have an

A26o/A28() ratio of about 1.60. The particles contain a single

protein species with an estimated mol. wt. of 28700.

Particles contain four linear ssRNA with approximate mol.

wt. of 1.1 (RNA-1), 0.9 (RNA-2), 0.7 x 10" daltons

(RNA-3),and0.3 x 10" daltons (RNA-4). Besides RNAs' 1

to 3, coat protein or RNA-4 is required for infectivity. The

physiochemical properties of the various strains that have

been isolated from Rubus (Converse and Lister 7969,-

Converse 1972; Jones and Mayo 1975; Brunt and StaceSmith 1976) are essentially the same as those of other strains

of TSV (Fulton 1981).

Detection and Identification

Since TSV induces no obvious symptoms in Rubus,

infections cannot be detected by visual observation.

Techniques such as graft transmission, sap transmission, or

serology must be used. Frazier (1966) detected the virus in

'Boysen' by graft transmission to sensitive Fragaria and

Rubus hosts. At the time that work was done, however, the

virus was not known to be sap transmissible from Rubus

hosts. Since sap transmission is a much simpler procedure, it

has superceded graft transmission as a detection technique.

The most widely used herbaceous indicator plant for sap

transmission is C. quinoa (fig. 296), although other hosts

237
Figure 295. — Electron microijiaph ol a purified

preparation of a Riibus isolate of tobacco streak virus,

fixed in glutaraldehyde and negatively stained. Bar

represents 100 nni.

Figure 296. — Local lesions in Chenopodium quiiiou 6

days after inoculation with a Ruhus isolate of tobacco

streak virus.

Figure 298. — Systemic symptoms in Nicoliana

clevelaiidii 12 days after inoculation with a Rubus

isolate of tobacco streak virus.

such as cucumber, bean (fig. 297), and Nicoliana clevelandii

Gray (fig. 298) are equally effective (Brunt and Stace-Smith

1976). The most reliable plant source is expanding leaf tissue

in the first growth from dormant plants; slow-growing plants

from the greenhouse or the summer growth on field-grown

plants are poor sources of inoculum (Converse and Lister

¡969; Brunt and Stace-Smith 7976). The sap should be

extracted in nicotine or polyvinylpyrrolidone to minimize

inactivation by host polyphenols.

Although sap transmission is the most widely used technique

for TSV detection, serological techniques are applicable,

particularly for extensive field surveys; however, because of

the diversity of serological relationships among TSV strains,

failure of virus isolates to react with antisera to some other

isolates need not indicate the absence of TSV. Tests should

include antisera to several TSV isolates.

Figure 297. — I,ocal lesions in Fhascalus vnlf;aris

(bean. cv. 'Black Turtle') 5 days after inoculation with a

Ruhus isolate of tobacco streak virus.

Converse (1976) successfully detected TSV in Rubus by the

agar gel double diffusion technique. The most consistent

results were obtained by grinding leaf tissue in a buffer of 0.1

M Tricine, pH 8, plus 4% polyethylene glycol. As noted by

Converse (1976), TSV cannot be identified on the basis of

symptoms produced on herbaceous hosts and, since isolates

must be identified serologically, direct seroassay in the Rubus

sap eliminates the need for the bioassay step. As with

detection of some other sap-transmissible viruses in Rubus,

the most useful serological technique may be the enzymelinked immunosorbent assay (ELISA) technique (Converse

1979).

Control Procedures

Of the many viruses that are known to infect Rubus hosts,

TSV appears to be one of the least significant in terms of

economic importance. For this reason, it is questionable

whether any special control measures are required other than

the standard precaution of establishing all new plantings with

238
virus-tested stock. Fulton (198]) noted that the virus is of

minor importance on most hosts in North America and no

controls have been necessary. This general statement is

probably true with respect to Rubus hosts, although it must be

recognized that controlled experiments on the possible

adverse effects associated with TSV infection, singly or in

complex with other viruses, have not been done.

The virus is known to be more prevalent in some Rubus hosts

than in others. The virus, for example, is rarely found in red

raspberry. Provided care is taken to establish new red

raspberry plantings with virus-tested clones, the virus will

probably remain rare in red raspberry. In contrast, the virus is

prevalent in black raspberry and some blackberry cultivars.

The reason for the high incidence is not known but, until

recently, plantings were probably established with infected

stock. Possibly, virus incidence will remain low in new

plantings that are established with healthy clones, although

preliminary evidence (Converse 1980) is not encouraging.

Virus-tested planting stock is available for most Rubus

cultivars so virus eradication procedures are rarely required;

however, should it be necessary to eradicate TSV from any

clone, the virus is amenable to eradication by heat therapy

(Converse 1978).

Á

r Wineberry Latent Virus//

By A. T.ljones

Additional Common Names

Initially code named Rp7 by Jones (1975).

History and Geographic Distribution

Wineberry latent virus (WLV) was first reported by Jones

(1974). He isolated it from a symptomless plant of R.

phoenicolasius Maxim, originally imported from the United

States but grown in the field at Invergowrie, Scotland, for at

least 10 yr (Jones 1977). The geographical origin of the virus

is therefore not known.

Economic Importance

Probably none.

Symptoms on Experimental Hosts

Rubus hosts. The single R. phoenicolasius plant found

infected with WLV was symptomless. This source plant also

contained raspberry bushy dwarf virus (RBDV, see "Raspberry Bushy Dwarf," p. 229) but was free from other

known Rubus viruses (Jones 1977). A culture of WLV free

from RBDV was obtained in herbaceous test plants by

passaging through Lycopersicon esculentum Mill., which is

immune to RBDV. However, as WLV was not transmissible

to Rubus spp. by mechanical inoculation, these species were

inoculated by grafting with tissue from the dually infected R.

phoenicolasius field plant. In these graft inoculation tests,

WLV infected the R. idaeus L. cvs. 'Lloyd George',

'Mailing Landmark', 'Norfolk Giant', and 'St Walfried', and

R. loganobaccus Bailey, R. mollacanus L., R. occidentalis

L.. R. phoenicolasius, and R. procenis P. J. Muell. None of

the plants showed symptoms apart from line-pattern in the

leaves of some grafted plants of R. mollacanus, R.

phoenicolasius, and R. procenis; however, identical symptoms are produced in these species by RBDV alone,

suggesting that these symptoms are not caused by WLV. R.

henryi Hemsl. and Kuntze; R. ideaus cvs. 'Glen Clova',

'Mailing Enterprise", and 'Mailing Jewel'; and R. laciniatus

Willd. appear to be resistant to infection with WLV by graft

inoculation.

Herbaceous hosts. After mechanical inoculation, the

following herbaceous species show symptoms: Chenopodium

album L., C. amaranticolor Coste and Reyn., C. foetidum

Schrad., C. murale L., C. quinoa Willd., and Tetragonia

expansa Murr, develop small necrotic local lesions in 5 to 8

days, which enlarge to form large necrotic spots or rings (fig.

299). Inoculated leaves of C. ambrosoides L. and Gomphrena globosa L. develop red rings in about 7 days (fig 300).

Beta macrocarpa L., Lycopersicon esculentum, Spinacia

oleraceae L., and Catharanthus roseus (L.) G. Don, also

known as Vinca rosea L., are symptomlessly infected. The

virus is systemic (but weakly so) only in a few Chenopodium

species. Datura stramonium L., several Nicotiana spp..

Petunia hybrida Vilm., and Phaseolus vulgaris L. were not

infected with WLV (Jones 1977).

Figure 299. — Necrolic local le.sion,s in a leaf of

Chenopodium amaraniiiolor 20 days after inoculation

with wineberry latent virus. (Copyright Scottish Crop

Research Institute.)

Figure .WO. — Local red rings caused by inoculation

with wineberry latent virus in a leaf of Gomphrena

glohosa. (Copyright Scottish Crop Research Institute.)

239
Figure 301. — Electron micrograph of a purified

preparation of wineberry latent virus stained in 2%

phosphotungstate, pH 6.5; it shows aggregated and

fragmented particles. Bar represents 500 nm. (Copyright Scottish Crop Research Institute.)

Natural and Experimental Transmission

The natural mode of transmission of WLV is not known. It is

transmissible experimentally to Rubus species by grafting. It

is also transmissible to several herbaceous species, but not to

Rubus, by inoculation of sap. It is not seed transmitted in R.

phoenicolasius (Jones 1977). Macrosiphum euphorbiae

(Thos.) failed to transmit WLV to C. quinoa when given

short or long acquisition feeds on WLV-infected C. quinoa

(Jones 1975a and unpublished data). No spread from the

single naturally infected plant of R. phoenicolasius to R.

phoenicolasius or to other Rubus spp. appears to have

occurred in Scotland.

Properties of the Causal Agent

WLV has flexuous filamentous particles with a modal length

in sap of C. quinoa of about 510 X 12 nm (fig. 301). In C.

quinoa sap, WLV lost infectivity after diluting to 10 ' to 10"*,

heating for 10 min at 65° to 70°C, or storing for 8 to 16 days

at I8°C.

WLV has been only partially purified, and, of several

purification methods studied, the following was found most

useful (Jones 1977). Sap from WLV-infected C. quinoa was

extracted in 0.05 M tris-HCl buffer (pH 7) containing 0.2%

thioglycerol and 10% (v/v) chloroform, and the virus was

precipitated from the aqueous phase with 7% polyethylene

glycol (mol. wt. 6(K}0) + 0.1 M NaCl. Virus recovered

from the resuspended precipitate was then further concentrated and clarified by differential centrifugation and/or

sucrose density gradient centrifugation. The virus yield and

clarification achieved varied with the time of year and other

undetermined factors, but particles purified in this way were

always both aggregated end-to-end and fragmented (fig. 301

and Jones 1977). Preparations of particles recovered from

sucrose density gradients had A26<y'A28o values of about 1.26.

Although morphologically similar to potexviruses (Koenig

and Lesemann 1978), WLV reaches lower concentrations in

plants and is less stable in plant sap than most potexviruses.

Furthermore, it is serologically unrelated to any of four

potexviruses: potato virus X, hydrangea ringspot, narcissus

mosaic, and white clover mosaic viruses (Jones 1977).

The virus also differs in properties from two other

filamentous viruses reported to occur in Rubus, namely bean

yellow mosaic (Provvidenti and Granett 7974) and bramble

yellow mosaic. (See "Bramble Yellow Mosaic," p. 243.)

Although RBDV was once thought to be serologically related

to apple chlorotic leaf spot virus (Cadman 1963), which has

filamentous particles, it is now known that this is not true and

that RBDV has isometric particles. (See "Raspberry Bushy

Dwarf Virus," p. 229.) WLV differs from apple chlorotic

leaf spot virus in several properties, and the two viruses are

serologically unrelated (Jones 1977).

Detection and Identification

WLV can be detected and identified in Rubus only by

mechanical transmission to herbaceous test plants followed

by serological tests. Transmissions from infected plants kept

in a heated greenhouse are often less reliable than those from

field-grown plants.

Control Procedures

As the virus has been isolated from only a single plant, no

attempts have been made to free plants from infection.

However, in the absence of information on its distribution,

mode of transmission, and effects in raspberry, it would seem

prudent to destroy any exotic plants found infected in the

field. The possibility of propagation from infected plants

should be avoided by indexing raspberry mother plants for

virus infection by inoculating leaf extracts to C. quinoa.

Remarks

Further studies on the virus particle may show affinities with

existing viruses or virus groups and thus provide indications

as to its possible mode of transmission. Difficulties in

producing preparations of virus particles in an unaggregated

state have hindered these studies.

Interestingly WLV was found in association with RBDV, and

in the limited experimental Rubus host range tested, red

raspberry cultivars known to be resistant to RBDV were also

resistant to WLV. However, not all Rubus species that are

susceptible to RBDV were also susceptible to WLV (Jones

1977).

In C. quinoa, WLV induces large spreading local lesions

unlike the pinpoint lesions induced by cucumber mosaic

virus. (See "Cucumber Mosaic Virus in Raspberry," p.

191). Also, in this host, WLV does not induce systemic

symptoms, and is thus unlike black raspberry necrosis

virus (see "Black Raspberry Necrosis," p. 178), bramble

240
yellow mosaic virus (see "Bramble Yellow Mosaic," p.

243), nepoviruses (see "Nematode-Bome Viruses" of this

Rubus section, p. 204-228), raspberry bushy dwarf virus

(see "Raspberry Bushy Dwarf," p. 229), and isolates of tobacco streak virus (see "Tobacco Streak Virus in Rubus,'' p.

235). Furthermore, apart from bramble yellow mosaic virus,

each of these viruses has isometric or quasi-isometric particles.

/-Cherry é. Rasp Leaf Virus in Rubus

By A. T. Jones

L—

Additional Common Names

None.

History and Geographic Distribution

Cherry rasp leaf disease was first described by Bodine and

Newton (1942) in cherry trees in Western United States and

British Columbia, Canada. Later workers showed that the

disease was associated with a virus that was transmitted

mechanically and also by the nematode Xiphinema americanum Cobb. to herbaceous plants (Nyland 1961 ; Nyland et al.

1969). The only report of this virus in Rubus is from red

raspberry sent from Quebec, Canada, to Scotland (Jones and

Badenoch 1981); this is also the only report of the virus

occurring outside the western seaboard of North America.

Economic Importance

The extent of infection in commercial raspberry crops is not

known. The few infected plants detected in Scotland showed

no obvious symptoms, and the effects on growth and yield

are not known.

Symptoms on Natural and Experimental Hosts

Rubus hosts. Naturally infected plants of a red raspberry

seedling showed no obvious foliar symptoms when kept in an

unheated gauze house. No symptoms developed in plants of

R. bartonianus Peck cv. 'Ashton Cross'; R. henryi Hemsl.

and Kunze, R. idaeus L. cvs. 'Glen Clova', 'Mailing Jewel',

and "Norfolk Giant'; R. laciniatus Willd.; and/?, occidentalis

L. infected by graft inoculation (Jones et al. 1985).

Herbaceous hosts. Cherry isolates of cherry rasp leaf virus

(CRLV) have been found symptomlessly infecting many

weed species in CRLV-affected cherry orchards. No

information is available for the Rubus isolate; however, this

isolate was mechanically transmitted to several herbaceous

plants and was symptomless in most. The following

developed symptoms: Chenopodium amaranticolor Coste

and Reyn. and C. quinoa Willd. showed occasional faint

chlorotic local lesions in 5 days followed by a weak systemic

veinclearing or mottle in 7 to 8 days (figs. 302 and 303). C.

murale developed necrotic local lesions in 4 to 5 days (fig.

304) followed by a pronounced systemic mottle or severe

systemic necrosis in 8 to 10 days (fig. 305). Cucumis sativus

L. cv. 'National Pickling' and Phaseolus vulgaris L. cv.

'The Prince' developed faint chlorotic local lesions in 7 days

Figure 302. — Systemic chlorotic veinclearing in

leaves of C. quinoa infected with cherry rasp leaf virus.

(Copyright Scottish Crop Research Institute.)

Figure 303. — Systemic mottle in leaves of Chenopodium quinoa Infected with cherry rasp leaf virus.

(Copyright Scottish Crop Research Institute.)

and symptomless systemic infection. Several other species

became infected symptomlessly (Jones et al. 1985). Cherry

isolates of CRLV differ in the severity of symptoms they

cause but, unlike all the cherry isolates reported by Hansen et

al. (1974), the Rubus isolate infected Spinacia olerácea L.

Natural and Experimental Transmission

Apart from experimental transmission by mechanical inoculation with sap and by grafting, no information is available

for the Rubus isolate. Natural transmission of CRLV in

cherry orchards, however, is by the nematode Xiphinema

americanum, which appears to be an efficient vector (Nyland

et al. 1969; Hansen et al. 1974). In one experiment, X.

diversicaudatum (Micol.) Thome failed to transmit CRLV

(Nyland et al. 1969).

Cherry isolates are seed-borne in C. quinoa and Taraxacum

officinale Weber and have been detected in pollen of infected

cherry (Williams et al. 1963). The role of pollen infection in

seed transmission was not determined. The pattern of spread

in cherry orchards suggests that transmission by nematodes is

the only natural means of spread (Hansen et al. 1974).

241
Properties of the Causal Agent

For a detailed description of the virus, see Stace-Smith and

Hansen (1976a) and Jones et al. (1985). The virus shows

many of the properties of nepoviruses. In sap of C. quinoa,

the Ruhus isolate survived dilution to 10^ but not 10-,

Figure 304. — Necrotic local lesions in a C. murale

leaf caused by cherry rasp leaf virus infection.

(Copyright Scottish Crop Research Institute.)

Figure .305. — Severe systemic necrosis in C. nuinile

caused by cherry rasp leaf virus. (Copyright Scottish

Crop Research Institute.)

heating for 10 min at 55° but not 60°C, and storage for at least

16 days at 18° or 4°C (Jones et al. 1985). The virus is

relatively unstable and difficult to purify in quantity; however

the following two methods seem better than most others: (1)

Extract infected tissue in cold 0.5 M borate buffer containing

0.05 M EDTA + 0.02 M mercaptoethanol (pH 6.5), clarify

with ammonium sulphate (15 g/100 ml extract), and

concentrate the virus by differential centrifugation (StaceSmith and Hansen 1976b). (2) Extract infected tissue in 0.1

M tris-HC 1 + 0.2% thioglycerol (pH 7) and chloroform ( 1 g

leaf: 2 ml buffer: 2 ml chloroform). Precipitate the virus

from the aqueous phase by adding 4% polyethylene glycol

(mol. wt. 6000). Further clarification and concentration is by

differential centrifugation and resuspending pellets in 0.01 M

tris-HCl + 0.2 M NaCl (pH 7) (Jones et al. 1985).

Purified virus preparations contain isometric particles about

28 nm in diameter. Few particles observed in the electron

microscope are penetrated by negative stain (fig. 306).

Preparations of particles of the Rubus isolate sediment as two

nuclcoprotein components with sedimentation coefficients of

about 89 S and 115 S. Particles of CLRV isolates studied

contain three polypeptides of estimated mol. wts. of 26,000,

23.000 and 21,000 and two RNA species of mol. wts. 2.56

X 10" and 1.26 x 10" daltons. and appear to contain a

genome-linked protein necessary for infectivity (Jones et al.

1985).

AU cherry isolates appear to be serologically indistinguishable (Hansen et al. 1974; Stace-Smith and Hansen 1976b),

and the Rubus isolate was serologically indistinguishable

from a cherry isolate (Jones et al. 1985).

Detection and Identification

No symptoms occurred in the few red raspberry plants

infected naturally or in graft-inoculated plants of R. henryi,

R. idaeus cvs. 'Glen Clova' and 'Norfolk Giant', or R.

occidentalis. species used as indicators for other Rubus

viruses (Jones et al. 1985). Detection, therefore, has relied

on mechanical transmission to herbaceous test plants;

however at certain times of the year, only very faint

symptoms develop in C. quinoa and A', clevelandii, which

could make detection difficult. The use of species such as

Chenopodium murale and Cucumis sativus that develop more

diagnostic symptoms might help overcome this. The virus

can be identified only by serological tests.

Control Procedures

The cherry isolate is efficiently transmitted by Xiphinema

americanum, and it is likely that the Rubus isolate is also

spread by this means. Control measures, therefore, are the

same as for other nematode-transmitted viruses (see the

chapters on "Nematode-Borne Diseases" in the Rubus section,

p. 204-228). Virus-detection tests can be used to eliminate

infected plants from material to be propagated, thus

preventing the widespread distribution of infected material.

No attempts have been made to eliminate the virus from

infected plants.

242
i

Figure 306. — Elcclmn micrograph of a purified

preparation of cherry ra^p leaf virus particles stained in

2% ammonium molybdate, pH 6.5. Bar represents 100

nm. (Copyright Scottish Crop Research Institute.)

Remarks

Symptoms of the virus in some herbaceous hosts could be

confused with those of some nepoviruses (see above) or

isolates of tobacco streaic virus (see "Tobacco Streak Virus in

Rubus," p. 235), and the virus can be identified

unequivocally only by serological tests. The virus is

serologically unrelated either to nepoviruses, or to the virus

causing cherry Eola rasp leaf or other viruses inducing

enations in cherry (Stace-Smith and Hansen 1976a).

%'1Í- Bramble^ Yellow Mosaicy;

By D. J.¿Engelbrecht

Additional Common Names

None.

History and Geographic Distribution

Bramble yellow mosaic disease, caused by bramble yellow

mosaic virus (BrYMV), was found in an isolated patch of

wild trailing blackberry (Riihus rigidus Smith) in the Western

Cape Province of South Africa and described by Engelbrecht

and van der Walt (1974).

Economic Importance

Unknown.

Symptoms

Natural host. Pronounced yellow mosaic and line-pattern

symptoms develop on the leaves of the only known natural

host, R. rigidus. during early spring (fig. 307). Usually, no

distinctive symptoms are detectable on the foliage of young

canes after early spring. Furthermore, as the season

advances, the yellow areas on affected leaves tend to bleach

to a bright calico.

Figure 307. — Leaves of Ruhus rigidus naturally

infected with bramble yellow mosaic virus, showing

yellow mosaic and line-patterns.

Figure 308. — Mild transient mottle on a leaf of/?«è«i

henryi experimentally infected with bramble yellow

mosaic virus.

Experimental hosts by grafting. Leaves of grafted R.

henryi Hemsl. and Kuntze developed a mild transient

chlorotic mottling (fig. 308). On 'Royal Sovereign' {Fragaria X ananassa Duch.), a mild mottling accompanied by a

pronounced veinal necrosis was evident. Symptoms persisted

in affected plants; however, in Fragaria vesca L. cv. 'EM-l'

symptoms were more severe and progressive. An initial

interveinal chlorosis (fig. 309), followed by a leaf-necrosis

and dwarfing, led to the eventual death of affected plants.

Experimental hosts by sap transmission. Chenopodium

murale L. is an excellent host for the detection of BrYMV by

mechanical inoculation with infected blackberry or strawberry plant sap, but the virus is difficult to transfer from C.

murale to other herbaceous hosts. Large irregular yellow

chlorotic lesions developed on inoculated C. murale leaves

243
Figure 309. — Interveinai chlorosis on a leaf of

Fragaria vesca newly infected with bramble yellow

mosaic virus.

Figure 310. — Bramble yellow mosaic virus symptoms

on Chenopodium murale. Left, irregular necrotic

lesions on inoculated leaf; right, systemic necrotic

rings.

after 7 to 10 days. The lesions, which gradually coalesced,

became necrotic. This was followed by the development of

systemic yellow necrotic rings (fig. 310).

Symptoms were also observed on the following plants tested:

C. quinoa Willd. Pinpoint necrotic lesions appeared 10 to 15

days after inoculation, followed by a mild systemic chlorotic

mottling.

Gomphrena globosa L. cv. 'Rosé'. Local white necrotic

spots surrounded by purple halos.

Nicotiana tabacum cv. 'White Burley'. Chlorotic spots on

inoculated leaves about 3 wk after inoculatioin. Virus was

not recovered from symptomless secondary tobacco leaves.

Species that did not show symptoms and from which virus

could not be retrieved included Cucumis sativus L.

(cucumber). Petunia hybrida Vilm. (petunia), and Phaseolus

vulgaris L. (bean) (Engelbrecht 1963, 1976).

Transmission

Natural spread. Unknown in Rubus.

Graft transmission. BrYMV transmission by cane inarching

and runner-to-cane inarching has been demonstrated for R.

henryi and strawberry, respectively. Back transmission of

BrYMV to F. vesca cv. 'EM-l' plants, following inarching

of the stems of infected C. murale plants, was also confirmed

(Engelbrecht 1976).

Mechanical transmission. BrYMV is easily transmitted

mechanically from blackberry and strawberry to C. murale.

provided nicotine is added to the extracting solution. Infected

R. henryi failed to yield virus.

Seed transmission. Progeny seedlings raised from systemically infected C. murale showed 86 to 100% infected

seedlings. Symptoms usually appeared 2 to 3 wk after

transplanting and were similar to the systemic reaction,

though milder, on the mother plant.

Detection

The mosaic and line-pattern symptoms on leaves of affected

blackberry plants can be readily recognized throughout the

growing season.

Identification

BrYMV possesses filamentous particles with a modal length

of 730 nm (Engelbrecht 1976). The characteristic particles

have only been detected in sap from C. murale infected with

BrYMV from blackberry and experimentally infected

strawberry. The virus remains infective in C. murale sap

after dilution to 10"' or 10 min at 50°C or 8 days at 20°C.

Infectivity was lost at pH 6.0 and after prolonged freezing but

was only slightly decreased after 24 h at -20°C. Attempts to

purify sufficient virus for antiserum production have not yet

succeeded.

Control Measures

No information is available.

Remarks

This virus differs in properties from two other filamentous

viruses reported to occur in Rubus. namely, bean yellow

mosaic (Provvidenti and Granett 1974) and wineberry latent

virus (Jones 1974). (See "Wineberry Latent Virus," p.

239.) A previous suggestion (Engelbrecht 1976) that

BrYMV virus be classified as a potyvirus on the basis of

particle length must be considered premature.

244
t

4iBlackberry Calico y

By R. H.[Converse

Additional Common Names

Loganberry calico, Boysenberry calico, Chehalem calico.

Marion calico, yellow blotch mosaic; blackberry calico

disease (BCD).

History and Geographic Distribution

The disease was described by Wilhelm (¡951) and Wilhelm

et al. (1951). It occurs in California and Oregon and probably

is present wherever U.S. Pacific coast trailing blackberry

cultivars like 'Boysen', 'Logan', 'Thornless Logan' ('Loganberry'), and 'Marion' are grown throughout the world.

Economic Importance

The disease almost universally infects some cultivars like

'Thornless Logan' and 'Chehalem', which nevertheless bear

productive, horticulturally acceptable crops. In California,

'Thornless Logan' with BCD grown without irrigation may

develop yellow areas in leaves of floricanes, which may then

become damaged by sun and wind, especially in dry years.

Symptoms on Natural and Experimental Hosts

On naturally infected clones of 'Boysen', 'Chehalem',

'Marion', 'Ollalie', and 'Thornless Logan', chlorotic areas

appear on leaves of floricanes at fruiting time. The chlorosis

may be blotchy and without pattern or may occur as distinct

rings and line patterns. Various shades of yellow, verging on

white, occur and occasionally some red coloration (fig. 311).

Leaves exhibiting severe calico symptoms may wither and

drop off in periods of high light intensity and drought stress.

On graft-inoculated 'Boysen', 'Marion', 'Thornless Logan',

and 'Young' blackberries in the greenhouse, BCD caused

symptoms similar to those expressed naturally in the field,

but often only a few leaves showed symptoms, which were

sometimes limited to a few, very small, chlorotic spots on

leaf blades (Converse and Kowalczyk 1980). Symptom

expression of BCD in floricanes appears to be favored by

high light intensity, and some BCD-infected cultivars like

'Thornless Logan' rarely develop symptoms in the greenhouse or outdoors in predominantly cool, cloudy growing

conditions.

Natural and Experimental Transmission

Much Pacific coast blackberry nursery stock, particularly

'Thornless Logan', is infected with BCD. BCD has been

observed to spread naturally in the field in 'Chehalem' and

'OR-US 1600' blackberries.The wild Pacific coast trailing

blackberry (Riibii.s iir.sinu.s Cham. & Schlecht.) has been

found to be naturally infected (R. H. Converse, unpublished

data).

Experimentally, BCD has been transmitted by approach graft

to 'Boysen', 'Marion', 'Thornless Logan', 'Young', and R.

ulmifolius Schott var. inermis (Willd.) Focke (Converse and

Kowalczyk 1980; Wilhelm 1951: Wilhelm et al. 1951).

BF^3

I^^HÍVB? ^

mLmñ

Figure 311.—Calico disease symptoms in leaves oí (A)

'Logan' and (B) 'Marion' blackberries.

Symptoms did not develop after BCD was graft inoculated to

R. henryi Hemsl. and Kuntze, Fragaria ve.^ca L. var.

semperflorens (Duch.) Ser. cv. 'Alpine', or after sap

transmission to Nicotiaiui tabaciim L. cv. 'Turkish' (Williams and Wagnon 1970). Contradictory results were

obtained when BCD was approach grafted to R. procerus

P. J. Muell. and R. occidentalis L. (Wilhelm et al. 1951;

Williams and Wagnon 1970; Converse and Kowalczyk

1980).

Vector transmission of BCD has not been studied. A leaf

variegation that was graft transmissible from wild R.

allegheniensis Porter to blackberry and black raspberry was

reported in Maryland (Horn 1948). Its relationship to BCD is

unknown. Johnson (1972) has reported the graft transmissibility of a calico disorder in 'Puyallup' red raspberry. BCD

sources grafted to 'Puyallup' failed to induce any symptoms

(Converse and Kowalczyk 1980).

Properties of the Causal Agent

Nothing is known of the nature of the causal agent of BCD

except that it is graft transmissible and that raspberry bushy

dwarf virus is not necessarily associated with it. Comparable

graft transmission studies indicate that BCD from

245
'Chehalem' blackberry had a different host range and

symptomatology than BCD from 'Marion' and 'Thomless

Logan' blackberry (Converse and Kowalczyk 1980). The

names "Chehalem calico," "Loganberry calico," "Boysenberry calico," and "Ollalie calico" will probably continue to

be useful in designating individual variants of BCD until their

etiology is better understood.

Detection and Identification

'Logan' seedlings and 'Marion' blackberry have been

used as indicator hosts for BCD in graft transmission studies

(Wilhelm et al. 7957; Converse and Kowalczyk 1980). On

'Marion', the minimum incubation period in the greenhouse

after grafting varied from 6 mo to 2 yr. Exposing grafted

'Marion' plants to winter dormancy conditions may shorten

incubation time and heighten symptoms. Many trailing

blackberries are infected with tobacco streak virus. (See

"Tobacco Streak Virus in Rubus,"' p. 235.) 'Marion-65',

a clone that is free from known viruses and viruslike

diseases, is killed back along the shoot below the graft for a

few nodes when approach-grafted with a plant infected with

tobacco streak virus, so that it is not possible to use

'Marion-65' as an indicator for BCD in plants infected with

both diseases. In such cases, 'Logan' seedlings can be used as

indicators.

Control Procedures

The principal control method is the use of Pacific coast

trailing blackberry cultivars that are known to be free of

BCD. Recently, a heat-treated, shoot-tip-propagated clone of

'Thornless Logan' from Canada (R. Stace-Smith, unpublished results) has been found to be free of BCD and has been

released as 'Thomless Logan AC-2', completing a collection

of clones of major Pacific coast blackberry cultivars that are

known to be free from BCD (Converse and Kowalczyk

1980).

Heat treatment of 'Thornless Logan' plants at 37°C for 17

days did not eliminate BCD (Williams and Wagnon 1970),

but the AC-2 clone was derived form a shoot tip that was

propagated from a 'Thornless Logan' plant held for 35 days

at 37°C (R. Stace-Smith, unpublished results).

Remarks

BCD is very poorly understood. The demonstration of its

graft transmissibility allows distinctions to be made between

this infectious disease and purely genetic disorders, with

which it has often been confused in the past. Because BCD is

so widely distributed in many Pacific coast blackberry

clones, often without visible symptoms, its possible

deleterious effects in Rubus, alone and in combination with

other viruses or viruslike diseases, have been largely ignored.

Further research on the identification and relationships of the

causal agent(s) and its rapid identification will permit the true

economic impact of BCD to be more correctly evaluated and

its control to be improved.

Miscellaneous Virus and Viruslike Conditions and

Disorders

/

,^^Apple Mosaic Virus in Rubusj/ .

By G.IBaumann, R.[Casper, and R. H. Converse

Additional Common Names

None.

History And Geographic Distribution

Apple mosaic virus (ApMV), a member of the ilarvirus

group, was found in samples of symptomless plants of Rubus

ursinus Cham, and Schlecht., R. idaeus L., and R.

occidentalis L. on both coasts of the United States (Converse

and Casper 7975). Latent infection of red raspberry (R.

idaeus L.) plants by ApMV was reported in Germany

(Baumann et al. 1982). These authors also reported the

association of ApMV with yellow mottling and line-pattern

symptoms in one plant of red raspberry cv. 'Schoenemann',

which was found in northwest Germany.

Economic Importance

The economic importance of ApMV in Rubus is not yet

known.

Symptoms on Natural and Experimental Hosts

Natural hosts of ApMV include the genera Malus (Bradford

and Joley 1933), Prunus (Barbara 1980), Rosa (Fulton 1952,

1968), Aesculus (Sweet and Barbara 1979), Betula (Gotlieb

and Berbee 7973), Humulus (Albrechtova et al. 7979), and

Rubus (Converse and Casper 7975). Although ApMV is

generally symptomless in infected Rubus, infected plants of

the other genera mentioned frequently show yellow or white

leaf mosaic and line-pattern symptoms. Virus isolates from

naturally infected hosts have been transmitted by grafting to a

wide range of species in the genera Aesculus, Betula,

Chaenomeles, Crataegus, Cydonia, Fragaria, Malus, Prunus, Pyrus, Rosa, and Sorbus. Mosaic and leaf-pattern

symptoms were produced in each of these genera (Posnette

1963; Gotlieb and Berbee 1973; Sweet and Barbara 7979).

Latent occurrence of ApMV was found in Rubus ursinus

Cham, and Schlect. cv. 'Boysen' (California and Oregon), in

R. occidentalis L. cvs. 'AUeghany' and 'Munger' (Massachusetts and Oregon, respectively), and in R. idaeus cvs.

'Willamette' (Oregon), 'Korbfüller', and 'Schoenemann'

(Germany).

In a red raspberry field in Germany (cv. 'Schoenemann'), in

which latent infection by ApMV had been identified

(Baumann et al. 7982), one plant was found showing

conspicuous leaf symptoms. These consisted of a bright

yellow-white mosaic (fig. 312), sometimes accompanied by

246
Figure 312.—A. Bright yellow mottling and line-pattern

on leaves of red raspberry plants from which apple

mosaic virus has been isolated; B. leaf symptoms of red

raspberry cv. 'Mailing Landmark' graft inoculated with

the apple mosaic virus isolate from 'Schoenemann'.

small, light-green rings and spots. No fruit symptoms were

observed, and there appeared to be no significant reduction in

the growth of canes showing leaf symptoms.

The disease was transmitted by shoot or bark shield grafts to

virus-indexed red raspberry plants (cvs. 'Schoenemann',

'Mailing Landmark", and 'Baumforth's Seedling B') which

developed leaf symptoms similar to those shown by the

original source plant. Prunus serrulata L. cv. 'Shirofugen'

grafted with bark shields from visibly infected 'Schoenemann' developed necrosis and gum production around the

inserted bark shields. However, the reaction was less severe

than that usually demonstrated by Prunus necrotic ringspot

virus (Baumann et al. I9H2).

The original source plant as well as the experimentally

infected woody hosts were found to react in ELISA tests with

ApMV antiserum. No other known Rubus viruses were found

in these plants. The ApMV isolate from the 'Schoenemann"

field plant showing symptoms was transmitted by sap

inoculation from infected raspberry to several herbaceous

hosts, producing the symptoms noted, which in general

resemble those of previously described ApMV isolates on the

following hosts:

Cucumis sativus L. cv. 'Straight Eight' developed

green-yellow local lesions on the rubbed cotyledons.

Sometimes, chlorotic spots developed on the first true leaves,

often leading to their death.

Chenopodium quinoa Willd. Chlorotic-necrotic lesions

developed on the inoculated leaves, and systemic symptoms

consisted of sharply defined water-soaked rings, lines, and

spots.

C. amaranticolor Coste and Reyn. Inoculated plants

showed chlorotic-necrotic lesions on the rubbed leaves but no

systemic symptoms.

C. capitatum (L.) Asch. Numerous small chlorotic lesions

developed on the inoculated leaves and single chlorotic rings

around dark-green or necrotic centers on systemically

infected leaves.

Phaseolus vulgaris L. cvs. 'Pinto' and 'Black Turtle'

showed severe vein necrosis on the inoculated leaves

followed by tip necrosis.

Vif^na unguiculata (L.) Walp. Inoculated leaves showed

chlorotic lesions and red or brown necrotic spots and lines.

The tips curled downward, and the plants stopped growing.

Nicoticma clevelcmdii Gray, N. rustica L., N. uibacum L.

'White Burley", and Petunia hybrida Vilm. did not become

infected.

Natural and Experimental Transmission

Converse and Casper (1975) stated that field transmission of

ApMV occurred in Oregon where root graft transmissions

were unlikely to have occurred when plants of red raspberry,

black raspberry, and blackberry that had indexed free from

ApMV were planted in the field. About 92% of red raspberry

plants became infected by ApMV within 24 mo and 16% of

the blackberry plants became infected after 12 mo. ApMV is

not known to spread naturally other than by root grafting in

any of its other reported hosts (Fulton 1972). Thus, the mode

of field transmission of ApMV in its Rubus hosts requires

further investigation.

247
Experimental transmission of the yellow mosaic and linepattern found in the 'Schoenemann' plant in West Germany

was conducted by bottle grafting (shoot grafting) or bark

shield grafting (Baumann et al. 1982). Symptoms developed

on leaves of inoculated plants 7 mo after inoculation when

the experiment was started in August, but 4 wk after it was

started in March or April. The 'Schoenemann' isolate of

ApMV was transmitted by sap inoculation to herbaceous

hosts when buds from infected red raspberry plants were

ground in 0.05 M phosphate buffer (pH 7.0) containing 2%

polyvinylpyrrolidone (mol. wt. 10000) (Martin and Converse 1982) and rubbed on leaves of young herbaceous

indicator plants.

Properties of the Causal Agent

ApMV is a member of the ilarvirus group and is an isometric

virus for which particles 25 to 26 and 29 to 30 nm in diameter

have been reported, corresponding to sedimentation coefficients of 88 and 1175, respectively (de Sequiera 7967).

Only the heavier particles are infective, but all are

serologically and electrophoretically homogenous. The

A260/A280 for ApMV is about 1.5 (Fulton 7972). The RNA

content of ApMV has not been determined directly, but it is

16% for the distantly serologically related Prunus necrotic

ringspot virus. The mechanism of natural transmission in

Rubus is unknown; however, ApMV is commonly transmitted by vegetative propagation and natural root grafts of other

woody hosts.

Detection and Identification

ApMV was easily detected and identified by ELISA using

antiserum against the RV-1 (rose virus-1) isolate of apple

mosaic virus (Casper 1973). Tests by agar gel diffusion are

also possible (Converse and Casper 1975). Indexing should

be done between the end of March and the end of April using

leaf buds of very young primocanes. Results of tests

conducted later in the season may not be reliable.

Control Procedure

The use of certified planting stock and the selection of

nuclear stock materials shown to be free from ApMV by

serological tests are recommended. Both apple mosaic and

rose mosaic viruses have been easily eliminated from

cultivars of several rosaceous hosts other than Rubus by brief

hot air therapy (Nyland and Goheen 1969).

Remarks

In Oregon, plants of red raspberry cv. 'Willamette' which

had indexed positive for ApMV were also found to react

positively with tomato ringspot virus antiserum. Tobacco

streak virus was found to occur together with ApMV in

Rubus ursinus 'Boysen' and also in R. occidentalis cvs.

'Alleghany' and 'Munger' (Converse and Casper 1975). The

significance of double infections in the occurrence of ApMV

in U.S. Rubus is not known.

Since the 'Schoenemann' isolate of ApMV has not yet been

transmitted from herbaceous hosts to red raspberry plants, it

is not known whether more than one ApMV strain exists in

Rubus or whether the yellow mosaic and line pattern found in

'Schoenemann' is due to a mixed infection by ApMV and an

unknown Rubus virus. Symptoms of the 'Schoenemann'

isolate of ApMV and raspberry bushy dwarf virus (see

"Raspberry Bushy Dwarf," p. 229) in sap inoculated

Chenopodium quinoa are very similar to each other and can

be differentiated by ELISA (Baumann et al. 1982).

J-

^ Rubus Virus Diseases of Minor or Undetermined

Significance //

By R.|Stace-Smith

Those involved in compiling literature on virus diseases

affecting a particular crop are always faced with the awkward

task of attempting to relate some of the early published work,

usually of a preliminary and descriptive nature, with more

comprehensive reports that followed. We would prefer to

have the tidy situation where early observations and reports

could be correlated with what is known today to form a more

comprehensive picture of how the significance of individual

diseases has changed with the introduction of new cultivars

and modified cultural practices. Alas, such a Utopian state is

not possible with respect to the Rubus virus diseases. It is

almost impossible to relate some of the earlier work,

compiled on the basis of acceptable standards at the time,

with the various diseases that are recognized today.

This is not meant to downgrade the value of the earlier work.

With the many developments in the science of plant virology,

the accepted criteria as to what body of information is

necessary to designate a causal agent as "new" or "previously

undescribed" has been upgraded considerably. The literature

contains many examples of known viruses redescribed under

new names or viruses so inadequately described that it is

doubtful that they are really new. The purpose of this chapter

is to include a brief description of a few viruses that exist in

the literature but whose identity is still uncertain and to

record reports of isolation of viruses from Rubus crops that

are of local or minor significance. A similar chapter was

included in "Virus Diseases of Small Fruits and Grapevines"

(Converse 1970b).

Tobacco necrosis virus. Tobacco necrosis virus (TNV) is

detected by transmission to herbaceous indicator plants from

root extracts of a wide range of herbaceous and woody plants.

The virus occasionally invades woody crop plants systemically and, in such instances, TNV can be transmitted to

indicator plants from aboveground plant parts. Although

sporadic disease losses have been reported, TNV is not

usually considered to cause any significant damage to a crop.

Cadman (1961b) reported that TNV was commonly isolated

from roots of field-grown raspberry plants in Scotland. The

248
virus has not been isolated from other raspberry-growing

areas, probably because most inoculations are made from

aboveground plant parts.

Tobacco rattle virus. Tobacco rattle virus (TRV) infects

many species of cultivated and wild plants in many parts of

the world. Many of the infected plants develop symptoms,

but others can be infected symptomlessly. Symptomless

infections also occur when TRV is confined to the roots of

infected plants. Cadman (1961b) reported that the virus was

occasionally isolated from the roots of raspberry plants in

Scotland.

Black raspberry streak. This virus disease was allotted a

full chapter in "Virus Diseases of Small Fruits and

Grapevines" (Converse 1970a). However, since no new

information has been published since 1970 and since little is

known about the disease, it was considered appropriate to

relegate it to the minor disease category. The disease was

named for the characteristic faint blue or gray streaks that

develop on or under the surface bloom of young canes.

Positive identification of the disease is difficult because

streak development is influenced by environmental conditions. Other than black raspberry, there is no satisfactory

indicator host. Graft and dodder transmission have been

demonstrated, but the mechanism of natural spread is

unknown.

Bean yellow mosaic virus. Provvidenti and Granett (1974)

reported the isolation of a severe strain of bean yellow mosaic

virus from several plants in New York State, including two

red raspberry plants. No information is given as to whether

the infected raspberry plants showed any symptoms.

Blackberry sterility. Blackberry sterility is occasionally a

major problem in nurseries and fruiting fields in some areas

of eastern and central United States, where blackberries are

grown. In affected plants the flowers appear normal but none

or only a few of the drupelets develop (fig. 313). Some of the

affected plants may exhibit a mosaic pattern on the leaves,

but, as noted by Hemphill (1970), this symptom may be

caused by the presence of other viruses. Further, sterility in

Rubus may be induced by environmental and genetic factors

(Hemphill 7970). At present, it is not possible to say whether

there is a virus, distinct from the viruses that are known to

affect Rubus, which induces sterility symptoms.

Necrotic fernleaf mosaic. The disease was described on the

basis of observations and grafting experiments on a single

'Cuthbert' red raspberry plant in Ontario, Canada (Chamberlain 1941). Leaves of the affected plant were small, narrow,

and extensively serrated, giving a "fernleaf appearance. In

addition, leaves of the affected plant exhibited ringspot

markings, necrotic spots, stunting, and retarded foliation,

symptoms that are similar to the yellow blotch curl disease of

red raspberry in Ontario (Chamberlain 1938). Clones of these

two field diseases have not been retained, so at this time one

Figure 313.—Blackberry sterility disease: A. Completely sterile flowers of infected 'Lawton' blackberry;

B. partially to completely sterile flowers of an unnamed

blackberry cultivar. (Courtesy D. D. Hemphill, University of Missouri.)

can only speculate on the identity of the viruses involved. As

noted by Freeman and Stace-Smith (1968), circumstantial

evidence strongly suggests that the yellow blotch curl disease

was caused by infection with tomato ringspot virus. One

could speculate further that necrotic fernleaf mosaic disease

was induced by a complex of viruses, one of which was

tomato ringspot virus (see "Tomato Ringspot Virus in

Rubus," p. 223).

Raspberry yellow spot. Yellow spot was the name applied

to a virus disease of wild and cultivated raspberries in Poland

(Basak 1974). The most characteristic symptom of the

disease, as the name implies, is the yellow spotting of the

leaves. The spots are of variable size and shape, scattered

irregularly over the leaflets, occasionally so numerous that

they cover most of the leaf blade, giving the entire plant a

yellow cast. As the season progresses, the yellow color

gradually fades. The spotting causes uneven growth of the

leaflets and results in leaf curiing and deformity. Plants that

are severely affected are stunted. Intensity of the symptoms

249
varies from year to year depending upon weather conditions

—particularly severe symptoniis occur in years with cold

springs.

The virus was graft transmitted and induced symptoms on

Rubusprocerus P. J. Muell., R. phoenicolasius Maxim., and

R. occidentalis L. R. henryi Hemsl. and Kuntze and R.

xanthocarpus Rur. and Franch., which were infected by

grafting, did not show symptoms. The virus was also

transmitted from red raspberry to black raspberry seedlings

by means of the aphid Amphorophora idaei Borner, and it was

concluded that this aphid is the vector under natural field

conditions. Wild raspberries appear to be the main source of

the disease; the virus is transmitted from them by aphids to

commercial plantings.

While direct comparisons have not been made with other

raspberry viruses that are transmitted by A. idaei, Basak

(¡974) is of the opinion that raspberry yellow spot differs

from virus diseases reported from other countries.

J:" l Rubus Diseases in Great Britain With Presumed but

Unproved Viral Etiology "^

By A. T.jJones [J, "

A mottling disease of 'Bedford Thornless' blackberry.

This disease has been observed in Scotland. It is

characterized by a chlorotic mottling of leaves, often

adjacent to the main veins. Symptoms are most pronounced

on leaves on fruiting canes (fig. 314) and are most evident in

late spring. Similar symptoms have been observed in

'Bedford Giant' blackberry plants in England and Scotland.

No virus was detected by mechanical inoculation of sap from

such affected plants to herbaceous test plants. However, graft

inoculation of diseased material to Rubus indicators detected

raspberry leaf mottle and raspberry leaf spot viruses in some

affected plants but not others, whereas scions from all

diseased plants induced tip necrosis in graft-inoculated R.

occidentalis suggesting that black raspberry necrosis virus,

raspberry leaf mottle virus, or raspberry leaf spot virus were

present. Whether these viruses are causal agents of the

disease is not known. (See "Black Raspberry Necrosis,"

p. 178.)

Grinkle and sterility of 'Bedford Thornless' blackberry.

This disease is characterized by a mottling and severe

crinkling of the leaves, especially in fruiting canes (fig. 314).

Most laterals are sterile (fig. 315). The cause of this disease

is not known, but no virus was detected by mechanical

inoculation of sap from such plants to herbaceous test plants.

Leaf curling in 'Norfolk Giant' red raspberry. A single

plant of this cultivar showing severe curling of the young

leaves of primocanes (ñg. 316) was observed in southern

England. The plant contained raspberry bushy dwarf virus (see

"Raspberry Bushy Dwarf," p. 229) but was apparently free

of other mechanically transmissible viruses. The agent of the

Figure 314.—Leaves from fruiting cane of 'Bedford

Thornless' blackberry from plants affected with:

mottling (left), crinkle (right), and unaffected (center).

(Copyright Scottish Crop Research Institute.)

Figure 315.—Fruiting canes of 'Bedford Thornless'

blackberry from plants affected with: mottling (left),

crinkle and sterility (right), and unaffected (center).

(Copyright Scottish Crop Research Institute.)

Figure 316.—A cane of 'Norfolk Giant" red raspberry

showing small, tightly curied leaves at the tip.

(Copyright Scottish Crop Research Institute.)

disease was graft transmitted to other 'Norfolk Giant' plants in

which it induced leaf curling. Although the symptoms closely

resemble those of raspberry leaf curl that occurs in North

America (see "Raspberry Leaf Curi," p. 187), no symptoms

occurred in graft-inoculated plants of/?, henryi, R. occidentalis, and R. phoenicolasius 3 mo after inoculation.

250
V

t}^

Viruslike Disease Symptoms in Rubus in Great Britam jj

By A. T.!Jones ' ^ c

A number of viruslike symptoms in Rubus spp. are known to

be caused by factors other than virus infection. These are most

frequently symptoms induced by chemical or pest damage or

by genetic causes. A discussion of viruslike symptoms in

North America Rubus was prepared by Converse (1970d).

Chemical Damage

Several chemicals frequently used in the management of

raspberry and blackberry plantations are known to induce

some damage in these crops. At least three chemicals have

been observed to induce viruslike symptoms in some Rubus

cultivars in Great Britain.

Fenitrothion (an organophosphorus insecticide). In Scotland, Woodford and Gordon (1978) observed that plants of

the red raspberry cvs. 'Mailing Admiral' and 'Mailing

Delight' showed numerous chlorotic spots and flecks in

leaves sprayed a few days previously with fenitrothion (fig.

317). Greenhouse experiments confirmed that these symptoms in these two cultivars and somewhat milder symptoms

in cv. 'Glen Clova' were due to their response to the

chemical; cv. 'Mailing Jewel' showed no symptoms after

spraying. They also observed that the leaf symptoms were

more pronounced after plants were sprayed in bright sunlight.

Such symptoms could easily be confused with virus infection

or could mask symptoms due to virus infection; however, in

commerce, symptoms would tend to develop uniformly on

almost all sprayed plants.

Glyphosate (a translocated herbicide). Plants of the red

raspberry cv. 'Glen Clova' have been observed with extensive

proliferation of fruiting laterals; leaves of such laterals tended

to be thin and distorted (fig. 318). Such plants occurred along

the periphery of a plantation adjacent to a crop sprayed several

months earlier with glyphosate, and such sytmptoms are

believed to be due to spraydrift. Individual plants of the cvs.

'Glen Clova' and 'Mailing Jewel' showing similar symptoms

have also been observed in plantations where spot treatment

with glyphosate has been used for weed control. Similar

symptoms frequently occur in many Rubus cultivars in North

America after plants have been accidentally sprayed with

glyphosate during in-row weed control operation. Symptoms

frequently take several months to develop after application of

the chemical, and great care should be taken to avoid drift to

crops.

Figure 317.—Chlorotic mottling in a leaf of 'Mailing

Admiral' red raspberry sprayed with fenitrothion (left)

and sprayed with water (right). (Copyright Scottish Crop

Research Institute.)

Figure 318.—Proliferation of fruiting laterals and thm,

deformed leaves of "Glen Clova' red raspberry caused by

spray drift of glyphosate. (Copyright Scottish Crop

Research Institute.)

Figure 319.—Leaves of young primocanes of 'Glen

Clova' red raspberry showing chlorotic veinbanding

(left) and veinclearing (right) symptoms following

treatment of the plantation with bromocil. (Copyright

Scottish Crop Research Institute.)

251
Bromocíl (a soil-acting herbicide). A few weeks after

application ofthis chemical in the spring, leaves on new canes

of 'Glen Clova' red raspberry and 'Tayberry' often show

a mild chlorosis. This frequently takes the form of a

veinbanding or vein clearing symptom (fig. 319). Plants tend

to grow out of this symptom, and thus it is distinguishable

from veinbanding mosaic disease (see "Raspberry Mosaic,"

p. 168), the symptoms of which usually persist in plants and

are more extensive.

Pest Damage

In Great Britain, the only pest damage likely to be confused

with symptoms due to virus infection is that caused by the

raspberry leaf and bud mite Phyllocoptes gracilis Nal. (also

known as Eriophyes gracilis Nal.). Feeding damage on leaves

of primocanes and fruiting canes of many red raspberry,

blackberry, and 'Tayberry' cultivars causes chlorotic spots

and blotches of the upper leaf surface. On the lower leaf

surface, areas of feeding damage appear pale green when

compared with the grayish bloom of the unaffected leaf

surface (fig. 320 and 321). Although symptoms can easily be

confused with those of virus infection, the characteristic

appearance of the chlorotic areas on the lower leaf surface

and examination of such leaf areas under the microscope for

evidence of these small, translucent, cigar-shaped eriophyid

mites should prevent misidentification. In exposed raspberry

plantations, mites do not normally reach sufficient numbers

to induce feeding damage, but in sheltered areas, and

especially in hot dry summers, numbers of mites may

increase enormously. Under such favorable conditions, mites

may not only induce symptoms in many leaves but can also

cause malformation and uneven ripening of the fruit (Gordon

and Taylor 7976).

Genetic Causes

Rubus species are prone to genetic abnormalities of one kind

or another and, although many can be identified as such, a

few are similar to those induced by virus infection. Perhaps

one of the most common abnormalities is leaf chlorosis in

raspberry seedlings. In some of these instances, such

chlorosis is associated with infection with raspberry bushy

dwarf virus (see "Raspberry Bushy Dwarf", p. 229), but in

others it is not (Jones et al. 1982), presumably being caused

by genetic abnormality.

The following are some of the kinds of genetically induced

changes that may be confused with virus infection.

Crumbly fruit. This is a condition in which some drupelets

fail to set, often producing malformed fruits. The reduced

number of drupelets that do set are often enlarged and cohere

imperfectly so that the fruit crumbles when picked. Although

infection with some viruses, for example, raspberry mosaic

disease, raspberry bushy dwarf, tomato black ring, and

tomato ringspot viruses, is associated with this condition in

some raspberry cultivars in Great Britain and North America,

it is also known that in many instances it is induced by

Figure 320.—Raspberry leaf and bud mite (Phyllocoptes

gracilis) damage in red raspberry. Upper leaf surface

shows chlorotic spots and blotches. (Copyright Scottish

Crop Research Institute.)

Figure 321.—Raspberry leaf and bud mite (Phyllocoptes

gracilis) damage in red raspberry. Lower surface of the

same leaf shown in figure 320, showing pale green areas

of feeding damage. (Copyright Sottish Crop Research

Institute.)

Figure 322.—Leaves of a red raspberry seedling showing

frilly leaf symptom. (Copyright Scottish Crop Research

Institute.)

252
genetic alterations in the plant. Some of these are associated

with gene mutation, meiotic irregularities, and degeneration

of the embryo sac (Murant et al. 1973\ Jennings 7967;

Daubeny et al. 1967, Virdi et al. 1972a,b). Suitable tests on

affected plants to determine the presence of virus should be

used to determine the cause of the condition.

Frilly leaf. This condition, first noted by Knight et al. (7959),

occurred in self-bred progeny of the red raspberry cvs.

'Baumforth A' and 'Canby'. Affected plants have distorted

young leaves with chlorotic flecks (fig. 322), and the stems fail

to elongate. The condition in cv. 'Baumforth A' is determined

by gene /r, which is linked with gene A, which confers

resistance to the aphid Amphorophora idaei Borner.

A somewhat similar condition has been observed by A. T.

Jones and D. L. Jennings (unpublished observations) in

raspberry seedlings (figs. 323 and 324). However, although

the symptoms were pronounced when plants were grown in a

heated greenhouse, they were inconspicuous or absent when

grown outdoors. No symptoms developed in apparently

normal seedlings from the same family or in the Rubus virus

indicators R. henryi Hemsl. and Kuntze, R. occidentalis L.,

and the R. idaeus L. cvs. 'Mailing Landmark' and 'Norfolk

Giant' when these were graft inoculated with tissue from

affected plants.

Catkin in cv. 'Mailing Jewel'. This condition, reported by

Jennings (7977) and believed to be due to a mutation, was

characterized by some canes of a plant bearing catkinlike

flowers. The flower parts on such canes were replaced by

bractlike structures of decreasing size (figs. 325 and 326)

produced a catkinlike effect.

Lateral-leaf crinkle in cv. 'Glen Clova'. An aberrant cane

of this red raspberry cultivar, showing severely crinkled

leaves which were free from chlorosis (fig. 327), was reported

in Scotland by Jennings (7977). As raspberry leaf curl virus is

not known to occur in Scotland and the condition did not recur,

it is suspected that a mutation from a recessive to a dominant

condition was involved.

^Hl^H^Hn^ i? I^^^H

^^^^^ ^

^cAHiÀk^ 11

à

%

ir

g1

k %V él111

Figure 324.—Enlargement of ligure 323 to sliow delail

of frilly leaf symptom. (Copyright Scottish Crop

Research Institute.)

Figure 325.—A fruiting cane of 'Mailing Jewel' red

raspberry showing 'catkin" symptom of the flowers.

(Copyright Scottish Crop Research Institute.)

Figure 323.—Red raspberry seedlings. Left: normal

seedling; right: seedling showing frilly leaf symptom.

(Copyright Scottish Crop Research Institute.)

253
Figure 326.—Detail of 'catkin' symptom in lig. 325.

(Copyright Scottish Crop Research Institute.)

Rubus Literature Cited

Albrechtova, L., J. Chod, J. Kriz and J. Fencl. 1979.

Nachweis des apple mosaic virus und des tobacco necrosis

virus in Hopfen. Phytopathologische Zeitschrift 94:45-55.

Alcorn, S. M., S. Wilhelm, and H. E. Thomas. 1955. A

mosaic disease of Himalaya blackberry. Phytopathology

45:272-274.

Allen. W. R., T. R. Davidson, and M. R. Briscoe, 1970.

Properties of a strain of strawberry latent ringspot virus

isolated from sweet cherry growing in Ontario. Phytopathology 60:1262-1265.

Ameson, P. A., and A. J. Braun. 1975. Virus diseases of

raspberries. New York State College of Agriculture and Life

Sciences, Cooperative Extension Service. Information Bulletin No. 74. Plant Sciences, Plant Pathology 7, 4 p.

Auger, J., and R. H. Converse. 1982. Raspberry bushy dwarf

and tomato ringspot viruses in Chilean red raspberries. Acta

Horticulturae 129:9. [Abstract.]

Barbara, D. J. 1980. Detecting Prunus necrotic ringspot virus

in rosaceous hosts by enzyme-linked immunosorbent assay.

Acta Phytopatholgica Academiae Scientiarum Hungaricae

15:329-332.

Bamett, O. W., and A. F. Murant. 1970. Host range,

properties and purification of raspberry bushy dwarf virus.

Annals of Applied Biology 65:435-449.

and A. F. Murant. 1971. Differential hosts and some

properties of raspberry bushy dwarf virus. Annales de

Phytopathologie, numéro hors série: 129-139.

Basak, W. 1971. Hosts and properties ofraspberry line pattern

virus. Bulletin de l'Académie Polonaise des Sciences. Série

des sciences biologiques Cl. V: 19:681-684.

1974. Yellow spot — a virus disease of raspberry.

Figure 327.—Lateral-leaf crinkle symptom in a fruiting

cane of 'Glen Clova' red raspberry. (After Jennings

1977: copyright Scottish Crop Research Institute.)

Bulletin de l'Académie Polonaise des Sciences. Série des

sciences biologiques Cl. V. 22:47-51.

Baumann, G. 1980. Gewinnung von gesundem Himbeerpflanzgut. Erwerbsobstbau 22:148-151.

1981. Möglichkeiten und Grenzen der Virusfreimachung von Himbeeren durch Gewebekultur. Obstau

6:88-89.

1982. Elimination of a heat-stable raspberry virus by

combining heat treatment and meristem culture. Acta

Horticulturae 129:11-12.

254
R. Casper, andR. H. Converse. 1982. The occurrence

of apple mosaic virus in red and black raspberry and in

blackberry cultivars. Acta Horticulturae 129:13-20.

and L. H. Turner. 1962. Note on obtaining virus-free

plants of red raspberry through the use of tip cuttings.

Canadian Journal of Plant Science 42:210-211.

Baumeister, G. 1961. Untersuchungen zur Resistenz verscheidener Himbeersorten gegen die virusüberträger Amphorophora rubi (Kalt.) Siñá Aphis idaei (v.d. Goot). Der Züchter

31:351-357.

1962. Untersuchungen zur Genetik der Resistenz

gegen den Vektor Amphorophora rubi (Kalt.) bei

Himbeersorten. Der Züchter 32:1-7.

Beime, B. P. 1954. T\itPrunus- dináRubus-íttáing species of

Macropsis (Homoptera: Cicadellidae). The Canadian Entomologist 86:86-90.

Bennett, C. W. 1927. Virus diseases ofraspberries. Michigan

Agricultural Experiment Station Technical Bulletin No. 80,

38 p.

1930. Further observations on the curl disease of

raspberries. Phytopathology 20:787-802.

1932. Further observations and experiments with

mosaic diseases of raspberries, blackberries, and dewberries.

Michigan Agricultural Experiment Station Technical Bulletin

No. 125,32 p.

Bercks, R. 1962. Serologische Überkreuzreaktionen zwischen Isolaten des Tomatenschwarzringflecken-Virus. Phytopathologische Zeitschrift 46:97-100.

H. Krczl, and G. Querfurth. 1976. Untersuchungen

über einem aus Roter Johannisbeere (Ribes rubrum) isolierten

Stamm des arabis mosaic virus. Phytopathologische Zeitschrift 85:139-148.

Bj0mstad, A. 1958. Virussjukdommer pâ bringebaer. Norsk

Hagetidende 74:80-82. [In Norwegian.]

Blackman, R. L., V. F. Eastop, and M. Hills. 1977.

Morphological and cytological separation of Amphorophora

Buckton (Homoptera: Aphididae) feeding on European

raspberry and blackberry {Kubus spp.). Bulletin of Entomological Research 67:285-296.

Bock, K. R. 1966. Arabis mosaic and Prunus necrotic

ringspot viruses in hop (Humulus lupulus L.). Annals of

Applied Biology 57:131-140.

Bodine, E. W., and J. H. Newton. 1942. The rasp leaf of

cherry. Phytopathology 33:333-335.

Bolton, A. T. 1970. Spread of raspberry leaf curl virus.

Canadian Journal of Plant Science 50:667-671.

Bos L. 1981. Hundred years of Koch's postulates and the

history of etiology in plant virus research. Netherlands Journal

of Plant Pathology 87:91-110.

Bouchery, Y., and C. Putz. 1972. La mosaïque du

framboisier: Propriétés particulières de la viróse en France.

Annales de Phytopathologie 4:393-403.

Bradford, F. C, and L. Joley. 1933. Infectious variegation in

the apple. Journal of Agricultural Research 46:901-908.

Braun, A. J., and J. A. Keplinger. 1973. Seed transmission of

tomato ringspot virus in raspberry. Plant Disease Reporter

57:431-432.

Briggs, J. B. 1965. The distribution, abundance, and genetic

relationships of four strains of the Rubus aphid, Amphorophora rubi (Kalt.), in relation to raspberry breeding. Journal

of Horticultural Science 40:109-117.

Brodel, C. F., and G. A. Schaefers. 1979. An "interval timer"

for the production of oviparae in Aphis rubicola (Homoptera:

Aphididae). Entomología Experimentalis et Applicata 25:1-8.

and G. A. Schaefers. 1980a. The influence of

temperature on the production of sexuals by Aphis rubicola

under short-day conditions. Entomología Experimentalis et

Applicata 27:127-132.

and G. A. Schaefers. 1980b. Use of excised leaflets of

red raspberry to screen for potential nonpreference resistance

to Amphorophora agathonica. HortScience 15:513-514.

G. A. Schaefers, and D. K. Ourecky. 1979. Field

evaluation of red raspberry for resistance to Aphis rubicola.

HortScience 14:726-727.

Brown, D. J. F., and B. Boag. 1975. Longidorus

macrosoma. Descriptions of Plant-parasitic Nematodes, Set

5, No. 67. Commonwealth Institute of Helminthology. St.

Albans, Herts., England. 4 p.

and B. Boag. 1977. Longidorus attenuatus.

Descriptions of Plant-parasitic Nematodes, Set 7, No. 101.

Commonwealth Institute of Helminthology. St. Albans,

Herts., England, 4 p.

and C. E. Taylor. 1981. Variazoni nella transmissione di virus tra populazioni di nematodi vettori Longidoridae, p. 191-204. In R. Lamberti, A. M. Palmisano, and M.

T. Vinciguerra, editors, Atti Giomate Nematologiche 1979.

Pappagallo, Florence, 336 p.

255
Brunt, A. A. 1970. Cacao swollen shoot virus. Descriptions of

Plant Viruses No. 4. Commonwealth Mycological Society and

the Association of Applied Biologists. Kew, Surrey, England,

4 p.

and R. Stace-Smith. 1976. The occurrence of the

black raspberry latent strain oftobacco streak virus in wild and

cultivated Rubus species in British Columbia. Acta Horticulturae 66:71-76.

Bubaker, A., and Y. I. Pomazkov. 1978. Vozbuditel

skruchivaniya list'ev na kostochkovykh kul'turakh. Izvestiya

Timiryazevskoi Sel'skokhozyaistvennoi Akademii No. 5:219-

222. [In Russian.]

1963. Affinities of viruses infecting fruit trees and

raspberry. Plant Disease Reporter 47:459-462.

1965. Filamentous viruses infecting fruit trees and

raspberry and their possible mode of spread. Plant Disease

Reporter 49:230-232.

and A. G. Fisken. 1958. Susceptibility of raspberry

varieties to infection by aphid-borne viruses. Journal of

Horticultural Science 33:13-20.

and R. V. Harris. 1951. Raspberry virus diseases: a

survey of recent work. East Mailing Research Station Report

for 1950, p. 127-130.

Cadman, C. H. 1951. Studies in Rubus virus diseases. I. A

latent virus of Norfolk Giant raspberry. Annals of Applied

Biology 38:801-811.

andR. V. Harris. 1952. A lethal virus disease ofLloyd

George raspberry in Scotland. Journal ofHorticultural Science

27:212-214.

1952a. Studies inRubus virus diseases. II. Three types

of vein chlorosis of raspberries. Annals of Applied Biology

39:61-68.

1952b. Studies in Rubus virus diseases. III. A

vein-banding disease of raspberries. Annals of Applied

Biology 39:69-77.

1952c. Studies inRubus virus diseases. IV. Yellows

diseases of raspberries. Annals of Applied Biology 39:495-

500.

1952d. Studies in Rubus virus diseases. V. Experiments in analysis of Lloyd George decline. Annals of Applied

Biology 39:501-508.

1954. Studies in Rubus virus diseases. VI. Aphid

transmission of raspberry leaf mottle virus. Annals of Applied

Biology 41:207-214.

1956. Studies on the etiology and mode of spread of

Scottish raspberry leaf curl disease. Journal of Horticultural

Science 31:111-118.

1960a. Mechanical transmission of viruses from

raspberry. I. Scottish Horticultural Research Institute Annual

Report 7:50-51.

1960b. Studies on the relationship between soil-borne

viruses of the ringspot type occurring in Britain and

continental Europe. Virology 11:653-664.

1961a. Mechanical transmission of viruses from

raspberry. II. Scottish Horticultural Research Institute Annual

Report 8:57.

and A. R. Hill. 1947. Aphid vectors of European

raspberry viruses. Nature (London) 160:837-838.

and R. Stace-Smith. 1970. Raspberry vein chlorosis.

p. 119-120. In N. W. Frazier, editor, Virus diseases of small

fruits and grapevines. University of California, Division of

Agricultural Sciences, Berkeley, 290 p.

California Department of Food and Agriculture. California

Administrative Code. 1973. Registration and certification of

caneberry plants. Title 3, chapter 4, subchapter 3, article

2-Am, sections 3012-3012.5.

Callahan, K. L. 1957a. Pollen transmission of elm mosaic

virus. Phytopathology 47:5.

1975b. Prunus host range and pollen transmission of

elm mosaic virus. Dissertation Abstracts 17:1861.

Calvert, E. L., andB. D. Harrison. 1963. Outbreaks oftomato

black ring virus in onion and leek crops in Northern Ireland.

Horticultural Research 2:115-120.

Caron, M., R. O. Lachance, C. Richard, and B. Routhier.

1977. Détection des viroses dans framboisières au Québec.

Phytoprotection 58:29-33.

Casper, R. 1973. Serological properties of Prunus necrotic

ringspot and apple mosaic virus isolates from rose. Phytopathology 63:238-240.

Chamberlain, G. C. 1938. Yellow blotch-curl. A new virus

disease of the red raspberry in Ontario. Canadian Journal of

Research (section C) 16:118-124.

1941. A necrotic "fern leaf" mosaic of raspberry.

1961b. Raspberry viruses and virus diseases in Scientific Agriculture 22:119-124.

Britain. Horticultural Research 1:47-61.

256
Chambers, J. 1954. Heat therapy of virus-infected raspberries. Nature (London) 173:595-596.

1961. The production and maintenance of virus-free

raspberry plants. Journal of Horticultural Science 36:48-54.

Clark, M. F., and A. N. Adams. 1977. Characteristics of the

microplate method of enzyme-linked immunosorbent assay

(ELISA) for the detection of plant viruses. Journal of General

Virology 34:475-483.

Converse, R. H. 1960. Wineberry, Rubus phoenicolasis, a

wild host of raspberry mosaic, and an aphid vector.

Phytopathology 50:570. [Abstract.]

1961. Occurrence of viruses causing raspberry mosaic

in some commercial stocks of red raspberry in the eastern

United States. Plant Disease Reporter 45:882-883.

1970d. Viruslike disorders oí Rubus, p. 163. In N.

W. Frazier, editor. Virus diseases of small fruits and

grapevines. University of California, Division of Agricultural Sciences, Berkeley, 290 p.

1972. Tobacco streak virus in black raspberry.

Phytopathology 62:1001-1004.

1973. Occurrence and some properties of raspberry

bushy dwarf virus in Rubus species in the United States.

Phytopathology 63:780-783.

1975. Virus-tested caneberry stock in the Pacific

Northwest: supply, usage, and findings. Proceedings of the

Oregon State Horticultural Society 66:114-116.

1976. Serological detection of viruses in Rubus sap.

Acta Horticulturae 66:53-61.

1962. Insect and graft transmissions of alpha- and

beta-curl viruses of raspberries. Phytopathology 52:728.

[Abstract.]

1963. Influence of heat-labile components of the

raspberry mosaic complex on growth and yield of red

raspberries. Phytopathology 53:1251-1254.

1964. Raspberry mosaic and rate of infection under

field conditions. Plant Disease Reporter 48:839-842.

1965. The reliability of leaf grafting to Rubus henryi

for the detection of two viruses of the raspberry mosaic

complex. Phytopathology 55:276-280.

1966a. Diseases of raspberries and erect and trailing

blackberries. U.S. Department of Agriculture, Agriculture

Handbook No. 310, 111 p.

1977. Rubus virus diseases important in the United

States. HortScience 12:471-476.

1978. Detection of tomato ringspot virus in red

raspberry by enzyme-linked immunosorbent assay (ELISA).

Plant Disease Reporter 62:189-192.

1978. Uneven distribution of tobacco streak virus in

Santiam blackberry before and after heat therapy. Phytopathology 08:241-244.

1979. Recommended virus-indexing procedures for

new USDA small fruit and grape cultivars. Plant Disease

Reporter 63:848-851.

1980. Transmission of tobacco streak virus in Rubus.

Acta Horticulturae 95:53-61.

1981. Virus-tested Rubus cultivars in the USDA

1966b. Effect of heat treatment on the raspberry research collection. Fruit Varieties Journal 35:141-145.

mosaic complex in 'Latham' red raspberry. Phytopathology

56:556-559.

1970a. Black raspberry streak, p. 155-157. In N. W.

Frazier, editor. Virus diseases of small fruits and grapevines.

University of California, Division of Agricultural Sciences,

Berkeley, 290 p.

1970b. Minor viruses and virus diseases associated

with Rubus, p. 161. In N. W. Frazier, editor. Virus diseases

of small fruits and grapevines. University of California,

Division of Agricultural Sciences, Berkeley, 290 p.

1970c. The occurrence, detection, and control of

and J. S. Bailey. 1961. Resistance of some Rubus

varieties to colonization by Amphorophora rubi in Massachusetts. Proceedings of the American Society for

Horticultural Science 78:251-255.

and A. B. Bartlett. 1979. Occurrence of viruses in

some wild Rubus and Rosa species in Oregon. Plant Disease

Reporter 63:441-444.

and R. Casper. 1975. A member of the apple mosaic

Rubus viruses, p. 107-110. In N. W. Frazier, editor. Virus

diseases of small fruits and grapevines. University of

California, Division of Agricultural Sciences, Berkeley,

290 p.

virus group occurring in Rubus. Acta Horticulturae 44:63.

and R. Casper. 1977. Raspberry bushy dwarf virus in

cultivated red raspberry in Germany. Phytopathologische

Zeitschrift 89:187-190.

257
R. G. Clarke, P. W. Oman, Sr., andG. M. Milbrath.

1982. Witches'-broom disease of black raspberry in Oregon.

Plant Disease Reporter 66:949-951.

H. A. Daubeny, R. Stace-Smith, L. M. Russell, and

others. 1971. Search for biological races in Amphorophora

agathonica Hottes on red raspberries. Canadian Journal of

Plant Science 51:81-85.

and K. L. Kowalczyk. 1980. Graft transmission of

calico from three blackberry cultivars. Acta Horticulturae

112:47-52.

Costa, A. S., and V. da Costa Lima Neto. 1976. Transmiäo

do virus da necrose branca do fumo por Frankliniella sp. IX

Congreso Sociedad Brasiliero Fitopatología, 1 p.

Gotten, J., A. W. Pemberton, and P. L. Mathias. 1978. An

outbreak of raspberry yellow dwarf (arabis mosaic virus) in

raspberry entered for Special Stock Certificate. Plant

Pathology 27:145-146.

Cropley, R. 1961. Viruses causing rasp-leaf and similar

diseases of sweet cherry. Annals of Applied Biology

49:530-534.

and R. M. Lister. 1969. The occurrence and some

properties of black raspberry latent virus. Phytopathology

59:325-333.

and R. Stace-Smith. 1971. Rate ofspread and effect of

tomato ringspot virus on red raspberry in the field.

Phytopathology 61:1104-1106.

and J. A. Tomlinson. 1971. Cherry leaf roll virus.

Descriptions of Plant Viruses No. 80. Commonwealth

Mycological Institute and the Association of Applied

Biologists. Kew, Surrey, England, 4 p.

Dale, W. T., and E. B. Brown. 1973. NEPO viruses in

raspberries in the West Midlands. Plant Pathology 22:65-66.

R. Stace-Smith, and C. H. Cadman. 1970a.

Raspberry mosaic, p. 111-119. In N. W. Frazier, editor,

Virus diseases of small fruits and grapevines. University

of California, Division of Agricultural Sciences, Berkeley,

290 p.

R. Stace-Smith, and F. Johnson. 1970b. Virus

diseases observed in cultivated red raspberries in the Pacific

Northwest. Plant Disease Reporter 54:701-703.

Cooley, L. M. 1936a. Retarded foliation in black raspberries

and its relation to mosaic. New York Agricultural Experiment Station (Geneva) Bulletin No. 665, 15 p.

1936b. The identity of raspberry mosaics. Phytopathology 26:44-56.

1936c. Wild brambles in relation to spread of virus

diseases in cultivated black raspberries. New York State

Agricultural Experiment Station (Geneva) Bulletin No. 66,

15 p.

Cooper, J. I. 1976. The possible epidemiological significance of pollen and seed transmission in the cherry leaf roll

virus/Betula spp. complex. Mitteilungen aus der Biologischen Bundesanstalt für Land- and Forstwirtschaft 170:17-22.

and M. A. Atkinson. 1975. Cherry leaf roll virus

causing a disease of Betula spp. in the United Kingdom.

Forestry 48:193-203.

and M. L. Edwards. 1980. Cherry leaf roll virus in

Juglans regia in the United Kingdom. Forestry 53:41-50.

virus

16:187-191.

- and A. F. Hendy. 1967. Control of arabis mosaic

in strawberry with nematicides. Plant Pathology

Daubeny, H. A. 1966. Inheritance of immunity in the red

raspberry to the North American strain of the aphid,

Amphorophora ruhi Kltb. Proceedings of the American

Society for Horticultural Science 88:345-351.

1972. Screening red raspberry cultivars and

selections for immunity to Amphorophora agathonica

Hottes. HortScience 7:265-266.

1982. Breeding for insect, mite and nematode

resistance, p. 185-223. In J. N. Moore and J. Janick, editors.

Methods in fruit breeding. Purdue University Press,

Lafayette, Ind., 650 p.

P. C. Crandall, and G. W. Eaton. 1967. Crumbliness

in the red raspberry with special reference to the 'Sumner'

variety. Proceedings of the American Society for Horticultural Science 91:224-230.

J. A. Freeman, and R. Stace-Smith. 1970. Effects of

virus infection on drupelet set of four red raspberry cultivars.

Journal of the American Society of Horticultural Science

95:730-731.

J. A. Freeman, and R. Stace-Smith. 1975. Effects of

tomato ringspot virus on drupelet set of red raspberry

cultivars. Canadian Journal of Plant Science 55:755-759.

J. A. Freeman, and R. Stace-Smith. 1982. Effect of

raspberry bushy dwarf virus on yield and cane growth in

susceptible red raspberry cultivars. HortScience 17:645-657.

258
and R. Stace-Smith. 1963. Note on the immunity to

the North American strain of the red raspberry mosaic vector,

the aphid Amphorophora ruhi Kalb. Canadian Journal of

Plant Science 43:413-414.

R. Stace-Smith, and J. A. Freeman. 1978. The

occurrence and some effects of raspberry bushy dwarf virus

in red raspberry. Journal of the American Society for

Horticultural Science 103:519-522.

and D. Stary. 1982. Identification of resistance to

Amphorophora agathonica in the native North American red

raspberry. Journal of the American Society of Horticultural

Science 107:593-597.

Davis, R. E., and R. F. Whitcomb. 1971. Mycoplasmas,

Rickettsiae, and Chlamydiae: Possible relation to yellows

diseases and other disorders of plants and insects. Annual

Review of Phytopathology 9:119-154.

Debrot, D. A. 1964. Studies on a strain of raspberry ringspot

virus occurring in England. Annals of Applied Biology

54:183-191.

Desvignes, J. C, and A. Savio. 1975. Cydonia C l-\ et

Pyronia veitchii, deux indicateures complémentaires. Acta

Horticulturae 44:139-146.

Dicker, G. H. L. 1940. The biology of the Rubus aphids.

Journal of Pomology and Horticultural Science 18:1-33.

Dijkstra, J. 1973. Heksenbezemziekte bij braam. [Witches'-

broom in blackberries.] Fruitteelt 63:1235-1236. [In Dutch.]

Doi, Y., M. Teranaka, K. Yora, and H. Asuyama. 1967.

Mycoplasma- or PLT group-like microorganisms found in the

phloem elements of plants infected with mulberry dwarf,

potato witches'-broom, aster yellows, or Paulownia witches'-broom. Annals of the Phytopathological Society of Japan

33:259-266.

East Mailing Research Station. 1963. Virus diseases of fruit

trees. East Mailing Research Station Report for 1962, p. 127.

1970. Blackberry. East MalUng Research Station

Report for 1969, p. 54.

Eaton, G. W., and N. Turner. 1971. Embryo sac development

in relation to virus infection of four red raspberry cultivars.

Journal of the American Society for Horticultural Science

96:159-161.

Engelbrecht, D. J. 1963. Sap-transmission of viruses from

pear, grapevines and bramble to herbaceous hosts. South

African Journal of Laboratory and Clinical Medicine

9:140-141.

1976. Some properties of a yellow mosaic virus

isolated from bramble. Acta Horticulturae 66:79-83.

and W. J. K. van der Walt. 1974. Host reaction and

some properties of a virus causing a yellow mosaic in wild

bramble {Rubus sp.). Phytophylactica 6:311-313.

Fluiter, H. J. de, and F. A. van der Meer. \95?>. Rubus siwni, a

leafhopper-bome virus disease. Tijdschrift over Planteziekten

59:195-197.

and F. A. van der Meer. 1955. De dwergziekte van de

framboos, haar verspreiding en bestrijding. [Stunt disease of

raspberry, its spread and control.] Mededelingen van de

Landbouwhogeschool en de Opzoekings-stations van de Staat

te Gent 20:419-434. [In Dutch.]

and F. A. van der Meer. 1958. The biology and

control of Macropsisfuscula Zett., the vector of Rubus stunt

virus. Proceedings of the Tenth International Congress of

Entomology 3 (1956):341-346.

and T. H. Thung. 1951. Waamemingen omtrent de

dwergziekte bij framboos en wilde braam. [Observations on

the stunt disease ofraspberry and wild blackberry.] Tijdschrift

over Planteziekten 57:108-114. [In Dutch.]

Forer, L. B., and R. F. Stouffer. 1982. Xiphinema spp.

associated with tomato ringspot virus infection of Pennsylvania fruit crops. Plant Disease 66:735-736.

Forster, R. L. S. 1980. Production and properties of mutants

of tomato black ring virus. Ph.D. Thesis, University of

Dundee, 279 p.

Francki, R. I. B., D. W. Mossop, and T. Hatta. 1979.

Cucumber mosaic virus. Descriptions of Plant Viruses No.

213. Commonwealth Mycological Institute and the Association of Applied Biologists. Kew, Surrey, England, 6 p.

Frazer, B. D., and A. R. Forbes. 1968. Masonaphis maxima

(Mason) (Homoptera: Aphididae), an aphid on thimbleberry

with an unusual life history. Journal of the Entomological

Society of British Columbia 65:36-39.

Frazier, N. W. 1966. Natural and experimental infection of

Rubus with strawberry necrotic shock virus. Phytopathology

56:568-569.

P. S. Jorgensen, H. E. Thomas, and H.A. Johnson, Jr.

1962. Necrotic shock: a virus disease of strawberries. Plant

Disease Reporter 46:547-550.

Freeman, J. A., H. A. Daubeny, and R. Stace-Smith. 1969.

Increased pollen abortion caused by viruses in four red

raspberry cultivars. Canadian Journal of Plant Science

49:373-374.

259
and R. Stace-Smith. 1965. Systemic invasion of the

root system of raspberr)^ plants by the component viruses of

red raspberry mosaic. Canadian Journal of Plant Science

45:296- 297.

and R. Stace-Smith. 1968. Effect of tomato ringspot

virus on plant and fruit development of raspberries. Canadian

Journal of Plant Science 48:25-29.

1981. Ilarviruses, p. 377-413. In E. Kurstak, editor,

Handbook of plant virus infections and comparative

diagnosis. Elsevier/North Holland Biomédical Press, New

York, 943 p.

Gehring, F., and R. Bercks. 1956. Untersuchungen über das

Bukett- und Pseudo-Aucuba-Virus der Kartoffel. Phytopathologische Zeitschrift 27:215-234.

and R. Stace-Smith. 1970. Effects of raspberry

mosaic viruses on yield and growth of red raspberries.

Canadian Journal of Plant Science 50:521-527.

R. Stace-Smith, and H. A. Daubeny. 1975. Effects of

tomato ringspot virus on the growth and yield ofred raspberry.

Canadian Journal of Plant Science 55:749-754.

Freitag, J. H. 1951. Host range ofthe Pierce 's disease virus of

grape, as determined by insect transmission. Phytopathology

41:921-934.

Fritzsche, R. 1964. Untersuchungen über die Virusübertragung durch Nematoden. Wissenschaftliche Zeitschrift der

Universität Rostock 13:343-347.

and H. Kegler. 1964. Die Übertragung des Blattrollvirus der Kirsche (cherry leaf-roll virus) durch Nematoden.

Naturwissenschaften 51:299.

Fry, P. R., and G. A. Wood. 1973. Further viruses oíPrunus

in New Zealand. New Zealand Journal of Agricultural

Research 16:131-142.

and G. A. Wood. 1978. Two berry fruit virus diseases

newly recorded in New Zealand. New Zealand Journal of

Agricultural Research 21:543-547.

Fulton, R. W. 1948. Hosts of the tobacco streak virus.

Phytopathology 38:421-428.

1952. Mechanical transmission and properties of rose

mosaic virus. Phytopathology 42:413-416.

1968. Serology of viruses causing cherry necrotic

ringspot, plum line pattern, rose mosaic and apple mosaic.

Phytopathology 58:635-638.

1971. Tobacco streak virus. Description of Plant

Viruses No. 44. Commonwealth Mycological Institute and

the Association ofApplied Biologists. Kew, Surrey, England,

4p.

1972. Apple mosaic virus. Descriptions of Plant

Viruses No. 83. Commonwealth Mycological Institute and

the Association ofApplied Biologists. Kew, Surrey, England,

4 p.

Giles, F. E. 1966. The seasonal history and geographic

distribution of aphids infesting raspberry, blueberry, and

strawberry in the lower peninsula of Michigan. Dissertation

Abstracts 27B: 1729-1730.

Gordejchuk, O. G., A. V. Krylov, N. V. Krylova, and I. N.

Samonina. 1977. Virus diseases of berry crops in the Soviet

Far East. I. Identification of some mechanically transmitted

viruses, detected in Primorye Territory. Zentralblatt für

Bakteriologie, Parasitenkunde, Infektionskrankheiten und

Hygiene, Abteilung II 132:686-707.

Gordon, S. C, and C. E. Taylor. 1976. Some aspects of the

biology of the raspberry leaf and bud mite {Phyllocoptes

[Eriophyes] gracilis Nal.) Eriophyidae in Scotland. Journal of

Horticultural Science 51:501-508.

Gotlieb, A. R., and J. G. Berbee. 1973. Line pattern of birch

caused by apple mosaic virus. Phytopathology 63:1470-1477.

Guy, G., P. Y. Sampson, J. McGechan, and R. Stace-Smith.

1982. Occurrence of viruses in Rubus cultivars and species in

Australia. Acta Horticulturae 129:31-39.

Hanada, K., and B. D. Harrison. 1977. Effects of virus

genotype and temperature on seed transmission of nepoviruses. Annals of Applied Biology 85:79-92.

Hansen, A. J., G. Nyland, F. D. McElroy, and R.

Stace-Smith. 1974. Origin, cause, host range and spread of

cherry rasp leaf disease in North America. Phytopathology

64:721-727.

and R. Stace-Smith. 1971. Properties of a virus

isolated from golden elderberry, Sambucus nigra aurea.

Phytopathology 61:1222-1229.

Hanson, C. M., andR. N. Campbell. 1979. Strawberry latent

ringspot virus from 'Plain' parsley in California. Plant Disease

Reporter 63:142-146.

Harris, R. V. 1933. Mosaic disease of the raspberry in Great

Britain. I. Symptoms and varietal susceptibility. Journal of

Pomology and Horticultural Science 11:237-255.

1935. Some observations on the raspberry disease

situation in North America. East Mailing Research Station

Report for 1934, p. 157-164.

260
1939. Mosaic disease of the raspberry in Great

Britain. II. Experiments in transmission and symptom

analysis. Journal of Pomology 17:318-343.

A. D. Bryce, and C. E. Polster. 1943. A leaf curl

disease of raspberry in Scotland. East Mailing Research

Station Report for 1942, p. 48-50.

Harrison, B. D. 1956. Soil transmission of Scottish raspberry

leaf-curl disease. Nature (London) 178:553.

1957. Studies on the host range, properties and mode

of transmission of beet ringspot virus. Annals of Applied

Biology 45:462-472.

1958a. Cucumber mosaic virus in raspberry. Plant

Pathology 7:109-111.

1958b. Further studies on raspberry ringspot and

tomato black ring, soil-borne viruses that affect raspberry.

Annals of Applied Biology 46:571-584.

1958c. Raspberry yellow dwarf, a soil-borne virus.

Annals of Applied Biology 46:221-229.

1958d. Relationship between beet ringspot, potato

bouquet and tomato black ring viruses. Journal of General

Microbiology 18:450-460.

1959. The pattern of field infection of potato by the

beet ringspot strain of tomato black-ring, a soil-borne virus.

Annals of Applied Biology 47:557-564.

1961. Identity of red currant spoon leaf virus.

Tijdschrift over Planteziekten 67:562-565.

1964. Specific nematode vectors for serologically

distinctive forms of raspberry ringspot and tomato black ring

viruses. Virology 22:544-550.

1967. The transmission of strawberry latent ringspot

virus by Xiphinema diversicaudatum (Nematoda). Annals of

Applied Biology 60:405-409.

and C. H. Cadman. 1959. Role of a dagger nematode

{Xiphinema sp.) in outbreaks of plant diseases caused by

arabis mosaic virus. Nature (London) 184:1624-1626.

W. P. Mowat, and C. E. Taylor. 1961. Transmission

of a strain of tomato black ring virus by Longidorus elongatus

(Nematoda). Virology 14:480-485.

and A. F. Murant. 1977a. Nematode transmissibility

of pseudo-recombinant isolates of tomato black ring virus.

Annals of Applied Biology 86:209-212.

and A. F. Murant. 1977b. Nepovirus group.

Descriptions of Plant Viruses No. 185. Commonwealth

Mycological Institute and the Association of Applied

Biologists. Kew, Surrey, England, 4 p.

A. F. Murant, and M. A. Mayo. 1972. The two

properties of raspberry ringspot virus determined by its

smaller RNA. Journal of General Virology 17:137- 141.

-A. F. Murant, M. A. Mayo, and I. M. Roberts. 1974.

Distribution of determinants for symptom production, host

range and nematode transmissibility between the two RNA

components of raspberry ringspot virus. Journal of General

Virology 22:233-247.

and H. L. Nixon. 1960. Purification and electron

microscopy of three soil-borne plant viruses. Virology

12:104-117.

- J. E. Peachey, and R. D. Winslow. 1963. The use of

nematicides to control the spread of arabis mosaic virus by

Xiphinema diversicaudatum (Micol.). Annals of Applied

Biology 52:243-255.

and I. M. Roberts. 1973. Association of virus-like

particles with internal brown spot of yam (Dioscorea

fl/ömj.Tropical Agriculture 50:335-340.

and R. D. Winslow. 1961. Laboratory and field

studies on the relation of arabis mosaic virus to its nematode

vector, Xiphinema diversicaudatum (Micoletzky). Annals of

Applied Biology 49:621-633.

Helebrant, L. 1958. Pfispëvek k poznání virovych chorob

maliniku a ostruziniku. [A contribution to the knowledge of

virus diseases of raspberry and blackberry.] Sbomik

Ceskoslovenské Akademie Zemëdèlskych Ved. Rostlinná

Vyroba 31:599-620. [In Czech, with EngUsh summary.]

Hemphill, D. D. 1970. Sterility in Rubus, p. 159. In N. W.

Frazier, editor. Virus diseases of small fruits and grapevines.

University of California, Division of Agricultural Sciences,

Berkeley, 290 p.

Hille Ris Lambers, D. 1950. The Netheriands aphids of

raspberry and blackberry. Tijdschrift over Planteziekten

56:253-261.

Hollings, M. 1963. Cucumber stunt mottle, a disease caused

by a strain of arabis mosaic virus. Journal of Horticultural

Science 38:138-149.

1965. Some properties of celery yellow vein, a virus

serologically related to tomato black ring virus. Annals of

Applied Biology 55:459-470.

261
Hooper, D. J. 1973. Longidorus elongatus. Descriptions of

Plant-parasitic Nematodes, set 2, No. 30. Commonwealth

Institute of Helminthology. St. Albans, Herts., England, 4 p.

Horn, N. L. 1948. A new virus disease of blackberry,

Phytopathology 38:827-830.'

Hottes, F. C, and T. H. Frison. 1931. The plant lice, or

Aphidae, of Illinois. Bulletin of the Illinois Natural History

Survey 19(3): 121-447.

and A. F. Posnette. 1961. Transmission of arabis

mosaic virus by the nematode Xiphinema diversicaudatum

(Micol.). Virology 13:119-123.

Johnson, F. 1972. Raspberry calico, a transmissible disorder.

Plant Disease Reporter 56:779-782.

Jones, A. T. 1973. A comparison of some properties of four

strains of cherry leaf roll virus. Annals of Applied Biology

74:211-217.

Huber, G. A. 1939. Transmission of black raspberry mosaic

by the cane-feeding aphid Amphorophora rubicumberlandi.

Phytopathology 29:85. [Abstract.]

and F. Johnson. 1952. Black raspberry mosaic in

western Washington. Plant Disease Reporter 36:239-240.

and CD. Schwartze. 1938. Resistance in the red

raspberry to the mosaic vector Amphorophora rubi (Kalt.).

Journal of Agricultural Research 57:623-633.

1974. Other sap transmissible viruses found in Rubus.

Scottish Horticultural Research Institute Annual Report for

1973, p. 64.

1975a. Rp7 virus. Scottish Horticultural Research

Institute Annual Report for 1974, p. 71.

1975b. Viruses infecting raspberry. Scottish

Horticultural Research Institute Annual Report for 1974, p.

69-70.

Ikin, R., and R. R. Frost. 1976. Virus diseases of roses. II.

Strawberry latent ringspot virus R/l:2.6 or 2 x 1.6/38:S/

S:S/Ne. Phytopathologische Zeitschrift 87:205-223.

Iwaki, M., and Y. Komuro. 1974. Viruses isolated from

narcissus (Narcissus spp.) in Japan. V. Arabis mosaic virus.

Annals of the Phytopathological Society of Japan 40:344-

353.

James, M., R. H. Kenton, andR. D. Woods. 1973. Virus-like

particles associated with two diseases of Colocasia esculenta

(L.) Schott in the Solomon Islands. Journal of General

Virology 21:145-153.

Jennings, D. L. 1963. Preliminary studies on breeding

raspberries for resistance to mosaic disease. Horticultural

Research 2:82-96.

1964. Studies on the inheritance in red raspberry of

immunities from three nematode-bome viruses. Genética

35:152-164.

1967. Observations on some instances of partial

sterility in red raspberry cultivars. Horticultural Research

7:116-122.

1977. Somatic mutation in the raspberry.

Horticultural Research 17:61-63.

Jenser, G., A. Hegab, and L. Kollányi. 1981. Vectors of

Rubus stunt in Hungary. Proceedings of the Ninth Conference

of the Czechoslovak Plant Virologists:73-75.

Jha, A., and A. F. Posnette. 1959. Transmission of a virus to

strawberry plants by a nematode (Xiphinema sp.). Nature

(London) 184:962-963.

1976a. An isolate of cucumber mosaic virus from

Rubus phoenicolasius Maxim. Plant Pathology 25:137-140.

1976b. Purification of aphid-borne viruses directly

from raspberry. Scottish Horticultural Research Institute

Annual Report for 1975, p. 73-74.

1976c. Serological specificity of different isolates of

cherry leaf roll virus from different natural hosts.

Poljoprivredna znanstvena smotra-Agriculturae Conspectus

Scientificus 39:527-532.

1976d. The effect ofresistance io Amphorophora rubi

in raspberry (Rubus idaeus) on the spread of aphid-borne

viruses. Annals of Applied Biology 82:503-510.

1977. Partial purification and some properties of

wineberry latent, a virus obtained from Rubusphoenicolasius.

Annals of Applied Biology 86:199-208.

1979a. Further studies on the effect of resistance to

Anphorophora idaei in raspberry (Rubus idaeus) on the

spread of aphid-borne viruses. Annals of Applied Biology

92:119-123.

1979b. The effects of black raspberry necrosis and

raspberry bushy dwarf viruses in Lloyd George raspberry and

their involvement in raspberry bushy dwarf disease. Journal of

Horticultural Science 54:267-272.

1980a. Records of sap-transmissible viruses in Rubus

plants. Scottish Horticultural Research Institute Annual

Report for 1979, p. 102.

262
1980b. Some effects of latent virus infection in red

raspberry. Acta Horticulturae 95:63-70.

1981a. Effects of aphid-borne viruses latent in

raspberry. Scottish Horticultural Research Institute Annual

Report for 1980, p. 99.

1981b. Recent research on virus diseases of red

raspberry—the viruses, their effects and control. Scottish

Horticultural Research Institute Association Bulletin No.

19:15-25.

1981c. Performance of aphid-resistant cultivars.

Scottish Horticultural Research Institute Annual Report for

1980, p. 98-99.

and S. Badenoch. 1981. New virus in raspberry from

Canada. Scottish Horticultural Research Institute Annual

Report for 1980, p. 100.

A. F. Murant, D. L. Jennings, and G. A. Wood.

1982. Association of raspberry bushy dwarf virus with

raspberry yellows disease; reaction of Rubus species and

cultivars, and the inheritance of resistance. Annals of

Applied Biology 100:135-147.

A. F. Murant, and R. Stace-Smith. 1977. Raspberry

vein chlorosis virus. Descriptions of Plant Viruses No. 174.

Commonwealth Mycological Institute and the Association of

Applied Biologists. Kew, Surrey, England, 4 p.

and I. M. Roberts. 1976. Ultrastructural changes and

small bacilliform particles associated with infection by rubus

yellow net virus. Annals of Applied Biology 84:305-310.

and I.M. Roberts. 1977. Rubus host range,

symptomatology and ultrastructural effects of a British

isolate of black raspberry necrosis virus. Annals of Applied

Biology 86:381-387.

and D. L. Jennings. 1980a. Disease and pest

resistance. Scottish Horticultural Research Institute Annual

Report for 1979, p. 52-53.

and D. L. Jennings. 1980b. Genetic control of the

reactions of raspberry to black raspberry necrosis, raspberry

leaf mottle, and raspberry leafspot viruses. Annals of Applied

Biology 96:59-65.

and M. A. Mayo. 1972. The two nucleoprotein

particles of cherry leaf roll virus. Journal of General Virology

16:349-358.

and M. A. Mayo. 1975. Further properties of black

raspberry latent virus, and evidence for its relationship to

tobacco streak virus. Annals of Applied Biology 79:297-306.

M. A. Mayo, and S. J. Henderson. 1985. Biological

and biochemical properties of an isolate of cherry rasp leaf

virus from red raspberry. Annals of Applied Biology

106:101-110.

F. D. McElroy, and D. J. F. Brown. 1981. Tests for

transmission of cherry leaf roll virus using Longidorus,

Paralongidorus and Xiphinema nematodes. Annals of

Applied Biology 99:143-150.

and A. F. Murant. 1971. Serological relationship

between cherry leaf roll, elm mosaic and golden elderberry

viruses. Annals of Applied Biology 69:11-15.

and A. F. Murant. 1972. Some properties of a

mechanically transmissible virus widespread in raspberry

(Rubus idaeus) in Scotland. Plant Pathology 21:166-170.

and A. F. Murant. 1975. Etiology of a mosaic

disease of 'Glen Clova' red raspberry. Horticultural Research

14:89-95.

1. M. Roberts, and A. F. Murant. 1974. Association

of different kinds of bacilliform particle with vein chlorosis

and mosaic disease of raspberry (Rubus idaeus). Annals of

Applied Biology 77:283-288.

and G. A. Wood. 1978. The occurrence of cherry

leaf roll virus in red raspberry in New Zealand. Plant Disease

Reporter 62:835-838.

and G. A. Wood. 1979. The virus status of

raspberries (Rubus idaeus L.) in New Zealand. New Zealand

Journal of Agricultural Research 22:173-182.

Jordovic, M. 1963. Investigation of the economically most

important virus diseases of raspberries in Yugoslavia. Archiv

za Poljoprivredne Nauke 16:3-27.

B. Dimitrijevic, and M. Rankovic. 1972. Identifikacija virusa prstenaste pegavosti paradajza (tomato ringspot

virus) na malini u Jugoslaviji. [Identification of tomato

ringspot virus on raspberry in Yugoslavia.] Zastita Bilja

23:147-158. [In Serbo-Croatian.]

Kaiser, W. J., S. D. Wyatt, and G. R. Pesho. 1982. Natural

hosts and vectors of tobacco streak virus in eastern

Washington. Phytopathology 72:1508-1512.

Keep, E., and R. L. Knight, 1967. A new gene from Rubus

occidentalis L. for resistance to strains 1, 2 and 3 ofthe Rubus

aphid, Amphorophora rubi Kalt. Euphytica 16:209-214.

R. L. Knight, and J. H. Parker. 1972. Two new

raspberry varieties, 'Mailing Orion' and 'Mailing Admiral'.

East Mailing Research Station Annual Report for 1971, p.

147-159.

263
Kennedy, G. G., and G. A. Schaefers. 1974a. Evaluation of

immunity in red raspberry to Amphorophora agathonica via

cuttings. Journal of Economic Entomology 67:311-312.

and G. A. Schaefers. 1974b. Evidence for

nonpreference and antibiosis in aphid-resistant red raspberry

cultivars. Environmental Entomology 3:773-777.

and G. A. Schaefers. 1974c. The distribution and

seasonal history of Amphorophora agathonica Hottes on

'Latham' red raspberry. Annals of the Entomological Society

of America 67:356-358.

G. A. Schaefers, and D. K. Ourecky. 1973.

Resistance in red raspberry to Amphorophora agathonica

Hottes 2iná Aphis rubicola Oestlund. HortScience 8:311-313.

Kennedy, J. S., M. F. Day, and V. F. Eastop. 1962. A

conspectus of aphids as vectors of plant viruses. Commonwealth Institute of Entomology (London), 114 p.

Keplinger, J. A., A. J. Braun, and R. Provvidenti. 1968.

Crumbly berry of red raspberry caused by tomato ringspot

virus. Plant Disease Reporter 52:386-390.

Klein, M., A. Zelcer, Z. Fleischer, and G. Loebenstein.

1976. Mycoplasmalike organisms associated with witches'-

broom disease oiRubussanguineus. Hassadeh 56:1103-1104.

[In Hebrew.]

Knight, R. L., E. Keep, and J. B. Briggs. 1959. Genetics of

resistance to Amphorophora rubi (Kalt.) in the raspberry. I.

The gene Ai from Baumforth A. Journal of Genetics

56:261-280.

Knight, V. H., and D. J. Barbara. 1981. Susceptibility of red

raspberry varieties to raspberry bushy dwarf virus and its

genetic control. Euphytica 30:803-811.

Koenig, R., and D. E. Lesemann. 1978. Potexvirus Group.

Descriptions of Plant Viruses No. 200. Commonwealth

Mycological Institue and the Association of Applied

Biologists. Kew, Surrey, England, 6 p.

Kooyman, P., D. J. Engelbrecht, and G. G. F. Kasdorf. 1982.

Isolation of raspberry bushy dwarf virus from Youngberry in

South Africa. Acta Horticulturae 129:59-62.

Kristensen, H. R. 1962. Dvaergsyge hos hindbaer og andre

Rubus-diVitr. [Rubus stunt in raspberries and other Rubus

species.] Erhvervsfrugtavleren 3:3-7. [In Danish.]

Kronenberg, H. G., and H. J. de Fluiter. 1951. Resistentie

van frambozen tegen de grote frambozenluis, Amphorophora

rubi (Kalt.). [Resistance of raspberries to the large raspberry

aphid, Amphorophora rubi (A^alt.)] Tijdschrift over Planteziekten 57:114-123. [In Dutch.]

Kusnetsova, A. A., and Y. I. Pomazkov. 1971. [Mosaic

virus in raspberry.] Nauchnye Doklady Vysshei Shkoly

Biologicheskie Nauki 85:92-96. [In Russian.]

Lamberti, F. 1980. Taxonomic status ofthe nematode vectors

of grapevine viruses, p. 133-137. In A. J. McGinnis, editor.

Proceedings of the Seventh Meeting of the International

Council for the Study ofViruses and Virus-like Diseases ofthe

Grapevine. Agriculture Canada, Research Branch.

Legg, J. T. 1960. A virus-degeneration of loganberry. East

Mailing Research Station Report for 1959, p. 102-103.

Lehmann, W. 1973. Euscelis plebejus (Fallen) und macrosteles cristatus Ribaut als Überträger von Pflanzenkrankheiten

von vermuteter Mykoplasma-Ätiologie. Archiv für Phytopathologie und Pflanzenschutz 9:363-370.

Lister, R. M. 1960. Transmission of soil-borne viruses

through seed. Virology 10:547- 549.

1964. Strawberry latent ringspot: a new nematodebome virus. Annals of Applied Biology 54:167-176.

and A. F. Murant. 1967. Seed-transmission of

nematode-bome viruses. Annals of Applied Biology 59:49-

62.

Maat, D. Z., F. A. van der Meer, and H. J. Pfaeltzer. 1962.

Serological identification of some soil-borne viruses causing

diseases in fruit crops in The Netherlands. Tijdschrift over

Planteziekten 68:120-122.

Mandahar, C. L. 1981. Virus transmission through seed and

pollen, p. 241-292. In K. Maramorosch, and K. F. Harris,

editors. Plant diseases and vectors: ecology and epidemiology. Academic Press, New York, 368 p.

Marani, F., A. Pisi, and A. Bertaccini. 1977. The association

of mycoplasmalike bodies with Rubus stunt disease.

Phytopathologia Mediterránea 16:150-153.

Martin, R. R., and R. H. Converse. 1982. An improved buffer

for mechanical transmission of viruses from Fragaria and

Rubus. Acta Horticulturae 129:69-74.

Maryland Agricultural Experiment Station. 1942. Mineral

deficiency symptoms of black raspberries. Maryland Agricultural Experiment Station Annual Report 55:37.

Matthews, R. E. F. 1979. Classification and nomenclature of

viruses. Intervirology 12:247-248.

1981. Plant virology (second edition). Academic

Press, New York, 897 p.

264
Mayo, M. A., A. F. Murant, andB. D. Harrison. 1971. New

evidence on the structure of nepoviruses. Journal of General

Virology 12:175-178.

A. F. Murant, B. D. Harrison, and R. A. Goold.

1974. Two protein and two RNA species in particles of

strawberry latent ringspot virus. Journal of General Virology

24:29-37.

McElroy, F. D. 1977. Distribution of stylet-bearing

nematodes associated with raspberries and strawberries in

British Columbia. Canadian Plant Disease Survey 57:3-8.

McGuire, J. M. 1964. Efficiency of Xiphinema americanum

as a vector of tobacco ringspot virus. Phytopathology

54:799-801.

Meer, F. S. van der. 1954. De incubatietijd van de

dwergziekte bij verschillende fambozenrassen. [The incubation period of stunt in different raspberry varieties.]

Tijdschrift over Planteziekten 60:69-71. [In Dutch.]

1957. Warrom winterbespuiting in frambozen? [Why

spray raspberries during the winter?] Fruitteelt 47:34-35. [In

Dutch.]

1958. Overdacht van frambozenvirussen door

bladenting. [Transmission of raspberry viruses by leaf

grafting.] Tijdschrift over Planteziekten 64:273-275. [In

Dutch.]

— 1975. Heat therapy as a tool for the elimination of

plant viruses. Bulletin des Recherches Agronomiques de

Gemblouz, special volume, p. 109-117.

1980. De bestrijding van virussen in bessen,

frambozen en bramen. [Control of viruses in currants,

raspberries and blackberries.] Fruitteelt 70:342-344. [In

Dutch.]

and H. J. de Fluiter. 1962. Bestrijding van de

heksenbezemziekte van de framboos door middel van een

chemische bestrijding van de vector. [Control of the

witches'-broom disease of raspberry by means of chemical

control of the vector.] Mededelingen Landbouwhogeschool

en de Opzoekingsstations van de Staat te Gent 27:1053-1059.

[In Dutch.]

and H. J. de Fluiter. 1970. Rubus stunt, p. 128-132.

/n N. W. Frazier, editor. Virus diseases of small fruits and

grapevines. University of California, Division of Agricultural Sciences, Berkeley, 290 p.

Mellor, F. C, and R. Stace-Smith. 1976. Inñuence of heat

therapy on rooting of, and elimination of raspberry bushy

dwarf virus from shoot cuttings of red raspberry. Acta

Horticulturae 66:63-70.

and R. Stace-Smith. 1979. A heat-stable black

raspberry necrosis virus. Acta Horticulturae 95:71-75.

Mircetich, S. M., R. R. Sanbom, and D. E. Ramos. 1980.

Natural spread, graft-transmission and possible etiology of

walnut blackline disease. Phytopathology 70:962-968.

Mollenhauer, H. H., and D. L. Hopkins. 1974. Ultrastructural study of Pierce's disease bacterium in grape xylem tissue.

Journal of Bacteriology 119:612-618.

Morand, J. C. 1963. Sélection sanitaire du framboisier.

CTIFL Documents, May 1963. (Unnumbered.) 10 p.

Müller, H. M., H. Kleinhempel, E. Zimmermann, and

others. 1977. Electronenmikroskopische Untersuchungen an

verzwergungskranken Himbeeren {Rubus idaeus L.). Archiv

für Phytopathologie und Pflanzenschutz (BerUn) 13:293-295.

Murant, A. F. 1970a. Arabis mosaic virus. Descriptions of

Plant Viruses No. 16. Commonwealth Mycological Institute

and the Association of Applied Biologists. Kew, Surrey,

England, 4 p.

1970b. The importance of wild plants in the ecology

of nematode transmitted plant viruses. Outlook on Agriculture 6:114-121.

1970c. Tomato black ring virus. Descriptions of

Plant Viruses No. 38. Commonwealth Mycological Institute

and the Association of Applied Biologists. Kew, Surrey,

England, 4 p.

1974a. Strawberry latent ringspot virus. Descriptions

of Plant Viruses No. 126. Commonwealth Mycological

Institute and the Association of Applied Biologists. Kew,

Surrey, England, 4 p.

1974b. Viruses affecting raspberry in Scotland.

Scottish Horticultural Research Institute Association Bulletin

No. 9:37-43.

1976a. Raspberry bushy dwarf virus. Descriptions of

Plant Viruses No. 165. Commonwealth Mycological Institute

and the Association of Applied Biologists. Kew, Surrey,

England, 4 p.

1976b. The development of our knowledge of Rubus

viruses. Acta Horticulturae 66:13-17.

1978. Raspberry ringspot virus. Descriptions of Plant

Viruses No. 198. Commonwealth Mycological Institute and

the Association ofApplied Biologists. Kew, Surrey, England,

5 p.

265
1981a. Nepoviruses, p. 197-238. In E. Kurstak,

editor, Handbook of plant virus infections and comparative

diagnosis. Elsevier/North-Holland Biomédical Press, Amsterdam, 943 p.

1981b. The role of wild plants in the ecology of

nematode-bome viruses, p. 237-248. In J. M. Thresh, editor.

Pests, pathogens and vegetation. Pitman, London, 517 p.

J. Chambers, and A. T. Jones. 1974. Spread of

raspberry bushy dwarf virus by pollination, its association

with crumbly fruit, and problems of control. Annals of

Applied Biology 77:271-281.

and R. A. Goold. 1969. Strawberry latent ringspot

virus. Scottish Horticultural Research Institute Report for

1968, p. 48.

D. L. Jennings, and J. Chambers. 1973. The problem

of crumbly fruit in raspberry nuclear stocks. Horticultural

Research 13:49-54.

and A. T. Jones. 1976. Comparison of isolates of

raspberry bushy dwarf virus from red and black raspberries.

Acta Horticulturae 66:47-52.

A. T. Jones, and I. M. Roberts. 1976. Recent research

on 52V virus of raspberry. Acta Horticulturae 66:39-46.

and R. M. Lister. 1967. Seed-transmission in the

ecology of nematode-bome viruses. Annals of Applied

Biology 59:63-76.

M. A. Mayo, B. D. Harrison, andR. A. Goold. 1972.

Properties of virus and RNA components ofraspberry ringspot

virus. Journal of General Virology 16:327-338.

M. A. Mayo, B. D. Harrison, andR. A. Goold. 1973.

Evidence for two functional RNA species and a 'satellite'

RNA in tomato black ring virus. Journal of General Virology

19:275-278.

C. E. Taylor, and J. Chambers. 1968. Properties,

relationships and transmission of a strain of raspberry

ringspot virus infecting raspberry cultivars immune to the

common Scottish strain. Annals of Applied Biology

61:175-186.

-M. Taylor, G. H. Duncan, and J. H. Raschké. 1981.

Improved estimates of molecular weight of plant virus RNA

by agarose gel electrophoresis and electron microscopy after

denaturation with glyoxal. Journal of General Virology

53:321-332.

Nichols, C. W., T. R. Carpenter, and D. Y. Rosenberg.

1957. New disease detection in cooperation with county

agricultural commissioners. I. California Department of

Agriculture Bulletin 46:166-169.

Nienhaus, P., and R. A. Sikora. 1979. Mycoplasmas,

Spiroplasmas, and Rickettsia-like organisms as plant

pathogens. Annual Review of Phytopathology 17:37-58.

Nyland, G. 1961. Mechanical transmission of the strains of

sweet cherry rugose mosaic, mild rusty mottle and rasp leaf

viruses. Phytopathology 51:66-67.

and A. C. Goheen. 1969. Heat therapy of virus

diseases of perennial plants. Annual Review of Phytopathology 7:331-354.

B. F. Lownsbery, S. K. Lowe, and J. F. Mitchell.

1969. The transmission of cherry rasp leaf virus by

Xiphenema americanum. Phytopathology 59:1111-1112.

Ontario Horticultural Experiment Station. 1966. New

Ontario-certified raspberry plants. Ontario Horticultural

Experiment Station, Vineland, Ontario, 1 p.

Ormerod, P. J. 1970. A virus associated with loganberry

degeneration disease. East Mailing Research Station Report

for 1969, p. 165-167.

1972a. Rubus virus investigations. Blackberry. East

and I. M. Roberts. 1971. Mycoplasma-like bodies Mailing Research Station Report for 1971, p. 127

associated with Rubus stunt disease. Annals of Applied

Biology 67:389-393.

and I. M. Roberts. 1980. Particles of raspberry vein

chlorosis virus in the aphid vector. Aphis idaei. Acta

Horticulturae 95:31-35.

and C. E. Taylor. 1965. Treatment of soil with

chemicals to prevent transmission of tomato blackring and

raspberry ringspot viruses by Longidorus elongatus (de

Man). Annals of Applied Biology 55:227-237.

1972b. Rubus virus investigations. Loganberry. East

Mailing Research Station Report for 1971, p. 127.

1975. Virus diseases of blackberry. East Mailing

Research Station Report for 1974, p. 124.

Persic, M., and M. Babovic. 1978. [Occurrence of an

unknown blackberry virus disease in Yugoslavia.] Zastita

Bilja 29:197-202. [In Serbo-Croatian.] Abstracted in Biological Abstracts. 1980. 69:583 (No. 5485).

266
Peters, D. 1981. Plant rhabdovirus group. Descriptions of

Plant Viruses No. 244. Commonwealth Mycological Institute

and the Association of Applied Biologists. Kew, Surrey,

England, 7 p.

Peterson, K. E., and M. K. Corbett. 1980. Latent infection

of red raspberries by tobacco streak virus. Phytopathology

70:692. [Abstract.]

Petzold, H. 1971. Der elektron mikroskopische Nachweis

eines bacilliformen Virus an blattfleckenkranken Dendrobien. Phytopathologische Zeitschrift 70:43-52.

Pitcher, R. S., M. R. Siddiqi, and D. J. F. Brown. 1974.

Xiphinema diversicaudatum. Descriptions of Plant-parasitic

Nematodes Set 4, No. 60. Commonwealth Institute of

Helminthology. St. Albans, Herts., England, 4 p.

Posnette, A. F. 1963. Apple mosaic, p. 19-21. In A. F.

Posnette, editor, Virus Diseases of Apples and Pears.

Technical Communication No. 30, Commonwealth Bureau

of Horticulture and Plantation Crops. East Mailing, Maidstone, Kent, England, 141 p.

Prentice, I. W. 1950. Rubus stunt: a virus disease. Journal of

Horticultural Science 26:35- 42.

Provvidenti, R., and A. L. Granett. 1974. Sweet violet, a

natural host of bean yellow mosaic virus. Plant Disease

Reporter 58:155-156.

Putz, C. 1971. Obtention de framboisiers (var. 'Bois Blanc')

sans virus par la technique des cultures de méristèmes.

Annales de Phytopathologie 3:493-501.

and R. Meignoz. 1972. Electron microscopy of

viruslike particles found in mosaic diseased raspberries in

France. Phytopathology 62:1477-1478.

and G. Stocky. 1970. Premières observations sur une

souche de strawberry latent ringspot virus transmise par

Xiphinema coxi Tarjan et associée à une maladie du

framoisier en Alsace. Annales de Phytopathologie 2:329-

347.

and G. Stocky. 1971. Identification du virus de la

mosaïque de l'arabis (arabis mosaic virus) chez le framboisier et le cassis en France. Annales de Phytopathologie

3:503-507.

Pyott, J. L., and R. H. Converse. 1981. In vitro propagation

of heat-treated red raspberry clones. HortScience 16:308-

309.

Rautapää, J. 1967. The bionomics of the raspberry aphids

Aphis idaei V. D. Goot and Amphorophora rubi (Kalt.)

(Hom. Aphididae). Annales Agriculturae Fenniae 6:127-

144.

Ramsfjell, T. 1952. Virussjukdommer pa hagebruksplanter.

[Virus symptoms in horticultural crops.] Frugt og Baer

5:44-55. [In Norwegian.]

Randies, J. W., B. D. Harrison, A. F. Murant, and M. A.

Mayo. 1977. Packaging and biological activity of the two

essential RNA species of tomato black ring virus. Journal of

General Virology 36:187-193.

Rankin, W. H. 1931. Virus diseases of black raspberries.

New York Agricultural Experiment Station Technical

Bulletin No. 175, 24 p.

and J. F. Hockey. 1922. Mosaic and leaf curl

(yellows) of the cultivated red raspberry. Phytopathology

12:253-264.

Reitzel, J. 1971. Cikaden Macropsis fuscula Zett. i

hindbaerkulturer. [The leafhopper Macropsisfuscula Zett. in

raspberry plantings.] Tidskrift for Planteavl 75:577-580. [In

Danish.]

Review of Applied Mycology. 1957. Common names of

plant virus diseases used in the Review of Applied

Mycology. Review of Applied Mycology 35 (Suppl.), 78 p.

Richter, J. 1962. Das Himbeermosaik in Europa. Archiv für

Gartenbau 2:79-87.

1963. Die Verzwergungskrankheit der Rubus-Arten

(Rubus-Stauche). Nachrichtenblatt für den Deutschen Pñanzenschutzdienst (Berlin) 17:170-173.

1964a. Untersuchungen über die Himbeermosaikkrankheiten im Gebiet der Deutschen Demokratischen

Republik. I. Die Verbreitung des Himbeermosaiks und seine

Ausbreitung im Freiland. Archiv für Gartenbau 12:485-502.

1964b. Untersuchungen über die Himbeermosikkrankheiten im Gebiet der Deutschen Demokratischen

Republik. II. Versuche für Differenzierung des Himbeermosaiks. Archiv für Gartenbau 12:517-538.

1964c. Versuche für mechanischen Übertragung und

Identifizierung von Himbeerviren. Zentralblatt für Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene

(section 2) 118:1-15.

and H. Kegler. 1967. Isolierung des Latenten

Erdbeerringñeckenvirus (strawberry latent ringspot virus) aus

stauchekranken Pfirsichbäumen. Phytopathologische Zeitschrift 58:298-301.

267
and E. ProU. 1970. Reinigung und Fraktionierung des

Latenten Erdbeerringfleckenvirus (strawberry latent ringspot

virus). Acta Phytopathologica Academiae Scientarium Hungaricae 5:151-166.

Rietsema, I. 1954. De heksenbezemziekte der frambozen.

[Witches'-broom of raspberries.] De Boer 26(10): 1. [In

Dutch.]

Rush, M. C., and G. V. Gooding, Jr. 1970. The occurrence of

tobacco ringspot virus strains and tomato ringspot virus in

hosts indigenous to North Carolina. Phytopathology 60:1756-

1760.

G. V. Gooding, Jr., and D. E. Ellis. 1968. Wild

Rubus spp. as natural hosts for tobacco ringspot virus.

Phytopathology 58:1065. [Abstract.]

Ryschkow, W. L. 1946. [Virus diseases in Rosaceae], p.

59-65. In [Phytopathogenic viruses.] Moscow. [In Russian.]

Saito, Y., M. Roechan, D. M. Tantera, and M. Iwaki. 1975.

Small bacilliform particles associated with penyakit habang

(tungro-like) disease of rice in Indonesia. Phytopathology

65:793-796.

Savino, v., M. Barba, G. Gallitelli, and G. P. MartelH. 1979.

Two nepoviruses isolated from olive in Italy. Phytopathologia

Mediterránea 18:135-142.

Schaefers, G. A. 1967. Aphid control in virus-free raspberry

nursery stock. Farm Research (New York) 33:14-15.

Schambach, H. 1972. Die Verzwergungskrankheit der

Brombeere. Gartenbauliche Versuchsberichte Landwirtschaftskammer Rheinland 11:184-185.

Schmelzer, K. 1962. Untersuchungen an Viren der Zier- und

Wildgehölze. 2 Mitteilung. Virusen an Forsythia, Lonicera,

Ligustrum und Laburnum. Phytopathologische Zeitschrift

46:105-138.

1963. Untersuchungen an Viren der Zier- und

Wildgehölze. 3 Mitteilung. Virusen Sin Robinia, Caryopteris,

Ptelea und anderen Gattungen. Phytopathologische Zeitschrift 46:235-268.

1969. Das Latente Erdeerringflecken-Virus aus

Evonymus, Robinia und Aesculus. Phytopathologische Zeitschrift 66:1-24.

Schimanski, H.-H., and K. Schmelzer. 1972. Zur Kenntnis

der Übertragbarkeit des Kirschenblattroll-Virus (cherry leafroll virus) durch dén Samen von Sambucus racemosa L.

Zentralblatt für Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene Abteilung II 127:673-675.

Schwartze, CD., and G. A. Huber. 1937. Aphis resistance in

breeding mosaic-escaping red raspberries. Science 86:158-

159.

and G. A. Huber. 1939. Further data on breeding

mosaic-escaping raspberries. Phytopathology 29:647-648.

Scotto la Massese, C, C. Marénaud, and J. Dunez. 1973.

Analyse d'un phénomène de dégénérescence du pêcher dans la

vallée de l'Eyrieux. Comptes Rendus des Séances de

l'Académie d'Agriculture de France 59:327-339.

Sequiera, O. A. de. 1967. Purification and serology of an

apple mosaic virus. Virology 31:314-322.

Slate, G. L., and W. H. Rankin. 1933. Raspberry growing in

New York State: cultural practices and disease control. New

York Agricultural Experiment Station (Geneva) Bulletin No.

625,62 p.

Slits, H. J. A. 1964. Heksenbezems in frambozen. [Witches'-

broom in raspberries.] De Boer 26(50): 1. [In Dutch.]

1955. Nogmaals: Heksenbezems in frambozen.

[Again: Witches'-broom in raspberries.] De Boer 27(19): 1.

[In Dutch.]

Smith, F. T. 1925. The relation of insects to the transmission

of raspberry leaf curl. Journal of Economic Entomology

18:509-513.

Smith, K. M. 1946. Tomato black ring: a new virus disease.

Parasitology 37:126-130.

and R. Markham. 1944. Two new viruses affecting

tobacco and other plants. Phytopathology 34:324-329.

- and M. E. Short. 1959. Lettuce ringspot: a soil-borne

virus disease. Plant Pathology 8:54- 56.

Stace-Smith, R. 1954. Chlorotic spotting of black raspberry

induced by the feeding of Amphorophora rubitoxica

Knowlton. The Canadian Entomologist 86:232-235.

1955a. Studies on Rubus virus diseases in British

Columbia. I. Rubus yellow-net. Canadian Journal of Botany

33:267-274.

1955b. Studies on Rubus virus diseases in British

Columbia. II. Black raspberry necrosis. Canadian Journal of

Botany 33:314-322.

1956. Studies on Rubus virus diseases in British

Columbia. III. Separation of components ofraspberry mosaic.

Canadian Journal of Botany 34:435-442.

268
1958. Studies on Rubus virus diseases in British

Columbia. V. Thimbleberry ring spot. Canadian Journal of

Botany 36:385-388.

1960a. Current status of bramble viruses. Canadian

Plant Disease Survey 40:24-42.

1960b. Studies on Rubus virus diseases in British

Columbia. VI. Varietal susceptibility to aphid infestation in

relation to virus acquisition. Canadian Journal of Botany

38:283-285.

1961. Studies on Rubus virus diseases in British

Columbia. VII. Raspberry vein chlorosis. Canadian Journal of

Botany 39:559-565.

— 1962a. Studies on Rubus virus diseases in British

Columbia. VIII. Raspberry leaf curl. Canadian Journal of

Botany 40:651-657.

1962b. Studies on Rubus virus diseases in British

Columbia. IX. Ringspot disease of red raspberry. Canadian

Journal of Botany 40:905-912.

1968. Rubus viruses and virus diseases. Review of

Applied Mycology 47:97-109.

1970a. Tobacco ringspot virus. Descriptions of Plant

Viruses No. 17. Commonwealth Mycological Institute and the

Association ofApplied Biologists. Kew, Surrey, England, 4p.

1970b. Tomato ringspot virus. Descriptions of Plant

Viruses No. 18. Commonwealth Mycological Institute and the

Association ofAppliedBiologists. Kew, Surrey, England, 4p.

- and A. A. Brunt. 1974. Occurrence of tobacco streak

virus in the native trailing blackberry in British Columbia.

Proceedings of the American Phytopathological Society 1:52.

[Abstract.]

H. A. Daubeny, P. R. Bristow, and G. Baumann.

1982. Incidence ofsap transmitted viruses in experimental and

commercial plantings of red raspberries. Acta Horticulturae

129:91-98.

and N. W. Frazier. 1971. Tobacco streak virus

isolated from strawberry infected with necrotic shock.

Phytopathology 61:757- 758.

and A. J. Hansen. 1974. Occurrence of tobacco

ringspot virus in sweet cherry. Canadian Journal of Botany

52:1647-1651.

and A. J. Hansen. 1976a. Cherry rasp leaf virus.

Descriptions of Plant Viruses No. 159. Commonwealth

Mycological Institute and the Association of Applied

Biologists. Kew, Surrey, England, 4 p.

and A. J. Hansen. 1976b. Some properties of cherry

rasp leaf virus. Acta Horticulturae 67:193-197.

and A. T Jones. 1978. Rubus yellow net virus.

Descriptions of Plant Viruses No. 188. Commonwealth

Mycological Institute and the Association of Applied

Biologists. Kew, Surrey, England, 4 p.

and E. Leung. 1976. Small bacilliform particles

associated with Rubus yellow net virus. Proceedings of the

American Phytopathological Society 3:320. [Abstract.]

and E. Lo. 1973. Morphology of bacilliform

particles associated with raspberry vein chlorosis virus.

Canadian Journal of Botany 51:1343-1345.

and T. Matsumoto. 1979. Virus diseases of small

fruits, a bibliography, 1973-1978. Agriculture Canada,

Vancouver, Canada, 39 p.

and T. Matsumoto. 1982. Virus diseases of small

fruits, a bibliography, 1979-1981. Agriculture Canada,

Vancouver, Canada, 20 p.

and F. C. Mellor. 1957. Studies on Rubus virus

diseases in British Columbia. IV. Transmission of raspberry

mosaic viruses to Fragaria vesea L. Canadian Journal of

Botany 35:287-290.

and F. C. Mellor. 1979. A heat-stable black

raspberry necrosis virus. Acta Horticulturae 95:71-75.

Stellmach, G. 1970. Tomato black ring in Vitis, p. 234-236.

InN. W. Frazier, editor. Virus diseases of small fruits and

grapevines. University of California, Division of

Agricultural Sciences, Berkeley, 290 p.

and R. Bercks. 1965. Fortgeführte Untersuchungen

zur Charakterisierung des Tomatenschwarzringflecken-Virus

(tomato black ring virus) in kranken Reben der Sorte

'Aramon X Riparia 143 A.M.G.' (Amerikanerrebe).

Phytopathologische Zeitschrift 53:383-390.

Sweet, J. B., and D. J. Barbara. 1979. A yellow mosaic

disease of horse chestnut {Aesculus spp.) caused by apple

mosaic virus. Annals of Applied Biology 92:335-341.

Swenson, K. G., and J. A. Milbrath. 1964. Insect and mite

transmission tests with the Prunus ringspot virus.

Phytopathology 54:399-404.

Szilágyi, K. 1980. Small fruit cultivation in Hungary. Acta

Horticulturae 95:21-22.

Tapio, E. 1961. Vadelman Virustaudit. [Virus diseases on

raspberry.] Valtion Maatalouskoetoiminnan Julkaisuja No.

184, 21 p. [In Finnish; with English summary.] Abstracted in

Review of Applied Mycology 40:759. 1961.

269
Taylor, C. E. 1962. Transmission of raspberry ringspot virus

by Longidorus elongatus (de Man) (Nematoda:

Dorylaimidae). Virology 17:493-494.

1967. The multiplication oíLongidorus elongatus (de

Man) on different host plants with reference to virus

transmission. Annals of Applied Biology 59:275-281.

1970. The association oí Longidorus elongatus with

raspberry ringspot and tomato black ring viruses. Proceedings

of the Ninth International Nematology Symposium. Warsaw,

1967, p. 283-289.

1980. Nematodes, p. 375-416. In K. Harris, and K.

Maramorosch, editors, Vectors of plant pathogens. Academic

Press, New York, 467 p.

-and J. Chambers. 1969. Effects of insecticide

treatments on aphid populations and on spread oflatent viruses

in raspberry cane nurseries. Horticultural Research 9:37-43.

J. Chambers, and W. I. Pattullo. 1965. The effect of

tomato black ring virus on the growth and yield of Mailing

Exploit raspberry. Horticultural Research 5:19-24.

and A. F. Murant. 1965. The use of quintozene

(PCNB) as a nematicide. Proceedings of the Third British

Insecticide and Fungicide Conference, 1965, p. 514-520.

and A. F. Murant. 1966. Nematicidal activity of

aqueous extracts from raspberry canes and roots.

Nematologica 12:488-494.

and A. F.

raspberry ringspot

Murant. 1968. Chemical control of

and tomato black ring viruses in

strawberry. Plant Pathology 17:171-178.

and A. F. Murant. 1969. Transmission of strains of

raspberry ringspot and tomato black ring viruses by

Longidorus elongatus (de Man). Annals of AppHed Biology

64:43-48.

P. R. Thomas, and R. H. Converse. 1966. An

outbreak of arabis mosaic virus and Xiphinema

diversicaudatum (Micoletzky) in Scotland. Plant Pathology

15:170-174.

Téliz, D., R. G. Grogan, and B. F. Lownsbery. 1966.

Transmission of tomato ringspot, peach yellow-bud mosaic,

and grape yellow vein viruses by Xiphinema americanum.

Phytopathology 56:658-663.

Thomas, C. E. 1969. Transmission of tobacco ringspot virus

by Tetranychus sp. Phytopathology 59:633-636.

Thomas, P. R. 1969. Crop and weed plants compared as hosts

of viruliferous Longidorus elongatus (de Man). Plant

Pathology 18:23-28.

Thomas, W., and C. H. Procter. 1972. Arabis mosaic virus

in Cyphomandra betacea Sendt. New Zealand Journal of

Agricultural Research 15:395-404.

and C. H. Procter. 1977. Further studies on arabis

mosaic virus in Cyphomandra betacea Sendt. New Zealand

Journal of Agricultural Research 20:543-546.

Thung, T. H. 1952. Waamemingen omtrent de dwergziekte

bij framboos en wilde braam. II. [Observations on stunt in

raspberry and wild blackberry. IL] Tijdschrift over

Planteziekten 58:255-259. [In Dutch.] [For part I, see de

Fluiter and Thung (1951).]

Tilts, A. A. 1962. Vaarika viirushaigustest Eesti NSV-s.

[Virus diseases of soft fruit crops in the Eastern Estonian S.

S. R.] Trudy Instituta eksperimental' noi biologii Akademaja

nauk Estonskoi S. S. R. 2:128-139. [In Russian.] Abstracted

in Review of Applied Mycology 41:123. 1962.

Tomlinson, J. A., A. L. Carter, E. M. Faithfull, and M. J. W.

Webb. 1973. Purification and serology of the W strain of

cucumber mosaic virus. Annals of Applied Biology 74:181-

189.

and W. M. Robertson. 1969. The location of

raspberry ringspot and tomato black ring viruses in the

nematode vector, Longidorus elongatus (de Man). Annals of

Applied Biology 64:233-237.

and W. M. Robertson. 1970. Sites of virus retention in

the alimentary tract of the nematode vectors, Xiphinema

diversicaudatum (Micol.) and X. index (Thome and Allen).

Annals of Applied Biology 66:375-380.

and P. R. Thomas. 1968. The association of

Xiphinema diversicaudatum (Micoletzky) with strawberry

latent ringspot and arabis mosaic viruses in a raspberry

plantation. Annals of Applied Biology 62:147-157.

and D. G. A. Walkey. 1967. The isolation and

identification of rhubarb viruses occurring in Britain. Annals

of Applied Biology 59:415-427.

Tonks, N. V. 1960. Life history and behavior of the

leafhopper Macropsis fuscula Zett. (Homoptera:

Cicadellidae) in British Columbia. The Canadian

Entomologist 92:707-713.

Trifonov, D. 1961. Malinov snop.

Ovoshtarstvo 8:25-26. [In Bulgarian.]

[Rubus stunt.]

Trudgill, D. L., and T. J. W. Alphey. 1976. Chemical

control of the virus-vector nematode Longidorus elongatus

and oí Pratylenchus crenatus in raspberry plantations. Plant

Pathology 25:15-20.

270
United Kingdom, Department of Agriculture and Fisheries for

Scotland. 1965. Inspection and certification of raspberry

plants. Department of Agriculture and Fisheries for Scotland.

DE 1938/1, 7 p. [Mimeographed.]

Vaughan, E. K., F. Johnson, R. E. Fitzpatrick, and R.

Stace-Smith. 1951. Diseases observed on bramble fruits in

the Pacific Northwest. Plant Disease Reporter 35:34-37.

Vegetti, G., G. BelU, S. Cinquanta, and C. Soncini. 1979.

Identificazione e prime caratteristiche di un ceppo di SLRV

(strawberry latent ringspot virus) isolato da coltivazioni

di lampone in Lombardia. Rivista di Patologia Végétale

15:51-63.

Vertogradova, O. N. 1938. [Virus diseases of crops, and

their control.] Sbornik AkademiiaNauk S.S.S.R. 2:232-237.

[In Russian.]

Virdi, B. v., H. A. Daubeny, and G. W. Eaton. 1972.

Meiotic irregularities associated with a partially male-sterile

red raspberry selection. HortScience 7:263.

G. W. Eaton, and H. A. Daubeny. 1972. Embryo sac

development in a partially male-sterile red raspberry

selection. HortScience 7:263-264.

R. Stace-Smith, and J. H. Tremaine. 1973.

Serological, physical and chemical properties of strains of

cherry leaf roll virus. Phytopathology 63: 566-571.

and S. G. Whittingham-Jones. 1970. Seed transmission of strawberry latent ringspot virus in celery (Apium

graveolens var. dulce). Plant Disease Reporter 54:802-803.

Waterworth, H. E. 1975. Purification of arabis mosaic virus

isolated from a jasmine plant introduction. Phytopathology

65:927-928.

Whitcomb, R. F., and R. E. Davis. 1970. Mycoplasma and

Phytarboviruses as plant pathogens persistently transmitted

by insects. Annual Review of Entomology 15:405-464.

Wilcox, R. B. 1926. Observations on masking raspberry

mosaic by high temperatures. Phytopathology 16:80.

[Abstract.]

from

[Abstract.]

- and F.

red to

F. Smith. 1924. Transfer of mosaic disease

black raspberry. Phytopathology 14:55.

Wilhelm, S. 1951. Diseases of trailing blackberries. Western

Fruit Grower 5(5):29-31.

Vries, H. de. 1896. Een epidemic van vergroeningen [An

epidemic of virescences.] Botanisch Jaarboek (Gent) 8:66-

91. [In Dutch.]

Vuittenez, A., J. Kuszala, M. Rudel, and H. Brückbauer.

1970. Détection et étude sérologique du virus latent des

taches annulaires du fraisier (strawberry latent ringspot), du

virus des anneaux noirs de la tomate (tomato black ring) et du

virus taches annulaires du framboisier (raspberry ringspot)

chez des vignes du Palatinat. Annales de Phytopathologie

12:279-327.

H. E. Thomas, and E.G. Koch. 1951. Diseases of the

loganberry. California Agriculture 5:11-14.

Williams, H. E., and H. K. Wagnon. 1970. Loganberry

calico, p. 160. In N.W. Frazier, editor. Virus diseases of

small fruits and grapevines. University of California, Division of Agricultural Sciences, Berkeley, 290 p.

J. A. Traylor and H. K. Wagnon. 1963. The

infectious nature of pollen from certain virus-infected stone

fruit trees. Phytopathology 53:1144.

Wagner, W. 1964. Die auf Rosaceen lebenden MacropsisArten der Niederlande. Entomologische Berichten 24:123-

136.

Winter, J. D. 1929. A preliminary account of the raspberry

aphids. Minnesota Agricultural Experiment Station Technical Bulletin No. 61, 30 p.

Walkey, D. G. A. 1967a. Chlorotic stunt of lettuce caused by

arabis mosaic virus. Plant Pathology 16:20-22.

1967b. Seed transmission of arabis mosaic virus in

lettuce (Lactuca sativa). Plant Disease Reporter 51:883-884.

1968. The production of virus-free rhubarb by apical

tip culture. Journal of Horticultural Science 43:283-287.

and J. Mitchell. 1969. Studies on a 'strap-leaf

disease of celery caused by strawberry latent ringspot virus.

Plant Pathology 18:167-172.

Wood, C. A., and M. M. Anderson. 1959. Raspberry

cultivation in light of recent research. Commercial Grower

3323:338-340.

Wood, G. A., and J. C. Todd. 1976. Crumbly berry and leaf

yellows in raspberry. New Zealand Commercial Grower

31:3-23.

Woodford, J. A. T., and S. C. Gordon. 1978. Virus-like

symptoms in red raspberry leaves caused by fenitrothion.

Plant Pathology 27:77-81.

Wormald, H., and R. V. Harris. 1932. Notes on certain plant

diseases observed in 1931. East Mailing Research Station

Report for 1931, p.47-50.

271
Yassin, A. M. 1968. Transmission of viruses by Longidorus

elongatus. Nematologica 14:419-428.

Zeller, S. M. 1923. Mosaic and other systemic diseases of

brambles in Oregon. Oregon Agricultural Experiment Station

Circular No. 49, 15 p.

and A. J. Braun. 1943. Decline disease of raspberry.

Phytopathology 33:156-161.

Zundel, G. L. 1931. New or unusual symptoms of virus

diseases of raspberries. Phytopathology 21:755-757.

272
Subject Index

Acyrthosiphon

malvae subsp. rogersii, 14

malvae zerozalphum, 14

Albinism in strawberry, 84-85

Alfalfa mosaic virus, 153-155

Allium

ascalonicum, 212

cepa, 212

porum, 212

schoenoprasum, 212

Allygus mayri, 200, 202

Alpine mosaic agent, 70

Amphorophora

agathonica, 14, 18, 167-72, 177, 181,

189,191,194-95,229

breeding host resistance, 174

idaei, 18, 172, 177, 181, 185-86, 195,

229, 250,253

breeding host resistance, 174

parviflori, 193-94

rubi, 185

rubicumberlandi, 171, 181

rubitoxica, 171, 175

ruborum, 171, 185

sensoriata, 171,181,189

Anagallis arvensis, 204

Animal taxa names

sources used, 1-2

Anoscopus albifrons, 36

Aphelenchoides

besseyi, 44, 72-73

fragariae, 72-73

ritzemabosi, 73

Aphid damage to black currant, 142; to

Rubus, 175

Aphis

forbesi, 23, 67

gossypii, 14, 60, 67

grossulariae, 130, 137, 140

idaei, 171,185,188,194-96

rubicola, 171,187-88

mbifolii, 18, 188, 190

schneiden, 130, 137, 140, 144

spiraecola, 189

triglochinis, 144

Aphrodes bicincta, 34, 36, 40, 45-46, 109

Apium graveolens var. dulce, 33, 45, 200,

204,212

Apple chlorotic leaf spot virus, 240

Apple mosaic, 70

Apple mosaic virus, 248

properties, 248

Rubus, 246-48

Apricot ring pox, 70

Arabis spp. 49

hirsuta, 204

Arabis mosaic virus

blackcurrant, 132

detection, 127

see also Yellow mottle of black

currant, 139

blackberry

cultivar susceptibility, 205

redcurrant, 132, 148-49

red raspberry

cultivar susceptibility, 205

Rubus

see Raspberry yellow dwarf, 204

strawberry, 49-51

see also Latent infection of gooseberry

with arabis mosaic virus; Yellow mottle

of black currant, 139

Armoracia rusticana, 204

Arthropod damage on strawberry, 76

mealybug, 76-77

shallot aphid, 77

spider mites, 78

spittlebug, 77

tarnished plant bug, 77-78

Asclepias syriaca, 14

Asparagus officinalis, 204, 212

Aster yellows in strawberry, 31-34

Aulacorthum solani, 18, 171, 181

Austroagallia tórrida, 43

B

Bean yellow mosaic virus, 240, 244, 249

Bellis perennis, 204

Beta

macrocarpa, 239

vulgaris subsp. saccharifera, 212

Big bud,70

Black currant yellows, 140-41

Black raspberry necrosis, 175, 178-83, 197

Blackraspberry necrosis virus, 173, 176,

185-86, 229,

240

see also Raspberry mosaic

Black raspberry streak, 249

Blackberry

'Bedford Thomless'

crinkle and sterility, 250

mottling disease, 250

Blackberry calico, 245-46

Blackberry sterility, 249

Blueberry leaf mottle, 102, 112-14

Blueberry mosaic, 119-120

Blueberry shoestring, 101-5

Blueberry stunt, 101, 106-8, 110

Blueberry witches'-broom, 101

Boron

deficiency

Rubus, 175

strawberry, 82

Bramble yellow mosaic, 240-41, 243-44

Brassica

napobrassica, 111

napus, 212

olerácea, 212

rapa. 111

Bromocil

damage to Rubus, 151

Bronze leaf wilt disease, 45

Budlessness of redcurrant, 158, 160-61

Calcium deficiency

strawberry, 83

Callistephus chinensis, 31, 33, 153

Capsella bursa-pastoris, 204, 212

Catharanthusroseus, 34, 36, 45, 106-7, 239

Catkin disorder (Rubus), 253-54

Cauliflower disease of strawberry, 72

Cauliflower mosaic virus, 19

Cecidophyopsis ribis, 133, 135, 142, 159

Cerastiumvulgatum, 111

Chaetosiphon

fragaefolii, 5, 14-15, 18, 20-23, 27-28,

30,67,77,171, 177

jacobi, 14, 18, 23-24, 27-28, 30, 40, 61,

64

minor, 14,23,27,30

tetrarhodum, 14, 18

thomasi, 14-15, 18,27,30,67

Chemical damage (see also herbicide

damage)

Rubus

bromocil, 252

fenitrothion, 251

glyphosate, 251

Chemotherapy, 8

Chenopodium

album, 13,239

amaranticolor, 13-14,59,65, 113-14,

116, 131-32,136,139,

146, 149-50, 179, 191-92,

207, 209, 214, 216-17,

219-20,225,228,231,

239,241,247

ambrosoides, 239

capitatum, 141

foetidum, 110, 239

murale, 179, 191, 207, 209, 231-32, 239,

241-43

quinoa, 13-14, 54, 59, 65-66, 102, 112,

114,116-18,131-32,136-37,

139-40, 145-46, 150-51, 153-55,

173, 179-82,185,191-92,207,

209-10,214,216-17,219-20,

222,225-26,228,231-34,

236-38, 239-40, 241-42, 244,

247-48

test plant for sap transmission, 5

Cherry leaf roll virus, 113

properties, 222

Rubus, 220-23

Cherry rasp leaf virus, 227-28

properties, 242-43

Rubus, 241-43

Chrysanthemum carinatum, 200

Clover phyllody

transmission efforts, 44

see also. Strawberry green petal

Clover rugose leaf curl, 43

Clover yellow edge, 45-46

Coelidia olitoria, 56

Colladonus

geminatus, 33, 40

montanus, 33, 40

Cornus nuttallii, 111

Corynebacteriumfascians, 73

Cranberry false blossom, 101, 110-11

Cranberry ringspot, 121

Crumbly fruit disorder in Rubus, 252-53

Cryptomyzus spp., 130

galeopsides subsp. citrinus, 144

ribis, 137-38, 144

Cucumber mosaic virus, 240

"arc mosaic" of golden currant, 136

green mottle of black currant, 136-37

detection, 127

273
green mottle ofred currant, 136, 145-46

in raspberry, 191-92

Cucumissativus, 54, 59, 102, 112, 114,

117-18, 149-50,191,204,

207-9,212,220,225-28,

232-33, 241-42, 244, 247

Cucúrbita pepo, 204

Cuscuta

arvensis, 36

campestris, 30, 34, 36, 44-45, 107,

109-10

epithymum, 109

europaea, 36

gorovonii, 14, 36

subinclusa, 14, 18, 30, 36, 40, 67, 106-7,

109

X-disease transmission, 39

Cyamopsis tetragonoloba, 13

Cyclamen mite damage in strawberry, 73-75

Cydonia oblonga, 231-32, 234

Cyphomandra betacea, 204

D

2, 4-D, 79-80

Datura stramonium, 114, 239

Daucus carota, 204, 212

Delphinium sp., 204

Delphinium yellows, 45

Dianthus caryophyllus, 204

Dinoseb, 80

Drepanopezzia ribis, 141

Duchesnea indica, 36

Dymicoccus sp., 121

E

Eastern aster yellows, 31

Empoasca solani, 109

Erdbeer-nekrosevirus, 16

ELISA, 57, 102, 104, 108, 115, 118, 127,

140, 149, 167, 226, 238, 248

seed transmission evaluation, 8

strawberry virus detection, 5,19

Empoascafabae, 75

Erigeron spp., 31

Eriophyes gracilis, 175

Eriophyid mite damage

black currant, 142-43

Euonymus europaea, 204

Euscelidius variegatus, 40

Euscelis spp., 43

incisus, 36, 45

lineolata, 36

lineolatus, 45

plebeja, 45,200,202

Fenitrothion

damage to Rubus, 251

Fiebierellaflorii, 40

Forsythia sp., 204

Fragaria

X annanassa, 61, 243

chiloensis, 16, 25, 38, 52, 66, 68

Orientalis, 67

ovalis, 25

vesca, 4, 11-13, 15-33, 36, 38-39, 41-43,

51-53,55-58,60-65,67,69,

176-77,195, 198,231,243-45

heatspot, 28,78

latent A infection, 3, 16, 20

steps in leaf grafting, 6-7

vesca var. alba, 67

vesca var. californica, 11, 17, 23, 31

vesca var. semperflorens, 4, 17, 21-23,

28,31,49,58,

64,66,71, 173,

176,187-88

vesca subsp. americana, 16

vesca subsp. bracteata, 67

virginiana, 4, 16-17, 19, 22, 24-25, 28,

30,39-40,46,53,55-56,58,

60-64

Fragaria (strawberry) diseases

aphid-borne diseases

strawberry crinkle, 20-25

strawberry latent C, 29-31

strawberry mild yellow-edge, 25-29

strawberry mottle, 10-16

strawberry vein banding, 16-20

detection and elimination, 2

detection methods

biochemical methods, 5, 8

grafting, 3-7

sap transmission to herbaceous plants, 5

self-indicating diseases and false

symptoms, 2-3

serological methods, 5

vector transmission, 5

elimination methods

chemotherapy, 8

seed transmission elimination, 8

thermotherapy, 8-9

tissue culture, 8-20

experimentally transmitted only diseases,

69-70

European nepoviruses, 36

identification methods, 3

indicator clones, 3-4

introduction, 1-2

leafhopper-bome diseases

aster yellows, 31-34

bronze leaf wilt, 45

clover yellow edge, 45-46

delphinium yellows, 45

other leafhopper-bome diseases, 45-46

strawberry green petal, 34-38

strawberry lethal decline, 38-41

strawberry rickettsia yellows and

mycoplasma yellows, 41-45

minor diseases

minor or little-known viruses, 68-69

strawberry leafroll, 61-62

strawberry feather-leaf, 62-63

strawberry pseudo mild yellow-edge,

63-64

strawberry witches'-broom and

multiplier diseases, 66-68

tobacco necrosis virus, 64-66

nongraft transmissible diseases and

disorders

bud and leaf nematodes, 72-73

cyclamen mite damage, 73-75

heat spot oíFragaria vesca, 78

herbicide damage, 79-81

miscellaneous arthropod damage,

76-78

nutritional imbalances, 81-85

potato leafhopper injury, 76-78

strawberry June Yellows, 69, 71-72

Frankliniella occidentalis, 237

Fraxinus excelsior, 204

Frilly leaf disorder {Rubus), 252

Full blossom of red currant, 155-57

Genetic disorders oíRubus, 252

catkin, 253-54

crumbly fruit, 252-53

frilly leaf, 253

lateral-leaf crinkle, 253-54

Geranium dissectum, 212

Glyphosate

damage to Rubus, 251

Gomphrena globosa, 13-14, 59, 179, 239,

244

Gooseberry deterioration, 131

Gooseberry vein banding, 129-30, 137

see also Vein cleaning of black currant,

137

Grapevine Bulgarian latent virus, 112

Graphocephala atropunctata, 40

Green mosaic (Rubus), 70

Green mottle of black currant, 136-37

Green mottle ofred currant, 145-46

H

Heat spot oíFragaria vesca, 62, IS

Helenium sp., 38

Herbicide damage

strawberry, 79-Sl, Rubus, 251-52

Humulus lupulus, 204

Hyperomyzus

lactucae, 24, 130, 137-38, 140, 142, 144

pallidus, 130, 140

I

Idiodonus cruentatus, 109

Illinoia

davidsoni, 193-94

maxima, 193-94

pepperi, 104, 121

rubicola. 111, 181, 189

Infectious variegation of black currant,

141-142

Interveinal white mosaic of red currant,

153-55

Jasminum officinale, 204

Lactuca sativa, 204, 212

Lamium amplexicaule, 204, 212

Latent infection of gooseberry with arabis

mosaic virus, 131-32

Lateral-leaf crinkle disorder oíRubus,

253-54

Leaf grafting, 55, 172

steps, 6-7

Leaf malformation of red currant, 158-59

274
Leaf pattern of red currant, 150-52

Ligustrum vulgäre, 204

Lolium perenne, 212

Longidorus elongatus, 46, 131, 209, 211,

217,219

Lycopersicum esculentum, 40, 45, 110,

149, 212,239

Lygocoris pabulinus, 135

Lycus

elisus, 11

hesperus, 11

lineolaris, 11

M

Macropsis brabantica, 201

fiiscula, 109, 200-2

scotti, 201

Macrosiphum

euphorbiae, 171, 181, 185, 191,240

fragariae, 171,181, 185

pelargonii, 18

rosae, 27

Macrosteles spp., 43

cristatus, 36

fascifrons, 31, 33, 36, 40, 67

viridigriseus, 36

Magnesium deficiency

strawberry, 82

Manganese deficiency

strawberry, 83

Mealybug damage in strawberry, 76-77

Medicago sativa,212

Melilotas officinalis, 204

Mentha arvensis, 204

Microsphaera alni war. vaccinii, 121

Mild streak of black raspberry, 70

Mite damage to Rubus, 252

Myosotis arvensis, 111

Myzaphis rosarum, 14

Myzus

ascalonicus, 14, 18, 77

persicae, 18, 27, 130, 137-38, 145, 171,

181,191

ornatus, 14, 18, 24

N

Napropamide, 80

Narcissus spp., 204

pseudo-narcissus, 212

Narcissus mosaic virus, 240

Nasonoviaribisnigri, 130, 137-38, 140, 144

Necrotic femleaf mosaic of red raspberry,

249

Necrotic ringspot of blueberry, 114-16, 227

Nematodes

strawberry

bud, 72-73

leaf, 72-73

Neophilaenus exclamationis, 109

NEPO Virus No. 1 (Strawberry vein

necrosis), 68

NEPO Virus No. 2, 68

Nesoclutha pallida, 44

Nicotiana, 131

clevelandii, 112-13, 114, 191-92,209,

212,218,220,222,228,

232-34, 238, 242, 247

debneyi, 179

glutinosa, 145, 153, 191, 220, 228

rustica, 114, 145,215,218,247

tabacum, 40, 54, 59, 114, 117-18, 145,

149-51, 191,207,216,220,

225,228,236,244-45,247

Nutrient imbalances

strawberry, 81-85

O

Olpidium brassicae, 4, 65-66

Oro5/M5 spp., 43

argentatus, 44

Paraphlepsius irroratus, 36

Pastinaca sativa, 212

Peach yellow-bud mosaic, synonym for

tomato ringspot virus, 52

Peach yellow leafroll strain of X-disease

MLO, relationship to strawberry lethal

decline MLO, 39-49

Peach rosette mosaic virus in blueberry,

102,116-17

Petroselinum crispum, 212

Petunia hybrida, 114, 149-50, 155, 179,

207-8,210,216-17,239,

244,247

Phaseolus

aureus, 65

multiflorus, 204

vulgaris, 65, 114, 149-50, 153, 191,

216-17,220,225,228,232-34,

238-39,241,244,247

Philaenus

leucophthalmus, 11

spumarius, 200, 202

Phyllocoptes gracilis, 252

Plant taxa names

source used, 2

Plantago

lanceolata, 204

major, 31, 33

Plum line pattern. Fragaria an experimental

host, 70

Polygonum

aviculare, 204, 212

convolvulus, 212

persicaria, 204

Potassium deficiency

strawberry, 82

Potato leafhopper injury in strawberry,

75-76

Potato spindle tuber viroid, 8

Potato virus X, 240

Potato virus Y as a contaminant with yellow

leaf spot of red currant, 153

Potentilla

adscherica, 12

canadensis, 12

sterilis, 12

táurica, 12

Prune dwarf, Fragaria an experimental

host, 70

Prune dwarf virus

complex with strawberry latent ringspot

virus in peach, 207

Prunus sp., 39-40

amygdalus, 212

avium, 204, 212

domestica, 204

pérsica, 204, 212, 225

serrulata, 247

Prunus (necrotic) ringspot virus, 247

Prunus ringspot. Fragaria an experimental

host, 70

Prunus ringspot virus

complex with arabis mosaic virus in

cherry, 207

Pseudococcus spp., 76

R

Ranunculus repens, 204

Raspberry bushy dwarf, 167-68, 185,

229-34, 241

Raspberry bushy dwarf virus, 239, 252

Raspberry chlorotic spot virus, 185

Raspberry leaf curi, 187-90, 211, 223

Raspberry leaf mottle, 178, 183-87, 198

Raspberry leaf mottle virus, 182-83

see also Raspberry mosaic, 168

Raspberry leaf spot, 178, 183-87

Raspberry leaf spot virus, 173, 182-83

see also Raspberry mosaic, 168

Raspberry mosaic, 167-75, 186, 196, 198,

223,252

Raspberry ringspot, 154, 211, 218-19

symptoms on experimental hosts, 214-17

symptoms on natural hosts, 211-14

Raspberry ringspot virus, 190, 209

blackcurrant, 140

blackberry

cultivar susceptibility, 205

gooseberry, 131

properties, 218

red currant, 131

see also Spoon leaf of red currant, 146

red raspberry

cultivar susceptibility, 205

symptoms, 213

strawberry, 46-48

Raspberry vein chlorosis, 185, 189, 194-97

Raspberry yellow dwarf, 204-11

arabis mosaic virus, 49

causal agents properties, 210

arabis mosaic virus, 210

strawberry latent ringspot virus, 210

in strawberry, 49

Raspberry yellow mosaic virus, 175

Raspberry yellow spot, 186, 249-50

Red currant vein banding, 143-45

Red raspberry

* Norfolk Giant'

leaf curling, 250

Red ringspot of blueberry, 102, 121-23

Reversion of blackcurrant, 133-36, 153,

155-56, 158-59

Rheum rhaponticum, 204

Rhodobium porosum, 14

Ribes

alpinum, 133

aureum, 136, 139, 146

bracteosum, 133

xCarrierei, 133

275
dikuscha, 133

divaricatum, 129, 132

Gordonianum, 132

xholosericeum, 129

Koehneaniim, 129

leptanthum, 129

longeracemosum, 129

multiflorum, 129

xnigrolaria, 132

nigrumwai. europaeum, 132

nigrumvar. sibiricum, 133, 135

petraeum, 158

prostratum, 132

X robusturn, 129

rubrum, 159

rubrumwar. pubescens, 133

xrusticum, 129

sanguineum, 129, 139, 152-53

sativum, 129, 160

spicatum, 133

ienwe, 132

ímí^, 132

Watsonianum, 129

/?/¿7^5 (gooseberry and black and red

currant) diseases

aphid-borne diseases

gooseberry vein banding, 129-30

green mottle of black currant, 136-37

green mottle ofred currant, 145-46

red currant vein banding, 143-45

vein clearing and vein net disease of

blackcurrant, 137-38

detection, 127-28

graft transmission, 127

indicator plants, 127-28

mechanical transmission, 127

serology, 127

introduction, 127

mite-borne diseases

reversion of black currant, 133-36

nematode-bome diseases

arabis mosaic virus, 131-32, 148-49

gooseberry deterioration, 130

leafpattem of red currant, 150-52

raspberry ringspot virus, 140

spoon leaf ofred currant, 146-48

strawberry latent ringspot virus,

140, 148-49

tomato black ring virus, 140

tomato ringspot virus, 140, 149-50

yellow mottle of black currant, 139-40

vectors unknown

black currant yellows, 140-41

full blossom of red currant, 154-57

infectious variegation, 141 -42

interveinal white mosaic, 153-54

yellow leaf spot of red currant, 152-53

viruslike disorders

aphid damage, 142

budlessness ofred currant, 160-61

gooseberry mosaic, 132

leafdamage by eriophyid mites, 142

leaf malformation, 132, 158-59

sectorial chimaera, 143

spring vein banding, 142

Ringspot of cranberry, 123-24

/?ö5aspp., 204

Rose virus-1 antiserum for detection of

apple mosaic virus in Rubus, 248

276

Rubus

albescens, 170, 176, 179, 187

allegheniensis, 170, 179, 187, 227, 245

argutus, 187, 227

baileyanus, 187

bartoni, 231

bartonianus, 241

caesius, 200-2

ellipticus, 170

flagellaris, 111

fruticosus, 170, 179

gracilis, 170, 183

henryi, 170-73, 176, 179, 181-82,185-87,

192-93, 195,231,236,241,

242-45, 250, 253

idaeus, 170, 175, 179, 187, 191, 193,

195,204,211,230,234,239,

241-42, 246, 253

idaeus YSûî. strigosus, 170, 179, 187, 195

innominatus, 170

laciniatus, 170, 179, 184, 202, 231, 239,

241

lasiocarpusvar. rosifolius, 170, 179

leucodermis, 170, 179

loganobaccus, 170, 179, 192, 195, 239

macropetalus, 230

molaccanus, 170, 179, 185, 195, 231-

32, 234, 239

neglectus, 187

occidentalism 170-73, 175-76, 178-79,

181-83, 185-87, 191, 193,

195-97, 202, 230, 233-34,

239,241-42,245-46,248,

250, 253

odoratus, 170

parviflorus, 170, 192,231

phoenicolasius, 170, 179, 185, 187,

191-92,195,230-31,

233,236,239-40

procerus, 170, 175, 179, 184, 187, 192,

195,201,204,211-12,220,

231,236,239,245,250

rigidus, 243

rubrum, 218

sachalinensis, 212, 230-31

saxatilis, 170, 185

spectabilis, 170

ulmifolius var. inermis, 245

ursinus, 59, 170, 179, 187, 225, 235-36,

245-46, 248

ursinus war. macropetalus, 170, 179

vulgatus subsp. buschii, 230-31

xanthocarpus, 250

/?M¿7M5 (raspberry and blackberry) diseases

aphid-borne diseases

black raspberry necrosis, 178-83

cucumber mosaic virus in raspberry,

191-92

raspberry leaf curl, 187-90

raspberry leaf mottle, 183-87

raspberry leaf spot 183-87

raspberry mosaic, 168-75

raspberry vein chlorosis, 194-97

Rubus yellow net, 175-78

thimbleberry ringspot, 192-94

introduction, 167-68

leafhopper-bome diseases

rubus stunt, 197-203

minor diseases, 248

Alpine mosaic agent, 70

bean yellow mosaic virus, 249

black raspberry streak, 249

blackberry sterility, 249

necrotic femleaf mosaic, 249

raspberry yellow spot, 249-50

tobacco necrosis virus, 248-49

tobacco rattle virus, 249

miscellaneous disorders

apple mosaic virus, 246-48

viruslike disease symptoms, 251-54

nematode-bome diseases

arabis mosaic virus, 204-11

cherry leaf roll virus, 220-23

raspberry ringspot virus, 211-20

raspberry yellow dwarf, 204-11

strawberry latent ringspot virus,

204-11

tobacco ringspot virus, 227-28

tomato black ring virus, 211-20

tomato ringspot virus, 223-27

pollen-borne diseases

raspberry bushy dwarf virus, 228-34

presumed virus diseases

blackberry crinkle and sterility, 250

blackberry mottling disease, 250

raspberry leaf curling, 250

vectors unknown

blackberry calico, 245-46

bramble yellow mosaic, 243-44

cherry rasp leaf virus, 241-43

tobacco streak virus, 235-39

wineberry latent virus, 239-41

Rubus stunt, 197-203

Rubus yellow net, 70, 175-79, 196-97

see also Raspberry mosaic, 168

Rugose mosaic, 70

Salt toxicity

strawberry, 84-85

Sambucus nigra, 204

Sanguisorba minor, 25, 28

Scaphytopius

acutus, 34, 36

magdalensis, 106-7

Scleroacus vaccinii, 110

Sectorial chimera of black currant, 143

Senecio vulgaris, 204

Senescence disorder, 70

Shallot aphid damage in strawberry, 77

Simazine, 80

Solanum

demissum, 153

tuberosum, 212

Spergulaarvensis, 212

Speudotettix subfusculus, 36

Sphaerotheca

humuli, 175, 194

mors-uvae, 130

Spider mite damage in strawberry, 78

Spinacia olerácea, 179, 241

Spiroplasma citri, 108

Spittlebug damage in strawberry, 77

Spoon leaf ofred currant, 131, 146-48

Spring dwarf of strawberry, 72-73

Spring vein banding of black currant, 142

Stellaria media, 204, 212, 219, 225

Strawberry band mosaic, 68
Strawberry chlorotic fleck, 60

Strawberry crinkle, 20-25, 76, 78, 188

control, 8-9, 24-25

indicator plant infection, 3

symptoms

in complexes, 4, 22-23, 26, 188

Strawberry feather-leaf, 62-63

Strawberry green petal, 8, 34-38, 45

Strawberry June yellows, 69-72

Strawberry latent A virus, 20

Strawberry latent B, 20

Strawberry latent C, 29-31

Strawberry latent ringspot virus, 49-51

blackberry

cultivar susceptibility, 205

in black currant, 140

in red currant, 148-49

red raspberry

cultivar susceptibility, 205

see also Raspberry yellow dwarf, 204-11

Strawberry leafroll, 8, 61-62, 73

Strawberry lesion A, 20

Strawberry lesion B, 20

Strawberry lethal decline, 2, 38-41

Strawberry mild yellow-edge, 4, 23-29,

64,78

Strawberry mottle, 4, 8, 10-16, 23

Strawberry multiplier disease, 66-68

Strawberry mycoplasma yellows, 41-45

Strawberry necrosis, 68

Strawberry pallidosis, 55-56, 62, 78

symptoms, 4, 26, 55-56

Strawberry pseudo mild yellow-edge, 63-64

Strawberry rickettsia yellows, 41-45

Strawberry rosette necrosis virus, 64

Strawberry stunt, 68

Strawberry vein banding 8, 16-20, 23

Strawberry vein chlorosis virus, 20

Strawberry vein necrosis (NEPO Virus

No. 1),68

Strawberry virus indicator clones, 3-4

Strawberry witches'-broom, 66-68

Summer dwarf of strawberry, 72-73

Symphytum officinale, 160

Syringa vulgaris, 204

Taraxacum officinale, 204, 241

Tarnished plant bug damage in strawberry,

77

Tetranychus sp., 228

turkestani, 78

urticae, 78, 175

Thermotherapy, 8-9, 29, 38

Thimbleberry ringspot, 192-94

Thrips tahaci, 237

Tissue culture, 8-10, 168

Tobacco mosaic virus

in strawberry, 61, 69

Tobacco necrosis virus, 64-66

Ruhus, 248

strawberry, 66

history and geographic distribution

Rubus, 248-49

strawberry, 64

symptoms

strawberry, 4, 29, 65

transmission

strawberry, 5, 65

Tobacco rattle virus

Rubus, 249

see also Leaf pattern of red currant, 150

Tobacco ringspot virus, 102

properties, 228

Rubus, 227-28

see also Necrotic ringspot of blueberry,

114

Tobacco streak virus, 234, 241, 243, 246

Rubus, 172, 235-39

strawberry, 5,8, 57-60

Tomato black ring virus, 190, 209

blackcurrant, 140

blackberry

cultivar susceptibility, 205

properties, 218-19

red raspberry

cultivar susceptibility, 205

symptoms, 213

strawberry, 46-49

see also Raspberry ringspot and associated

diseases, 211

Tomato ringspot virus, 113,211, 249

black currant, 140

blueberry, 102, 117-18

Rubus, 223-26

red currant, 149-50

strawberry, 52-55, 70

red raspberry, 223-25

Trichodorus spp., 151

Trifolium spp.

r^/7^n5, 40,45,200,204,212

symptoms

strawberry green petal, 35-36

Tulipa spp., 204

gesneriana, 212

U

Urtica

dioica, 204

urens, 204

Vaccinium

altomontanum, 101, 106

amoenum, 106

angustilfolium, 101, 103

atrococcum, 106

ashei, 101-2, 106-7

australe, 101-2, 112, 114, 119, 121

constablaei, 101

corymbosum, 101-3, 109, 112, 114, 119

121

darrowi, 106

elliotii, 106

macrocarpon, 101, 110

membranaceum, 101

myrtilloides, 101, 106

myrtillus, 101, 108-9, 121

myrtillusi. erecturn, 110

myrtillus Í. parvifolium, 109

myrtillus f. pygmaeum, 110

ovatum, 101

oxycoccus, 101, 108-10

pallidum, 101

stamineum, 106

uliginosum, 108-9

vacillans, 119

vitisidaea, 101, 108-10

Vaccinium (blueberry and cranberry)

diseases

aphid-borne diseases

blueberry shoestring, 103-5

introduction, 101-2

blueberry and cranberry culture history,

101

certification programs, 102

indexing and detection, 102

virus diseases, 101-2

leafhopper-bome diseases

blueberry stunt, 106-8

cranberry false blossom, 110-11

witches'-broom, 108-10

nematode-bome diseases

blueberry leaf mottle, 112-14

necrotic ringspot of blueberry,

114-16

peach rosette mosaic virus in blueberry,

116-17

tomato ringspot virus in blueberry,

117-19

vectors unknown

blueberry mosaic, 119-20

red ringspot of blueberry ,121 -23

ringspot of cranberry, 123

Vein clearing and vein net disease of black

currant, 137-38

Veronica

agrestis. 111

pérsica, 212

Vigna unguiculata, 149-50, 247

Virus groups 1-6 in strawberry, 69

Vitis

labrusca, 112, 116

vinifera, 112,204,212

W

Western X - disease, possible relationship

to strawberry lethal decline disease, 40

White clover mosaic virus, 240

White spot disease of plum experimentally

transmitted to Fragaria, 70

Wineberry latent virus, 239-41, 244

Witches'-broomof Vflccm/wm, 101, 108-10

X-disease possible relationship to

strawberry lethal decline disease, 39, 70

Xiphinema spp., 220

americanum, 53, 112-13, 115-17, 132,

225-28,241-42

coxi, 209

diversicaudatum, 46, 50, 139, 148, 150,

204,209,211,241

rivesi, 53, 225-26

Yellow blotch curl disease of red

raspberry, 249

Yellow leaf spot of red currant, 152-53

Yellow mottle of black currant, 139-40

Zinc deficiency

strawberry, 83

Zygina zealandica, 44

277