**Diseases Caused by Viruses**

**Virus Diseases Overview**

Viruses are obligate, acellular agents that reproduce inside living
cells, spread between tissues, and frequently cause diseases in plants.
They are a significant production constraint in chickpea and lentil.
Virus diseases are often misdiagnosed as physiological, toxicological,
or nutritional disorders because symptoms are similar and no pathogen is
visible, except under an electron microscope.

In chickpea and lentil, many types of viruses are involved with genomes
comprised of either single-stranded RNA or single-stranded DNA. Viruses
that naturally infect chickpea include at least 25 species and 14
candidates (isolates that are potentially species) in 16 genera and 9
families. Viruses that infect lentil include at least 15 species and 3
candidates in 12 genera and 6 families.

Entry of viruses into chickpea and lentil crops (primary infection) is
by vectors or infected seed. Spread from plant to plant within crops
(secondary infection) is by vectors, predominantly aphids (*Hemiptera*:
*Aphididae*). The pea aphid (*Acyrthosiphon pisum* Harris), cowpea aphid
(*Aphis craccivora* Koch), green peach aphid (*Myzus persicae* Sulzer),
and bean aphid (*Aphis fabae* Scopoli) are particularly important. For
chickpea, leafhoppers are vectors for important viruses of genus
*Mastrevirus* and also phytoplasmas, and thrips are vectors of less
important viruses of genus *Tospovirus* and genus *Ilarvirus*.

An understanding of dissemination mechanisms and reservoir hosts is
important in developing strategies for virus control. Viruses infecting
chickpea and lentil are different in terms of dissemination, even though
the same virus species, aphid species, and reservoir hosts are involved.
Chickpeas are colonized poorly or not at all by aphids. There are few
apterae (wingless aphids) that walk from plant to plant unless
colonizable weeds are present, Infection is by migrant alatae (winged
aphids) that fly that alight on individual chickpea plants and then fly
on to others, producing a scattered field distribution that is
characteristic for virus diseases in chickpea (Fig. 1). Plants with
symptoms are solitary or have only one or a few symptomatic plants
adjacent. Viruses acquired from hosts other than chickpea are generally
most damaging although secondary spread from chickpea has been shown to
occur for one virus species (*Cucumber mosaic virus*). Consequently,
control strategies that aim to reduce buildup of aphids, establishment
of early infection foci, or spread from these foci have limited benefit
for chickpea. Examples are use of virus-free seed, seed-applied
insecticide, and early aphicide sprays. In contrast, these same
strategies are commonly benefical for lentil, which is colonized
extensively by legume-feeding aphids that can walk as apterae to
adjacent plants or fly as alatae to other areas of crops. Secondary
spread in lentil is evident from patches of many infected plants (Fig.
2). Heavy aphid populations within lentil fields are often evidenced by
numerous molt cases under the plants at the soil surface (Fig. 3).

Losses in both chickpea and lentil can be minimized by optimizing
cultural practices. Sowing time, seeding rate, and fertilizer should aim
to give vigorous growth and early canopy closure. Broadleaf weeds in and
around crops should be controlled, as they can be sources of virus.
Poorly-established, weedy crops are most vulnerable to damaging
infestations (Fig. 4). Retention of standing stubble can deter flying
aphids. Sources of resistance to specific virus species have been
identified in lentil but are not widely available in commercial
cultivars. Chickpeas exhibiting low incidence of infection (tolremicity)
for a range of viruses have been identified in California, USA and
Australia, and released as cultivars.

The descriptions and illustrations that follow should be a useful for
distinguishing diseases caused by viruses from those caused by other
agents. However, the different virus species cannot be distinguished
reliably by symptoms in chickpea and lentil and infection by mixtures of
species is common. Identification of viruses by serological and nucleic
acid-based techniques is important for making informed decisions on
disease management strategies.

**Selected References**

Bosque-Perez, N. A., and Buddenhagen, I. W. 1990. Studies on
epidemiology of virus disease of chickpea in California. Plant Dis.
74:372-378.

Bos, L., Hampton, R. O., and Makkouk, K. M. 1988. Viruses and virus
diseases of pea, lentil, faba bean, and chickpea. Pages 591-615 in:
World crops: cool season food legumes. R. J. Summerfield, ed. Kluwer
Academic Publishers, The Netherlands.

Eastop, V. F. 1983. The biology of the principal aphid virus vectors.
in: Plant virus epidemiology. The spread and control of insect-borne
viruses, R. T. Plumb and J. M. Thresh, eds. Blackwell Scientific
Publications, Oxford, UK.

Klein, R. E., Larsen, R. C., and Kaiser, W. J. 1991. Virus epidemic of
grain legumes in eastern Washington. Plant Dis. 75: 1186.

Kumar, P. L., Kumari, S. M. G., and Waliyar, F. 2008. Virus diseases of
chickpea. Pages 213-234 in: Characterization, diagnosis & management of
plant viruses. Vol. 3: Vegetable and pulse crops, G. P. Rao, P. L. Kumar
and R. J. Holguín-Peña, eds. Studium Press LLC, Houston USA.

Latham, L. J., and Jones, R. A. C. 2001. Incidence of virus infection in
experimental plots, commercial crops, and seed stocks of cool season
crop legumes. Aust. J. Agric. Res. 52:397-413.

(Prepared by R.C. Larsen and M.W. Schwinghamer)

![](media/image1.png){width="3.0in" height="2.033333333333333in"}

Fig. 1. Scattered distribution of symptomatic plants, characteristic of
virus infection in chickpea crops. In chickpea there is little spread
between adjacent plants. (Courtesy M. W. Schwinghamer).

![](media/image2.png){width="3.0in" height="2.033333333333333in"}

Fig. 2. *Cucumber mosaic virus* (CMV)-infected lentils showing secondary
spread from first-infected (most stunted) plant at center. (Courtesy M.
W. Schwinghamer).

![](media/image3.jpeg){width="3.0in" height="1.875in"}

Fig. 3. White aphid molt casts are evident in lentil fields with high
aphid populations. (Courtesy R. C. Larsen)

![](media/image4.jpeg){width="2.665277777777778in"
height="1.9986111111111111in"}

Fig. 4. Poorly-established crops are most vulnerable to virus infection.
(Courtesy R.C. Larsen)

***Alfalfa mosaic virus***

*Alfalfa mosaic virus* (AMV) was first described in alfalfa (*Medicago
sativa* L.) in 1931 and later in pea (*Pisum sativum* L.) in 1933. The
virus has a natural and experimental host range that includes nearly 700
plant species in 70 families and is currently found worldwide. AMV is a
significant pathogen of chickpea and lentil in Australia, but apparently
not elsewhere.

**Symptoms**

**Lentil.** Infected plants exhibit a mild chlorosis with leaves reduced
in size, and are frequently malformed. Necrosis often occurs along
leaflet margins. Plants are usually stunted and may die prematurely.
Flowering and pod formation are reduced and seeds are small and
shriveled.

**Chickpea.** Both Kabuli and Desi type chickpeas become chlorotic and
stunted, and often with necrotic shoots and tips (Fig. 1). Plants often
die prematurely, especially when infected early. Desi chickpeas also may
exhibit marginal reddening of leaflets.

**Causal Agent**

AMV consists of a tripartite genome containing three single-stranded RNA
species, and a fourth sub-genomic RNA from which the coat protein is
translated. Virions vary in size and shape from spherical to bacilliform
measuring 18 nm in diameter and up to 56 nm in length. Transmission
requires the presence RNA-1 consisting of 3644 nucleotides (nt), RNA-2
(2593 nt), and RNA-3 (2037 nt) together with the coat protein or RNA-4
(881 nt). The coat protein has a molecular mass of 24.25 kDa. AMV is
serologically unrelated to any other known virus species.

**Epidemiology**

The natural host range of AMV includes approximately 150 plant species.
When combined with the experimental host range, the list of susceptible
plants is increased to over 600 species in 70 families. The virus is
transmitted in a non-persistent manner by at least 14 different aphid
species, of which the pea aphid (*Acyrthosiphon pisum*) is particularly
important \[See pea aphid under Insect pests\]. AMV may be introduced
into chickpea and lentil fields from infected weed or crop sources but
this can vary with geographical location and vector species. One other
source of infection is infected seed. AMV is seed-transmitted at levels
up to 5% in lentil and 2% in chickpea. Although secondary loci
infections can occur in lentil colonized by aphids, transmission is more
sporadic in chickpea as the aphid visits random plants in search of a
suitable host.

**Management**

An effective strategy for reducing incidence of AMV is to avoid
plantings near established alfalfa in which virus incidence can reach
near 100% after three years. Application of an approved insecticide may
be beneficial in lentil when high aphid populations occur. Insecticides
are not effective on chickpea. Use of certified virus-free lentil seed
eliminates seed-infected plants that can be a source of secondary
spread. The only resistant cultivar is the Australian chickpea cultivar
Gully which has tolremicity (low infection incidence) against aphid
transmitted virus species including AMV.

**Selected references**

Bol, J. E. 2003. Alfalfa mosaic virus coat protein-dependent initiation
of infection. Mol. Plant Pathol. 4:1--8.

Bosque-Perez, N. A., and Buddenhagen, I. W. 1990. Studies on
epidemiology of virus disease in chickpea in California. Plant Dis.
74:372-378.

Jones, R. A. C., and Coutts B. A. 1996. Alfalfa mosaic and cucumber
mosaic virus infection in chickpea and lentil: incidence and seed
transmission. Ann. Appl. Biol. 129:491-506.

Kaiser, W. J., and Danesh, D. 1971. Etiology of virus-induced wilt of
*Cicer arietinum*. Phytopathology 61:453-457

Kaiser, W. J. 1973. Etiology and biology of viruses affecting lentil
(*Lens esculenta* Moench.) in Iran. Phytopathol. Mediterr. 12:7-14.

Kaiser, W. J. 1981. Disease of chickpea, lentil, pigeonpea and tepary
bean in continental United States and Puerto Rico. Econ. Botany,
35:300-320.

Kaiser, W. J. 1987. Disease problems on dry peas, lentils, chickpea and
faba beans. Pages 157-174. In: Grain Legumes as Alternative Crops: A
Symposium. Centre for Alternative Crops and Products, University of
Minnesota, USA.

Latham, L.J., and Jones, R.A.C. 2001. Alfalfa mosaic and pea seed-borne
mosaic viruses in cool season crop, annual pasture, and forage legumes:
susceptibility, sensitivity, and seed transmission. Aust. J. Agri. Res.
52:771-790

(Prepared by R.C. Larsen and M.W. Schwinghamer)

![](media/image5.jpeg){width="3.1659722222222224in"
height="2.0743055555555556in"}

Fig. 1. Shoot tip symptoms caused by late infection with *Alfalfa mosaic
virus* (AMV) in Desi chickpea (three plants at left). (Courtesy M. W.
Schwinghamer).

![](media/image6.jpeg){width="2.7465277777777777in"
height="2.3868055555555556in"}

Fig.2. Shoot tip necrosis on chickpea caused by early infection with
*Alfalfa mosaic virus* (AMV). (Courtesy R. C. Larsen)

***Bean yellow mosaic virus***

*Bean yellow mosaic virus* (BYMV) (Family *Potyviridae*; Genus
*Potyvirius*) was previously known as bean virus 2 and *Phaseolus* virus
2. It was discovered in common bean (*Phaseolus vulgaris* L.) in 1925
and was the first virus reported to cause disease in chickpea in 1956.
Many different isolates of the virus occur in several important crops
throughout the world. It causes significant losses in lentil, common
bean, and faba bean, but is generally of minor importance in chickpea.

**Symptoms**

**Lentil.** Symptoms on lentil include chlorosis*,* mild mosaic or
mottling, and stunting. Leaves are often twisted or curled with necrosis
along margins as the effects of the virus infection progress. Flowering
and pod formation are reduced and consequently little seed is produced.

**Chickpea.** Chickpea is susceptible to BYMV, but has a much lower
incidence of natural infection than lentil. However, when infected, both
Kabuli and Desi type chickpeas develop apical necrosis (Figs. 1 and 2),
reddening of leaf margins, plant stunting and premature senescence.
Plants that are infected early but do not die may develop leaves that
are filiform (having very narrow leaflets) and sometimes distorted.

**Causal Agent**

BYMV is a flexuous rod-shaped virion 750 nm in length containing
single-stranded RNA and a coat protein with 282 amino acids. The genome
is monopartite with 10,000 nucleotides. BYMV is serologically related to
*Clover yellow vein virus* (ClYVV) which also infects many legume
species. The coat protein of BYMV is 68-76% identical at the amino acid
level with the coat protein of ClYVV. BYMV is more distantly related to
the legume-infecting potyviruses *Bean common mosaic virus, Bean common
mosaic necrosis virus, Pea seed-borne mosaic virus* and *Soybean mosaic
virus*. In chickpea, a number of *Potyvirus* isolates have been
described that are similar biologically to BYMV. These include Chickpea
yellow mosaic virus and Chickpea bushy dwarf virus which are distinct
serologically from BYMV, and Chickpea distortion mosaic virus and
Chickpea filiform virus which are related serologically to, and may be a
strains of BYMV. These appear to be of only minor or localized
importance, along with the recognized potyvirus species *Lettuce mosaic
virus* and *Turnip mosaic virus* (Fig. 2) that have also been reported
in chickpea.

**Disease Cycle and Epidemiology**

BYMV has a broad host range of over 200 plant species, predominantly
legumes. The virus is acquired from infected weed and perennial plant
sources by more than 20 aphid species and transmitted in a
non-persistent manner. The most common aphids associated with
transmission of BYMV to legume crops are *Acyrthosiphon pisum,
Macrosiphum euphorbiae* (Thomas)*, Myzus persicae*, *Aphis gossypii*
(Glover) and *Aphis fabae,* but other species including cereal aphids
may be important if present in high numbers. Common sources for the
virus in the field include clover (*Trifolium* spp. and *Melilotus
albus*), vetch (*Lathyrus* spp.), and alfalfa (*Medicago sativa*).
Consistent with other potyviruses, BYMV is mechanically transmissible.
Faba bean (*Vicia faba*) and pea (*Pisum sativum*) are common pulse
crops that are generally susceptible to BYMV and are also suitable hosts
for colonization by aphids, thus providing a ready source of inoculum. A
significant reduction in yield can occur in lentil fields when the
incidence of BYMV is high.

**Management**

BYMV is transmitted by seed at levels of up to 1% in lentil but is not
reported to be seed-borne in chickpea. Use of lentil seed certified to
be free of BYMV will aid in reduction of the virus within the crop.
Maintaining low levels of the virus in surrounding crops and weed hosts
can be difficult because of the wide host range of BYMV but spread of
the virus can be managed by eliminating local weed hosts. As with other
non-persistently transmitted viruses, application of insecticides to
control spread of the virus by aphids is ineffective except where the
vector has built up large populations in lentils. No resistance has been
identified in chickpea and only a few sources of tolerance have been
identified in lentil. Lentil accession ILL7163 has been reported in
Australia to be resistant to BYMV.

**Selected References**

Cheng, Y., and Jones, R. A. C. 2000. Biological properties of necrotic
and non-necrotic strains of bean yellow mosaic virus in cool season
grain legumes. Ann. App. Biol. 136:215-227.

Kaiser, W. J., and Danesh, D. 1971. Etiology of virus-induced wilt of
*Cicer arietinum.* Phytopathology 61:453-457.

Larsen, R. C., Kaiser, W. J., Wyatt, S. D., Buxton-Druffel, K. L., and
Berger, P. H. 2003. Characterization of a new potyvirus naturally
infecting chickpea. Plant Dis. 87:1366-1371.

Makkouk, K. M., Kumari, S. G., and Al-Daoud, R. 1992. Survey of viruses
affecting lentil (*Lens culinaris* Med.) in Syria. Phytopathol.
Mediterr. 31:188-190.

Mali, V. R., Polajiwar, B., Nirmal, D. D., and Patil, F. S. 1988.
Purification and properties of a virus causing distortion mosaic of
chickpea. Indian Phytopath. 41:336-343.

McKirdy, S. J., Jones, R. A. C., Latham, L. J., and Coutts, B. A. 2000.
Bean yellow mosaic potyvirus infection of alternative annual pasture,
forage, and cool season crop legumes: susceptibility, sensitivity, and
seed transmission. Aust. J. Agric. Res. 51:325-345.

Schwinghamer, M. W., Thomas, J. E., Parry, J. N., Schilg, M. A., and
Dann, E. K. 2007. First record of natural infection of chickpea by
*Turnip mosaic virus*. Australasian Plant Disease Notes 2:41-43.

Shukla, D. D., Ward, C. W., and Brunt, A. A. 1994. The Potyviridae. CAB
International, Wallingford, UK.

Snyder, W. C., Paulus, A. O., and Gold, A. H. 1956. Virus yellows of
garbanzo bean. Phytopathology 46:27.

(Prepared by R.C. Larsen and M.W. Schwinghamer)

![](media/image7.jpeg){width="2.7493055555555554in"
height="2.0131944444444443in"}

Fig. 1. Shoot tip necrosis in chickpea caused by early infection with
*Bean yellow mosaic virus* (BYMV). (Courtesy R. C. Larsen)

![](media/image8.jpeg){width="1.426388888888889in" height="2.0in"}

Fig. 2. Shoot tip necrosis in seedling chickpea caused by early
infection with a chickpea isolate of *Turnip mosaic virus* (TuMV), a
*Potyvirus* species related to *Bean yellow mosaic virus* (BYMV).
(Courtesy M. W. Schwinghamer)

***Cucumber mosaic virus***

*Cucumber mosaic virus* (CMV) was first described in 1916 and has a
large host range that includes over 1000 plant species in 85 families.
 It can cause severe losses in lentil during seasons of high aphid
populations when infection incidences exceed 50%, but rarely causes
significant damage in commercial chickpea crops.

**Symptoms**

**Lentil.** Symptoms in lentil include a general chlorosis of the plant,
leaf malformation and stunting (See Fig. 2 in Virus Diseases
Introduction), often followed by premature death (Fig. 1). Leaflets may
show a mild mosaic or reddening of leaf margins. A reduction in pod
number or filling of pods generally occurs resulting in yield loss.

**Chickpea.** For many CMV isolates and chickpea genotypes, symptoms are
more distinctive than for other virus species in chickpea. The most
distinctive feature is internode reduction (Fig. 2), shoot
proliferation, and slight stem kinking that can be described as bushy
stunting (Fig. 3). Leaflets show pale chlorosis, reduction in size, and
sometimes narrowing and pale mosaic (Fig. 4). Reddening may also occur
on leaf margins of Desi chickpea lines. Chickpea seedlings may show
necrosis of shoot tips. Plants sometimes die prematurely, but mortality
is generally less than for other viruses and small groups of infected
plants may persist after surrounding uninfected ones mature due to less
use of soil moisture. Even when plants survive, seed yield is reduced
greatly through failure of seed set.

**Causal Agent**

CMV is a member of the Family *Bromoviridae,* Genus *Cucumovirus.* It
has a tripartite genome encapsidated in isometric particles ca. 29 nm in
diameter that contain RNA-1 (3389 nucleotides), RNA-2 (3035
nucleotides), or RNA-3 (2197 nucleotides). A sub-genomic RNA-4 is also
encapsidated in the particles that contain RNA-3. The coat protein
consists of 218 amino acids with a molecular weight of 24.2 kDa. The
species has been divided into distinct serogroups called subgroups I and
II, with the latter comprising 70% of isolates. Phylogenetic analyses
have shown that subgroup I can be divided into subgroups IA and IB both
of which are distantly related to isolates belonging to subgroup II. CMV
is distantly related to other *Cucumovirus* species *Peanut stunt virus*
and *Tomato aspermy virus*.

**Epidemiology**

CMV can survive from year to year in many weed species, or in green
vegetation and crops in temperate areas. Perennial legumes such as
clover and alfalfa are ready sources of inoculum and many of these hosts
may remain symptomless. The virus is transmitted in a non-persistent
manner by many different aphid species. A number of these species
including cereal aphids may be important in the case of lentil, but
*Acyrthosiphon pisum* (pea aphid), where present, is likely to be the
most important for chickpea. Aphids can acquire the virus within a few
seconds and transmission can occur in an equally short time period.
Infectiveness is lost after brief probing but can be retained for hours
by alate aphids if they do not probe. CMV is seed transmitted in lentil
and chickpea, forage legumes, and in may weed species. Transmission by
seed is erratic in lentil and chickpea but can average 0.1% to 1%,
occasionally reaching 2% or higher within seed lots. In chickpea,
infected seed does not appear to lead to major losses in commercial
crops but major losses have been demonstrated in experimental plots.
There is more secondary spread in lentil than in chickpea, and
consequently lentil seed infected with CMV can lead to major losses in
commercial crops.

**Management**

CMV in lentil can be controlled by planting certified virus-free seed in
localities where other sources of infection are not present. Application
of systemic insecticides to lentil may be useful in reducing aphid
populations, especially if colonization is observed. However,
insecticides are not effective in chickpea and sometimes they increase
infection incidence on colonizable crops such as lentil, due to
increased movement of alate aphids. Allowing standing stubble to remain
from the previous cereal crop is partially effective in deterring alate
aphids in chickpea and lentil crops. Lentil lines L-4, PAK 3598,
ILL1983, Mizia, Medovina 1-G, ILL788, ILL7700, ILL7163, and ILL5405 have
been identified with tolerance or partial resistance to CMV. Some
tolerance in lentil may exist in ILL590 and the red lentil cultivar
Cobber. The Australian chickpea cultivar Gully has a reduced incidence
of infection by CMV and other aphid transmitted viruses.

**Selected References**

Chalam, T. V., Reddy, M. V., Nene, Y. L., Beniwal, S. P. S., and
Subbayya, J. 1986. Some properties of a strain of cucumber mosaic virus
isolated from chickpea in India. Plant Dis. 70:128-130.

Fletcher, J. D. 1993. Surveys of virus disease in pea, lentil, dwarf and
broad bean crops in South Island, New Zealand. N. Z. J. Crop Hortic.
Sci..21:45-53.

Fletcher, J. D., Russell, A. C., and Butler, R. C. 1999. Seed-borne
cucumber mosaic virus in New Zealand lentil crops: yield affects and
disease incidence. N. Z. J. Crop Hortic. Sci. 27:197-204.

Hsu, H. T., Barzuna, L., Hsu, Y. H., Bliss, W., and Perry, K. L. 2000.
Identification and subgrouping of *Cucumber mosaic virus* with mouse
monoclonal antibodies. Phytopathology 90:615-620.

Jones, R. A. C., and Coutts, B. A. 1996. Alfalfa mosaic and cucumber
mosaic virus infection in chickpea and lentil: incidence and seed
transmission. Ann. Appl. Biol. 129:491-506.

Jones, R. A. C., B. A. Coutts, L. J. Latham, and S. J. McKirdy. 2008.
*Cucumber mosaic virus* infection of chickpea stands: temporal and
spatial patterns of spread and yield-limiting potential. Plant Pathology
57:842-853.

Kaiser, W. J., and Danesh, D. 1971. Etiology of virus-induced wilt of
*Cicer arietinum*. Phytopathology 61:453-457.

Latham, L. J., and Jones, R. A. C. 2001. Incidence of virus infection in
experimental plots, commercial crops, and seed stocks of cool season
crop legumes. Aust. J. Agric. Res. 52:397-413.

Makkouk, K. M., Bashir, M., Jones, R. A. C., and Kumari, S. G. 2001.
Survey for viruses in lentil and chickpea crops in Pakistan. Z.
Pflanzenkr. Pflanzenschutz 108:258-268.

Moury, B. 2004. Differential selection of genes of Cucumber mosaic virus
subgroups. Mol. Biol. Evol. 21:1602-1611.

(Prepared by R.C. Larsen and M.W. Schwinghamer)

![](media/image9.png){width="2.25in" height="1.5263888888888888in"}

Fig. 1. Symptoms of viruses (predominantly *Cucumber mosaic virus*) in
experimental plots of lentil. (Courtesy M. W. Schwinghamer)

![](media/image10.jpeg){width="2.192361111111111in"
height="2.904166666666667in"}

Fig. 2. Internode reduction at shoot tips and kinking of stems in
chickpea caused by *Cucumber mosaic virus* (CMV). (Courtesy M. W.
Schwinghamer)

![](media/image11.png){width="2.498611111111111in"
height="1.6972222222222222in"}

Fig. 3. Symptoms of bushy stunting caused by *Cucumber mosaic virus*
(CMV) in desi chickpea (three plants at right). (Courtesy M. W.
Schwinghamer)

![](media/image12.jpeg){width="2.0034722222222223in"
height="1.4381944444444446in"}

Fig 4. Symptoms of early infection with *Cucumber mosaic virus*
including stunting, necrosis of primary shoot top and reduction and
narrowing of leaves on earliest growth. Healthy plant is at left. (
Courtesy R. C. Larsen)

***Faba bean necrotic yellows virus***

*Faba bean necrotic yellows virus* (FBNYV) is the causal agent of a
destructive disease of chickpea, lentil and other food and fodder
legumes in some arid regions of the Old World, such as countries of
North Africa, West Asia (Near East) and southern Europe. From chickpea
and/or lentil it was first reported in Syria in 1991 and subsequently in
Egypt (1993), Jordan (1998), Pakistan (1998), Ethiopia (1999), Iraq
(1999), Spain (2000), Iran (2001), and Sudan (2003). Viruses closely
related to FBNYV and *Milk vetch dwarf virus* from Japan, but clearly
distinct from typical FBNYV isolates from Syria and Egypt, occur in
Ethiopia, Morocco, and China.

**Symptoms.**

**Chickpea.** Characteristic symptoms of infection in chickpea include
leaf rolling, yellowing (or reddening) and stunting. Symptoms on
chickpea are similar to those caused by luteoviruses and mastreviruses.

**Lentil.** Field symptoms in lentil include stunting with leaf
malformation, yellowing, twisting and mottle. Flower formation is
reduced and pods are also reduced in number or size. Seed from affected
pods are significantly reduced in size.

**Causal Agent**

FBNYV is a nanovirus (Family: *Nanoviridae*). Its isometric virus
particles measure approximately 18 nm in diameter and contain a
multipartite single-stranded DNA genome. The nanovirus genome is thought
to be comprised of eight circular DNA components ranging in size from
985 to 1005 nucleotides. Each component is individually encapsidated and
encodes a different protein that is required for replication,
encapsidation, cell-to-cell transport or various other functions within
the nanovirus life cycle. In addition to the eight genomic DNAs, up to
five (additional) DNAs that encode different replication initiator
proteins (Rep) have been found in plants infected with nanoviruses.
Since these DNAs occur only erratically in nanovirus infections, they
are regarded as non-integral (satellite-like) DNAs, which depend on
their helper virus for various functions.

FBNYV is serologically unrelated to luteoviruses, such as *Bean leafroll
virus*, *Beet western yellows virus* (or Beet western yellows-like
species)*,* and *Soybean dwarf virus*. Hence, FBNYV can be easily
differentiated from luteoviruses using available monoclonal or
polyclonal antibodies. However, members of the genus *Nanovirus* are
serologically related. The serological relationships of FBNYV to the
nanoviruses *Milk vetch dwarf virus* (MDV; from Japan) and *Subterranean
clover stunt virus* (SCSV; from Australia) are close and distant,
respectively. This difference is reflected by the coat protein amino
acid sequence identities between the pairs FBNYV/MDV (83 %) and
FBNYV/SCSV (54 %). For the differentiation and specific detection of
closely related nanoviruses, species-specific monoclonal antibodies or
primers for use with RT-PCR are required.

**Epidemiology**

FBNYV was first described infecting faba bean (*Vicia faba* L.). Now it
is known to infect more than 50 legume species and only few non-legume
species (*Stellaria media,* *Arabidopsis thaliana,* *Amaranthus,* and
*Malva* spp.) under experimental and/or natural conditions. In addition
to faba bean, lentil, and chickpea, major legume crops naturally
infected by FBNYV are common bean (*Phaseolus vulgaris* L.), cowpea
(*Vigna unguiculata*), medicago (*Medicago* spp.), pea (*Pisum
sativum*), clover (*Trifolium* spp.), soybean (*Glycine max*), and vetch
(*Lathyrus* spp.). Some wild *Malva* spp. may serve as a reservoir host
of the virus.

The cowpea aphid (*Aphis craccivora)* appears to be the major natural
vector of FBNYV as it is the most abundant aphid species on legume crops
in the afflicted areas and is among the most efficient vectors under
experimental conditions. Other aphid vectors of FBNYV are the black bean
aphid (*Aphis fabae*) and the pea aphid (*Acyrthosiphon pisum)* but in
no case were *Myzus persicae* and *Aphis gossypii* able to transmit this
virus. FBNYV is transmitted in a persistent manner by aphids but does
not replicate in them. While the minimum access feeding periods for
FBNYV acquisition and inoculation range from 15 to 30 min, longer
acquisition access feeding periods render many individuals viruliferous
throughout their life (about 30 days). The median latency period
(LP~50~) is about 105 hours. The virus is retained through aphid moults,
and aphids acquiring FBNYV as nymphs are much more efficient vectors
than adults. In infected plants FBNYV is confined to phloem tissues,
rendering it non-transmissible by sap (or contact) and through seed or
pollen.

**Management**

Applications of systemic insecticides to lentil crops may reduce primary
and secondary infection and may reduce primary infection in chickpea
under high aphid population pressure. Because the aphid vectors do not
colonize chickpea, application of insecticides for control of the virus
is not cost effective. Although no cultivars of chickpea or lentil with
resistance to FBNYV are commercially available, screening for FBNYV
resistance with viruliferous aphids at ICARDA, Aleppo, Syria, identified
a number of promising lentil genotypes with high levels of resistance.
The same screening approach resulted in very inefficient FBNYV
transmission rates for chickpea, indicating the need for an improved
screening methodology before progress in identifying resistant chickpea
lines can be made. The resistant lentil genotypes include ILL 74 (PI
612870), ILL 75 (PI 612871), ILL 85 (PI 612872), ILL 213(PI 612873), ILL
214 (PI 612874), and ILL 6816 (PI 612875).

**Selected References**

Franz, A., Makkouk, K. M., Katul, L., and Vetten, H. J. 1996. Monoclonal
antibodies for the detection and differentiation of *Faba bean necrotic
yellows virus* isolates. Ann. App. Biol. 128:255--68.

Franz, A., Makkouk, K. M., and Vetten, H. J. 1998, Acquisition,
retention and transmission of *Faba bean necrotic yellows virus* by two
of its aphid vectors, *Aphis craccivora* (Koch) and *Acyrthosiphon
pisum* (Harris). J. Phytopathol. 146:347-355.

Katul, L., Maiss, E., and Vetten, H. J. 1995. Sequence-analysis of a
*Faba bean necrotic yellows virus*-DNA component containing a putative
replicase gene. J. Gen. Virol. 76:475-479.

Katul, L., Timchenko, T., Gronenborn, B., and Vetten, H. J. 1998. Ten
distinct circular ssDNA components, four of which encode putative
replication-associated proteins, are associated with the *Faba bean
necrotic yellows virus* genome. J. Gen. Virol. 79:3101-3109.

Katul, L., Vetten, H. J., Maiss, E., Makkouk, K. M., Lesemann, D. E. and
Casper, R. 1993. Characterisation and serology of virus-like particles
associated with faba bean necrotic yellows. Ann. App. Biol. 123,
629-647.

Makkouk, K. M., Bashir, M., Jones, R. A. C., and Kumari, S. G. 2001.
Survey for viruses in lentil and chickpea crops in Pakistan. Z.
Pflanzenkr. Pflanzenschutz 108:258-268.

Makkouk, K. M., Kumari, S. G., Shahraeen, N., Fazlali, Y., Farzadfar, S.
Ghotbi, T., and Mansouri, A. R. 2003. Identification and seasonal
variation of viral diseases of chickpea and lentil in Iran. Z.
Pflanzenkr. Pflanzenschutz 110: 157-169.

Makkouk, K. M., Bashir, M., and Jones, R. 1998. First record of faba
bean necrotic yellows virus and beet western yellows luteovirus
affecting lentil and chickpea in Pakistan. Plant Dis. 82: 591.

Tadesse, N., Ali, K., Gorfu, D., Yusuf, A., Abraham, A., Ayalew, M.,
Lencho, A., Makkouk, K. M. and Kumari, S. G. 1999. Survey for chickpea
and lentil virus diseases in Ethiopia. Phytopathol. Mediterr.
38:149-158.

Ortiz, V., Navarro, E., Castro, S., Carazo, G., and Romero, J. 2006.
Incidence and transmission of *Faba bean necrotic yellows virus* (FBNYV)
in Spain. Span. J. Agric. Res. 4:255-260.

(Prepared by H. J. Vetten and R. C. Larsen)

(No Figures, photos will be added when become available)

**Luteoviruses (*Bean leafroll virus*, *Soybean dwarf virus*, *Beet
western yellows virus*, and related viruses)**

Luteoviruses probably cause greater losses in chickpea than any other
group of viruses, and are among the most damaging to lentil. They and
their aphid vectors are common in virtually all regions of the world
where chickpea and lentil are grown and infection is commonly lethal.
The first report of a legume disease ascribed now to a luteovirus was
for *Bean leafroll virus* (BLRV) in faba bean in Germany in 1954. It was
followed in the 1960s and 1970s by *Beet western yellows virus* (BWYV)
in several food legumes and *Soybean dwarf virus* (SbDV syn.
Subterranean clover red leaf virus) in soybean and subterranean clover.
The first reports for chickpea were BLRV syn. Pea leaf roll virus in
Iran in 1971, BWYV in California in 1979, and SbDV in California in
1990. At least six species three to five isolates that are candidates
for species have now been reported as infecting chickpea and/or lentil.

**Symptoms**

Luteovirus symptoms, illustrated for chickpea in Figs. 1-5 and lentil
are essentially the same as for other phloem-limited viruses including
mastreviruses and *Faba bean necrotic yellows virus*. Infection causes
degeneration or necrosis of phloem cells, disrupting movement of
assimilates in plants.

In chickpea, phloem necrosis can often be seen as brown discoloration at
the collar, revealed by making a shallow cut near ground level (Fig. 1).
Foliage shows yellowing (Figs. 2) or reddening (Fig. 3) that is most
pronounced at the margins of leaflets. The yellowing symptom gave rise
to the name 'legume yellows' in chickpea and other legumes in California
in the 1970s. Reddening occurs in cultivars that have highest
anthocyanin content. Kabuli type chickpeas usually turn yellow, whereas
many Desi types turn red. Leaves have a stressed appearance with
leaflets folded upward along the rachis and midveins (Fig. 2). Affected
leaves frequently are thickened and brittle, and may produce an audible
snap when folded. Topmost leaves of shoots often show particularly
strong epinasty, yellowing, or reddening, but necrosis of the top does
not precede that of the whole plant. Reduction of yield results from
premature cessation of flowering and pod fill (Fig. 4) and reduction of
seed size. Plants that survive the onset of symptoms are stunted, hence
the name 'chickpea stunt' disease used originally in Asia. Plants die
prematurely (Fig. 5), whether or not they are stunted, unless plants
become infected late in the podding stage.

Foliar symptoms in lentil are similar to those in chickpea and include
yellowing or bronzing (Fig. 6), with leaflets that become leathery and
brittle. Leaf margins may exhibit a reddish color and entire leaflets
can become red usually under cool temperatures (Fig. 7). Plants are
severely stunted or may die if infected early (Fig. 8). Internode
lengths become shortened on upper portions of plants infected later in
the growth stage. Pods are reduced in size and are poorly filled or not
at all, resulting in significant losses in yield.

**Causal agents**

Luteoviruses are literally "yellowing viruses". They were recognized in
1976 as a group that included BLRV, BWYV, SbDV, Barley yellow dwarf
virus isolates, and other tentative members. The group was divided in
1997 into genus *Luteovirus* (BLRV, SbDV, and others) and genus
*Polerovirus* (*Potato leafroll virus*, BWYV and others). These two
genera were assigned to family *Luteoviridae* together with *Pea enation
mosaic virus-1* (PEMV-1; genus *Enamovirus*) and a number of unassigned
species. In present usage, "luteoviruses" usually applies to species in
family *Luteoviridae* but excluding PEMV-1 which is distinct
biologically and does not occur naturally in the absence of its
symbiotic *Umbravirus*, PEMV-2.

Luteovirus characteristics are: icosahedral particles 25-30 nm in
diameter that appear hexagonal in outline under the electron microscope;
a monopartite genome consisting of single-strand, positive sense RNA
(5,600-5,900 nucleotides) containing 5-6 open reading frames; infection
specifically of phloem; and transmission by aphids in a persistent
(circulative, non-propagative) manner. RNA sequences have been
determined for some chickpea or lentil isolates, including the complete
sequence of one isolate of the proposed species Chickpea chlorotic stunt
virus (CpCSV), partial sequence of two BWYV-like isolates, and partial
sequence of one isolate each of proposed species Chickpea stunt disease
associated virus (CpSDaV), Chickpea yellows virus (CpYV), and Lentil
Stunt virus (LStV).

Luteovirus species have most often been distinguished by serological
tests including ELISA and tissue blot immunoassay (TBIA). There is an
element of doubt in these identifications, however, because all legume
(*Fabaceae*)-infecting luteoviruses apart from PEMV-1 show some degree
of serological relatedness. Monoclonal antibody (MAb) B-2-5G4 reacts
with all of them and polyclonal antisera (PAs) to BRLV, SbDV, and BWYV
often cross react weakly. On the other hand, some MAbs and that were
reported to be species-specific have sometimes failed to detect all
isolates of a target species. Nucleic acid-based techniques including
reverse transcription polymerase chain reaction (RT-PCR) and membrane
hybridization are presently the most reliable way to distinguish
luteovirus species. Serological tests are still valuable for processing
large numbers of samples due to ease of sample preparation and
specificity should improve as a better range of MAbs becomes available.

BLRV, BWYV, and SbDV are regarded as important chickpea and lentil
pathogens. However, BWYV is best considered as a group of assigned or
likely poleroviruses (genus *Polerovirus*) that will be referred to here
as BWYV-like luteoviruses. The latter include BWYV and at least seven
other species or isolates that cross-react substantially with each
others' PAs and could not be distinguished until recently. BWYV-like
species and their diverse biological properties are detailed below under
Epidemiology. Poleroviruses distinct from BWYV including *Cucurbit
aphid-borne yellows virus* and *Potato leafroll virus* may also infect
chickpea and lentil based on serological identifications. LStV from
lentil is probably a polerovirus, but it and CpYV, which is more
SbDV-like, are not assigned yet to a particular genus or group as they
are known only from serology and partial RNA sequence.

**Epidemiology**

*Acyrthosiphon pisum* (pea aphid), *Aphis craccivora* (cowpea aphid)*,*
and *Myzus persicae* (green peach aphid) are considered to be important
vectors of chickpea and lentil luteoviruses worldwide. A few other aphid
species that feed on legumes may be important in some situations.
Chickpea is not colonized by aphids apart from minor or sporadic
occurrences of *A. pisum* and *A. craccivora*, but lentil is colonized
by *A. pisum*, *A. craccivora*, *M. persicae*, and at least three other
species.

Aphids need to feed for an extended period (usually several hours) to
acquire luteoviruses from an infected plant. They do not transmit during
latent periods of about 12 hours after acquisition feeding, but can then
transmit repeatedly by feeding for approximately 10 minutes and remain
transmissive for weeks or even months. This persistent manner of
transmission, which is essentially the same for *Faba bean necrotic
yellows virus* (FBNYV) and PEMV, may account for why luteoviruses,
FBNYV, and PEMV are relatively important viruses in chickpea. Migrant
flying aphids carry viruses into chickpea crops after acquiring them
from other hosts. Each migrant can infect numerous plants with
persistent viruses (multiple primary infections) rather than just the
first plant visited as is likely with nonpersistent viruses. Lentil is a
better acquisition host than chickpea and supports large populations of
colonizing aphids as well as migrants. This leads to secondary infection
and more opportunity than in chickpea for spread of nonpersistent
viruses including *Pea seed-borne mosaic virus* and *Cucumber mosaic
virus* that can be introduced through infected seed.

Migrant aphids carrying luteoviruses can reach such high numbers that
the primary infection sites in chickpea or lentil crops, i.e. individual
plants on which flying aphids land, reach high numbers. Infection
incidences of 50-100% occur occasionally in the USA, Australia (Fig. 5),
and possibly in other countries. This can lead to yield losses up to
100% alone or in combination with other viruses, although such
occurrences are sporadic.

Luteoviruses are not transmitted in seed, and none that infect legumes
can infect grasses. Their survival requires dicotyledonous host plants
(mostly legumes) that act as 'green bridges' between crops and
'reservoirs' during cropping. The most important reservoirs are plant
species that are plentiful, tolerant of luteovirus infection, and
colonized by aphids that visit chickpea and lentil. Perennial species
are particularly important, but in sub tropical and tropical latitudes,
annual weeds and food and forage crops are potentially important as
well.

BLRV occurs worldwide. Its main vector is considered to be *A. pisum*
and hosts include many legumes but very few non-legumes. Known
reservoirs include alfalfa (*Medicago sativa*) and white clover
(*Trifolium repens*).

SbDV occurs worldwide and is biologically diverse. Four (D, P, S and Y)
biotypes of SbDV are recognized. Isolates that are vectored primarily by
pea aphid *A. pisum* are P biotype, and those by foxglove aphid
*Aulacorthum solani* are S biotype. Isolates that are severe, cause
yellowing in soybean (*Glycine max*), and infect white clover are Y
biotype as distinct from D biotype which is commonly milder, causes
dwarfing in soybean, and infects red clover (*Trifolium pratense*). Y
and D biotypes are also distinct in their infection of other legumes and
Y biotype at least can infect some non-legumes. For chickpea and lentil,
Y and D biotypes have not been distinguished but P biotype is probably
more common than S biotype due to prevalence of *pea aphid* in these
crops. White clover and red clover are recognized reservoirs of Y and D
biotypes, respectively. Alfalfa does not appear to be an important
reservoir for SbDV although experimental and natural infections have
been recorded.

BWYV-like luteoviruses are even more diverse than SbDV. Broadly they can
be considered as two biotypes: one transmitted by *M. persicae* and
infecting many hosts including legumes, the other transmitted by *A.
craccivora* and restricted almost entirely to certain legumes. Virus
species of the *M. persicae*/many host biotype occur worldwide. They
include *Turnip yellows virus* (TuYV), Chickpea luteovirus (CpLV), and
BWYV which infect legumes and potentially *Beet chlorosis* virus (BChV)
and *Beet mild yellowing virus (*BMYV) which have not yet been shown to
infect legumes. *A. craccivora* appears to be a non-vector. TuYV and
CpLV are distinct from BChV, BWYV, and BMYV in that they do not infect
beet (*Beta vulgaris*). BWYV, TuYV, CpLV, BChV, and BMYV all infect at
least some *Brassicaceae* that are potential reservoirs. Virus species
of the *A. craccivora*/legume biotype are known only from West Asia and
North Africa. They include CpCSV, a luteovirus designated as A24
isolate, and possibly CpSDaV for which there is limited vector/host
information. *M. persicae* is a non-vector of CpCSV and an inefficient
vector of A24 isolate and CpSDaV. Naturalized or cultivated legumes are
likely reservoirs for the *A. craccivora*/legume biotype, but the
particular legume species are not known. A generalization for BWYV-like
luteoviruses of both biotypes is that alfalfa and white clover are not
known to be reservoirs although natural infection has been recorded.

Mixed infection between BLRV, SbDV, and BWYV-like luteoviruses is common
in legumes including chickpea. In seasons and localities where this
occurs (e.g. BLRV and SbDV in Australia), its incidence is higher than
would be expected if the individual species were acquired and
transmitted independently. Reservoir hosts may contain such luteovirus
combinations. Transencapsidation, as is known to occur between cereal
luteoviruses, has potential to broaden the range of aphid vectors or
increase transmission efficiency.

**Management**

Optimizing cultural practices as described above in the beginning
section (Virus Diseases Overview) is beneficial for commercial crops of
both chickpea and lentil. Insecticides applied as sprays or seed
treatment are effective against secondary spread in lentil but not in
chickpea. Roguing out early-infected plants can also be effective for
high value crops or germplasm collections of lentil. Germplasm lines of
lentil that are resistant to BLRV and SbDV, and for some lines FBNYV as
well, are available from the Genetic Resources Unit at ICARDA, Aleppo,
Syria. A trait identifiable by low or delayed infection incidence
(tolremicity) is available in chickpea cultivars from Australia (cv.
Gully and cv. Garnet in Fig. 5) and California. In cv. Gully this trait
appears to be effective against aphid-transmitted viruses of several
families.

**Selected references**

Abraham, A. D., Verrelmann, M., and Vetten, H. J. 2008. Molecular
evidence for the occurrence of two new luteoviruses in cool season food
legumes in Northeast Africa. Afr. J. Biotechnol.:414-420

Bosque-Perez, N. A., and Buddenhagen, I. W. 1990. Studies on
epidemiology of virus disease in chickpea in California. Plant Dis.
74:372-378.

D'Arcy, C. J., and Domier, L. L. 2005. Family *Luteoviridae*. Pages
891-900 in: Virus Taxonomy. Classification and Nomenclature of Viruses.
Eighth Report of the International Committee on the Taxonomy of Viruses.
C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger, and L. A. Ball,
eds. Elsevier Academic Press, San Diego, CA.

Number range CHAPTERDomier, L. L., McCoppin, N. K., Larsen, R. C., and
D\'Arcy, C. J. 2002. Nucleotide sequence shows that *Bean leafroll
virus* has a *Luteovirus*-like genome organization. J. Gen. Virol.
83:1791-1798.

Duffus, J. E. 1979. Legume yellows virus, a persistent aphid-transmitted
virus of legumes in California. Phytopathology 69:217-221.

Makkouk, K. M., Damsteegt, V., Johnstone, G. R., Katul, L., Lesemann,
D.-E, and Kumari, S. G. 1997. Identification and some properties of
soybean dwarf luteovirus affecting lentil in Syria. Phytopathol.
Mediterr. 36:135-144.

Makkouk, K. M., Kumari, S. G., Sarker, A., and Erskine, W. 2001.
Registration of six lentil germplasm lines with combined resistance to
viruses. Crop Sci. 41:931-932.

Makkouk, K. M., Kumari, S. G., Shahraeen, N., Fazlali, Y., Farzadfar,
S., Ghotbi, T., and Mansouri, A. R. 2003. Identification of seasonal
variation of viral diseases of chickpea and lentil in Iran. Z.
Pflanzenkr. Pflanzenschutz 110:157-169.

Naidu, R. A., Mayo, M. A., Reddy, S. V., Jolly, C. A., and Torrance, L.
1997. Diversity of coat proteins among luteoviruses associated with
chickpea stunt disease in India. Ann. Appl. Biol. 130:37-47.

Reddy, S. V., and Kumar, P. L. 2004. Transmission and some properties of
a new luteovirus associated with chickpea stunt disease in India. Curr.
Sci. (Bangalore) 86:1157-1161.

Schwinghamer, M. W., Johnstone, G. R., and Johnson-Lord, C. F. 1999.
First records of bean leafroll luteovirus in Australia. Australas. Plant
Pathol. 28:260.

(Prepared by M. W. Schwinghamer and R.C. Larsen)

![](media/image13.jpeg){width="1.44375in" height="2.0284722222222222in"}

**Fig. 1.** Phloem browning symptom in chickpea infected with the
luteovirus *Soybean dwarf virus* (SbDV). A shallow cut was made at the
collar to reveal the discoloration. (Courtesy M. W. Schwinghamer)

![](media/image14.jpeg){width="2.25in"
height="1.667361111111111in"}![](media/image15.jpeg){width="2.0in"
height="1.6263888888888889in"}

**Fig. 2**. A. Stunting and yellowing in a chickpea breeding line
inoculated (left) with an isolate of *Bean leafroll virus* (BLRV, a
luteovirus) compared with an uninfected plant (right). (Courtesy M. W.
Schwinghamer). B. Stunting and yellowing of leaf margins in chickpea
infected with *Bean leafroll virus.* (Courtesy R. C. Larsen)

![](media/image16.jpeg){width="2.25in" height="1.7569444444444444in"}

**Fig. 3.** Symptoms of yellowing, reddening of leaf margins, epinasty,
leaf folding, and stunting in desi chickpea cv. Amethyst inoculated with
an isolate of *Bean leafroll virus* (BLRV, a luteovirus). Two infected
plants are surrounded by uninfected ones. (Courtesy M. W. Schwinghamer)

![](media/image17.jpeg){width="3.0in" height="2.0131944444444443in"}

**Fig. 4**. Effects at harvest of earlier inoculation with *Bean
leafroll virus* (BLRV, a luteovirus) on chickpea: uninfected/symptomless
(left), and plants for which symptoms were first noted at 28 days post
inoculation (center) and 55 days (right) post inoculation. (Courtesy M.
W. Schwinghamer)

![](media/image18.png){width="3.0in" height="2.033333333333333in"}

**Fig. 5.** Natural infection of chickpea at podding with the
luteoviruses *Soybean dwarf virus* (SbDV) and *Bean leafroll virus*
(BLRV)*.* Plots of all genotypes except cv. Gully (3 near green plots)
and cv. Garnet (3 distant green plots) died prematurely due to a higher
incidence of infected plants. Gully and Garnet are resistant (tolremic)
and do not mature later than other genotypes in the absence of viruses.
(Courtesy M. W. Schwinghamer)

![](media/image19.jpeg){width="1.3597222222222223in" height="2.0in"}

**Fig. 6.** Leaf mottling and yellowing in lentil caused by infection
with *Bean leafroll virus* (BLRV, a luteovirus). (Courtesy R. C. Larsen)

![](media/image20.jpeg){width="2.0in" height="1.5131944444444445in"}

**Fig. 7.** Stunting, yellowing and reddening of leaves in lentil
infected with *Bean leafroll virus* (BLRV, a luteovirus). (Courtesy R.
C. Larsen)

![](media/image21.jpeg){width="2.0in" height="1.6131944444444444in"}

**Fig. 8.** Severe stunting and plant death of lentil field caused by
infection with *Bean leafroll virus* (BLRV, a luteovirus). (Courtesy R.
C. Larsen)

**Mastreviruses including Chickpea chlorotic dwarf virus**

Mastreviruses (genus *Mastrevirus*) are DNA-containing viruses that are
transmitted by leafhoppers (*Hemiptera: Cicadellidae*). Most infect
grasses, but a group of serologically interrelated species infects
dicotyledonous plants including legumes. The first report of a
dicot-infecting mastrevirus was in 1980 for *Tobacco yellow dwarf virus*
(TYDV syn Bean summer death virus) in tobacco (*Nicotiana tabacum*) and
bean (*Phaseolus vulgaris*) in Australia where it was found subsequently
in chickpea. In 1993 a mastrevirus named Chickpea chlorotic dwarf virus
(CpCDV) was identified in chickpea in India where it and several
luteoviruses were shown to cause chickpea stunt disease in India. At
least six additional mastreviruses from chickpea in North Africa,
Central and West Asia, and Australia have been distinguished recently by
DNA sequencing. Collectively they are common in chickpea but uncommon in
lentil.

**Symptoms**

**Chickpea**. Symptoms of mastrevirus infection are like those for other
phloem-limited viruses. In chickpea they include yellowing of foliage in
Kabuli type cultivars, reddening in Desi types (Figs. 1 and 2), phloem
browning at the collar, and stunting and premature death of plants.
Phloem browning is not always evident for mastrevirus infection in
Australia as it reportedly is for CpCDV in Asia and Africa.

**Lentil.** Stunting and yellowing have been recorded as symptoms.

**Causal agents**

Mastreviruses are members of the family *Geminiviridae* (geminiviruses),
so called because the virus particles appear as twinned isometric
particles under the electron microscope (from Latin *gemini*, 'twins').
They have a monopartite genome of single-stranded circular DNA comprised
of 2,600-2,800 nucleotides and encoding four proteins. Physico-chemical
and biological properties have been determined for bean and tobacco
isolates of TYDV from Australia and chickpea isolates of CpCDV from
India and Syria. Complete DNA sequences have been determined for
chickpea isolates from Sudan (Chickpea chlorotic dwarf Sudan virus),
Pakistan (Chickpea chlorotic dwarf Pakistan virus and *Bean yellow dwarf
virus*), and Australia (TYDV and three other unnamed species with less
than 80% overall sequence identity to other mastreviruses). All
dicot-infecting mastrevirus species identified so far react with CpCDV
and/or TYDV antiserum. Consequently, CpCDV is best interpreted as
"*Mastrevirus* sp." in reports from North Africa, Western Asia, and
Central Asia wherever identification was limited to serological tests
with CpCDV antiserum.

**Epidemiology**

Mastreviruses infect many legume crop species naturally: chickpea and
lentil in Western and Central Asia, faba bean in North Africa and West
Asia, chickpea, faba bean, bean (*Phaseolus vulgaris*), pigeon pea
(*Cajanus cajan*), and lablab (*Dolichos lablab*) in North Africa, and
chickpea and bean in Australia. Other natural hosts include legume and
non-legume wild plants in Sudan and subterranean clover (*Trifolium
subterraneum*), *Datura stramonium*, coriander (*Coriandrum sativum*),
tobacco and *Brassicaceae* weeds in Australia. Experimental inoculation
with viruliferous leafhoppers indicates a wide range of dicotyledonous
hosts, including families *Chenopodiaceae* and *Solanaceae* for CpCDV
isolates and at least seven families of plants for TYDV.

The vectors of mastreviruses are leafhoppers of the family Cicadellidae,
subfamily Deltocephalinae. These are small (2-7 mm), flying, cicada-like
insects that feed on the phloem of a wide range of plants. For CpCDV,
two species are vectors: *Neolimnus aegyptiacus* (Matsumura) in Sudan
and *Orosius albicinctus* (Matsumura) (Fig. 3, top) in India and Syria.
The vector of CpCDV in India was reported as *Orosius orientalis*
(Matsumura) but this was probably a misidentification of *O.
albicinctus. O. orientalis* (Fig. 3, bottom) is recorded from East Asia,
Oceania, and Australia. It has been known in Australia as *Orosius
argentatus* (Evans) which is reported to be a vector of TYDV and likely
to be a vector of other mastreviruses. None of the above three species
occurs in North America or South America. The geographical range of
chickpea mastreviruses is consistent with that of the known vectors, and
is mainly subtropical to tropical, extending sometimes to temperate
regions.

Leafhoppers probably acquire mastreviruses from wild *Fabaceae*,
*Chenopodiaceae*, or *Solanaceae* plants, crop legumes, or forage
legumes. Acquisition requires minimum feeds of only a few minutes. After
a latent period of several hours, mastreviruses persist and continue to
be transmitted by leafhoppers for most of their life during feeds
lasting several hours or longer. The insects alight and feed on
individual plants, producing a scattered pattern of primary infection.
On chickpea, they are not known to produce offspring or walk to adjacent
plants. Leafhoppers of subfamily Deltocephalinae are also vectors of the
phytoplasmas that cause phyllody, described in a separate section.

Mastreviruses often account for a substantial proportion of virus-like
symptoms when overall infection incidence (including aphid-transmitted
viruses) is low. It is unusual for mastreviruses to exceed 5% infection
in chickpea crops in most countries. However, in Sudan CpCDV incidence
reportedly reaches 60-70%, causing major losses. In India,seed yield
losses for individual CpCDV-infected plants were estimated at 75-100%
with crop losses nearly equivalent to infection incidence at medium
plant densities (10-20 plants/m^2^). Little or no yield compensation by
healthy plants occurred at these densities.

In lentil, mastreviruses are less common than in chickpea and do not
appear to cause significant losses.

**Management**

There are no reliable management options for mastreviruses. Resistance
due to decreased replication or in-plant virus movement of CpCDV has
been identified among chickpea and wild *Cicer* genotypes in India.
However, it is not clear whether this resistance is available or
promoted for farmers, or whether it is effective across the geographic
range of CpCDV. There is no evidence for control by insecticides. In
Sudan, reduced incidence of CpCDV has been reported in one chickpea
cultivar, in late-sown experimental plots, and frequently-irrigated
experimental plots.

**Selected references**

Hammed, A. A., and Makkouk, K. M. 2002. Occurrence and management of
Chickpea chlorotic dwarf virus in chickpea fields in northern Sudan.
Phytopathol. Mediterr. 41:193-198.

Horn, N. M., Reddy, S. V., Roberts, I. M., and Reddy, D. V. R. 1993.
Chickpea chlorotic dwarf virus, a new leafhopper-transmitted geminivirus
of chickpea in India. Ann. Appl. Biol. 122:467-479.

Horn, N. M., Reddy, S. V., van den Huevel, J. F. J. M., and Reddy, D. V.
R. 1996. Survey of chickpea (*Cicer arietinum* L.) for chickpea stunt
disease and associated viruses in India and Pakistan. Plant Dis.
80:286-290.

Kumari, S. G., Makkouk, K. M., Attar, N., and Ghulam, W. 2004. First
report of *Chickpea chlorotic dwarf virus* infecting spring chickpea in
Syria. Plant Dis. 88:424

Kumari, S. G., Makkouk, K. M., and Attar, N. 2006. An improved antiserum
for sensitive serologic detection of *Chickpea chlorotic dwarf virus*.
J. Phytopathol. 154:129-133.

Makkouk, K. M., Kumari, S. G., Shahraeen, N., Fazlali, Y., Farzadfar,
S., Ghotbi, T., and Mansouri, A. R. 2003. Identification of seasonal
variation of viral diseases of chickpea and lentil in Iran. Z.
Pflanzenkr. Pflanzenschutz 110:157-169.

Nahid, N., Amin, I., Mansoor, S., Rybicki, E. P., van der Walt, E., and
Briddon, R. W. 2008. Two dicot-infecting mastreviruses (family
*Geminiviridae* ) occur in Pakistan. Arch. Virol. 153:1441-1451.

Nault, L. R., and Ammar, E. D. 1989. Leafhopper and planthopper
transmission of plant viruses. Annu. Rev. Entomol. 34:503-529

Stanley, J., Bisaro, D. M., Briddon, R. W., Brown, J. K., Fauquet, C.
M., Harrison, B. D., Rybicki, E. P., and Stenger, D. C. 2005. Family
Geminiviridae. Pages 301-326 in: Virus Taxonomy. Classification and
Nomenclature of Viruses. Eighth Report of the International Committee on
the Taxonomy of Viruses. C. M. Fauquet, M. A. Mayo, J. Maniloff, U.
Desselberger, and L. A. Ball, eds. Elsevier Academic Press, San Diego,
CA.

Thomas, J. E., and Bowyer, J. W. 1984. Tobacco yellow dwarf virus.
CMI/CAB Descr. Pl. Viruses No. 278, 4pp.

(Prepared by M. W. Schwinghamer, J. E. Thomas, and M. J. Fletcher)

![](media/image22.jpeg){width="1.5083333333333333in"
height="1.9243055555555555in"}

Fig. 1. Reddening in a Desi chickpea variety caused by an unnamed
Australian mastrevirus. (Courtesy J. E. Thomas).

![](media/image23.png){width="1.6166666666666667in"
height="1.8645833333333333in"}

Fig. 2. Symptoms of late infection with an unnamed Australian
mastrevirus in a desi chickpea cultivar. (Courtesy M. W. Schwinghamer)

![](media/image24.jpeg){width="3.0in" height="1.2534722222222223in"}

![](media/image25.jpeg){width="3.0in" height="1.2333333333333334in"}

Fig. 3. Leafhoppers that are vectors of mastreviruses and phytoplasmas:
*Orosius albicinctus* (top), a vector of Chickpea chlorotic dwarf virus,
and *Orosius orientalis* (bottom), vector of *Tobacco yellow dwarf
virus* (TYDV), actual length 2.0 to 2.9 mm. (Courtesy M. J. Fletcher)

***Pea enation mosaic virus***

*Pea enation mosaic virus* (PEMV) is one of the most important and
destructive virus diseases of lentil in temperate zones of the world. It
has been reported in the Pacific Northwest states and California in the
U.S, Canada, Europe, West Asia, North Africa, Egypt, and Iran but is not
known to occur in New Zealand and Australia. Severe epidemics occurred
in the Pacific Northwest region in 1983, 1990, 1996 and 2005. The host
range of PEMV is primarily limited to members of the *Fabaceae*
including chickpea, lentil, pea (*Pisum sativum*), faba bean (*Vicia
faba*), common vetch (*Vicia sativa*), and crimson clover (*Trifolium
incarnatum*) although it can also be propagated on non-legume hosts such
as *Gomphrena globosa*, *Chenopodium* spp. and *Nicotiana* spp.

**Symptoms**

**Chickpea.** Chickpea plants infected with PEMV typically are severely
stunted showing twisted and malformed leaves (Fig. 1). Pods also are
misshapen, poorly filled and often show outgrowths that appear as bumps
on the surface (Fig. 2). Plants infected at an early growth stage may
die. Infected plants rarely yield seed of any quality.

**Lentil.** Infected lentil plants typically show a reduction in growth.
Plants infected at an early growth stage may die, especially if
co-infected with another virus such as *Bean leafroll virus*. Leaves
frequently exhibit leaf rolling and mottling, severely malformed leaves
and tip growth (Fig. 3), vein clearing and translucent flecks. Pods are
also malformed or misshapen. The most characteristic symptom of PEMV
infection is the development of enations (hyperplastic outgrowths) on
leaf and pod surfaces. While this is common in pea, it rarely occurs on
lentil or chickpea.

**Causal Agent**

The disease is caused by a symbiotic co-infection of two single-stranded
RNA viruses: PEMV-1 (genus *Enamovirus*, family *Luteoviridae*) and
PEMV-2 (genus *Umbravirus,* not assigned to a family). The monopartite
ssRNA genome of PEMV-1 is 5.7 kb, while that of PEMV-2 is 4.35 kb. A
third small RNA of 717 nucleotides has been identified as a satellite
RNA whose replication is controlled by PEMV-2. The genome of PEMV-1
contributes the encapsidating coat protein gene required for aphid
transmissibility and the PEMV-2 genome enables systemic movement in the
plant. The genomes are encapsidated separately in icosohedral virion
particles 25 and 28 nm in diameter with three structural proteins of 54
kDa, 21 kDa, and 17.5 kDa. The two particle types are transmitted
together, naturally by aphids or experimentally by mechanical
inoculation.

**Epidemiology**

PEMV is transmitted in a persistent manner by aphids, most commonly the
pea aphid (*Acythosyphon pisum*), cowpea aphid (*Aphis craccivora*),
green peach aphid (*Myzus persicae*), potato aphid (*Macrosiphum
euphorbiae*), and foxglove aphid (*Aulacorthum solani*). The pea aphid
can acquire the virus after a minimum of 15 min and transmit after a
latent period of 10-12 hr. Transmission is very efficient, as
susceptible hosts can become infected after a 1 min feeding period.
Transmission efficiency is enhanced with longer acquisition and
inoculation access periods. The virus is circulative in aphids but not
propagative and not tranmitted transovarially or parthenogenically. Only
one strain of the virus has been reported. PEMV is not transmitted by
seed in lentil or chickpea.

**Management**

No resistant varieties are known for chickpea or lentil although lentil
Plant Introduction (PI) accessions PI 472547 and PI 472609 have been
identified with tolerance to PEMV. Aphids can be controlled in lentils
by carefully timed applications of appropriate insecticides to reduce
colonization and resulting population build-up. Due to their transient
feeding behavior on chickpea plants, aphids are rarely seen on these
plants in the field even though infection may be widespread. Control of
aphids is best done by eliminating them in other nearby crops such as
pea or faba bean where unchecked, populations are subject to increase.
Although alfalfa is not a known host of PEMV, avoid planting lentils
near these fields, as alfalfa also is one of the primary host plants of
the pea aphid.

**Selected references**

Aydin, H., Muehlbauer, F. J., and Kaiser, W. J. 1987. *Pea enation
mosaic virus* resistance in lentil (*Lens culinaris*). Plant Dis. 71:
635-638.

Demler, S. A., and De Zoeten, G. A. 1989. Characterization of a
satellite RNA associated with *Pea enation mosaic virus*. J Gen Virol.
70:1075-1084.

Demler, S. A., and de Zoeten, G. A. 1991. The nucleotide sequence and
luteovirus-like nature of RNA1 of an aphid non-transmissible strain of
*Pea enation mosaic virus*. J. Gen. Virol. 72:1819-1834.

Demler, S. A., Rucker, D. G., and de Zoeten, G. A. 1993. The chimeric
nature of the genome of *Pea enation mosaic virus*: the independent
replication of RNA2. J. Gen. Virol. 74, 1-14.

Edwardson, J. R., and Christie, R. G.. 1986. Viruses infecting forage
legumes. Agricultural Experiment Station, Institute of Food and
Agricultural Sciences, University of Florida, Gainesville. 3 volumes,
742 pp.

Kaiser, W. J. 1987. Disease problems on dry peas, lentils, chickpea and
faba beans. Pages 157-174. In: Grain Legumes as Alternative Crops: A
Symposium. Centre for Alternative Crops and Products, University of
Minnesota.

Klein, R. E., Larsen, R. C., and Kaiser, W. J. 1991. Virus epidemic of
grain legumes in eastern Washington. Plant Dis. 75:1186.

Larsen, R. C., Kaiser, W. J., and Klein, R. E. 1996. Alfalfa, a non-host
of pea enation mosaic virus in Washington State. Can. J. Plant Sci. 76:
521-524

Makkouk, K. M., Kumari S. G., and Bayaa, B. 1999. First report of *Pea
enation mosaic virus* affecting lentil (*Lens culinaris* Medik.) in
Syria. Plant Dis. 83:303.

Makkouk, K. M., and Kumari, S. G. 2001. First record of *Pea enation
mosaic virus* naturally infecting chickpea and grasspea crops in Syria.
Plant Dis. 85:1032.

(Prepared by R. C. Larsen and M. W. Schwinghamer)

![](media/image26.jpeg){width="2.0in" height="1.3534722222222222in"}

**Fig. 1.** Prominent leaf malformation and mosaic caused by *Pea
enation mosaic virus* (PEMV) on chickpea. Healthy plant is on the left.
(Courtesy W. J. Kaiser)

![](media/image27.jpeg){width="2.0in" height="1.7798611111111111in"}

**Fig. 2.** Malformed seed pods from chickpea infected with *Pea enation
mosaic virus* (PEMV). Healthy pod is at upper left. (Courtesy W. J.
Kaiser)

![](media/image28.jpeg){width="1.5534722222222221in" height="2.0in"}

**Fig. 3.** Severe twisting and malformation of leaves stems and pods in
lentil infected with *Pea enation mosaic virus* (PEMV). (Courtesy W. J.
Kaiser)

***Pea seed-borne mosaic virus***

*Pea seed-borne mosaic virus* (PSbMV) was first identified in Europe in
1966 and then in Japan in 1967. It was subsequently discovered in the
U.S in 1969 and in New Zealand in 1980. PSbMV is now found throughout
the world. The virus naturally infects lentil, chickpea, pea, faba bean,
and other legumes, but is only a minor problem in chickpea. PSbMV
continues to be a highly significant disease in many pulse crops because
of potentially high rates of transmission by seed and the ease of
international dissemination of breeding lines and cultivars. Losses in
these crops can be severe under conditions of high infection levels.

**Symptoms**

**Chickpea.** Symptoms resemble those of other *Potyvirus* species
including BYMV. Severity varies with isolate and stage plants are
infected, but symptoms can include very narrow (filiform) leaflets
(Fig. 1) that may be twisted or turned down, indistinct mosaic,
mottling, or necrotic lesions on leaflets, necrosis of shoot tips,
stunting of plants, proliferation of stems, and abortion of podding.

**Lentil.** Symptoms may vary in lentil due to cultivar differences,
virus strain and environmental effects. Leaves are narrowed, reduced in
size with mosaic and mottling, and chlorosis or necrosis of shoot tips
may occur. A downward leafroll is common and plants are usually stunted
(Fig. 2). Seed pods may be abnormal in shape and size with reduced fewer
seed. Necrotic line patterns that are common on infected pea and faba
bean seed are rare on seed of lentil.

**Causal Agent**

PSbMV is a member of the family *Potyviridae*, Genus *Potyvirus* and
consists of flexuous rod-shaped particles with a modal length of ca. 770
nm containing a monopartite genome of single-stranded RNA. The genome
size is 9924 nucleotides and the coat protein has a molecular mass of 34
kDa. PSbMV has a distant serological relatedness to *Bean yellow mosaic
virus*. Four pathotypes designated P-1, P-2 (also called lentil strain),
P-3, and P-4 have been distinguished by susceptibilities of differential
lines of pea and differences in sequence in two coding regions of the
RNA. All isolates tested so far on lentil and chickpea, including
pathotypes P-1, P-2, and P-3 have been found to infect both hosts.

**Epidemiology**

The primary source of inoculum in lentil fields is infected seed. Once
present in the field, the mechanism of plant to plant spread is by
aphids which transmit the virus in a non-persistent manner. PSbMV is
also mechanically transmissible. Other significant pulse crops that may
serve as inoculum sources for the virus include pea, faba bean, and
vetch. At least 22 different aphid species are known to transmit PSbMV
but the pea aphid (*Acyrthosiphon pisum*)*,* cowpea aphid (*Aphis
craccivora*), green peach aphid (*Myzus persicae*), bean aphid (*Aphis
fabae*), and the foxglove aphid (*Aulacorthum solani*) are probably the
most common vectors. Seed transmission up to 44% has been reported in
lentil seed lots. Seed production is severely reduced in infected
lentil, with losses over 77% when plants are infected at the pre-flower
stage, and germination of infected seed can be reduced by nearly 50%.
Seed transmission in chickpea is generally less than 1% and secondary
spread is minor. A major contributing factor to the persistence of PSbMV
is the continuous use of contaminated seed collected at the end of a
season and then used in subsequent plantings.

**Management**

Because infected seed is the primary source of PSbMV, the use of
certified virus-free seed is the most effective method for control of
the virus. Chemical control of the aphid vector is generally ineffective
because of the transient nature and non-persistent manner by which the
virus is transmitted,. However, pesticide applications can reduce
secondary spread of the virus in lentil crops where large aphid vector
populations have become established. Avoid planting near established
fields where known infection sources may exist. No lentil cultivars have
been developed with complete resistance to PSbMV, although some plant
introduction (PI) accessions that include PI 212610, PI 251786, PI
207745, and PI 368648 have been identified that were immune to the
virus. The cultivars Crimson, Palouse and Red Chief, and Ill 6198 are
reported to be tolerant to PSbMV. Resistance to PSbMV in lentil is
controlled by a single recessive gene for which the symbol *sbv* has
been proposed. No chickpea cultivars have been developed with resistance
to PSbMV.

**Selected references**

Alconero, R., Provvidenti, R., and Gonsalves, D. 1986. Three pea
seedborne mosaic virus pathotypes from pea and lentil germ plasm. Plant
Dis. 70:783-786.

Haddad, N. I., Muehlbauer, F. J., and Hampton, R. O. 1978. Inheritance
of resistance to pea seed-borne mosaic virus in lentils. Crop Sci.
18:613-615.

Hampton, R. O. 1982. Incidence of the lentil strain of pea seedborne
mosaic virus as a contaminant of *Lens culinaris* germplasm.
Phytopathology. 72:695-698.

Hampton, R. O., and Muehlbauer, F. J. 1977. Seed transmission of the pea
seedborne mosaic virus in lentils. Plant Dis. Rep. 61:235-238.

Iqbal, S. M., Tahir, M. H. N., Asghar A., and Anjum, M. S. 2005.
Evaluation of lentil genotypes for resistance to *Pea seed-borne mosaic
virus*. Int. J. Agric. Res. Gov. Ecol. 7:148-149.

Johansen, E., Rasmussen, O. F., Heide, M., and Borkhardt, B. 1991. The
complete nucleotide sequence of *Pea seed-borne mosaic virus* RNA. J.
Gen. Virol. 72:2625-32.

Hjulsager, C. K., Lund, O. S., and Johansen, I. E. 2002. A new pathotype
of *Pea seedborne mosaic virus* explained by properties of the P3-6k1-
and viral genome-linked protein (VPg)-coding regions. Mol. Plant-Microbe
Interact.15:169-171.

Johansen, I. E., Keller, K. E., Dougherty, W. G., and Hampton, R. O.
1996. Biological and molecular properties of a pathotype P-1 and a
pathotype P-4 isolate of *Pea seed-borne mosaic virus*. J. Gen. Virol.
77:1329-1333.

Latham, L.J., and Jones, R. A. C.. 2001. Incidence of virus infection in
experimental plots, commercial crops and seed stocks of cool season crop
legumes. Aust. J. Agric. Res. 52: 397-41.

Makkouk, K. M., Kumari, S. G., and Bos, L. 1993. Pea seed-borne mosaic
virus: occurrence in faba bean (*Vicia faba*) and lentil (*Lens
culinaris*) in West Asia and North Africa, and further information on
host range, transmission characteristics, and purification. Eur. J.
Plant Pathol. 99:115-124.

Makkouk, K. M., Bashir, M., Jones, R. A. C., and Kumari, S. G. 2001.
Survey for viruses in lentil and chickpea crops in Pakistan. Z.
Pflanzenkr. Pflanzenschutz 108:258-268.

(Prepared by R. C. Larsen and M. W. Schwinghamer)

![](media/image29.jpeg){width="2.3333333333333335in"
height="1.8069444444444445in"}

Fig. 1. Filiform leaves (with small, narrow leaflets) in chickpea
infected with *Pea seed-borne mosaic virus* (PSbMV). (Courtesy M. W.
Schwinghamer).

![](media/image30.jpeg){width="2.0in" height="1.2798611111111111in"}

**Fig. 2.** Stunting and downward cupping of leaflets of lentil plant on
the right infected with *Pea seed-borne mosaic virus* (PSbMV). (Courtesy
W. J. Kaiser)

***Pea streak virus***

*Pea streak virus* (PeSV) was first reported causing a streak disease of
pea (*Pisum sativum* L.) in 1938 and 1940 in Virginia and Wisconsin,
respectively. It occurs in the Pacific Northwest region of the U.S.,
Canada, and Eurasia and New Zealand. The virus was first detected in
chickpea in the Palouse region of eastern Washington in 1979. PeSV has
since been involved in severe epidemics in 1983, 1990, 1996, and 2005 in
lentil and chickpea crops in the Pacific Northwest states. PeSV is also
known by several synonyms such as Alfalfa latent virus, Wisconsin pea
streak and pea streak New Zealand virus.

**Symptoms**

**Chickpea.** Typical symptoms in chickpea caused by PeSV include
yellowing of the foliage, stunting, necrosis of leaflets, wilting of
terminal shoots and phloem discoloration (Fig. 1). Infected seedlings
wilt and die prior to pod formation, and seed in infected mature plants
are small, discolored and misshapened. Wilted chickpea plants infected
with PeSV resemble symptoms caused by common root rotting fungi (Fig.
2). PeSV has not been reported to be seed transmitted, but germination
is poor with seed collected from infected plants.

**Lentil.** Infection in lentil results in wilting of the terminal
shoots. Vascular discoloration may be observed, a condition that
contributes to plant death, especially at the seedling stage. Infected
plants exhibit stunting, yellowing of leaflets, and wilting. Pods that
do form usually are poorly filled, seed shape is misshapen, and yield
losses can be significant.

**Causal Agent**

PeSV is a member of genus *Carlavirus* in the family *Flexiviridae*
consisting of flexuous rod-shaped particles 630 nm in length. The
monopartite viral genome consists of single-stranded RNA of
approximately 8100 nucleotides. The 294 amino acid coat protein has a
predicted molecular size of 33 kDa although the size estimate on
polyacrylamide gels is 28 kDa. The genome is comprised of five open
reading frames compared to all other known carlaviruses which have six.
PeSV is serologically indistinguishable from Alfalfa latent virus
although it has long been contended to be a distinct virus. A coat
protein amino acid comparison of the two viruses resulted in 95%
identity which strongly suggests that Alfalfa latent virus is only a
strain of PeSV.

**Epidemiology**

PeSV is transmitted in North America primarily by the pea aphid
(*Acyrthosiphon pisum*) in a non-persistent manner and transmission is
inefficient, at least under experimental conditions. In experiments
conducted on pea (*Pisum sativum*), only about 3% of test plants became
infected after a 24 hr acquisition feeding period and a 24 hr
inoculation period. The virus is easily transmitted mechanically to
other legume hosts including faba bean (*Vicia faba*), and fenugreek
(*Trigonella foenum-graecum*). It is symptomless in alfalfa (*Medicago
sativum*), the most important reservoir host from which the pea aphid
acquires the virus in the spring and transmits it to lentil and chickpea
crops. PeSV is less prevalent and more sporadic in chickpea fields
because of the transient behavior of aphids on that host. Consistent
with other carlaviruses, PeSV is not seed or pollen transmitted.

**Management**

No known resistance to PeSV is available in current chickpea varieties.
Management options include avoiding proximity to crops such as pea, faba
bean and alfalfa which are hosts for both the virus and aphids. As with
other viruses transmitted in a non-persistent manner, control of the
virus by insecticide application is not effective.

**Selected references**

Hagedorn, D. J., and Walker, J. C. 1949. Wisconsin pea streak.
Phytopathology, 39:837--847.

Hampton, R. O. 1983. Pea streak virus. In: Brunt, A.A., Crabtree, K.,
Dallwitz, M.J., Gibbs, A.J., Watson, L. and Zurcher, E.J. (eds.) (1996
onwards). \`Plant Viruses Online: Descriptions and Lists from the VIDE
Database. Version: 20th August 1996.

Kaiser, W. J., Klein, R. E., Larsen, R. C., and Wyatt, S. D. 1993.
Chickpea wilt incited by pea streak carlavirus. Plant Dis. 77:922-926.

Kaiser, W. J. 1987. Disease problems on dry peas, lentils, chickpea and
faba beans. Pages 157-174. In: Grain Legumes as Alternative Crops: A
Symposium. Centre for Alternative Crops and Products, University of
Minnesota, USA.

Virus Taxonomy. Classification and Nomenclature of Viruses. Eighth
Report of the International Committee on the Taxonomy of Viruses. C. M.
Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger, and L. A. Ball, eds.
Elsevier Academic Press, San Diego, CA.

(Prepared by R. C. Larsen)

![](media/image31.jpeg){width="2.1645833333333333in"
height="1.8131944444444446in"}

Fig 1. Foliar wilt symptoms on chickpea caused by *Pea streak virus*
(PeSV). (Courtesy R. C. Larsen)

![](media/image32.jpeg){width="2.1277777777777778in"
height="1.8111111111111111in"}

Fig 2. Advanced symptoms in chickpea infected with *Pea streak virus*
(PeSV). (Courtesy R. C. Larsen)

**At A Glance: Viruses reported to infect chickpea and/or lentil
naturally\***

+----------+----------+---+--------+----+-----------------+---+----+
| Virus    | Virus    | A | Sy     | C  | Reference       | T | C  |
| family   | spe      | c | nonyms | ou |                 | r | ro |
| or other | cies\*\* | r | a      | nt |                 | a | ss |
| group/   |          | o | pplied | ry |                 | n | r  |
| genus    |          | n | to     |    |                 | s | ea |
|          |          | y | ch     |    |                 | m | ct |
|          |          | m | ickpea |    |                 | i | io |
|          |          |   | and    |    |                 | s | ns |
|          |          |   | lentil |    |                 | s | \* |
|          |          |   |        |    |                 | i | \* |
|          |          |   |        |    |                 | o | \* |
|          |          |   |        |    |                 | n |    |
+----------+----------+---+--------+----+-----------------+---+----+
| **Family |          |   |        |    |                 |   |    |
| *        |          |   |        |    |                 |   |    |
| Bromovir |          |   |        |    |                 |   |    |
| idae/*** |          |   |        |    |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
| *Alfa    | *Alfalfa | A |        | A  | Jones and       | A | Nr |
| movirus* | mosaic   | M |        | us | Coutts 1996     | p |    |
|          | virus*   | V |        | tr |                 | h |    |
|          |          |   |        | al | Bekele et al.   | i |    |
|          |          |   |        | ia | 2005            | d |    |
|          |          |   |        |    |                 | s |    |
|          |          |   |        | Et | Makkouk et al.  | , |    |
|          |          |   |        | hi | 2001            | s |    |
|          |          |   |        | op |                 | e |    |
|          |          |   |        | ia | Kaiser and      | e |    |
|          |          |   |        |    | Danesh 1971;    | d |    |
|          |          |   |        | I  | Makkouk et al.  |   |    |
|          |          |   |        | nd | 2003b           |   |    |
|          |          |   |        | ia |                 |   |    |
|          |          |   |        |    | Al-Mabrouk and  |   |    |
|          |          |   |        | Ir | Mansour. 2000   |   |    |
|          |          |   |        | an |                 |   |    |
|          |          |   |        |    | Fletcher 1993   |   |    |
|          |          |   |        | Jo |                 |   |    |
|          |          |   |        | rd | Makkouk et al.  |   |    |
|          |          |   |        | an | 2001            |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | N  | Mouhanna et al  |   |    |
|          |          |   |        | ew | 1994            |   |    |
|          |          |   |        | Z  |                 |   |    |
|          |          |   |        | ea | Bosque-Perez    |   |    |
|          |          |   |        | la | and Buddenhagen |   |    |
|          |          |   |        | nd | 1990, Kaiser    |   |    |
|          |          |   |        |    | 1981            |   |    |
|          |          |   |        | Pa |                 |   |    |
|          |          |   |        | ki |                 |   |    |
|          |          |   |        | st |                 |   |    |
|          |          |   |        | an |                 |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | S  |                 |   |    |
|          |          |   |        | yr |                 |   |    |
|          |          |   |        | ia |                 |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | U  |                 |   |    |
|          |          |   |        | SA |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
| *Bro     | *Broad   | B |        | Et | Bekele et al.   | B | Nr |
| movirus* | bean     | B |        | hi | 2005            | e |    |
|          | mottle   | M |        | op |                 | e |    |
|          | virus*   | V |        | ia | Fortass and     | t |    |
|          |          |   |        |    | Diallo 1993     | l |    |
|          |          |   |        | M  |                 | e |    |
|          |          |   |        | or |                 | s |    |
|          |          |   |        | oc |                 | , |    |
|          |          |   |        | co |                 | \ |    |
|          |          |   |        |    |                 | s |    |
|          |          |   |        |    |                 | e |    |
|          |          |   |        |    |                 | e |    |
|          |          |   |        |    |                 | d |    |
+----------+----------+---+--------+----+-----------------+---+----+
| *Cucu    | *        | C | Ch     | A  | Jones and       | A | Nr |
| movirus* | Cucumber | M | ickpea | us | Coutts 1996     | p |    |
|          | mosaic   | V | leaf   | tr |                 | h |    |
|          | virus*   |   | red    | al | Tadesse et al.  | i |    |
|          |          |   | uction | ia | 1999            | d |    |
|          |          |   | virus  |    |                 | s |    |
|          |          |   |        | Et | Dhingra et al   | , |    |
|          |          |   |        | hi | 1979; Chalam et | s |    |
|          |          |   |        | op | al. 1986\       | e |    |
|          |          |   |        | ia | Rangaraju and   | e |    |
|          |          |   |        |    | Chenulu 1981    | d |    |
|          |          |   |        | I  |                 |   |    |
|          |          |   |        | nd | Kaiser and      |   |    |
|          |          |   |        | ia | Danesh 1971;    |   |    |
|          |          |   |        |    | Makkouk et al.  |   |    |
|          |          |   |        | Ir | 2003b;          |   |    |
|          |          |   |        | an |                 |   |    |
|          |          |   |        |    | Kaiser 1973\    |   |    |
|          |          |   |        | M  | El Maataoui and |   |    |
|          |          |   |        | or | Ameziane-El     |   |    |
|          |          |   |        | oc | Hassani 1984    |   |    |
|          |          |   |        | co |                 |   |    |
|          |          |   |        |    | Fletcher 1993\  |   |    |
|          |          |   |        | N  | Bashir and      |   |    |
|          |          |   |        | ew | Malik 1993;     |   |    |
|          |          |   |        | Z  | Bahsir et al.   |   |    |
|          |          |   |        | ea | 1994;\          |   |    |
|          |          |   |        | la | Makkouk et al.  |   |    |
|          |          |   |        | nd | 2001            |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | Pa | Carazo et al.   |   |    |
|          |          |   |        | ki | 1993            |   |    |
|          |          |   |        | st |                 |   |    |
|          |          |   |        | an | Mouhanna et al  |   |    |
|          |          |   |        |    | 1994            |   |    |
|          |          |   |        | S  |                 |   |    |
|          |          |   |        | pa | Bosque-Perez    |   |    |
|          |          |   |        | in | and Buddenhagen |   |    |
|          |          |   |        |    | 1990            |   |    |
|          |          |   |        | S  |                 |   |    |
|          |          |   |        | yr |                 |   |    |
|          |          |   |        | ia |                 |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | U  |                 |   |    |
|          |          |   |        | SA |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
| *Il      | *Tobacco | T |        | A  | Sharman et al.  | T | Nr |
| arvirus* | streak   | S |        | us | (unpublished)   | h |    |
|          | virus*   | V |        | tr |                 | r |    |
|          |          |   |        | al | Kaiser et al.   | i |    |
|          |          |   |        | ia | 1991            | p |    |
|          |          |   |        |    |                 | s |    |
|          |          |   |        | U  |                 | , |    |
|          |          |   |        | SA |                 | p |    |
|          |          |   |        |    |                 | o |    |
|          |          |   |        |    |                 | l |    |
|          |          |   |        |    |                 | l |    |
|          |          |   |        |    |                 | e |    |
|          |          |   |        |    |                 | n |    |
|          |          |   |        |    |                 | , |    |
|          |          |   |        |    |                 | s |    |
|          |          |   |        |    |                 | e |    |
|          |          |   |        |    |                 | e |    |
|          |          |   |        |    |                 | d |    |
+----------+----------+---+--------+----+-----------------+---+----+
| **Family |          |   |        |    |                 |   |    |
| *        |          |   |        |    |                 |   |    |
| Bunyavir |          |   |        |    |                 |   |    |
| idae/*** |          |   |        |    |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
| *Tos     | *Tomato  | T |        | A  | Thomas et al.   | T | Nr |
| povirus* | spotted  | S |        | us | 2004            | h |    |
|          | wilt     | W |        | tr |                 | r |    |
|          | virus*   | V |        | al | Boiteux et al.  | i |    |
|          |          |   |        | ia | 1995            | p |    |
|          |          |   |        |    |                 | s |    |
|          |          |   |        | Br |                 |   |    |
|          |          |   |        | az |                 |   |    |
|          |          |   |        | il |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
| **Family |          |   |        |    |                 |   |    |
| *Comovir |          |   |        |    |                 |   |    |
| idae/*** |          |   |        |    |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
| *Co      | *Broad   | B |        | Et | Tadesse et al   | W | Nr |
| movirus* | bean     | B |        | hi | 1999            | e |    |
|          | stain    | S |        | op |                 | e |    |
|          | virus*   | V |        | ia | Bos et al. 1988 | v |    |
|          |          |   |        |    |                 | i |    |
|          |          |   |        | Eu | Makkouk et al.  | l |    |
|          |          |   |        | ro | 2003b           | s |    |
|          |          |   |        | pe |                 | , |    |
|          |          |   |        |    | Al-Mabrouk and  | s |    |
|          |          |   |        | Ir | Mansour 2000    | e |    |
|          |          |   |        | an |                 | e |    |
|          |          |   |        |    | Bashir et al.   | d |    |
|          |          |   |        | Jo | 2005            |   |    |
|          |          |   |        | rd |                 |   |    |
|          |          |   |        | an | Mouhanna et al. |   |    |
|          |          |   |        |    | 1994            |   |    |
|          |          |   |        | Pa |                 |   |    |
|          |          |   |        | ki | Bayaa et a.     |   |    |
|          |          |   |        | st | 1998            |   |    |
|          |          |   |        | an |                 |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | S  |                 |   |    |
|          |          |   |        | yr |                 |   |    |
|          |          |   |        | ia |                 |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | Tu |                 |   |    |
|          |          |   |        | rk |                 |   |    |
|          |          |   |        | ey |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
| *Fa      | Broad    | B | *Broad | Et | Tadesse et al.  | A | Nr |
| bavirus* | bean     | B | bean   | hi | 1999            | p |    |
|          | wilt     | W | wilt   | op |                 | h |    |
|          | virus    | V | virus  | ia | Makkouk et al.  | i |    |
|          |          |   | 1*     |    | 1992            | d |    |
|          |          |   |        | S  |                 | s |    |
|          |          |   | *Broad | yr |                 |   |    |
|          |          |   | bean   | ia |                 |   |    |
|          |          |   | wilt   |    |                 |   |    |
|          |          |   | virus  |    |                 |   |    |
|          |          |   | 2*     |    |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
| *Ne      | *Tobacco | T |        | I  | Dhingra 1981    | U | Nr |
| povirus* | ringspot | R |        | nd |                 | n |    |
|          | virus*   | S |        | ia |                 | k |    |
|          |          | V |        |    |                 | n |    |
|          |          |   |        |    |                 | o |    |
|          |          |   |        |    |                 | w |    |
|          |          |   |        |    |                 | n |    |
+----------+----------+---+--------+----+-----------------+---+----+
| **Family |          |   |        |    |                 |   |    |
| *        |          |   |        |    |                 |   |    |
| Flexivir |          |   |        |    |                 |   |    |
| idae/*** |          |   |        |    |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
| *Car     | *Pea     | P |        | U  | Kaiser et al.   | A | Nr |
| lavirus* | streak   | e |        | SA | 1993            | p |    |
|          | virus*   | S |        |    |                 | h |    |
|          |          | V |        |    |                 | i |    |
|          |          |   |        |    |                 | d |    |
|          |          |   |        |    |                 | s |    |
+----------+----------+---+--------+----+-----------------+---+----+
|          | *Red     | R |        | U  | Larsen et al.   | A | Nr |
|          | clover   | C |        | SA | 1996            | p |    |
|          | vein     | V |        |    |                 | h |    |
|          | mosaic   | M |        |    |                 | i |    |
|          | virus*   | V |        |    |                 | d |    |
|          |          |   |        |    |                 | s |    |
+----------+----------+---+--------+----+-----------------+---+----+
| **Family |          |   |        |    |                 |   |    |
| *G       |          |   |        |    |                 |   |    |
| eminivir |          |   |        |    |                 |   |    |
| idae/*** |          |   |        |    |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
| *Mast    | *Bean    | B |        | Pa | Nahid et al.    | L | T  |
| revirus* | yellow   | e |        | ki | 2008            | e | YD |
|          | dwarf    | Y |        | st |                 | a | V, |
|          | virus*   | D |        | an |                 | f | C  |
|          |          | V |        |    |                 | - | pC |
|          |          |   |        |    |                 | h | DV |
|          |          |   |        |    |                 | o |    |
|          |          |   |        |    |                 | p |    |
|          |          |   |        |    |                 | p |    |
|          |          |   |        |    |                 | e |    |
|          |          |   |        |    |                 | r |    |
|          |          |   |        |    |                 | s |    |
|          |          |   |        |    |                 | ? |    |
+----------+----------+---+--------+----+-----------------+---+----+
|          | Chickpea | C | Ch     | I  | Horn et al.     | L | TY |
|          | c        | p | ickpea | nd | 1993            | e | DV |
|          | hlorotic | C | chl    | ia |                 | a |    |
|          | dwarf    | D | orotic |    | Makkouk et al.  | f |    |
|          | virus    | V | dwarf  | Ir | 2003b           | - |    |
|          |          |   | Sudan  | an |                 | h |    |
|          |          |   | virus  |    | El-Muadhidi et  | o |    |
|          |          |   |        | Ir | al. 2001        | p |    |
|          |          |   | Ch     | aq |                 | p |    |
|          |          |   | ickpea |    | Horn et al.     | e |    |
|          |          |   | chl    | Pa | 1996; Nahid et  | r |    |
|          |          |   | orotic | ki | al. 2008        | s |    |
|          |          |   | dwarf  | st |                 |   |    |
|          |          |   | Pa     | an | Hamed and       |   |    |
|          |          |   | kistan |    | Makkouk 2002    |   |    |
|          |          |   | virus  | S  |                 |   |    |
|          |          |   |        | ud | Kumari et al.   |   |    |
|          |          |   |        | an | 2004            |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | S  |                 |   |    |
|          |          |   |        | yr |                 |   |    |
|          |          |   |        | ia |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
|          | *Mast    |   |        | A  | Thomas et al.   | L | Cp |
|          | revirus* |   |        | us | (unpublished)   | e | CD |
|          | spp.\    |   |        | tr |                 | a | V, |
|          | (four    |   |        | al |                 | f | TY |
|          | distinct |   |        | ia |                 | - | DV |
|          | unnamed  |   |        |    |                 | h |    |
|          | species) |   |        |    |                 | o |    |
|          |          |   |        |    |                 | p |    |
|          |          |   |        |    |                 | p |    |
|          |          |   |        |    |                 | e |    |
|          |          |   |        |    |                 | r |    |
|          |          |   |        |    |                 | s |    |
|          |          |   |        |    |                 | ? |    |
+----------+----------+---+--------+----+-----------------+---+----+
|          | *Tobacco | T | Bean   | A  | Thomas et       | L | C  |
|          | yellow   | Y | summer | us | a               | e | pC |
|          | dwarf    | D | death  | tr | l.(unpublished) | a | DV |
|          | virus*   | V | virus  | al |                 | f |    |
|          |          |   |        | ia |                 | - |    |
|          |          |   |        |    |                 | h |    |
|          |          |   |        |    |                 | o |    |
|          |          |   |        |    |                 | p |    |
|          |          |   |        |    |                 | p |    |
|          |          |   |        |    |                 | e |    |
|          |          |   |        |    |                 | r |    |
|          |          |   |        |    |                 | s |    |
+----------+----------+---+--------+----+-----------------+---+----+
| **Family |          |   |        |    |                 |   |    |
| *Luteo   |          |   |        |    |                 |   |    |
| viridae* |          |   |        |    |                 |   |    |
| (        |          |   |        |    |                 |   |    |
| luteovir |          |   |        |    |                 |   |    |
| uses)/** |          |   |        |    |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
| *Lut     | *Bean    | B | Pea    | A  | Schwinghamer et | A | Nr |
| eovirus* | leafroll | L | le     | us | al. 1999        | p |    |
|          | virus*   | R | afroll | tr |                 | h |    |
|          |          | V | virus  | al | Bakr 1993       | i |    |
|          |          |   |        | ia |                 | d |    |
|          |          |   | Legume |    | Tadesse et al.  | s |    |
|          |          |   | y      | Ba | 1999            |   |    |
|          |          |   | ellows | ng |                 |   |    |
|          |          |   | virus  | la | Kaiser and      |   |    |
|          |          |   |        | de | Danesh 1971;    |   |    |
|          |          |   |        | sh | Makkouk et al.  |   |    |
|          |          |   |        |    | 2003b           |   |    |
|          |          |   |        | Et |                 |   |    |
|          |          |   |        | hi | El-Muadhidi et  |   |    |
|          |          |   |        | op | al. 2001        |   |    |
|          |          |   |        | ia |                 |   |    |
|          |          |   |        |    | Horn et al.     |   |    |
|          |          |   |        | Ir | 1996            |   |    |
|          |          |   |        | an |                 |   |    |
|          |          |   |        |    | Carazo et al.   |   |    |
|          |          |   |        | I  | 1993            |   |    |
|          |          |   |        | nd |                 |   |    |
|          |          |   |        | ia | Kumari et al.   |   |    |
|          |          |   |        |    | 2004            |   |    |
|          |          |   |        | Pa |                 |   |    |
|          |          |   |        | ki | Horn and Van    |   |    |
|          |          |   |        | st | den Heuvel 1994 |   |    |
|          |          |   |        | an |                 |   |    |
|          |          |   |        |    | Duffus 1979;    |   |    |
|          |          |   |        | S  | Bosque-Perez    |   |    |
|          |          |   |        | pa | and Buddenhagen |   |    |
|          |          |   |        | in | 1990            |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | S  |                 |   |    |
|          |          |   |        | yr |                 |   |    |
|          |          |   |        | ia |                 |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | Tu |                 |   |    |
|          |          |   |        | rk |                 |   |    |
|          |          |   |        | ey |                 |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | U  |                 |   |    |
|          |          |   |        | SA |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
| *Lut     | *Soybean | S | Subter | A  | Schwinghamer et | A | B  |
| eovirus* | dwarf    | b | ranean | us | al. 1999        | p | LR |
|          | virus*   | D | clover | tr |                 | h | V, |
|          |          | V | red    | al | Tadesse et      | i | BW |
|          |          |   | leaf   | ia | al.1999         | d | YV |
|          |          |   | virus  |    |                 | s |    |
|          |          |   |        | Et | Makkouk et al.  |   |    |
|          |          |   |        | hi | 2003b           |   |    |
|          |          |   |        | op |                 |   |    |
|          |          |   |        | ia | Fletcher 1993   |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | Ir | Makkouk et al.  |   |    |
|          |          |   |        | an | 1997            |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | N  | Bosque-Perez    |   |    |
|          |          |   |        | ew | and Buddenhagen |   |    |
|          |          |   |        | Z  | 1990            |   |    |
|          |          |   |        | ea |                 |   |    |
|          |          |   |        | la |                 |   |    |
|          |          |   |        | nd |                 |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | S  |                 |   |    |
|          |          |   |        | yr |                 |   |    |
|          |          |   |        | ia |                 |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | U  |                 |   |    |
|          |          |   |        | SA |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
| *Pole    |          |   |        |    |                 |   |    |
| rovirus\ |          |   |        |    |                 |   |    |
| *(i      |          |   |        |    |                 |   |    |
| ncluding |          |   |        |    |                 |   |    |
| likely   |          |   |        |    |                 |   |    |
| polero   |          |   |        |    |                 |   |    |
| viruses) |          |   |        |    |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
|          | A24      |   | Ch     | I  | Reddy and Kumar | A | BW |
|          | isolate  |   | ickpea | nd | 2004            | p | YV |
|          |          |   | stunt  | ia |                 | h |    |
|          |          |   | d      |    |                 | i |    |
|          |          |   | isease |    |                 | d |    |
|          |          |   | asso   |    |                 | s |    |
|          |          |   | ciated |    |                 |   |    |
|          |          |   | virus? |    |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
| *Pole    | Beet     | B | In     | A  | Schwinghamer et | A | BL |
| rovirus* | western  | W | cludes | us | al. 2003        | p | RV |
|          | yellows  | Y |        | tr |                 | h |    |
|          | virus    | V | *      | al | Tadesse et al.  | i |    |
|          |          |   | Turnip | ia | 1999            | d |    |
|          | (one to  |   | y      |    |                 | s |    |
|          | four     |   | ellows | Et | Makkouk et al.  |   |    |
|          | serol    |   | virus* | hi | 2003b           |   |    |
|          | ogically |   |        | op |                 |   |    |
|          | related  |   | May    | ia | Fortass et al.  |   |    |
|          | species, |   | also   |    | 1997            |   |    |
|          | not      |   | in     | Ir |                 |   |    |
|          | distin   |   | clude: | an | Fletcher 1993   |   |    |
|          | guished) |   |        |    |                 |   |    |
|          |          |   | *Beet  | M  | Makkouk et al.  |   |    |
|          |          |   | chl    | or | 2001            |   |    |
|          |          |   | orosis | oc |                 |   |    |
|          |          |   | virus* | co | Carazo et al.   |   |    |
|          |          |   |        |    | 1993            |   |    |
|          |          |   | *Beet  | N  |                 |   |    |
|          |          |   | mild   | ew | Hamed and       |   |    |
|          |          |   | yel    | Z  | Makkouk 2002    |   |    |
|          |          |   | lowing | ea |                 |   |    |
|          |          |   | virus* | la | Kumari et al.   |   |    |
|          |          |   |        | nd | 2004; Makkouk   |   |    |
|          |          |   | *Beet  |    | et al. 1992     |   |    |
|          |          |   | w      | Pa |                 |   |    |
|          |          |   | estern | ki | Horn et al.     |   |    |
|          |          |   | y      | st | 1995; Bayaa et  |   |    |
|          |          |   | ellows | an | al. 1998        |   |    |
|          |          |   | virus* |    |                 |   |    |
|          |          |   |        | S  | Duffus 1979 ;   |   |    |
|          |          |   |        | pa | Bosque-Perez    |   |    |
|          |          |   |        | in | and Buddenhagen |   |    |
|          |          |   |        |    | 1990            |   |    |
|          |          |   |        | S  |                 |   |    |
|          |          |   |        | ud |                 |   |    |
|          |          |   |        | an |                 |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | S  |                 |   |    |
|          |          |   |        | yr |                 |   |    |
|          |          |   |        | ia |                 |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | Tu |                 |   |    |
|          |          |   |        | rk |                 |   |    |
|          |          |   |        | ey |                 |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | U  |                 |   |    |
|          |          |   |        | SA |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
|          | Chickpea | C |        | Et | Abraham et al.  | A | BW |
|          | c        | p |        | hi | 2006            | p | YV |
|          | hlorotic | C |        | op |                 | h |    |
|          | stunt    | S |        | ia | Kumari et al.   | i |    |
|          | virus    | V |        |    | 2007            | d |    |
|          |          |   |        | S  |                 | s |    |
|          |          |   |        | yr |                 |   |    |
|          |          |   |        | ia |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
| *s*      | Chickpea | C |        | I  | Horn et al.     | A | Nr |
|          | lu       | p |        | nd | 1996            | p |    |
|          | teovirus | L |        | ia |                 | h |    |
|          |          | V |        |    | Horn et al.     | i |    |
|          |          |   |        | Pa | 1996            | d |    |
|          |          |   |        | ki |                 | s |    |
|          |          |   |        | st | Horn et al.     | ? |    |
|          |          |   |        | an | 1995            |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | S  | Horn et al.     |   |    |
|          |          |   |        | yr | 1995            |   |    |
|          |          |   |        | ia |                 |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | Tu |                 |   |    |
|          |          |   |        | rk |                 |   |    |
|          |          |   |        | ey |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
|          | *        | C | A24    | I  | Naidu et al.    | A | BW |
|          | Chickpea | p | is     | nd | 1997            | p | YV |
|          | stunt    | S | olate? | ia |                 | h |    |
|          | di       | D |        |    |                 | i | Cp |
|          | sease-as | a |        |    |                 | d | LV |
|          | sociated | V |        |    |                 | s |    |
|          | virus*   |   |        |    |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
|          | *        | C |        | Pa | Makkouk et al.  | A | Nr |
|          | Cucurbit | A |        | ki | 2001            | p |    |
|          | aph      | B |        | st |                 | h |    |
|          | id-borne | Y |        | an |                 | i |    |
|          | yellows  | V |        |    |                 | d |    |
|          | virus*   |   |        |    |                 | s |    |
+----------+----------+---+--------+----+-----------------+---+----+
|          | Lentil   | L |        | Et | Abraham et al.  | A | Nr |
|          | stunt    | S |        | hi | 2008            | p |    |
|          | virus    | t |        | op |                 | h |    |
|          |          | V |        | ia |                 | i |    |
|          |          |   |        |    |                 | d |    |
|          |          |   |        |    |                 | s |    |
+----------+----------+---+--------+----+-----------------+---+----+
|          | *Potato  | P |        | I  | Horn and Van    | A | Nr |
|          | leafroll | L |        | nd | den Heuvel 1994 | p |    |
|          | virus*   | R |        | ia |                 | h |    |
|          |          | V |        |    | El-Muadhidi et  | i |    |
|          |          |   |        | Ir | al. 2001        | d |    |
|          |          |   |        | aq |                 | s |    |
|          |          |   |        |    | Makkouk et al.  |   |    |
|          |          |   |        | S  | 1992            |   |    |
|          |          |   |        | yr |                 |   |    |
|          |          |   |        | ia |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
| Un       | Chickpea | C |        | S  | Abraham et al.  | A | Nr |
| assigned | yellows  | h |        | ud | 2008            | p |    |
|          | virus    | Y |        | an |                 | h |    |
|          |          | V |        |    |                 | i |    |
|          |          |   |        |    |                 | d |    |
|          |          |   |        |    |                 | s |    |
+----------+----------+---+--------+----+-----------------+---+----+
| **Family |          |   |        |    |                 |   |    |
| *Nanovi  |          |   |        |    |                 |   |    |
| ridae*** |          |   |        |    |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
| *Na      | *Faba    | F |        | Et | Tadesse et al.  | A | Nr |
| novirus* | bean     | B |        | hi | 1999 ; Bekele   | p |    |
|          | necrotic | N |        | op | et al. 2005     | h |    |
|          | yellows* | Y |        | ia |                 | i |    |
|          |          | V |        |    | Makkouk et al.  | d |    |
|          |          |   |        | I  | 2003b\          | s |    |
|          |          |   |        | ra | Al-Nsour et al. |   |    |
|          |          |   |        | n\ | 1998\           |   |    |
|          |          |   |        | J  | Horn et al.     |   |    |
|          |          |   |        | or | 1995\           |   |    |
|          |          |   |        | da | Makkouk et al.  |   |    |
|          |          |   |        | n\ | 2001            |   |    |
|          |          |   |        | Le |                 |   |    |
|          |          |   |        | ba | Ortiz et al.    |   |    |
|          |          |   |        | no | 2006\           |   |    |
|          |          |   |        | n\ | Makkouk et al.  |   |    |
|          |          |   |        | Pa | 2003a           |   |    |
|          |          |   |        | ki |                 |   |    |
|          |          |   |        | st | Kumari et a.    |   |    |
|          |          |   |        | an | 2004\           |   |    |
|          |          |   |        |    | Horn et al.     |   |    |
|          |          |   |        | Sp | 1995            |   |    |
|          |          |   |        | ai |                 |   |    |
|          |          |   |        | n\ |                 |   |    |
|          |          |   |        | S  |                 |   |    |
|          |          |   |        | ud |                 |   |    |
|          |          |   |        | an |                 |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | Sy |                 |   |    |
|          |          |   |        | ri |                 |   |    |
|          |          |   |        | a\ |                 |   |    |
|          |          |   |        | Tu |                 |   |    |
|          |          |   |        | rk |                 |   |    |
|          |          |   |        | ey |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
| **Family |          |   |        |    |                 |   |    |
| *Potyvir |          |   |        |    |                 |   |    |
| idae/*** |          |   |        |    |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
| *Po      | *Bean    | B |        | A  | Jones and       | A | Nr |
| tyvirus* | yellow   | Y |        | us | Coutts 1996;    | p |    |
|          | mosaic   | M |        | tr | McKirdy et al.  | h |    |
|          | virus*   | V |        | al | 2000            | i |    |
|          |          |   |        | ia |                 | d |    |
|          |          |   |        |    | Bakr 1993       | s |    |
|          |          |   |        | Ba |                 |   |    |
|          |          |   |        | ng | Russo et al.    |   |    |
|          |          |   |        | la | 1981            |   |    |
|          |          |   |        | de |                 |   |    |
|          |          |   |        | sh | Tadese et al.   |   |    |
|          |          |   |        |    | 1999; Bekele et |   |    |
|          |          |   |        | E  | al. 2005        |   |    |
|          |          |   |        | gy |                 |   |    |
|          |          |   |        | pt | Chalam et al.   |   |    |
|          |          |   |        |    | 1985            |   |    |
|          |          |   |        | Et |                 |   |    |
|          |          |   |        | hi | Kaiser and      |   |    |
|          |          |   |        | op | Danesh 1971;    |   |    |
|          |          |   |        | ia | Makkouk et al.  |   |    |
|          |          |   |        |    | 2003b           |   |    |
|          |          |   |        | I  |                 |   |    |
|          |          |   |        | nd | El-Muadhidi et  |   |    |
|          |          |   |        | ia | al. 2001        |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | Ir | Al-Mabrouk and  |   |    |
|          |          |   |        | an | Mansour 2000    |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | Ir | Fletcher 1993   |   |    |
|          |          |   |        | aq |                 |   |    |
|          |          |   |        |    | Makkouk et al.  |   |    |
|          |          |   |        | Jo | 1992            |   |    |
|          |          |   |        | rd |                 |   |    |
|          |          |   |        | an | Bayaa et al     |   |    |
|          |          |   |        |    | 1998            |   |    |
|          |          |   |        | N  |                 |   |    |
|          |          |   |        | ew |                 |   |    |
|          |          |   |        | Z  |                 |   |    |
|          |          |   |        | ea |                 |   |    |
|          |          |   |        | la |                 |   |    |
|          |          |   |        | nd |                 |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | S  |                 |   |    |
|          |          |   |        | yr |                 |   |    |
|          |          |   |        | ia |                 |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | Tu |                 |   |    |
|          |          |   |        | rk |                 |   |    |
|          |          |   |        | ey |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
|          | Chickpea | C |        | I  | Anjaiah et al.  | A | A  |
|          | bushy    | p |        | nd | 1989            | p | BM |
|          | dwarf    | B |        | ia |                 | h | V, |
|          | virus    | D |        |    |                 | i | Pe |
|          |          | V |        |    |                 | d | Mo |
|          |          |   |        |    |                 | s | V, |
|          |          |   |        |    |                 | ? | S  |
|          |          |   |        |    |                 |   | MV |
+----------+----------+---+--------+----+-----------------+---+----+
|          | Chickpea | C |        | I  | Mali et al.     | A | B  |
|          | di       | p |        | nd | 1988            | p | YM |
|          | stortion | D |        | ia |                 | h | V, |
|          | mosaic   | M |        |    |                 | i | B  |
|          |          | V |        |    |                 | d | CM |
|          |          |   |        |    |                 | s | V, |
|          |          |   |        |    |                 |   | a  |
|          |          |   |        |    |                 |   | nd |
|          |          |   |        |    |                 |   | fo |
|          |          |   |        |    |                 |   | ur |
|          |          |   |        |    |                 |   | o  |
|          |          |   |        |    |                 |   | th |
|          |          |   |        |    |                 |   | er |
|          |          |   |        |    |                 |   | p  |
|          |          |   |        |    |                 |   | ot |
|          |          |   |        |    |                 |   | yv |
|          |          |   |        |    |                 |   | ir |
|          |          |   |        |    |                 |   | us |
|          |          |   |        |    |                 |   | es |
+----------+----------+---+--------+----+-----------------+---+----+
|          | Chickpea | C | *Bean  | U  | Kaiser et al.   | A | B  |
|          | filiform | p | yellow | SA | 1988            | p | YM |
|          | virus    | F | mosaic |    |                 | h | V, |
|          |          | V | v      |    |                 | i | Bl |
|          |          |   | irus*? |    |                 | d | CM |
|          |          |   |        |    |                 | s | V, |
|          |          |   |        |    |                 |   | CA |
|          |          |   |        |    |                 |   | MV |
+----------+----------+---+--------+----+-----------------+---+----+
|          | Chickpea | C |        | B  | Larsen et al.   | A | Nr |
|          | yellow   | p |        | ol | 2003            | p |    |
|          | mosaic   | Y |        | iv |                 | h |    |
|          | virus    | M |        | ia |                 | i |    |
|          |          | V |        |    |                 | d |    |
|          |          |   |        |    |                 | s |    |
|          |          |   |        |    |                 | ? |    |
+----------+----------+---+--------+----+-----------------+---+----+
|          | *Lettuce | L | * *    | U  | Bosque-Perez    | A | Nr |
|          | mosaic   | M |        | SA | and Buddenhagen | p |    |
|          | virus*   | V |        |    | 1990            | h |    |
|          |          |   |        |    |                 | i |    |
|          |          |   |        |    |                 | d |    |
|          |          |   |        |    |                 | s |    |
+----------+----------+---+--------+----+-----------------+---+----+
|          | *Pea     | P |        | A  | Makkouk et 1993 | A | Nr |
|          | se       | S |        | lg |                 | p |    |
|          | ed-borne | b |        | er | Latham and      | h |    |
|          | mosaic   | M |        | ia | Jones 2001      | i |    |
|          | virus*   | V |        |    |                 | d |    |
|          |          |   |        | A  | Russo et al.    | s |    |
|          |          |   |        | us | 1981; Makkouk   | , |    |
|          |          |   |        | tr | et 1993         | s |    |
|          |          |   |        | al |                 | e |    |
|          |          |   |        | ia | Tadesse *et     | e |    |
|          |          |   |        |    | al*. 1999 ;     | d |    |
|          |          |   |        | E  | Bekele et al    |   |    |
|          |          |   |        | gy | 2005            |   |    |
|          |          |   |        | pt |                 |   |    |
|          |          |   |        |    | Makkouk et al.  |   |    |
|          |          |   |        | E  | 2003b           |   |    |
|          |          |   |        | th |                 |   |    |
|          |          |   |        | io | Al-Mabrouk and  |   |    |
|          |          |   |        | pi | Mansour. 2000   |   |    |
|          |          |   |        | a\ |                 |   |    |
|          |          |   |        | Ir | Makkouk et al.  |   |    |
|          |          |   |        | an | 1993            |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | Jo | Fletcher 1993   |   |    |
|          |          |   |        | rd |                 |   |    |
|          |          |   |        | an | Makkouk et al.  |   |    |
|          |          |   |        |    | 2001            |   |    |
|          |          |   |        | M  |                 |   |    |
|          |          |   |        | or | Makkouk et al   |   |    |
|          |          |   |        | oc | 1992; Mouhanna  |   |    |
|          |          |   |        | co | et al 1994      |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | N  | Makkouk et 1993 |   |    |
|          |          |   |        | ew |                 |   |    |
|          |          |   |        | Z  | Bayaa et al     |   |    |
|          |          |   |        | ea | 1998            |   |    |
|          |          |   |        | la |                 |   |    |
|          |          |   |        | nd | Hampton and     |   |    |
|          |          |   |        |    | Muehlbauer,     |   |    |
|          |          |   |        | Pa | 1977; Hampton   |   |    |
|          |          |   |        | ki | 1982            |   |    |
|          |          |   |        | st |                 |   |    |
|          |          |   |        | an |                 |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | S  |                 |   |    |
|          |          |   |        | yr |                 |   |    |
|          |          |   |        | ia |                 |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | T  |                 |   |    |
|          |          |   |        | un |                 |   |    |
|          |          |   |        | is |                 |   |    |
|          |          |   |        | ia |                 |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | Tu |                 |   |    |
|          |          |   |        | rk |                 |   |    |
|          |          |   |        | ey |                 |   |    |
|          |          |   |        |    |                 |   |    |
|          |          |   |        | U  |                 |   |    |
|          |          |   |        | SA |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
|          | *Turnip  | T |        | A  | Schwinghamer et | A | Nr |
|          | mosaic   | u |        | us | al. 2007        | p |    |
|          | virus*   | M |        | tr |                 | h |    |
|          |          | V |        | al |                 | i |    |
|          |          |   |        | ia |                 | d |    |
|          |          |   |        |    |                 | s |    |
+----------+----------+---+--------+----+-----------------+---+----+
| **Family |          |   |        |    |                 |   |    |
| *R       |          |   |        |    |                 |   |    |
| habdovir |          |   |        |    |                 |   |    |
| idae/*** |          |   |        |    |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
| *        | *Lettuce | L |        | A  | Behncken 1983   | A | Nr |
| Cytorhab | necrotic | N |        | us |                 | p |    |
| dovirus* | yellows  | Y |        | tr |                 | h |    |
|          | virus*   | V |        | al |                 | i |    |
|          |          |   |        | ia |                 | d |    |
|          |          |   |        |    |                 | s |    |
+----------+----------+---+--------+----+-----------------+---+----+
| **S      |          |   |        |    |                 |   |    |
| ymbiotic |          |   |        |    |                 |   |    |
| infe     |          |   |        |    |                 |   |    |
| ction/** |          |   |        |    |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+
| *Ena     | Pea      | P | *Pea   | Et | Tadesse et al.  | A | Nr |
| movirus* | enation  | E | e      | hi | 1999            | p |    |
| (*Luteov | mosaic   | M | nation | op |                 | h |    |
| iridae*) | virus    | V | mosaic | ia | Makkouk et al.  | i |    |
|          |          |   | vi     |    | 2003b           | d |    |
| *+\      |          |   | rus-1* | Ir |                 | s |    |
| Umb      |          |   |        | an | Vovlas and Rana |   |    |
| ravirus\ |          |   | \+     |    | 1972            |   |    |
| *(*Una   |          |   |        | I  |                 |   |    |
| ssigned* |          |   | *Pea   | ta | Kumari et al    |   |    |
| to       |          |   | e      | ly | 2001            |   |    |
| family)  |          |   | nation |    |                 |   |    |
|          |          |   | mosaic | Sy | Larsen et al.   |   |    |
|          |          |   | vi     | ri | 1996a ; Klein   |   |    |
|          |          |   | rus-2* | a\ | et al 1991      |   |    |
|          |          |   |        | U  |                 |   |    |
|          |          |   |        | SA |                 |   |    |
+----------+----------+---+--------+----+-----------------+---+----+

\*AMV, BBMV, BLRV, BWYV, BYMV, BBWV, CABYV, CMV, CpCDV, CpLV, FBNYV,
PEMV, PLRV, PSbMV, SbDV have been recorded naturally infecting chickpea
and lentil. BBSV and LStV have been recorded only in lentil. All other
species and isolates in the Table have been recorded only in chickpea.

\*\*Species recognized by the International Committee on Taxonomy of
Viruses (ICTV) are shown in italics; isolate and proposed species names
are not italicized. Many identifications, especially older ones, were
based on limited methodologies which probably distinguished genus but
not necessarily species.

\*\*\*Heterologous antisera that cross react with lentil or chickpea
isolates. Nr denotes 'none reported'. Virus species not listed in
columns 1 and 2 are: ABMV, Azuki bean mosaic virus = *Bean common mosaic
virus*; BlCMV, Blackeye cowpea mosaic virus = *Bean common mosaic
virus*; CABMV, *Cowpea aphid-borne mosaic virus*; PeMoV, *Peanut mottle
virus*; SMV, Soybean mosaic virus = *Watermelon mosaic virus.*

**References**

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H. J. 2006. Chickpea chlorotic stunt virus: A new polerovirus infecting
cool-season food legumes in Ethiopia. Phytopathology 96:437-446.

Abraham, A. D., Varrelmann, M., and Vetten, H. J. 2008. Molecular
evidence for the occurrence of two new luteoviruses in cool season food
legumes in Northeast Africa. Afr. J. Biotechnol. 7:414-420.

Al-Mabrouk, O., and Mansour, A.N. 2000. Viruses affecting lentil in
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Al-Nsour, A., Mansour, A., Al-Musa, A., and Salem, N. 1998. Distribution
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Anjaiah, V., Reddy, D. V. R., Manohar, R. A., Naidu, R. A., Nene, Y. L.,
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associated with bush dwarf symptom in chickpea, *Cicer arietinum*, in
India. Plant Pathol. 38:520-526.

Bakr, M.A. 1993. Plant Protection of lentil Bangladesh. Pages 177-184.
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Asia, 11-15 March 1991, New Delhi, India. W. Erskine and M.C. Saxena
(eds.). International Center for Agricultural Research in the Dry Areas
(ICARDA), Aleppo, Syria. 236 pp.

Bashir, M., and Malik, B. A. 1993. Natural occurrence of cucumber mosaic
virus in chickpea in Pakistan. International Chickpea Newsletter 29:10.

Bashir, M., Tahir, M., and Malik, B.A. 1994. Natural occurrence of
cucumber mosaic virus in lentil in Pakistan. Lens Newsletter, 21(1):
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Bashir, M. , Azeem, T., Ali, A., and Ijaz, M. 2005. Variation in lentil
germplasm for reaction to virus infection. Pak. J. Bot. 37:53-60

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(Prepared by M. W. Schwinghamer and R. C. Larsen)