> **Evaluation of the need for continued quarantine of foreign strains
> of the wheat flag smut pathogen, *Urocystis agropyri* (Preuss)
> Schroet.**
>
> **Pest-Specific Plant Pest Risk Analysis**
>
> Version 3.2
>
> June 2001
>
> Agency Contacts:
>
> Michael J. Firko, Chief Operations Officer
>
> Cooperative Assessment: Permits and Risk Analysis
>
> Plant Protection and Quarantine
>
> Animal and Plant Health Inspection Service
>
> U.S. Department of Agriculture
>
> 4700 River Road, Unit 133
>
> Riverdale, MD 20737-1236
>
> [and]{.underline}
>
> Dr. Gordon Gordh, Director
>
> Center for Plant Health Science and Technology
>
> USDA-APHIS-PPQ
>
> 1730 Varsity Drive, Suite 400
>
> Raleigh, NC 27606
>
> **Table of Contents**
>
> **Executive Summary**
>
> A. Background i
>
> B. Brief Description of the Pest and Its Impact i
>
> C. Scope of Assessment and Summary Conclusions ii

D.  Likely consequences of discontinuing quarantine by APHIS iii

E.  Recommendation iv

> **I.** **Introduction**
>
> A. Purpose 1
>
> B. Legal Authorities 1
>
> C. Initiation and Consistency with International Guidelines 2
>
> D. Pathogen Species Covered By This Risk Analysis 2
>
> E. Description of the Pest and Its Impact 4
>
> F. Current and Previous Importations and Previous Risk Assessments 6
>
> G. Brief Discussion of Issues Regarding the Quarantine of Foreign
> Strains of
>
> *Urocystis agropyri* 6
>
> **II. Risk Assessment**
>
> A. Regulatory Literature on Flag Smut Occurrence/Distribution 7
>
> B. Geographic and Regulatory Criteria 8
>
> C-a. Economic Importance / Consequences of Introduction 8
>
> C-b. Consequences of Introduction: Cumulative Risk Element Score 12
>
> D. Likelihood of Introduction (Entry and Establishment) 13
>
> E. Assessment Conclusion: Risk Potential and Quarantine Status 13
>
> **III. Risk Management and Decision on Quarantine Status** 14
>
> **IV. References** 15
>
> **V. Preparation, Consultation and Review** 18
>
> **Executive Summary**
>
> **A. Background**
>
> The Animal and Plant Health Inspection Service (APHIS) of the United
> States Department of Agriculture (USDA) conducted a plant pest risk
> assessment to evaluate the potential risks associated with changing
> the quarantine status of foreign strains of the fungus *Urocystis
> agropyri* (Preuss) Schroet. (=*Urocystis tritici* Koernicke), the
> causal agent of the flag smut disease of wheat. The quarantine was
> established in 1919 to prohibit the introduction of *U. agropyri*
> contaminating wheat seed or other plant parts originating from
> countries that have reported flag smut disease of wheat. At the time
> that the quarantine was established, wheat growers did not have the
> option to use other disease control strategies such as resistant
> varieties of wheat and highly effective seed treatments. Since that
> time, scientists and growers have gained a greater understanding of
> effective, practical measures that can mitigate flag smut.
>
> The flag smut quarantine (Title 7, Code of Federal Regulations, Part
> 319.59) prohibits movement, from countries where flag smut is
> reported, of commodity wheat seed and grain, and commodity shipments
> of grains other than wheat when wheat seed is found admixed with the
> crop (as occurs in crop rotation systems where volunteer wheat plants
> occur among subsequent crops). APHIS has received requests from
> scientists and grain traders to modify or eliminate the quarantine in
> the light of current agricultural practices that mitigate the
> potential plant pest risks presented by all strains of *U. agropyri*
> and questions as to whether foreign strains pose any greater risk than
> those already present in the United States.

# B. Brief Description of the Pest and Its Impact

> In 1868, flag smut was first described in Australian wheat fields
> (McAlpine, 1910). It was not until 1919 that flag smut was first
> reported in the United States, in Illinois and Indiana (Humphrey and
> Johnson, 1919). Based on the circumstantial evidence that the disease
> occurred in Australia and appeared in the United States
> contemporaneously with wheat shipments from Australia to the US,
> officials concluded that the pathogen may have entered the United
> States in those wheat shipments (Tisdale, *et al.*, 1923).
> Consequently, in August of 1919, the USDA promulgated Federal
> Quarantine No. 39, which prohibited importation of raw, unprocessed
> cereal grain from countries affected by flag smut and take-all
> disease. Quarantine 39 was superceded in 1926 by Quarantine 59 which
> removed restrictions regarding take-all but prohibited the
> "importation into the United States . . . of all species and varieties
> of wheat and wheat products, except such as have been so milled or so
> processed as to destroy all flag smut spores." By 1932, flag smut had
> essentially been eradicated from the Midwestern United States through
> the use of resistant varieties, seed treatments, and the
> implementation of quarantines as a precaution to protect domestic
> wheat production from potentially damaging foreign strains of the flag
> smut pathogen. The quarantine prohibited the importation of wheat
> seeds or other plant parts from countries where flag smut was known to
> occur. Agricultural officials considered a domestic quarantine of
> wheat grown in Illinois and Indiana, but decided against such
> measures.
>
> Flag smut of wheat occurs in the United States and elsewhere in the
> world where autumn-sown wheat is grown in regions with dry summers and
> mild winter temperatures. These conditions occur in some limited areas
> of the northwestern United States as well as parts of Australia, South
> America, Asia, and Europe. Flag smut does not occur in spring-sown
> wheat even when highly susceptible cultivars are grown (Line, 1998),
> due to current agronomic practices in the United States.
>
> The disease cycle begins in the autumn. Teliospores of the fungus that
> are present either in the soil or as a contaminant of seed germinate
> to produce an infectious spore, the sporidium. These sporidia directly
> infect wheat seedlings prior to emergence. Mild temperatures between
> 10 and 20ºC and soil moisture conditions that are optimum for seed
> germination and seedling emergence favor infection of wheat. The
> fungus overwinters as a mycelium within the seedling. In spring, the
> mycelium systemically invades the host and eventually produces
> teliospores within the upper portions of host plants, particularly the
> flag leaf, but not in the developing seed. The teliospores are
> long-lived (up to 3 years in the soil and 4 years as contaminants of
> seed) and are spread by wind. Contamination of seed and soil by
> wind-blown spores and from spores shed during harvest is the source of
> inoculum for subsequent crops. Pathotypes that can infect a range of
> grass species and wheat exist but there is no clear description
> available of the races and their host specificity. U*. agropyri* has
> been reported to infect wheat, barley and a number of other grasses.
> However, isolates show marked host specialization and most wheat
> isolates will not infect other grass species (Mordue and Waller,
> 1981).
>
> Affected plants within the growing crop are often severely stunted and
> plants may tiller excessively. Major symptoms include long
> grayish-black streaks on leaf blades, especially the flag leaf, and on
> leaf sheaths. In some cases, the head fails to emerge. Where heads do
> emerge the glumes and necks may be striped. Throughout the world's
> wheat growing regions today, flag smut is not as damaging as it once
> was reported. Flag smut is no longer a major problem in the United
> States. Where flag smut occurs, losses are largely controlled through
> the use of resistant wheat cultivars, fungicidal seed treatments, and
> crop rotation.
>
> Like other plant diseases, the control of flag smut can be achieved
> through a variety of strategies or disease control measures which aim
> to influence one or more of the three components of the disease
> triangle: host, pathogen and environment. Disease control measures can
> be classed in accordance with the four basic principles of disease
> prevention they exemplify: (1) exclusion and (2) eradication; which
> involve control of the pathogen; and (3) protection (treating a
> healthy plant before it becomes diseased) and (4) development of
> resistance; which deal with the plant's defense mechanisms (Pscheidt,
> 1997).

## C. Scope of Assessment and Summary Conclusions

> APHIS concludes that categorization of these foreign strains of *U.
> agropyri* as quarantine pests is not supported by the available
> biological/ scientific information, international agreements on
> criteria for quarantine pests, the United States Acts cited in Section
> I.B., and existing USDA policies regarding quarantine pests. It
> appears that the circumstances under which the quarantine was
> established in 1919 no longer apply. Therefore, we conclude and we
> recommend that APHIS discontinue the quarantine of foreign strains of
> *U. agropyri*. As part of the pest risk assessment, APHIS has
> considered the following:
>
> 1\. Although the first reports of flag smut in the United States were
> from the Midwest region, flag smut has not been reported in the
> literature from these locations since 1934 (Line, 1998).
>
> 2\. Because of temperature and moisture requirements of the pathogen,
> flag smut occurs in the United States only on wheat in the Pacific
> Northwest when seed is sown in late August and early September at
> depths of more than 2 inches (Line, 1998).
>
> 3\. The incidence and severity of flag smut on wheat grown in the
> United States has declined as scientists and growers developed
> reliable strategies to minimize the impact of this disease.
>
> 4\. Currently, effective flag smut control strategies include the use
> of (a) resistant wheat varieties, (b) chemical treatments to eliminate
> viable spores of the pathogen on seeds or in the soil, and (c) crop
> rotation and other agronomic practices.
>
> 5\. There is no evidence in the scientific literature which
> unequivocally confirms that foreign strains of *U. agropyri* pose a
> greater risk than domestic strains to wheat production in the United
> States. Current control strategies should be effective in limiting the
> impact of foreign strains of *U. agropyri.* In fact, research
> comparing the morphological, biological, and molecular characteristics
> of Australian and U.S. isolates suggested there were few if any
> differences (Brown, *et al.*, 1994).
>
> 6\. The fungus is unlikely to be eradicated since once established it
> can survive as persistent teliospores within spore balls, both in the
> soil and also as a seed contaminant for up to 3 or 4 years,
> respectively (Griffiths, 1924; Sattar and Hafiz, 1952).

## D. Likely consequences of discontinuing quarantine by APHIS

> [Plant pest risk]{.underline}: A discontinuation of the quarantine
> appears to pose little, if any, increased plant pest risk for domestic
> wheat production. The limited distribution of flag smut disease in the
> United States and its lack of spread despite being present for decades
> with no domestic quarantines provide circumstantial evidence that
> suitable environments are restricted. Earlier occurrences of the
> disease in the central United States were attributed to a combination
> of factors: (1) use of highly susceptible cultivars, (2) inadequate
> crop rotation, (3) cultural practices, and (4) lack of satisfactory
> seed treatments. This combination led to an inoculum build-up
> sufficient for disease expression. Current agricultural practices
> would not allow such a build-up to occur (Line, 1998).
>
> The flag smut quarantine was originally promulgated based on the
> possibility that foreign strains of the fungus, more virulent than
> those already in the United States, might exist in flag smut countries
> and should be excluded. However, as stated in Line (1998), "Evidence
> for the existence of pathogenic races of *U. agropyri* is based on
> reports that flag smut collections from different regions of the world
> have different virulences. However, some of the conclusions are based
> on nonreplicated data consisting of a small population of plants
> compared under greenhouse conditions in different years, and the
> development of new pathogenic races has not been confirmed. In regions
> where flag smut is endemic, new races of the pathogen have not been
> detected even with the selection pressure via the use of resistant
> cultivars for decades." A recent research study conducted in Australia
> and presented to APHIS (Brown, *et al.*, 1994) concluded genetic and
> cytological features of *U. agropyri* spores make genetic
> recombination between different strains extremely rare, hence the
> "fungus should be genetically very uniform with little opportunity of
> different races within a given population."
>
> Pest risk encompasses not only the likelihood of a hazardous event
> occurring, but also the consequences of such an event. Given the
> cultural practices in use today and the control measures available, it
> seems unlikely that flag smut would ever become a major disease of
> wheat in the United States. The economic impact of the disease where
> it occurs in the Pacific Northwest is virtually nil and at times the
> disease is difficult to find (Line, 1998; MacLatchy, 1995). A number
> of plant pathologists contend that the quarantine against foreign
> strains of *U. agropyri* is not necessary to protect the wheat grown
> in the United States. This view was expressed by scientific experts at
> the 1997 International Workshop on Smuts and Bunts that was
> co-sponsored by APHIS and NAPPO (North American Plant Protection
> Organization). Relevant scientific literature suggests that
> introduction of foreign strains of *U. agropyri* would not trigger any
> significant environmental impacts. Non-wheat strains of the fungus are
> reported from 36 States and seed treatments effective against *U.
> agropyri* are already in use on wheat for control of this and other
> pathogens. Two recent plant pest risk assessments by Canada
> (MacLatchy, 1995) and the United Kingdom (Sansford, 1998) concluded
> that the pest risk posed by *U. agropyri* did not warrant specific
> quarantine measures.
>
> [Impacts on Trade]{.underline}: The current quarantine restricts the
> importation of crops that are grown in rotation with wheat, such as
> oats grown in Australia. Domestic production of oats has declined in
> recent years, and a discontinuation of the quarantine would permit the
> importation of oats from Australia or any of the 33 other quarantined
> countries to meet the needs of producers of animal feeds. *U.
> agropyri* is listed as a prohibited pest by several countries,
> including Brazil, Canada, Kenya, Oman, South Africa, Tanzania, Turkey,
> Uganda and Venezuela. Since the United States does not have, nor has
> it ever had any domestic flag smut quarantines, relaxation of our
> external quarantine would likely not have any impact on trading
> partners' willingness to accept U.S. grain. Also, unlike other bunts
> and smuts of wheat (*e.g.*, Karnal bunt), the quality of harvested
> grain both for feed and flour is unaffected by *U. agropyri* since the
> grain does not become infected.
>
> [Impacts on Treaty Obligations]{.underline}: Under the provisions of
> the General Agreement on Tariffs and Trade (GATT), phytosanitary trade
> restrictions are permissible if they are justified by scientific
> evidence. In addition, GATT stipulates that any restrictions of pest
> introductions via importation must be consistent with domestic
> restrictions on the movement of the pest. There are no domestic
> restrictions on the movement of wheat seeds or plant parts from
> regions of the country where flag smut occurs.
>
> **E. Recommendation:**
>
> Evidence suggests that the *Urocystis agropyri* organism which causes
> flag smut disease of wheat was unintentionally introduced into the
> United States with wheat seed imported from Australia. Additional
> research has demonstrated that comparative inoculations of both
> susceptible and resistant wheat cultivars detected no significant
> pathogenic differences among U. S. and Australian isolates of *U.*
> *agropyri*. In the Pacific Northwest of the U. S. flag smut disease
> has shown little or no ability to genetically modify itself and "new
> races of the pathogen have not been detected even with selection
> pressure via the use of resistant cultivars for decades." (Line,
> 1998). "*Urocystis agropyri* test results indicate very little
> susceptibility in wheat to the flag smut of grasses" (Fischer and
> Holton, 1943). We conclude that the quarantine for flag smut disease
> of wheat imported into the United States may be discontinued, and
> therefore we recommend that action.
>
> **I**. **Introduction**

###  A. Purpose

> This plant pest risk analysis was prepared by the Animal and Plant
> Health Inspection Service (APHIS) of the United States Department of
> Agriculture (USDA). We conducted the analysis to examine the plant
> pest risk posed by foreign strains of the fungus, *Urocystis
> agropyri*, the causal agent of the wheat disease called flag smut.
> Currently, foreign strains of this fungus are the subject of a
> quarantine (Title 7, Code of Federal Regulations, Part 319.59). The
> flag smut quarantine prohibits movement, from countries where flag
> smut is reported, of commodity wheat seed and grain, and commodity
> shipments of grains other than wheat when wheat seed is found admixed
> with the crop (as occurs in crop rotation systems where volunteer
> wheat plants occur among subsequent crops). Plant Protection and
> Quarantine (PPQ, within USDA-APHIS) has taken action on (*i.e.*,
> denied entry) shipments of oat grain found to be contaminated with
> wheat seeds when these shipments originated from countries where flag
> smut is known to occur. The decision to take action on these shipments
> was correct, based on scientific information available at the time of
> the decision and longstanding USDA practices. In response to requests
> from our trading partners and interested parties in the United States,
> APHIS agreed to reconsider the quarantine and the action status of
> these pathogens and to analyze in greater detail the risk posed by
> foreign strains of *U. agropyri*. This analysis addresses two basic
> questions: (1) Is there compelling evidence to warrant continued
> quarantine actions to minimize the introduction of foreign strains of
> *U. agropyri* into the United States, *i.e*., do the foreign strains
> pose a risk which is greater than that posed by the strains of *U.
> agropyri* that are already in the United States, and (2) Is the
> Federal quarantine an appropriate control mechanism in light of the
> biology of the fungus and our national obligations under treaties
> relevant to trade and plant pests?

###  B. Legal Authorities

> Under the Federal Plant Pest Act, as amended 1957 (7 United States
> Code 150aa *et seq*.) and the Plant Quarantine Act of 1912, as amended
> 1967 (7 United States Code 150aa *et seq*.), USDA has broad authority
> to regulate the importation and interstate movement of organisms that
> may directly or indirectly injure, damage, or cause disease in plants.
> APHIS's authority to regulate these organisms is granted by Title 7 of
> the Code of Federal Regulations (CFR), Part 330 (*i.e.*, 7 CFR §330).
> Section 330.101 states: "The purpose of the regulations in this part
> is to prevent the dissemination of plant pests into the United States
> or interstate, by regulating the movement of plant pests into or
> through the United
>
> States . . .".
>
> Part 319 of Title 7 (7 CFR §319) establishes foreign quarantines,
> specifically: 319.37 covers Nursery Stock, Plants, Roots, Bulbs,
> Seeds, and Other Plant Products and 319.59 covers diseases of wheat.
>
> The APHIS regulations as amended in 1983 provide the following
> definition for "foreign strains of flag smut: Plant diseases caused by
> foreign strains of highly infective fungi, *Urocystis agropyri*
> (Preuss) Schroet., which attack wheat and substantially reduce its
> yield, and which are new or not widely prevalent or distributed within
> and throughout the United States." In practice, APHIS quarantine
> actions exclude wheat seeds and plant parts originating from other
> countries which have flag smut. Those countries are specifically
> listed in 7 CFR 319.59- 2.a.2 as Afghanistan, Algeria, Australia,
> Bangladesh, Bulgaria, Chile, People's Republic of China, Cyprus,
> Egypt, Falkland Islands, Greece, Guatemala, Hungary, India, Iran,
> Iraq, Israel, Italy, Japan, Korea, Libya, Morocco, Nepal, Oman,
> Pakistan, Portugal, Romania, Spain, Tanzania, Tunisia, Turkey,
> Republic of South Africa, Union of Soviet Socialist Republics, and
> Venezuela.

###  C. Initiation and Consistency with International Guidelines

> International plant protection organizations such as the North
> American Plant Protection Organization (NAPPO) and the International
> Plant Protection Convention (IPPC) of the United Nations Food and
> Agriculture Organization (FAO) provide guidance for conducting pest
> risk analyses. This analysis was pest-initiated according to
> international standards, *i.e.*, "A policy decision is taken to revise
> phytosanitary regulations or requirements concerning specific pests"
> (FAO, 1996; NAPPO, 1993). The methods we used to initiate, conduct,
> and report this plant pest risk analysis are consistent with
> guidelines provided by NAPPO, IPPC and FAO. Our use of biological and
> phytosanitary terms (*e.g.*, introduction, quarantine pest) conforms
> with the *NAPPO Compendium of Phytosanitary Terms* (NAPPO, 1996) and
> the *Definitions and Abbreviations* (Introduction Section) in
> *International Standards for Phytosanitary Measures, Section
> 1---Import Regulations: Guidelines for Pest Risk Analysis* (FAO,
> 1996).
>
> The *Guidelines for Pest Risk Analysis* provided by FAO (1996)
> describes three stages in pest risk analysis: initiation, risk
> assessment, and risk management. This document satisfies the
> requirements of all three FAO Stages. FAO (1996) defines "pest risk
> assessment" as "Determination of whether a pest is a quarantine pest
> and evaluation of its introduction potential." "Quarantine pest" is
> defined as "A pest of potential economic importance to the area
> endangered thereby and not yet present there, or present but not
> widely distributed and being officially controlled" (FAO, 1996; NAPPO,
> 1996). Thus, the pest risk assessment portion should consider both the
> likelihood and consequences of introduction of quarantine pests. Both
> issues are addressed in this qualitative pest risk analysis. Risk
> management is the decision-making process of dealing with the risk of
> introduction of a quarantine pest (NAPPO, 1993). This analysis
> satisfies that requirement by documenting PPQ's decision regarding the
> quarantine status of foreign strains of *U. agropyri* from the
> countries listed in 7 CFR Part 319.

####  D. Pathogen Species Covered By This Risk Analysis

> We assess the risk posed to the United States by foreign strains of
> the wheat flag smut pathogen, *U. agropyri*. The risk of the foreign
> strains is evaluated in light of the impacts of domestic strains of
> *U. agropyri*. The regulations found at 7 CFR Part 319 specifically
> identify the quarantined organisms as "foreign strains of flag smut."
> The domestic strains of flag smut are not regulated by APHIS. The
> definition of strain in this case has both biological and legal
> relevance.
>
> Like the concept of speciation, the designation of a strain is shaped
> by the perceptions and values of the people evaluating the strain. In
> the case of plant pests, designations often are used to indicate
> populations of the organism which differ in their biological
> properties which influence pathogenicity or virulence with respect to
> host plants: "pathotype -- variant of a given pathogen; pathogenic
> reaction on a given host"; "race \-- group of individuals within a
> variety or species distinguished by behavior but not by morphology";
> "strain \-- descendants of an isolated organism; biotype; race"
> (Wiese, 1987). This is the interpretation that APHIS will utilize to
> assess whether the foreign strains need to be quarantined.
>
> Pathogenicity (*i.e.*, the capability of a pathogen to cause disease)
> is a consequence of inherent traits of the pathogen, as influenced by
> the host genotype as well as abiotic environmental factors such as
> temperature and moisture. Agriculturalists can frequently mitigate the
> effects of plant pathogens by means that enable the host plant to
> escape overwhelming challenges by the pathogen propagules. Altering
> crop rotations, sowing times and depths, other cultural practices such
> as planting cultivars which resist the pathogen modify the
> host-pathogen- environment disease triangle to prevent or reduce
> infection.
>
> Two organisms may have many characteristics, such as morphological or
> physiological attributes, in common, yet they may form biologically
> distinct subsets of a fungal species. From 1877 until 1943 *U.
> tritici* was accepted as the valid name for the wheat flag smut fungus
> (Purdy, 1965). Then, on the basis of morphological similarities with
> *U. agropyri*, a species causing flag smut of various grasses, it was
> recommended that the two species be synonymized under the *agropyri*
> epithet (Fischer and Holton, 1943). The names *U. tritici* and *U.
> agropyri* were synonymized, but without an unequivocal demonstration
> of the interspecific host preference of the fungi from wheat and those
> from grasses. Thus, ***U**. agropyri* has been reported to infect
> wheat, barley and a number of other grasses. However, isolates show
> marked host specialization and most wheat isolates will not infect
> other grass species (Mordue and Waller, 1981). Many grasses,
> especially *Poa* spp., are susceptible to the other strains of the
> pathogen (MacLatchy, 1995). Wheat **or** grass isolates of *U.
> agropyri* have been reported from 36 States and Canada even though the
> wheat flag smut disease only occurs in the Pacific Northwest.
>
> An early study comparing U.S. and South African wheat isolates
> suggested the isolates did not differ in pathogenicity, although the
> South African isolates appeared to be more virulent (where virulence
> is defined as the degree of pathogenicity) (Verwoerd, 1929). Studies
> in China (Yu, *et al.*, 1945), Pakistan (Hafiz, 1951) and the United
> States (Holton and Johnson, 1943) differentiated varying numbers of
> pathogenic races, while studies by Watson and Baker in Australia
> (Purdy, 1965) were unable to detect different races. More recently,
> research comparing the morphological, biological and molecular
> characteristics of Australian and U.S. isolates suggested there were
> few if any differences (Brown, *et al.*, 1994). Line (1998) states,
> "Evidence for the existence of pathogenic races of *U. agropyri* is
> based on reports that flag smut collections from different regions of
> the world have different virulences. However, some of the conclusions
> are based on nonreplicated data consisting of a small population of
> plants compared under greenhouse conditions in different years, and
> the development of new pathogenic races has not been confirmed. In
> regions where flag smut is endemic, new races of the pathogen have not
> been detected even with the selection pressure via the use of
> resistant cultivars for decades." Thus, the situation regarding the
> presence of races is not clear and there remains a question whether
> the foreign strains of *U. agropyri* meet the standard of a quarantine
> pest.

#####  

#####  E. Description of the Pest and Its Impact

> In 1868, flag smut was first described in Australian wheat fields
> (McAlpine, 1910). It was not until 1919 that flag smut was first
> reported in the United States, in Illinois and Indiana (Humphrey and
> Johnson, 1919). Based on the circumstantial evidence that the disease
> occurs in Australia and appeared in the United States
> contemporaneously with wheat shipments from Australia to the U. S.,
> officials concluded that the pathogen may have entered the United
> States in those wheat shipments (Tisdale, *et al.*, 1923).
> Consequently, in August of 1919, the USDA promulgated Federal
> Quarantine No. 39 as a precaution to protect domestic wheat production
> from potentially damaging foreign strains of the flag smut pathogen.
> The quarantine prohibited the importation of wheat seeds or other
> plant parts from countries where flag smut was known to occur.
> Agricultural officials considered a domestic quarantine of wheat grown
> in Illinois and Indiana, but decided against such measures.
>
> Flag smut of wheat occurs in the United States and elsewhere in the
> world where autumn-sown wheat is grown in regions with dry summers and
> mild winter temperatures. These conditions occur in some limited areas
> of the northwestern United States as well as parts of Australia, South
> America, Asia, and Europe. Flag smut does not normally occur in
> spring-sown wheat even when highly susceptible cultivars are grown
> (Line, 1998).
>
> The disease cycle begins in the autumn. Teliospores of the fungus that
> are present either in the soil or as a contaminant of seed germinate
> to produce an infectious spore, the sporidium. These sporidia directly
> infect wheat seedlings prior to emergence. Mild temperatures between
> 10 and 20ºC and soil moisture conditions that are optimum for seed
> germination and seedling emergence favor infection of wheat. The
> fungus overwinters as a mycelium within the seedling. In spring, the
> mycelium systemically invades the host and eventually produces
> teliospores within the upper portions of host plants, particularly the
> flag leaf, but not the developing seed. Although the pathogen
> initiates infection of the seedling before emergence from the soil,
> the characteristic disease symptoms become conspicuous at mid-season
> during stem elongation and heading when gray-black stripes appear
> between the veins of the leaf blades and sheaths. These stripes later
> break open and release masses of black spores. After this, the
> infected leaves look frayed. If the infection is severe, plants may be
> extremely dwarfed and will fail to produce heads. The teliospores are
> long-lived (up to 3 years in the soil and 4 years as contaminants of
> seed) (Griffiths, 1924; Sattar and Hafiz, 1952), and are spread by
> wind. Contamination of seed and soil by wind-blown spores and from
> spores shed during harvest is the source of inoculum for subsequent
> crops.
>
> Affected plants within the growing crop are often severely stunted and
> plants may tiller excessively. Major symptoms include long
> grayish-black streaks on leaf blades, especially the flag leaf, and on
> leaf sheaths. In some cases, the head fails to emerge. Where heads do
> emerge the glumes and necks may be striped.
>
> In this century, the importance of flag smut as a disease of wheat has
> varied with outbreaks generally associated with the growing of
> susceptible varieties (Mordue and Waller, 1981). Shortly after flag
> smut was reported in Illinois in 1919, losses were reported as within
> a range of 5 to 30 percent (Purdy, 1965). In the following five years,
> the average **incidence** was estimated to be 2 percent with localized
> areas ranging as high as 50 percent infected plants (Purdy, 1965).
> These localized areas were in "hot spots" in a small part of a field
> where threshing machines had operated (Line, 1998). Martens, *et al.*,
> (1984) calculated that every 1 percent incidence will cause a yield
> loss of 0.4 -- 0.6 percent. Flag smut has not been reported in the
> Midwestern United States since 1934 and is rare in the northwestern U.
> S. (Line, 1998).
>
> In the Pacific Northwestern United States, incidence and yield losses
> increased in the early 1960's with the advent of early fall "deep
> seeding" and the use of susceptible or moderately susceptible
> cultivars (MacLatchy, 1995). By the late 1960's, flag smut was the
> most important disease of wheat in two counties in the U. S. Pacific
> Northwest. Incidence ranged from trace amounts to 30 percent (Purdy,
> 1965). By the early 1970's the disease was effectively controlled with
> the introduction of resistant cultivars, effective seed treatments,
> and changes in cultural practices. The economic impact of the disease
> where it occurs in the Pacific Northwest today is virtually nil and at
> times the disease is difficult to find (Line, 1998; MacLatchy, 1995).
>
> Throughout the world's wheat growing regions today, flag smut is not
> as damaging as it once was reported. In Australia, where losses once
> ranged from 10-15 percent in the northeastern hard wheat areas, the
> disease has been all but eliminated through the use of crop rotation
> and resistant varieties (MacLatchy, 1995). Similarly, in Turkey where
> the disease was once considered to be of some importance, effective
> seed treatments have relegated flag smut to minor disease status
> (MacLatchy, 1995).
>
> Flag smut still occurs, but losses are largely controlled through the
> use of resistant wheat cultivars, fungicidal seed treatments, and crop
> rotation and other management methods. The limited distribution of the
> flag smut disease in the United States and its lack of spread despite
> being present for decades with no domestic quarantines provide
> circumstantial evidence that suitable environments are restricted.
> Earlier occurrences of the disease in the central United States were
> attributed to a combination of factors: (1) use of highly susceptible
> cultivars, (2) inadequate crop rotation, (3) cultural practices, and
> (4) lack of satisfactory seed treatments. This combination led to an
> inoculum build-up sufficient for disease expression. Current
> agricultural practices would not allow such a build-up to occur (Line,
> 1998).
>
> Like other plant diseases, the control of flag smut can be achieved
> through a variety of strategies or disease control measures which aim
> to influence one or more of the three components of the disease
> triangle: host, pathogen, and environment.
>
> For example, in the 1999 Online Guide for Plant Disease Control
> (Pscheidt, 1997), Oregon State University recommends the following
> cultural control measures for flag smut:
>
> 1\. Use resistant cultivars.
>
> 2\. Rotate 2 years out of winter wheat.
>
> 3\. Plant seed shallowly (less than 1 inch) when soils cool in fall.
>
> In addition, the guide describes the following chemical control agents
> which are effective against seedborne and soilborne spores
> (http://plant-disease.orst.edu/disease.cfm?RecordID=1135.00000):

A.  Vitavax®

B.  Dividend®

> C. Raxil-Thiram®
>
> Other fungicides have also been demonstrated to provide 100% control
> of flag smut, such as:

D.  triadimenol

E.  tebuconazole

F.  difenoconazole \[available as Dividend®\] (Line, 1998).

Line also listed:

G.  Plantvax® oxycarboxin

H.  Vitavax® carboxin

on his website: http://www.wsu.edu:8080/\~wheaties/fd96smut.html.

> Disease control measures can be classed in accord with the four basic
> principles of disease prevention they exemplify: (1) exclusion and (2)
> eradication; which involve control of the pathogen; and (3) protection
> (treating a healthy plant before it becomes diseased) and (4)
> development of resistance; which deal with the plant's defense
> mechanisms (Pscheidt, 1997).

###### F. Current and Previous Importations and Previous Risk Assessments

> Neither flag smut of wheat nor foreign strains of *U. agropyri* have
> been the subject of previously documented risk analyses by APHIS.
>
> **G. Brief Discussion of Issues Regarding the Quarantine of Foreign
> Strains of *Urocystis agropyri***

**G. Brief Discussion of Issues Regarding the Quarantine of Foreign
Strains of *Uromyces agropyri***

> The Animal and Plant Health Inspection Service (APHIS) of the United
> States Department of Agriculture (USDA) conducted a pest risk
> assessment to evaluate the potential plant pest risks associated with
> changing the quarantine status of foreign strains of *U. agropyri*,
> the causal agent of flag smut of wheat. The quarantine was established
> in 1919 to prohibit the introduction of *U. agropyri* spores
> contaminating wheat seed or other plant parts originating from
> countries which have reported flag smut of wheat. APHIS has received
> requests from scientists and grain traders to modify or eliminate the
> current quarantine in light of agricultural practices which mitigate
> the potential plant pest risks presented by foreign strains of *U.
> agropyri*.
>
> **Issue No. 1. Certain stakeholders have asserted that these foreign
> strains are no more of a threat to United States wheat production than
> the strains of *U. agropyri* which occur within the United States.**
>
> **[APHIS Response]{.underline}**: APHIS agrees that there is no
> definitive demonstration that foreign strains of *U. agropyri* pose a
> greater risk to U.S. grown wheat than the strains which are in the
> United States.
>
> **Issue No. 2. Certain stakeholders have maintained that there are
> adequate flag smut control measures available to U. S. wheat growers
> to minimize any impact of new strains of *U. agropyri*.**
>
> **[APHIS Response]{.underline}**: APHIS agrees that there are
> presently adequate disease control measures for flag smut of wheat.
> APHIS recognizes that both the incidence and severity of flag smut
> have been declining, especially during the past 30 years. Beginning in
> the late 1960s, research efforts have yielded effective disease
> control practices. These control practices have proven durable through
> decades of use.
>
> **Issue No. 3. Certain stakeholders have asserted that because species
> in this fungal genus occur in the United States, the intercepted
> species do not satisfy the geographic and regulatory criteria as
> quarantine pests**.
>
> **[APHIS Response]{.underline}**: Although *U. agropyri* occurs in the
> United States, the prevailing assumption from the institution of
> quarantine in 1919 has been that *U. agropyri* originated from outside
> the United States and quarantine of foreign strains of the pathogen
> would reduce the risk of continual re-introductions or introduction of
> more virulent strains. Historically, APHIS-PPQ has taken action on
> intercepted pests when the following conditions exist:

-   an intercepted pest is identifiable only to genus,

-   the intercepted species, although unnamed, has characteristics that
    allow it to be distinguished from species known to occur in the
    United States, and

-   one or more species in the genus are known to be plant pests, and

-   the commodity is destined for propagation.

> Action typically takes the form of requiring treatment of the
> commodity or prohibiting entry. It appears that the foreign strains of
> *U. agropyri* do not meet these criteria for quarantine.
>
> **Issue No. 4. Certain stakeholders have suggested that regardless of
> whether these foreign strains satisfy the geographic and regulatory
> criteria as quarantine pests, they may not satisfy the economic
> criteria because they are not significant plant pests.**
>
> **[APHIS Response]{.underline}**: APHIS agrees that the economic
> significance of flag smut to U.S. wheat production is slight, but the
> primary purpose of this plant pest risk analysis is to evaluate
> available information concerning the plant pest potential of these
> strains and to estimate their biological potential as plant pests in
> the United States.

####### Risk Assessment

> **A. Regulatory Literature on Flag Smut Occurrence/Distribution**
>
> Information regarding the flag smut pathogen was sought from a variety
> of sources including:

-   Literature reviews using electronic databases (*e.g.*, AGRICOLA,
    CABI database, *etc.*)

-   The USDA-APHIS files of previous decisions regarding importations.

-   The USDA-APHIS files and databases regarding previously intercepted
    pests.

-   C.M.I. Distribution Maps/Descriptions of Plant Pests (*e.g.*, Fungi)

-   Various texts and indices of plant diseases and pathogens.

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-   USDA-ARS plant pest database.

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-   EPPO (1994) plant pest database

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```
-   FAO (1993) plant pest database

> To be considered a quarantine pest, a pest must satisfy two criteria
> (FAO, 1996; NAPPO, 1996). First, the pest must satisfy geographic and
> regulatory criteria. With respect to the PRA area (*i.e.*, the United
> States), the pest must be "not yet present there, or present but not
> widely distributed and being officially controlled." Second, the pest
> must be "of potential economic importance" (FAO, 1996; NAPPO, 1996).

###  B. Geographic and Regulatory Criteria

> By the definition of foreign strains in the regulation, these foreign
> strains of *U. agropyri* are assumed not to occur in the United States
> and therefore satisfy a portion of the geographic and regulatory
> criteria of a quarantine pest. This assumption and its implications
> are complicated by the fact that the regulation does not provide
> detail on the definition of the term "strain." We utilize the
> following definitions: "race -- group of individuals within a variety
> or species distinguished by behavior but not by morphology"; "strain
> -- descendants of an isolated organism; biotype; race" (Wiese, 1987).
> It is therefore necessary to interpret the intent of the regulation in
> light of our current understanding of the plant pest risk (see Section
> **I. D. Pathogen Species Covered By This Risk Analysis**).
>
> **C-a. Economic Importance / Consequences of Introduction**
>
> In this section, we assess whether the foreign strains of *U.
> agropyri* satisfy the economic criteria of a quarantine pest.
> According to FAO (1996) and NAPPO (1996), an organism can be
> classified a quarantine pest when it is "of potential economic
> importance." We rate the potential consequences of introduction
> (*i.e.*, economic importance) according to five risk elements (RE's,
> described below). Our risk assessment process, and our five RE's in
> particular, are consistent with international guidelines (*e.g.*, FAO,
> 1996; NAPPO, 1993; NAPPO, 1996). These elements reflect the biology of
> the organism and its hosts. This is a qualitative ranking. For each
> RE, we assign the pest a rating of High, Medium, or Low according to
> the following criteria. A discussion of our findings is provided with
> each RE.
>
> RE #1: Climate---Host Interaction
>
> When introduced to new areas, pests can be expected to behave as they
> do in their native area if host plants are available and the climate
> is similar. We consider ecological zonation and the interaction
> between the geographic distributions of the fungus and host. Estimates
> are based on availability of both host material and suitable climate
> conditions. To rate this RE, we use the U.S. \"Plant Hardiness Zones\"
> as described by the U.S. Department of Agriculture (USDA, 1990)
> (Figure 1). We assign ratings as follows:
>
> Due to the availability of both suitable host plants and suitable
> climate, the fungus has potential to become established:

High (3): In four or more plant hardiness zones.

Medium (2): In two or three plant hardiness zones.

Low (1): In at most a single plant hardiness zone.

**[Finding]{.underline}** **Finding for RE#1**

> Flag smut occurs on autumn-sown wheat in regions of the world which
> have dry summers and mild (10 -- 20 deg. C.) winter temperatures
> (Wiese, 1987). Climatic conditions greatly influence the survival of
> the spores of *U. agropyri* which are borne on the seed or in the
> soil. These conditions occur in some limited areas of the northwestern
> United States as well as parts of Australia, South America, Asia and
> Europe. The most recent information on U.S. incidence of flag smut
> indicates that flag smut occurs only in the northwestern United
> States. But based on the biology of the pathogen it can survive
> anywhere that the host, autumn sown wheat, occurs and temperatures
> range between 10 - 25 C. during seedling emergence (Line, 1998).
> Previously recorded outbreaks of flag smut in the Central and Pacific
> Northwestern United States have occurred in essentially two, possibly
> three hardiness zones: zones 5, 6 and 7 (Figure 1). For these reasons,
> RE #1 is rated as **medium**.
>
> ![](media/image1.png){width="6.041666666666667in" height="4.6875in"}
>
> RE #2: Host range
>
> The risk posed by a plant pest depends on both its ability to
> establish a viable reproductive population and its potential for
> causing plant damage. For pathogens, risk is assumed to depend on host
> range, aggressiveness, virulence and pathogenicity; for simplicity, we
> rate risk as a function of host range.

High (3): Pathogen attacks multiple species within multiple plant
families.

Medium (2): Pathogen attacks multiple species within a single plant
family.

Low (1): Pathogen attacks a single species or multiple species within a
single genus.

> **[Finding for RE #2]{.underline}**
>
> While the species, *U. agropyri,* has been reported to infect wheat,
> barley and a number of other grasses, isolates show marked host
> specialization and wheat isolates do not naturally infect other grass
> species (Fischer and Holton, 1943; Mordue and Waller, 1981). Because
> wheat isolates of *U. agropyri* generally infect only wheat (*Triticum
> aestivum* L.), RE #2 is rated as **low**.
>
> RE #3: Dispersal Potential
>
> Fungi disperse after introduction to a new area. The following items
> are considered:

-   reproductive patterns of the fungus (*e.g.*, reproductive output)

-   innate dispersal capability of the fungus

-   what factors (*e.g.,* wind, water, animals, humans) facilitate
    dispersal

High (3): Fungus has high reproductive potential (*e.g.*, many
generations per year, many offspring per reproduction, high innate
capacity for population increase), ***AND*** evidence exists that the
pest is capable of rapid dispersal (*e.g.*, over 10 km per year) either
under its own power, human-assisted, or by natural forces such as wind
or water.

Medium (2): Fungus has either high reproductive potential ***OR*** is
capable of rapid dispersal.

Low (1): Neither high reproductive potential nor capable of rapid
dispersal.

> **[Finding for RE #3]{.underline}**
>
> Spore balls, "compact, round groups of spores, or of spores and
> sterile cells, that function as units of dispersal" (Ulloa and Hanlin,
> 2000) liberated from tattered infected leaves contaminate the soil and
> seed. There is usually one generation of spores produced per season.
> Spores may be spread by winds to some extent, especially after
> harvest; however such spread is expected to be limited to the local
> farm level. Overall, the reproductive potential is not considered to
> be particularly high, although spores may remain viable in the soil
> for up to four years under optimal*, i. e*.: warm and dry, soil
> conditions (Line, 1998; Wiese, 1987). Because of these considerations,
> RE #3 is rated as **medium**.
>
> RE #4: Economic Impact
>
> Although a variety of impacts may occur, economic impacts caused by
> introduced plant pests are divided into three primary categories:

-   Lower yield of the host crop (*e.g.*, by causing plant mortality).

-   Lower value of the commodity (*e.g*., by increasing costs of
    production, lowering market price, or a combination).

-   Loss of markets (foreign or domestic) due to presence of new
    quarantine pest.

High (3): Pathogen causes all three of the above impacts.

Med Medium (2): Pathogen causes any two of the above impacts.

Low (1): Pathogen causes any one or none of the above impacts.

**[Finding for RE #4]{.underline}**

> An analysis of the available evidence suggests that in the absence of
> current disease control practices, the foreign strains of *U.
> agropyri* could be just as detrimental as the strains of *U. agropyri*
> currently found in the United States. According to Line (1998), the
> "disease caused losses of three to four percent in south central
> Australia in 1931 and has reduced yields in individual fields by as
> much as 50 percent." Experimentally, under conditions conducive to
> disease development yield losses have exceeded 95 percent. Normally,
> however, conditions conducive to such severe losses are rare. In
> countries where the disease is established, breeding programs have
> incorporated durable resistance genes into wheat cultivars and this,
> combined with the use of systemic fungicide seed treatments and
> cultural practices, including late and shallow planting and non-host
> crop rotations, has reduced the effect of the disease to insignificant
> levels (Sansford, 1998). Disease control measures **are** already
> being used effectively in the United States. It appears likely that
> such measures would be effective against foreign strains, since
> physiologic specialization has not proven to be a problem in breeding
> programs (Ballantyne, 1996). "Resistance occurs in many cultivars, has
> been easy to transfer into new cultivars and has remained durable for
> decades. New races of the pathogen have never circumvented that
> resistance" (Line, 1998).
>
> Brazil and Turkey are important customers for U.S. wheat, and in
> addition to Canada, have laws prohibiting wheat from countries having
> flag smut disease. The United States presently does not have domestic
> flag smut quarantines to prevent movement of wheat from areas in the
> Pacific Northwest where the disease occurs. It seems unlikely that
> relaxation of our external quarantine would have any impact.
>
> Because of these considerations, RE #4 is rated as **low**.
>
> RE #5: Environmental Impact
>
> Our assessment of the potential of each pest to cause environmental
> damage (FAO, 1996) considers the following factors:

-   Introduction of the pest is expected to cause significant, direct
    environmental impacts (*e.g.*, ecological disruptions, reduced
    biodiversity). When used within the context of the National
    Environmental Policy Act (NEPA), \"significant\" has a special
    meaning different from its use in a scientific or statistical
    context (*e.g.*, different from its use in the term \"statistically
    significant\"). As used by NEPA, significance is qualitative and
    encompasses both the likelihood and severity of an environmental
    impact.

-   Pest is expected to have direct impacts on species listed by Federal
    or State agencies as endangered, threatened, or candidate. "An
    example of a direct impact would be feeding on a listed plant"
    (USDA, 2000). If feeding trials have not been conducted with the
    listed organism and the pest, a pest will be expected to feed on the
    plant if it feeds on other species within the genus or other genera
    within the family.

-   Pest expected to have indirect impacts on species listed by Federal
    or State agencies as endangered, threatened, or candidate (*e.g.*,
    by disrupting sensitive, critical habitat).

-   Introduction of the pest would stimulate control programs including
    chemical pesticides.

-   Introduction of the pest would stimulate control programs including
    release of nonindigenous biological control agents.

High (3): Two or more of the above.

Medium (2): One of the above.

Low (1): None of the above. It is assumed that introduction of a
nonindigenous pest will have some environmental impact (*e.g.,* by
definition, introduction of a nonindigenous species generates
competition or displacement).

> **[Finding for RE \#]{.underline}5**
>
> There is no evidence to suggest that the foreign strains of *U.
> agropyri* would present any direct or indirect environmental impacts.
> All available evidence indicates that the current flag smut disease
> control measures will be adequate for any strains of *U. agropyri*,
> consequently no new control programs would be expected. The wheat
> isolates of the pathogen naturally infect only wheat (Mordue and
> Waller, 1981), so there is no reason to believe that foreign strains
> of *U. agropyri* will have any impact on any organisms described on
> the Federal list of endangered, threatened, or candidate species.
> Likewise, these foreign strains should not produce any negative
> effects on biodiversity on the United States.
>
> Consequently, RE #5 is rated as **low**.

  -----------------------------------------------------------------------

  -----------------------------------------------------------------------

> **C-b. Consequences of Introduction: Cumulative Risk Element Score**
>
> > We sum the ratings for the five RE's to produce an overall estimate
> > of the Consequences of Introduction Risk Rating. The Consequences of
> > Introduction Risk Rating are considered to be a biological indicator
> > of the potential of the pest to become established and spread, and
> > its potential to cause economic and environmental impacts. The
> > overall risk rating is used to assign a Consequences of Introduction
> > Risk Score as follows:

+-----------------------------------------------------------------------+
| > **Table 1. Risk: Consequences of Introduction (Sum RE #1-5)**       |
| >                                                                     |
| > Cumulative Risk Element Score Risk Rating                           |
|                                                                       |
|   ---------------------- ---------------------- --------------------- |
|   **5 \-- 7**            **8 \-- 11**           **12 \-- 15**         |
|                                                                       |
|   **Low**                **Medium**             **High**              |
|   ---------------------- ---------------------- --------------------- |
+-----------------------------------------------------------------------+

> The Cumulative Risk Element Score for *U. agropyri* for RE #1-5 is 7,
> which is equivalent to a **low** "Consequences of Introduction" risk
> rating.

+-----------------------------------------------------------------------+
| > **Table 2. *U. agropyri* Risk Rating: Consequences of               |
| > Introduction**                                                      |
|                                                                       |
| +------------+---------+--------+--------+-----------+----------+     |
| | Cl         | Host    | Dis    | Ec     | Envi      | #####    |     |
| | imate/Host | Range   | persal | onomic | ronmental | #### Ris |     |
| |            |         |        |        |           | k Rating |     |
| +------------+---------+--------+--------+-----------+----------+     |
| | Med (2)    | Low (1) | Med    | Low    | Low (1)   | **Low    |     |
| |            |         | (2)    | (1)    |           | (7)**    |     |
| +------------+---------+--------+--------+-----------+----------+     |
+-----------------------------------------------------------------------+

> **D. Likelihood of Introduction (Entry and Establishment)**
>
> The foreign strains of *U. agropyri* covered by this risk analysis are
> assumed to be capable of following the pathways of shipments of wheat,
> oats, and other agricultural commodities which may be admixed with
> wheat seed or debris. Spores of *U. agropyri* are known to be carried
> as contaminants on the surface of seeds or plant debris (Brown, et.
> al., 1994; Pollack, 1945). USDA pest interception records indicate
> that since 1985, *U. agropyri* was intercepted at least once on a
> wheat seed shipment.
>
> It is reasonable to assume agricultural commodities (such as grain for
> animal feed) will be utilized in a variety of habitats, some of which
> may actually encourage spore survival. For such surviving spores to
> cause disease, they will have to reach a suitable host plant before
> they lose viability due to physical and biological environmental
> conditions. The presence of the flag smut disease in the United States
> provides unequivocal evidence that the fungus, once introduced, can
> become established even if only in limited geographic areas. On the
> other hand, even in the absence of domestic quarantines restricting
> the movement of seed and grain, the flag smut disease has not spread
> from areas in the United States where the disease does occur. This is
> likely the consequence of either unfavorable environment or commonly
> employed agricultural practices unfavorable for disease establishment,
> or both. In summary, the likelihood that *U. agropyri* could enter as
> a seed or grain contaminant seems quite high, but establishment and
> persistence of the pathogen outside of areas where the disease already
> occurs seems unlikely, and "quarantine regulations have not controlled
> flag smut and are not necessary" (Line, 1998).
>
> **E. Assessment Conclusion: Risk Potential and Quarantine Status**
>
> A considerable body of published evidence indicates that there is
> physiological specialization within the wheat infecting strains of
> *Urocystis agropyri* (Ballantyne, 1996; El-Khadem, *et al.* 1980;
> Hafiz, 1951; Holton and Johnson, 1943; Johnson, 1959; Yu, *et al.*,
> 1945) although the validity of some studies has been called into
> question (Line, 1998). What is less clear is whether, in fact, foreign
> strains differ genetically in such a way as to increase their
> potential capacity for causing economic damage. An early study
> comparing U.S. and South African wheat isolates suggested the isolates
> did not differ in pathogenicity (the capability to cause disease),
> although the South African isolates appeared to be more virulent ( the
> degree of pathogenicity) (Verwoerd, 1929). More recent research
> comparing Australian and U.S. isolates suggested there were few if any
> differences (Brown, *et al.*, 1994). What the literature does seem to
> indicate is that resistance to the flag smut fungus, currently
> incorporated into many if not most of the wheat varieties grown in at
> risk areas, is durable and broad spectrum (Ballantyne, 1996; Line,
> 1998). In addition to resistant varieties, simple chemical and
> cultural control practices have been widely adopted to effectively
> eliminate flag smut as a disease of economic consequence in the United
> States (Purdy, 1965; Line, 1998).
>
> Given the data outlined in the preceding paragraph, there is no
> compelling evidence to indicate that the foreign strains will differ
> from strains already present in their pathogenic or economic impact on
> wheat production in the United States. With the resulting
> "consequences of introduction risk rating" of low, we find that
> foreign strains of *U. agropyri* do not satisfy the economic/
> environmental criteria as quarantine pests. Furthermore, APHIS finds
> that the foreign strains of *U. agropyri* described in the regulations
> may not satisfy the international geographic and regulatory criteria
> of quarantine pests. That is, according to available survey data and
> other relevant scientific information, this species is known to occur
> in the United States, and there appears to be little difference
> between domestic and foreign strains with respect to the plant pest
> risk which they pose. It is not clear that foreign strains differ
> genetically in such a way as to increase their potential capacity to
> cause economic damage. Thus, *Urocystis agropyri* fails to satisfy
> both the geographic/regulatory criteria and the economic criteria as a
> quarantine pest.
>
> **III. Risk Management and Decision on Quarantine Status**
>
> Categorization of these foreign strains of *U. agropyri* as quarantine
> pests is not supported by the available biological/ scientific
> information, international agreements on criteria for quarantine
> pests, the United States Acts cited in Section I.B., and existing USDA
> policies regarding quarantine pests. It appears that the circumstances
> under which the quarantine was established in 1919 no longer apply.
> Therefore, it is appropriate for APHIS to discontinue the quarantine
> of foreign strains of *U. agropyri*.
>
> USDA and its stakeholders will continue to collect scientific
> information concerning the biology (*e.g.*, host range, pathogenicity)
> of *U. agropyri* as well as the incidence and severity of flag smut of
> wheat both in the United States and overseas in the unlikely event
> that the current situation regarding flag smut changes, and APHIS
> would take corrective measures to protect US agriculture from *U.
> agropyri* .
>
> **IV. References**
>
> Ballantyne, B. 1996. Chapter 5. Flag Smut. In: R.D. Wilcoxson and E.E.
> Saari, eds. Bunt and Smut Diseases of Wheat: Concepts and Methods of
> Disease Management. CIMMYT, Mexico City.
>
> Brown, J., *et. al*. 1994**.** A Comparative Study of the
> characteristics of Australian and United States isolates of wheat flag
> smut. Agriculture Victoria , Victoria, Australia. 37 pp.
>
> El-Khadem, M., Omar, R.A., Kamel, .H., and Abou El-Naga, S.A. 1980.
> Physiologic and pathogenic races of *Urocystis agropyri.*
> Phytopathologische Zeitschrift 98: 203-209.
>
> EPPO. 1994. European and Mediterranean Plant Protection Organization
> (EPPO) Plant Quarantine Retrieval (PQR) System, version 3.0,
> computerized database. Information in the database originates from:
> [Smith, I. M. 1992.]{.underline} Quarantine Pests for Europe. Oxon,
> UK: CAB International, Paris: Published in association with the
> European and Mediterranean Plant Protection Organization.
>
> FAO. 1993. Global plant quarantine information system, Plant Pest Data
> Base, version 2.1. (Computerized Plant Pest Data Base of the Food and
> Agriculture Organization (FAO) of the United Nations). IPPC
> Secretariat FAO/AGPP Viale delle Terme di Caracalla. Rome.
>
> FAO. 1996. International Standards for Phytosanitary Measures. Part
> 1---Import Regulations: Guidelines for Pest Risk Analysis.
> Secretariate of the International Plant Protection Convention, Food
> and Agriculture Organization (FAO) of the United Nations. Rome, Italy.
>
> Fischer, G. W., and C. S. Holton. 1943. Studies of the susceptibility
> of forage grasses to cereal smut fungi. IV. Cross-inoculation
> experiments with *Urocystis tritici*, *U. occulta*, and *U. agropyri*.
> Phytopathology 33: 910 -- 921.
>
> Griffiths, M.A. 1924. Experiments with flag smut of wheat and the
> causal fungus, *Urocystis agropyri* Kcke. Journal of Agricultural
> Research 27: 425-449.
>
> Hafiz, A. 1951. Physiologic specialization in *Urocystis tritici*
> Koern. Phytopathology 41: 809-812.
>
> Holton, C.S. and Johnson, A.G. 1943. Physiological races in *Urocystis
> tritici*. Phytopathology 33: 169-171.
>
> Humphrey, H.B. and Johnson, A.G. 1919. Take-all and flag smut, two
> wheat diseases new to the United States. U.S. Dept. Agr. Farmer's
> Bull. 1063: 1-8.
>
> Johnson, A.G. 1959. Further studies of physiologic races in *Urocystis
> tritici*. Phytopathology 49: 299-302.
>
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>
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>
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>
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>
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>
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>
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>
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> United States. 275 pp.
>
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>
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>
> **V. Preparation, Consultation and Review**
>
> This pest risk analysis was prepared by the Animal and Plant Health
> Inspection Service (APHIS):
>
> Plant Protection and Quarantine (PPQ): Scientific Services (SS) and
> Plant Epidemiology and Risk Analysis Laboratory (PERAL):
>
> Prepared by:

D. Heron, Ph.D., Biotechnologist (SS)

> E.V. Podleckis, Ph.D., Plant Virologist (SS)
>
> and
>
> J. W. Smith, Ph. D., Entomologist (PERAL)
>
> S. C. Redlin, Ph. D., Plant Pathologist (PERAL)
>
> Consultation and review:
>
> **APHIS:**
>
> R. Bech, Chief Operations Manager, Scientific Services
>
> M. Firko, Senior Operations Manager, National Identification Services
>
> E. Imai, Senior Operations Manager, Commodity and Biological Risk
> Analysis
>
> M. Palm, National Mycologist, National Identification Services
>
> J. Petit de Mange, Director European and African Regions,
> Phytosanitary Issues Management Team
>
> S. Poe, Senior Staff Officer, Safeguarding and Pest Management
>
> Laura Redmond, Plant Pathologist, Scientific Services
>
> A. Tschanz, National Plant Germplasm Quarantine Center
>
> J. White, Plants Team Leader
>
> **ARS:**
>
> M. Bonde, Foreign Diseases and Weed Science Laboratory
>
> B. Goates, National Small Grains Germplasm Research Facility
>
> R. Line, USDA, ARS, Washington State University
>
> G. Peterson, Foreign Diseases and Weed Science Laboratory
>
> **External:**
>
> J. Frahm, U.S. Wheat Associates
>
> S. Johnson, National Plant Board