Urocystis agropyri (flag smut of wheat)
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- Risk of Introduction
- Habitat List
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Seedborne Aspects
- Pathway Causes
- Pathway Vectors
- Plant Trade
- Impact Summary
- Economic Impact
- Risk and Impact Factors
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Gaps in Knowledge/Research Needs
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Urocystis agropyri (Preuss) A.A. Fisch. Waldh. 1867
Preferred Common Name
- flag smut of wheat
Other Scientific Names
- Polycystis agropyri (Preuss) Schroet. 1877
- Tuburcinia agropyri-campestris Massenot 1955
- Tuburcinia occulta var. agropyri (Preuss) Ellis 1879
- Tuburcinia tritici (Körn.) Liro 1922
- Turbucinia agropyri (Preuss) Liro 1922
- Uredo agropyri Preuss 1848
- Urocystis agropyri (Preuss) Schroet. 1869
- Urocystis agropyri-campestris (Massenot) H. Zogg 1986
- Urocystis preussii J.G. Kuhn 1874
- Urocystis tritici Körnicke 1877
International Common Names
- English: flag smut; leaf smut; stem smut; stripe smut
- Spanish: carbon de las hojas de la grama; carbon de las hojas del trigo; carbon del trigo; carbon foliar del trigo
- French: charbon des feuilles du blé; charbon des feuilles du chiendent; charbon du blé; charbon foliaire du blé
Local Common Names
- Germany: Brand, Blattstreifen-: Weizen; Brand, Stengel-: Weizen; Brand, Stengelstreifen-: Weizen
- India: patton ki kungi
- UROCAG (Urocystis agropyri)
Summary of InvasivenessTop of page
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Fungi
- Phylum: Basidiomycota
- Subphylum: Ustilaginomycotina
- Class: Ustilaginomycetes
- Order: Urocystidiales
- Family: Urocystidaceae
- Genus: Urocystis
- Species: Urocystis agropyri
Notes on Taxonomy and NomenclatureTop of page
U. agropyri was the name given to a smut on leaves of weedy grasses, including Elymus (Agropyron) repens (Vánky, 1994). Wolff (1873) identified the fungus causing flag smut of wheat [Triticum aestivum] in Australia as the species Urocystis occulta (Wallr.) Rabenh ex Fuckel found on rye [Secale cereale] a few years earlier. Körnicke (1877) studied the spore morphology of this fungus on the Australian plants and determined that it differed from U. occulta sufficiently to warrant the introduction of the name Urocystis tritici. Subsequently, Fischer (1943), on the basis of morphology, and Fischer and Holton (1943), on the basis of the results of cross-inoculation tests, suggested that U. tritici was synonymous with U. agropyri. This species concept is in agreement with the general one for smut fungi proposed by Fischer and Shaw (1953). On the basis of variability in U. agropyri and U. tritici, Savile (1953) stated that it was impossible to disagree with Fischer's wide species concept. Because the epithet “agropyri" has priority over “tritici”, the correct name for the fungus, then, is that of the fungus described on grasses. Nevertheless, the name Urocystis agropyri (Preuss) Schroet., as used by Fischer and subsequently by others, is incorrect due to a misdesignation of the type (USDA/SMML, 2005); the authority should be cited as (Preuss) A.A. Fisch. Waldh. Other workers have differed from Fischer and treated the flag smut of wheat and that of grasses as separate species (Purdy, 1965; Vánky, 1994; Denchev, 2001; Vánky, 2007; Vánky and Shivas, 2008).
DescriptionTop of page
DistributionTop of page
Urocystis tritici was first observed on wheat [Triticum aestivum], an introduced Eurasian crop, in Australia in the mid-nineteenth century (McAlpine, 1910), whereas U. agropyri was described somewhat earlier in Germany (Vánky, 1994). U. agropyri has been reported as the flag smut on wheat (Triticum spp.) and other Poaceae from many countries on all inhabited continents (UK CAB International, 1991). As a seedborne and soilborne pathogen, it is endemic in localized areas where soil temperature and moisture are favourable for teliospore germination and subsequent infection of susceptible hosts. Line (1998) notes that the environmental conditions and agronomic practices favourable to the pathogen on wheat, only occur in limited parts of the world, and those only include some wheat-growing areas. In some countries from which it has been reported, such as Canada (Sansford et al., 1999), U. agropyri may be known only on grasses and not on wheat. Although it was already familiar as a species on Agropyron species (Sampson, 1940), the flag smut fungus was not reported on wheat in the UK until 1998 (Sansford et al., 1998).
Reports on the occurrence of either species, particularly on grass hosts, may vary in accuracy depending on the reporter’s ability to separate smut species on the basis of small morphological differences and to determine the identity of the host grasses.
According to the NPPO of Argentina, U. agropyri is no longer present in Argentina (SENASA, 2020. Communication to CABI. SENASA-Argentina, Buenos Aires, Argentina). A literature survey of the pest and consultation with plant pathologists at the National Institute of Agricultural Technology (INTA), Argentina, has established that U. agropyri has not been reported in the country for more than 40 years.
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.Last updated: 23 Apr 2020
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Algeria||Present||UK, CAB International (1991); EPPO (2020)|
|Egypt||Present||UK, CAB International (1991); EPPO (2020)|
|Libya||Present||El-Buni and Rattan (1981)|
|Morocco||Present||UK, CAB International (1991); EPPO (2020)|
|South Africa||Present||UK, CAB International (1991); EPPO (2020)|
|Tunisia||Present||UK, CAB International (1991); EPPO (2020)|
|Afghanistan||Present||UK, CAB International (1991); EPPO (2020)|
|China||Present, Localized||EPPO (2020); UK, CAB International (1991);|
|-Anhui||Present||UK, CAB International (1991); EPPO (2020)|
|-Gansu||Present||EPPO (2020); Guo (2005)|
|-Henan||Present||UK, CAB International (1991); EPPO (2020)|
|-Inner Mongolia||Present||EPPO (2020)|
|-Jiangsu||Present||UK, CAB International (1991); EPPO (2020)|
|-Qinghai||Present||EPPO (2020); Guo (2005)|
|-Shandong||Present||UK, CAB International (1991); EPPO (2020)|
|-Xinjiang||Present||EPPO (2020); Guo (2005)|
|India||Present, Localized||EPPO (2020); UK, CAB International (1991);|
|-Bihar||Present||CABI (Undated)||Original citation: Goel (1991)|
|-Delhi||Present||Bhatnagar et al. (1978)|
|-Haryana||Present||Sharma et al. (2005)|
|-Himachal Pradesh||Present||Bansandrai et al. (1993)|
|-Jammu and Kashmir||Present||UK, CAB International (1991); EPPO (2020)|
|-Madhya Pradesh||Present||UK, CAB International (1991); EPPO (2020)|
|-Punjab||Present||UK, CAB International (1991); EPPO (2020)|
|-Rajasthan||Present||UK, CAB International (1991); EPPO (2020)|
|-Uttar Pradesh||Present||Bhatnagar et al. (1978)|
|Iran||Present||UK, CAB International (1991); EPPO (2020)|
|Iraq||Present||UK, CAB International (1991); EPPO (2020)|
|Israel||Present||UK, CAB International (1991); EPPO (2020)|
|Japan||Present||UK, CAB International (1991); EPPO (2020)|
|-Honshu||Present||BPI (US National Fungus Collections) (2009)||1896, 1899, 1946. On wheat, Tokyo & Nagano|
|Kazakhstan||Present||UK, CAB International (1991); EPPO (2020)|
|Mongolia||Present||UK, CAB International (1991); EPPO (2020)|
|Nepal||Present||UK, CAB International (1991); EPPO (2020)|
|North Korea||Present||UK, CAB International (1991); EPPO (2020)|
|Pakistan||Present||UK, CAB International (1991); EPPO (2020)|
|South Korea||Present||EPPO (2020)|
|Turkey||Present||UK, CAB International (1991); EPPO (2020)|
|Bulgaria||Present||UK, CAB International (1991); Denchev (2001); EPPO (2020)|
|Cyprus||Present||UK, CAB International (1991); EPPO (2020)|
|Czechia||Present||CABI (Undated); EPPO (2020)||Original citation: Dietrich Müller (2001)|
|Czechoslovakia||Present||UK, CAB International (1991); Zundel (1953); EPPO (2014)|
|Denmark||Present||UK, CAB International (1991); EPPO (2020)|
|Finland||Present||UK, CAB International (1991); EPPO (2020)|
|France||Present||UK, CAB International (1991); EPPO (2020)||south|
|Germany||Absent, Formerly present||EPPO (2020); UK, CAB International (1991);|
|Greece||Present||UK, CAB International (1991); EPPO (2020)|
|Hungary||Present, Few occurrences||Introduced||Invasive||UK, CAB International (1991); EPPO (2020)|
|Ireland||Present||UK, CAB International (1991); EPPO (2020)|
|Italy||Present||UK, CAB International (1991); EPPO (2020)|
|Norway||Present||UK, CAB International (1991); EPPO (2020)|
|Poland||Present||UK, CAB International (1991); EPPO (2020)|
|Portugal||Present, Few occurrences||EPPO (2020); UK, CAB International (1991);|
|Romania||Present||UK, CAB International (1991); EPPO (2020)|
|Russia||Present||UK, CAB International (1991); EPPO (2020)|
|-Eastern Siberia||Present||EPPO (2020)|
|-Russia (Europe)||Present||EPPO (2020)|
|-Siberia||Present||UK, CAB International (1991);|
|-Western Siberia||Present||EPPO (2020)|
|Serbia and Montenegro||Present||EPPO (2020)|
|Spain||Present||UK, CAB International (1991); EPPO (2020)|
|Sweden||Present, Few occurrences||Introduced||Invasive||UK, CAB International (1991); EPPO (2020)|
|Switzerland||Present||UK, CAB International (1991); EPPO (2020)|
|Ukraine||Present||UK, CAB International (1991); EPPO (2020)|
|United Kingdom||Present, Few occurrences||Introduced||Invasive||UK, CAB International (1991); Sansford et al. (1998); EPPO (2020)||First reported on wheat in 1998|
|Canada||Present, Widespread||UK, CAB International (1991); EPPO (2020)||Not on wheat|
|-Alberta||Present||UK, CAB International (1991); EPPO (2020)|
|-British Columbia||Present||UK, CAB International (1991); EPPO (2020)|
|-Manitoba||Present||UK, CAB International (1991); EPPO (2020)|
|-Ontario||Present||UK, CAB International (1991); EPPO (2020)|
|-Quebec||Present||UK, CAB International (1991); EPPO (2020)|
|Greenland||Present||UK, CAB International (1991); EPPO (2020)|
|Guatemala||Present||UK, CAB International (1991); EPPO (2020)|
|Mexico||Present||UK, CAB International (1991); EPPO (2020)|
|United States||Present, Widespread||UK, CAB International (1991); EPPO (2020)|
|-Alaska||Present||UK, CAB International (1991); McBeath et al. (2008); EPPO (2020)|
|-Arizona||Present||UK, CAB International (1991); EPPO (2020)|
|-Arkansas||Present||UK, CAB International (1991); EPPO (2020)|
|-California||Present||UK, CAB International (1991); EPPO (2020)|
|-Colorado||Present||UK, CAB International (1991); EPPO (2020)|
|-Connecticut||Present||UK, CAB International (1991); EPPO (2020)|
|-District of Columbia||Present||UK, CAB International (1991);|
|-Idaho||Present||UK, CAB International (1991); EPPO (2020)|
|-Illinois||Present||UK, CAB International (1991); EPPO (2020)|
|-Indiana||Present||UK, CAB International (1991); EPPO (2020)|
|-Iowa||Present||UK, CAB International (1991); EPPO (2020)|
|-Kansas||Present||UK, CAB International (1991); EPPO (2020)|
|-Maryland||Present||UK, CAB International (1991); EPPO (2020)|
|-Massachusetts||Present||UK, CAB International (1991); EPPO (2020)|
|-Michigan||Present||UK, CAB International (1991); EPPO (2020)|
|-Minnesota||Present||UK, CAB International (1991); EPPO (2020)|
|-Mississippi||Present||UK, CAB International (1991); EPPO (2020)|
|-Missouri||Present||UK, CAB International (1991); EPPO (2020)|
|-Montana||Present||Meiners and Fischer (1957)|
|-Nebraska||Present||UK, CAB International (1991); EPPO (2020)|
|-Nevada||Present||UK, CAB International (1991); EPPO (2020)|
|-New Hampshire||Present||UK, CAB International (1991); EPPO (2020)|
|-New Mexico||Present||UK, CAB International (1991); EPPO (2020)|
|-New York||Present||UK, CAB International (1991); EPPO (2020)|
|-North Dakota||Present||UK, CAB International (1991); EPPO (2020)|
|-Oklahoma||Present||UK, CAB International (1991); EPPO (2020)|
|-Oregon||Present||UK, CAB International (1991); EPPO (2020)|
|-Pennsylvania||Present||UK, CAB International (1991); EPPO (2020)|
|-South Dakota||Present||UK, CAB International (1991); EPPO (2020)|
|-Tennessee||Present||UK, CAB International (1991); EPPO (2020)|
|-Utah||Present||UK, CAB International (1991); EPPO (2020)|
|-Vermont||Present||UK, CAB International (1991); EPPO (2020)|
|-Virginia||Present||Roane and Roane (1996)|
|-Washington||Present||UK, CAB International (1991); EPPO (2020)|
|-West Virginia||Present||UK, CAB International (1991); EPPO (2020)|
|-Wisconsin||Present||UK, CAB International (1991); EPPO (2020)|
|-Wyoming||Present||UK, CAB International (1991); EPPO (2020)|
|Australia||Present, Widespread||EPPO (2020); Murray and Brown (1987); UK, CAB International (1991);|
|-New South Wales||Present||UK, CAB International (1991); EPPO (2020)|
|-Northern Territory||Present, Few occurrences||Murray and Brown (1987)|
|-Queensland||Present||UK, CAB International (1991); EPPO (2020)|
|-South Australia||Present||UK, CAB International (1991); EPPO (2020)|
|-Tasmania||Present||UK, CAB International (1991); EPPO (2020)|
|-Victoria||Present||UK, CAB International (1991); EPPO (2020)|
|-Western Australia||Present||UK, CAB International (1991); EPPO (2020)|
|New Zealand||Present||UK, CAB International (1991); EPPO (2020)|
|Argentina||Absent, Formerly present||SENASA (2020); UK, CAB International (1991); EPPO (2020)|
|Bolivia||Present||BPI (US National Fungus Collections) (2009)||1920. On Agropyron attenuatum|
|Chile||Present||UK, CAB International (1991); EPPO (2020)|
|Falkland Islands||Present||UK, CAB International (1991); EPPO (2020)|
|Uruguay||Present||UK, CAB International (1991); EPPO (2020)|
|Venezuela||Present||UK, CAB International (1991); EPPO (2020)|
IntroductionsTop of page
Risk of IntroductionTop of page
Rossman et al. (2006) placed U. agropyri in the category “Threat to Major Crop Plants” of North America. In contrast, neither U. agropyri nor Urocystis tritici appear as an invasive species in the ISSG database (ISSG, 2009). To a large extent, the risk of introduction of the smut depends on the taxonomy, that is, whether flag smut of wheat [Triticum aestivum] and some grasses is truly the same species as flag smut of other grasses. The risk to significant crops is from the “wheat isolates” of U. agropyri, otherwise known as U. tritici. If U. tritici is the same as the widely reported U. agropyri, U. agropyri is already present on all continents with wheat-growing areas (Purdy, 1965), and it may be difficult to exclude from additional areas due to its host range inclusive of many wild grasses. Purdy (1965) lists species of Aegilops, Agropyron, Elymus and Hordeum as having been determined by inoculation to be hosts of the wheat pathogen. U. agropyri in the restricted sense, as its host range is understood (Sampson and Watson, 1985; Vánky, 1994), is not a threat to cereals. Both smuts are seed and soil borne, causing systemic infections that can be perennial in weedy grasses, forage grasses or turfgrasses that are not grown as annuals. The spore balls are windborne (Purdy, 1965), but larger and presumably heavier, and so slower to spread than the single spores of other grass pathogens; local quarantines such as those imposed after an introduction in Mexico (Borlaug et al., 1946) may be successful.
Risk Criteria Category
Economic Importance Low
Seedborne Incidence Low
Seed Transmitted Yes
Seed Treatment Yes
Overall Risk Low
Habitat ListTop of page
|Terrestrial – Managed||Cultivated / agricultural land||Present, no further details||Harmful (pest or invasive)|
|Managed grasslands (grazing systems)||Present, no further details||Harmful (pest or invasive)|
|Terrestrial ‑ Natural / Semi-natural||Natural grasslands||Present, no further details||Natural|
Hosts/Species AffectedTop of page
Plants are initially attacked by U. agropyri at pre-emergence when seedlings are less than 10 mm long. Plants are affected from seedling stage to maturity. Under a wide and primarily morphological species concept for smut fungi (Fischer and Shaw, 1953), a large number of species in the grass subfamily Pooideae, in addition to the Triticum species, are reported to be attacked by U. agropyri in nature (Fischer, 1953; Zundel, 1953; Purdy, 1965; Duran, 1968; Hodges, 1970). Nevertheless, individual isolates show marked host specialization, and most wheat isolates will not infect other grass species (Mordue and Waller, 1981). Fischer and Holton (1943) found that some isolates from wheat in the USA differed in their ability to infect Agropyron and Elymus species. Currently, in Australia, grasses are not considered an important source of inoculum for flag smut on wheat (Vánky and Shivas, 2008). Despite the apparent host specialization, the following grass hosts have been successfully infected in artificial inoculation tests (Purdy, 1965) using isolates from wheat [Triticum aestivum]: Agropyron caninum [Elymus caninus]; Agropyron dasystachyum [Elymus lanceolatus]; Agropyrondesertorum; Agropyron elongatum [Thinopyrum elongatum]; Agropyron semicostatum; and Aegilops squarrosa. Rees and Platz (1973) obtained infection from a wheat isolate to Agropyron scabrum [Elymus scaber] and from that grass back to wheat. Conversely, Sampson and Watson (1985), using four inoculation methods, could not obtain infection by U. agropyri isolated from Agropyron repens [Elymus repens] in Canada on 47 other grasses, including A. dasystachyum, A. elongatum, several other Elymus species, and three cultivars of wheat.
Host Plants and Other Plants AffectedTop of page
|Aegilops triuncialis var. triuncialis||Poaceae||Wild host|
|Agrostis capillaris (common bent)||Poaceae||Wild host|
|Agrostis stolonifera var. palustris (bent grass)||Poaceae||Wild host|
|Avena sativa (oats)||Poaceae||Wild host|
|Bromus carinatus (California brome grass)||Poaceae||Wild host|
|Bromus marginatus (Mountain brome(grass))||Poaceae||Wild host|
|Calamagrostis canadensis||Wild host|
|Carex (sedges)||Cyperaceae||Wild host|
|Dactylis glomerata (cocksfoot)||Poaceae||Wild host|
|Elymus repens (quackgrass)||Poaceae||Wild host|
|Elymus smithii (Colorado bluestem)||Poaceae||Wild host|
|Festuca rubra (red fescue)||Poaceae||Other|
|Glyceria (mannagrass)||Poaceae||Wild host|
|Holcus (softgrasses)||Poaceae||Wild host|
|Hordeum (barleys)||Poaceae||Wild host|
|Lolium (ryegrasses)||Poaceae||Wild host|
|Lolium multiflorum (Italian ryegrass)||Poaceae||Wild host|
|Lolium perenne (perennial ryegrass)||Poaceae||Other|
|Phleum pratense (timothy grass)||Poaceae||Wild host|
|Poa (meadow grass)||Poaceae||Other|
|Poa pratensis (smooth meadow-grass)||Poaceae||Other|
|Thinopyrum elongatum||Poaceae||Wild host|
|Triticum aestivum (wheat)||Poaceae||Main|
|Triticum dicoccum||Poaceae||Wild host|
|Triticum turgidum (durum wheat)||Poaceae||Main|
Growth StagesTop of page Flowering stage, Fruiting stage, Pre-emergence, Seedling stage, Vegetative growing stage
SymptomsTop of page
List of Symptoms/SignsTop of page
|Inflorescence / discoloration panicle|
|Leaves / abnormal forms|
|Leaves / fungal growth|
|Leaves / leaves rolled or folded|
|Seeds / empty grains|
|Seeds / shrivelled|
|Stems / stunting or rosetting|
|Stems / witches broom|
|Vegetative organs / surface lesions or discoloration|
Biology and EcologyTop of page
Life Cycle and Transmission
The fungus is either 'seedborne' from spore balls containing teliospores that contaminate the seed surface or 'soilborne' from spore balls in the soil. Systemic mycelium may overwinter in infected wheat [Triticum aestivum] seedlings or survive continuously in crowns, rhizomes, leaves, etc., of perennial grasses (Smiley et al., 2005).
U. agropyri belongs to the 'seedling-infecting' group of smut fungi. Infection occurs before seedling emergence from the soil. Teliospores germinate to produce sporidia that fuse to form infection hyphae that infect young coleoptiles of hosts. Temperatures between 10 and 20°C, and moist soil favour the infection of wheat (Purdy, 1965).
According to Takahashi and Iwata (1964), hyphae penetrate through the epidermal cell walls of the coleoptile. After infection, the fungus grows both inter- and intra-cellularly until it begins to sporulate, initially in the leaf blades and then in the leaf sheath and all the other above-ground plant parts. Sporulation begins with the 'rounding up' of mycelial elements between the vascular tissue and the epidermis. These mycelial aggregations produce thick-walled teliospores and surrounding sterile cells. The sori containing the spore balls first appear as white streaks on the leaf at 6-10 weeks after planting and later change colour through grey to black. Infected plants may fail to produce seeds or have malformed inflorescences due to the pathogen’s growth and sporulation.
At harvest, sori on wheat plants are broken by drying out and the harvesting operations; spore balls are released and infest seeds and soil. The life cycle is completed when spores from one crop germinate and infect the developing seedlings of a new crop. Spores may be transported for long distances with seeds, on straw, or on farm machinery (Line, 1998). The smut spores can survive for 4 years in the soil and for up to 10 years under conditions of ideal seed storage (Neergaard, 1977). They are also able to survive passage through farm animals into manure (McAlpine, 1910).
According to El-Khadem et al. (1980), U. agropyri from wheat is heterothallic; monosporidial cultures did not form clamp connections. Only two different mating types were found among the monosporidial cultures, and successful matings formed dikaryotic infection hyphae and then teliospores.
Spore germination and infection by U. agropyri in the pre-emergence stage of plant development is influenced to a considerable degree by plant exudates (Goel and Jhooty, 1987), other ecological factors (e.g. soil moisture, soil temperature, soil pH) and also by cultural practices such as planting date, seed depth and genetic resistance of the host variety (Purdy, 1965). The incidence of disease caused by U. agropyri is therefore highly variable in individual fields and agroclimatic zones in the same or different seasons.
In Australia, flag smut posed a serious threat to wheat in the 1920s, but with the release of several resistant cultivars its incidence rapidly declined. With widespread cultivation of susceptible wheat, there was a resurgence of the flag smut problem (cf. Platz and Rees, 1980). The release and use of the susceptible wheat cultivar, Rosella, resulted in the spread of flag smut in New South Wales (Ballantyne, 1993). In the Pacific North-West region of the USA, damage and distribution of flag smut increased after the adoption of deep seeding in early autumn planting and the release of several susceptible wheat cultivars between 1955 and 1971. However, renewed attention to the use of resistant varieties later mitigated the problem (Allan, 1976).
In India, the incidence of flag smut in wheat is limited to some north-western states such as Haryana, Himachal Pradesh, Indian Punjab and Rajasthan, because adequate summer rainfall and favourable soil temperatures needed for spore germination and subsequent infection by U. agropyri do not occur in other wheat-growing regions (Goel and Jhooty, 1985b).
ClimateTop of page
|BS - Steppe climate||Preferred||> 430mm and < 860mm annual precipitation|
|BW - Desert climate||Preferred||< 430mm annual precipitation|
|Cf - Warm temperate climate, wet all year||Preferred||Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year|
|Cs - Warm temperate climate with dry summer||Preferred||Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers|
|Dw - Continental climate with dry winter||Preferred||Continental climate with dry winter (Warm average temp. > 10°C, coldest month < 0°C, dry winters)|
Seedborne AspectsTop of page
Seed lots of Agrostis spp., Elymus spp., Festuca spp., Hordeum vulgare (barley), Poa spp., Triticum aestivum (wheat) and other Triticum spp. can be contaminated with teliospores or spore balls of U. agropyri, released from infected leaves or plant parts (Neergaard, 1977; Richardson, 1990). These propagules can remain viable for several years (Purdy, 1965). Asaad and Abang (2009) report that, in more than 50,000 cereal seeds received from 41 countries and tested by the International Center for Agricultural Research in the Dry Areas (ICARDA) between 1995 and 2004, 0.02% of wheat and barley seeds were found to be infected with U.agropyri.
Effect on Seed Quality
The pathogen is a seed-surface contaminant and has not been reported as having any adverse effect on wheat seed appearance or germination. Seed inoculations with U. agropyri were reported to reduce germination of Poa pratensis seeds (Hodges, 1970).
It has been suggested that the development of flag smut in Australia in the nineteenth century and in the USA in the early twentieth century could be attributed to the introduction of the fungus on contaminated seeds (McAlpine, 1910; Purdy, 1965). Epidemiological knowledge of the pathogen suggests that this could well have happened. Seed infestation with dry teliospores of U. agropyri has been shown to be sufficient for creating an artificial epidemic of flag smut for reliable screening of wheat germplasm (Rewal et al., 1986). Flag smut incidence increases with an increase in inoculum load applied to the seeds (Goel and Jhooty, 1989). Seed inoculations of Poa pratensis resulted in coleoptile infection, followed by adult plant infection (Hodges, 1970). Fischer and Holton (1957) classified flag smut of wheat as a 'seedling-infecting smut'. Infection occurring in the pre-emergence phase of seedling growth originates either from seedborne inoculum (i.e. from the spores that contaminate the seed surface) or from soilborne inoculum (i.e. from the spores in the soil).
Quarantine regulations were issued in the early twentieth century in the USA to prevent further spread of the disease from the region where infested seed had been used (Anon., 1919; 1925; Purdy, 1965). Similar schemes are in operation in Belgium, the Netherlands, Germany, the UK and many other countries (Neergaard, 1977).
Copper carbonate was the first dry treatment used to control flag smut of wheat (Fischer and Holton, 1957). Effective control of flag smut of wheat originating from both seedborne and soilborne inoculum was achieved through seed treatment with quintozene (Yasu and Yoshino, 1963). With the advent of systemic fungicides, effective disease control without a marked reduction in seedling survival was obtained with benomyl, carboxin and oxycarboxin seed treatments (Metcalfe and Brown, 1969).
Current products for dry seed dressings include non-systemics such as copper carbonate and organomercurials. Systemics such as carboxin and oxycarboxin are also used (Neergaard, 1977). In addition, fenfuram, triadimefon, triadimenol and tebuconazole provide control of U. agropyri in the Indian subcontinent (Goel and Jhooty, 1985a; Tariq et al., 1992). Seed treatment with tebuconazole at 1.0, 1.5 and 2.0 g kg-1, or carboxin and carbendazim at 2.0 and 2.5 g kg-1 seeds reduced disease incidence in wheat (Kumar and Singh, 2004), as will tetramethyl thiuram disulphide (Thiram 75% DS) at 3 g/kg seed, thiophanate methyl (Topsin-M 70WP) at 1 and 2 g/kg seed, or a combination of tetramethyl thiuram disulphide and carboxin (Shekhawat et al., 2011). Flag smut of wheat has ceased to be a problem in the regions where seed treatment with systemics is routine practice for its control.
An alternative is solar energy treatment, which is practical in seasonally hot regions, such as the north-western plains of India. Seeds are soaked in water (1:1 w/v) in a galvanised tub which is tightly covered with a transparent polythene sheet and placed under the sun. Duhan and Beniwal (2004) placed such a tub under the sun in India for 6 hours (08.00-14.00) during September, and found that this gave more than 96% of loose smut.
Seed Health Tests
Pathway CausesTop of page
Pathway VectorsTop of page
Plant TradeTop of page
|Plant parts liable to carry the pest in trade/transport||Pest stages||Borne internally||Borne externally||Visibility of pest or symptoms|
|Bulbs/Tubers/Corms/Rhizomes||hyphae||Yes||Pest or symptoms not visible to the naked eye but usually visible under light microscope|
|Growing medium accompanying plants||Yes||Pest or symptoms not visible to the naked eye but usually visible under light microscope|
|Leaves||hyphae; spores||Yes||Yes||Pest or symptoms usually visible to the naked eye|
|Seedlings/Micropropagated plants||hyphae||Yes||Pest or symptoms not visible to the naked eye but usually visible under light microscope|
|Stems (above ground)/Shoots/Trunks/Branches||hyphae||Yes||Yes||Pest or symptoms usually visible to the naked eye|
|True seeds (inc. grain)||spores||Yes||Pest or symptoms not visible to the naked eye but usually visible under light microscope|
|Plant parts not known to carry the pest in trade/transport|
Impact SummaryTop of page
Economic ImpactTop of page
Reduced yield is the most significant reflection of losses due to U. agropyri in wheat [Triticum aestivum]. Infected plants usually represent a complete loss in yield (Purdy, 1965); the percentages of infected plants reported in commercial fields might therefore be regarded as a reliable measure of the economic importance of flag smut, either locally or regionally. Generally, losses from U. agropyri are discussed in terms of individual fields or localized areas of infection. Thus, although the economic impact of the disease on a region may be relatively small, the losses might be very significant to a farmer whose own crop is infected by flag smut. Losses of up to 100% are possible (Purdy, 1965).
It is difficult to evaluate the economic losses caused by U. agropyri in other grasses. However, Nus and Hodges (1990) reported that in Poa pratensis cv. Merion, flag smut infection decreased rhizome growth and increased tiller growth.
In general, plants infected with U. agropyri are more susceptible to drought and other adverse conditions (Smiley et al., 2005). Thus there is an indirect, as well as a direct, loss of stand, resulting in significant damage to turf or losses in pasturage.
In the USA in the early 1960s, flag smut of wheat occurred in Klickitat, Walla Walla and Yakima counties of Washington State, and in Wasco and Umatilla counties of Oregon, where the incidence varied from trace levels to about 30% (Purdy and Allan, 1967). According to Nelson and Duran (1984), this disease was destructive in localized areas in south-central and south-eastern Washington. Wiese (1987) reports that flag smut of wheat once reduced yield by an average of 1% in the western USA, with individual losses ranging up to 50%.
In pre-partition Punjab (India), flag smut was reported to cause an annual loss of 15,000 tonnes of wheat (Wattspadwick, 1948). It was later recorded in a severe form in Himachal Pradesh (Singh and Sethi, 1975) and Rajasthan (Bhatnagar et al., 1978).
Beniwal (1992) reported 23-65% yield losses from flag smut infection in nine commercial wheat cultivars in the Indian state of Haryana. Tillering was reduced by 15-45%, plant height by 37-62%, earhead length by 28-46% and 1000 grain weight by 19-37%.
Risk and Impact FactorsTop of page Invasiveness
- Invasive in its native range
- Proved invasive outside its native range
- Has a broad native range
- Highly adaptable to different environments
- Long lived
- Has high reproductive potential
- Has propagules that can remain viable for more than one year
- Reproduces asexually
- Host damage
- Negatively impacts agriculture
- Negatively impacts livelihoods
- Highly likely to be transported internationally accidentally
- Difficult to identify/detect as a commodity contaminant
- Difficult to identify/detect in the field
UsesTop of page
DiagnosisTop of page
Detection and InspectionTop of page
Similarities to Other Species/ConditionsTop of page
Prevention and ControlTop of page
Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.
U. agropyri is soilborne and externally seedborne. Therefore, in the past, quarantine regulations on the movement of infested seed, chaff and farm machinery from endemic areas were established to restrict its spread (Anon., 1919; 1925; 1931; 1935; 1946; 1953; 1955). However, quarantine restrictions have been gradually lifted or relaxed because U. agropyri has now been reported from many agroclimatic regions worldwide (UK CAB International, 1991). Line (1998) argues that quarantines were, and are, not necessary for the control of flag smut of wheat [Triticum aestivum], because seed treatment, the use of resistant cultivars, and appropriate cultural methods can control the disease. Nevertheless, in Canada, where the fungus does not occur on wheat (Sansford et al., 1999), restrictions on importation of wheat from parts of the USA and from countries worldwide where “wheat strains” of U. agropyri occur are maintained (CFIA, 2008). The USA maintains quarantine measures on various articles of wheat or those made from wheat, such as seeds, plants, straw, etc., which may carry “foreign strains” of the flag smut pathogen that could be introduced (Anon., 2005).
Sufficiently long cycles of crop rotation may result in eradication of inoculum in the soil, but the smut spore balls are known to persist for several years (Purdy, 1965). Repeated planting of resistant varieties may have the same local effect; Purdy (1965) attributes the decline or disappearance of flag smut on wheat from parts of the USA to the use of resistant varieties.
Cultural practices and sanitary methods that tend to reduce inoculum, such as rotation with non-hosts, early fallow with thorough working of the soil, and burning stubble, are quite useful. Nevertheless, as Wiese (1987) indicates, spore balls are capable of surviving in soil for at least 3 years, so shorter rotations or fallow periods may only reduce the soilborne inoculum to some extent. Manipulation of planting time and depth, to conserve soil moisture and avoid soil temperatures that are favourable for spore germination and subsequent infection, can also be effective in disease control in specific areas. However, such measures may not be profitable because they may result in lower yields (Purdy, 1965). The disease is favoured when practices such as deep planting, shallow tillage and early-autumn planting are followed in areas where soil moisture is a limiting factor for wheat production (Line, 1998).
In Egypt, the 'afir method' of planting wheat is better than the 'herati method' (Jones and El Nasr, 1938) for control of flag smut in endemic areas. In the afir method, seed is planted in dry soils that are later irrigated, so that the inoculum is 'dormant' while seedlings are at a susceptible stage, whereas in "herati", seed is planted in moist soil, where spore inoculum is able to germinate and infect seedlings.
In Australia, Greenhalgh and Brown (1984) found that the incidence of flag smut was higher at -126 kPa than at -37 kPa; however, it was generally unaffected by the depth of sowing.
Although the effects of fertilizers on flag smut of wheat are complicated (Purdy, 1965), increased levels of nitrogen are known to favour the disease in turfgrasses (Smiley et al., 2005). In India, Kumar and Singh (2004) found that higher levels of nitrogen and phosphorus fertilizer, as well as the addition of poultry manure to the soil, reduced the level of the disease in wheat, although not to the low level obtained with seed treatments.
Among all the cereal smuts, U. agropyri has shown the least tendency towards pathogenic specialization (Fischer and Holton, 1957). According to Hafiz (1986), only six races were reported, in all, from different countries. Some peculiar features in the life cycle of this fungus (e.g. production of fewer sporidia compared to related smut fungi, the absence of secondary sporidia, and sporidial fusions in situ) are probably responsible for limiting its variability (Nelson and Duran, 1984). As a consequence, resistance to flag smut has remained effective in Australia and elsewhere (Platz and Rees, 1980; Goel, 1992) and new races have not been detected (Line, 1998). Purdy (1965) and Line (1998) attribute disappearance of flag smut as a problem on wheat in parts of the USA primarily to the use of resistant varieties.
According to Johnson (1984), there is no evidence of genotype-specific pathogenicity of the type indicating a gene-for-gene relationship. Therefore, the incorporation of resistance into commercial cultivars offers prospects for continued effective disease management (Goel, 1992).
Effective control of flag smut of wheat originating from both seedborne and soilborne inoculum was achieved through seed treatment with quintozene (Yasu and Yoshino, 1963). With the advent of systemic fungicides, effective disease control without a marked reduction in seedling survival was obtained with benomyl, carboxin and oxycarboxin seed treatments (Metcalfe and Brown, 1969).
Dry seed-dressing with non-systemics such as copper carbonate, and systemics such as carboxin, oxycarboxin and pyracarbolid have also been used (Neergaard, 1977). In addition, fenfuram, triadimefon, triadimenol and tebuconazole provide control of U. agropyri in the Indian subcontinent (Goel and Jhooty, 1985a; Tariq et al., 1992).
Flag smut of wheat has ceased to be a problem in the regions where seed treatment with systemics is a routine practice for the control of this disease and for loose smut (Ustilago tritici). As Loughman (1989) states concerning flag smut on wheat in Australia, seed treatment may be applied, not so much for the resulting increase in yield (of susceptible varieties), as to prevent an increase in the fungus population in the soil. A reduction in the use of seed treatment with fungicide is considered to be one factor in the increase of flag smut in the Near East and North Africa (Mamluk, 1998). The fungus readily produces significant amounts of long-lived inoculum from a small number of infected plants.
Gaps in Knowledge/Research NeedsTop of page
The question of the number of distinct Urocystis species on Pooid grasses and cereals should be resolved by the use of molecular techniques, with the resulting data made publicly available for diagnostic purposes. Cross-inoculation tests of wheat [Triticum aestivum] and agriculturally important weedy grasses with molecularly characterized isolates from those species should clarify the possible or potential role of grasses in the epidemiology and spread of flag smut on wheat.
ReferencesTop of page
Anon., 1919. Federal Horticultural Board, United States Department of Agriculture, Quarantine on account of flag smut and take-all diseases. Notice of quarantine No. 39 (with regulations). United States Department of Agriculture, Service and Regulatory Announcements, 64:77-79.
Anon., 1925. Quarantine on account of the flag smut disease. Notice of quarantine No. 59. United States Department of Agriculture, Federal Horticultural Board leaflet.
Anon., 1931. Legislative and administrative measures, Mexico. International Bulletin of Plant Protection, 5:122-123.
Anon., 1935. List of insect pests and diseases prohibited by external quarantine legislation from importation into the USSR. USSR People's Commissariat Agriculture Section internal and external. Plant Quarantine, 2, Moscow
Anon., 1946. Plant Quarantine Import Restrictions, Iran. Service and Regulatory Announcements, Bureau of Entomology and Plant Protection, United States Department of Agriculture, 168:51-54.
Anon., 1953. Plant Quarantine Announcement 1953, Food and Agriculture Organization of the United Nations. FAO Plant Protection Bulletin, 1:158-159.
Anon., 1955. Plant Quarantine Announcements, Food and Agriculture Organization of the United Nations. FAO Plant Protection Bulletin, 3:110-111.
Asaad S, Abang MM, 2009. Seed-borne pathogens detected in consignments of cereal seeds received by the International Center for Agricultural Research in the Dry Areas (ICARDA), Syria. International Journal of Pest Management, 55(1):69-77. http://journalsonline.tandf.co.uk/link.asp?id=100665
BPI (US National Fungus Collections), 2009. Fungal Databases - Specimens. Beltsville, USA: Systematic Mycology and Microbiology Laboratory, Agricultural Research Service, USDA. www.nt.ars-grin.gov/fungaldatabases/specimens/specimens.cfm
Duran R, 1968. Subterranean sporulation by two graminicolous smut fungi. Phytopathology, 58:390
EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm
Fischer GW, 1943. Some evident synonymous relationships in certain graminicolous smut fungi. Mycologia, 35:610-619
Fischer GW, 1953. Manual of the North American Smut Fungi. New York, USA: The Ronald Press Company
Fischer GW, Holton CS, 1943. Studies on 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
Fischer GW, Holton CS, 1957. Biology and control of the smut fungi. New York, USA: The Ronald Press Company
Fischer GW, Shaw CG, 1953. A proposed species concept in the smut fungi with application to North American species. Phytopathology, 43:181-188
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Hodges CF, 1970. Comparative morphology and development of Poa pratensis infected by Ustilago striiformis and Urocystis agropyri. Phytopathology, 60:1794-1797
Hori S, 1907. Seed infection by smut fungus of cereals. Imperial Central Agricultural Experiment Station Bulletin, Japan, 1:163-176
Humphrey HB, Johnson AG, 1919. Take all and flag smut, two wheat diseases new to the United States. Farmers' Bulletin, 1063. USA: US Department of Agriculture
Johnson R, 1984. A critical analysis of durable resistance. Annual Review of Phytopathology, 22:309-330
Jones GH, El Nasr A El GS, 1938. Control of four smut diseases by regulation of planting method under irrigation. Nature, 142:917-918
Körnicke FA, 1877. Mykologische beitrage. Hedwigia, 16:33-40
Line RF, 1998. Quarantines for the control of flag smut of wheat: are they effective or necessary? In: Bunts and smuts of wheat: an international symposium. Raleigh, North Carolina, August 17-20, 1997 [ed. by Malik, V. S.\Mathre, D. E.]. Ottawa, Canada: North American Plant Protection Organization, 49-60
Liro JI, 1934. Mycotheca Fennica. Die Etiketten Nos. 1-300. Helsingfors, Finland: Institute für Phytopathologie, University Helsinkiensis
Metcalfe PB, Brown JF, 1969. Evaluation of nine fungicides in controlling flag smut of wheat. Plant Disease Reporter, 53:631-633
Purdy LH, 1965. Flag smut of wheat. Botanical Reviews, 31:565-606
Purdy LH, Allan RE, 1967. Heritability of flag smut resistance in three wheat crosses. Phytopathology, 57:324-325
Rossman AY, Britton K, Luster D, Palm M, Royer MH, Sherald J, 2006. Evaluating the threat posed by fungi on the APHIS List of Regulated Plant Pests. Plant Health Progress, May:1-3. http://www.plantmanagementnetwork.org/php/
Savile DBO, 1953. Notes on boreal Ustilaginales. Canadian Journal of Botany, 31:663-674
Takahashi K, Iwata Y, 1964. The mode of infection of flag smut fungus on wheat varieties differing in resistance. Annals of Phytopathological Society of Japan, 29:149-154
Thirumalachar MJ, Dickson JG, 1949. Chlamydospore germination, nuclear life cycle and artificial culture of Urocystis agropyri on Red Top. Phytopathology, 39:333-339
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USDA-ARS, 2009. Germplasm Resources Information Network (GRIN). Online Database. Beltsville, Maryland, USA: National Germplasm Resources Laboratory. https://npgsweb.ars-grin.gov/gringlobal/taxon/taxonomysearch.aspx
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Yasu M, Yoshino M, 1963. Studies on the ecology of the flag smut of wheat and its control. Saitama Agricultural Experiment Station, Japan Research Bulletin, 20:1-34
Zundel GL, 1953. The Ustilaginales of the World. Pennsylvania State College, School of Agriculture, Contribution No. 176. Pennsylvania, USA: Pennsylvania State College
BPI (US National Fungus Collections), 2009. Fungal Databases - Specimens., Beltsville, USA: Systematic Mycology and Microbiology Laboratory, Agricultural Research Service, USDA. http://www.nt.ars-grin.gov/fungaldatabases/specimens/specimens.cfm
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10/09/09 Updated by:
Distribution MapsTop of page
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