Invasive Species Compendium

Detailed coverage of invasive species threatening livelihoods and the environment worldwide

Datasheet

Urocystis agropyri
(flag smut of wheat)

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Datasheet

Urocystis agropyri (flag smut of wheat)

Summary

  • Last modified
  • 27 September 2018
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Natural Enemy
  • Preferred Scientific Name
  • Urocystis agropyri
  • Preferred Common Name
  • flag smut of wheat
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Fungi
  •     Phylum: Basidiomycota
  •       Subphylum: Ustilaginomycotina
  •         Class: Ustilaginomycetes
  • Summary of Invasiveness
  • U. agropyri causes flag smut on leaves of species in the family Poaceae. As a pathogen of grasses, it appears to have a wide host range (
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    Compendia
    CAB International
    Wallingford
    Oxfordshire
    OX10 8DE
    UK
    compend@cabi.org
  • Distribution map More information

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Pictures

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PictureTitleCaptionCopyright
Infected leaves of Agropyron repens, x2 (left). Spore balls x430 (right). CMI Descriptions of Pathogenic Fungi and Bacteria No. 716. CAB International, Wallingford, UK.
TitleSymptoms on leaves, and spore balls
CaptionInfected leaves of Agropyron repens, x2 (left). Spore balls x430 (right). CMI Descriptions of Pathogenic Fungi and Bacteria No. 716. CAB International, Wallingford, UK.
Copyright©CABI BioScience
Infected leaves of Agropyron repens, x2 (left). Spore balls x430 (right). CMI Descriptions of Pathogenic Fungi and Bacteria No. 716. CAB International, Wallingford, UK.
Symptoms on leaves, and spore ballsInfected leaves of Agropyron repens, x2 (left). Spore balls x430 (right). CMI Descriptions of Pathogenic Fungi and Bacteria No. 716. CAB International, Wallingford, UK.©CABI BioScience
Spore balls, surface ornamentation, x1100. CMI Descriptions of Pathogenic Fungi and Bacteria No. 716. CAB International, Wallingford, UK.
TitleSpore balls close up
CaptionSpore balls, surface ornamentation, x1100. CMI Descriptions of Pathogenic Fungi and Bacteria No. 716. CAB International, Wallingford, UK.
Copyright©CABI BioScience
Spore balls, surface ornamentation, x1100. CMI Descriptions of Pathogenic Fungi and Bacteria No. 716. CAB International, Wallingford, UK.
Spore balls close upSpore balls, surface ornamentation, x1100. CMI Descriptions of Pathogenic Fungi and Bacteria No. 716. CAB International, Wallingford, UK.©CABI BioScience
Flag smut symptoms on wheat.
TitleSymptoms on wheat
CaptionFlag smut symptoms on wheat.
CopyrightISU
Flag smut symptoms on wheat.
Symptoms on wheatFlag smut symptoms on wheat.ISU

Identity

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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

EPPO code

  • UROCAG (Urocystis agropyri)

Summary of Invasiveness

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U. agropyri causes flag smut on leaves of species in the family Poaceae. As a pathogen of grasses, it appears to have a wide host range (Mordue and Waller, 1981) and a worldwide distribution (UK CAB International, 1991). However, some authorities do not include the pathogen on wheat [Triticum aestivum], identified as Urocystis tritici, within U. agropyri. Rossman et al. (2006) place U. agropyri in the category of a “Threat to Major Crop Plants” and wheat and wheat straw imports are restricted in North America (Anon., 2005; CFIA, 2008). If the widespread species includes the wheat pathogen, then it is already present on all continents with agriculture and in major wheat-growing areas (Purdy, 1965), so it has already been introduced and may be difficult to exclude from additional areas. Both smuts are seed- and soil-borne, causing systemic infections that can be perennial in weeds and graminaceous crops, including turfgrasses. The spore balls are windborne (Purdy, 1965) and prevention of spread among wild grasses on land is not amenable to control.

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Fungi
  •         Phylum: Basidiomycota
  •             Subphylum: Ustilaginomycotina
  •                 Class: Ustilaginomycetes
  •                     Order: Urocystidiales
  •                         Family: Urocystidaceae
  •                             Genus: Urocystis
  •                                 Species: Urocystis agropyri

Notes on Taxonomy and Nomenclature

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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).

Description

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Sori commonly in leaves as narrow elongated blisters between the veins, covered by the epidermis when young, later ruptured to expose spore balls, splitting leaf to ribbons. Linear sori may also occur on the rachis, glumes and rhizomes of grasses.
 
Spore ball mass powdery, dark brown to black. Spore balls subspherical to oblong, 18-38 x 35-40 µm, composed of 1-5, usually 1-3, spores almost completely surrounded by sterile cells. Sterile cells hyaline to yellowish, sub-spherical to oblong, thin-walled, 3-12 µm diameter. Spores subglobose, slightly flattened, dark brown, smooth, 11-20 µm diameter, walls 1.5-2.0 µm.
 

Distribution

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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.

Distribution Table

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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.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

AfghanistanPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
AfghanistanPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
ChinaRestricted distributionIMI, 1991; UK CAB International, 1991; EPPO, 2014
-AnhuiPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-AnhuiPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-FujianPresentEPPO, 2014
-GansuPresentGuo, 2005; EPPO, 2014
-GuangxiPresentEPPO, 2014
-GuizhouPresentEPPO, 2014
-HebeiPresentEPPO, 2014
-HeilongjiangPresentEPPO, 2014
-HenanPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-HenanPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-HubeiPresentEPPO, 2014
-JiangsuPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-JiangsuPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-JiangxiPresentEPPO, 2014
-JilinPresentEPPO, 2014
-Nei MengguPresentEPPO, 2014
-NingxiaPresentGuo, 2005
-QinghaiPresentGuo, 2005; EPPO, 2014
-ShaanxiPresentEPPO, 2014
-ShandongPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-ShandongPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-ShanxiPresentEPPO, 2014
-SichuanPresentEPPO, 2014
-TibetPresentEPPO, 2014
-XinjiangPresentGuo, 2005; EPPO, 2014
-YunnanPresentEPPO, 2014
-ZhejiangPresentEPPO, 2014
IndiaRestricted distributionIMI, 1991; UK CAB International, 1991; EPPO, 2014
-BiharPresentGoel, 1991
-DelhiPresentBhatnagar et al., 1978
-HaryanaPresentSharma et al., 2005
-Himachal PradeshPresentBansandrai et al., 1993
-Indian PunjabPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-Indian PunjabPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-Jammu and KashmirPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-Jammu and KashmirPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-Madhya PradeshPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-Madhya PradeshPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-RajasthanPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-RajasthanPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-Uttar PradeshPresentBhatnagar et al., 1978
IranPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
IranPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
IraqPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
IraqPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
IsraelPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
IsraelPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
JapanPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
JapanPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-HonshuPresentBPI, US National Fungus Collections1896, 1899, 1946. On wheat, Tokyo & Nagano
KazakhstanPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
KazakhstanPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
Korea, DPRPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
Korea, DPRPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
Korea, Republic ofPresentEPPO, 2014
MongoliaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
MongoliaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
NepalPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
NepalPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
PakistanPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
PakistanPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
TaiwanPresentEPPO, 2014
TurkeyPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
TurkeyPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
UzbekistanPresentEPPO, 2014

Africa

AlgeriaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
AlgeriaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
EgyptPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
EgyptPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
LibyaPresentEl-Buni and Rattan, 1981
MoroccoPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
MoroccoPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
South AfricaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
South AfricaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
TunisiaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
TunisiaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014

North America

CanadaWidespreadIMI, 1991; UK CAB International, 1991; EPPO, 2014Not on wheat
-AlbertaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-AlbertaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-British ColumbiaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-British ColumbiaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-ManitobaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-ManitobaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-OntarioPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-OntarioPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-QuebecPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-QuebecPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
GreenlandPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
GreenlandPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
MexicoPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
MexicoPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
USAWidespreadIMI, 1991; UK CAB International, 1991; EPPO, 2014
-AlaskaPresentIMI, 1991; UK CAB International, 1991; McBeath et al., 2008; EPPO, 2014
-AlaskaPresentIMI, 1991; UK CAB International, 1991; McBeath et al., 2008; EPPO, 2014
-ArizonaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-ArizonaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-ArkansasPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-ArkansasPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-CaliforniaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-CaliforniaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-ColoradoPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-ColoradoPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-ConnecticutPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-ConnecticutPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-District of ColumbiaPresentIMI, 1991; UK CAB International, 1991
-District of ColumbiaPresentIMI, 1991; UK CAB International, 1991
-IdahoPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-IdahoPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-IllinoisPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-IllinoisPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-IndianaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-IndianaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-IowaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-IowaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-KansasPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-KansasPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-MarylandPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-MarylandPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-MassachusettsPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-MassachusettsPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-MichiganPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-MichiganPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-MinnesotaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-MinnesotaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-MississippiPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-MississippiPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-MissouriPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-MissouriPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-MontanaPresentMeiners and Fischer, 1957
-NebraskaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-NebraskaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-NevadaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-NevadaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-New HampshirePresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-New HampshirePresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-New MexicoPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-New MexicoPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-New YorkPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-New YorkPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-North DakotaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-North DakotaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-OklahomaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-OklahomaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-OregonPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-OregonPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-PennsylvaniaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-PennsylvaniaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-South DakotaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-South DakotaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-TennesseePresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-TennesseePresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-UtahPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-UtahPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-VermontPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-VermontPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-VirginiaPresentRoane and Roane, 1996
-WashingtonPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-WashingtonPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-West VirginiaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-West VirginiaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-WisconsinPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-WisconsinPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-WyomingPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-WyomingPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014

Central America and Caribbean

GuatemalaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
GuatemalaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014

South America

ArgentinaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
ArgentinaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
BoliviaPresentBPI, US National Fungus Collections1920. On Agropyron attenuatum
ChilePresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
ChilePresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
Falkland IslandsPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
Falkland IslandsPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
UruguayPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
UruguayPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
VenezuelaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
VenezuelaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014

Europe

Baltic statesPresentIMI, 1991; UK CAB International, 1991
Baltic statesPresentIMI, 1991; UK CAB International, 1991
BulgariaPresentIMI, 1991; UK CAB International, 1991; Denchev, 2001; EPPO, 2014
BulgariaPresentIMI, 1991; UK CAB International, 1991; Denchev, 2001; EPPO, 2014
CyprusPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
CyprusPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
Czech RepublicPresentDietrich Müller, 2001; EPPO, 2014
Czechoslovakia (former)PresentZundel, 1953; IMI, 1991; UK CAB International, 1991; EPPO, 2014
Czechoslovakia (former)PresentZundel, 1953; IMI, 1991; UK CAB International, 1991; EPPO, 2014
DenmarkPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
DenmarkPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
EstoniaPresentEPPO, 2014
FinlandPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
FinlandPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
FrancePresentIMI, 1991; UK CAB International, 1991; EPPO, 2014south
FrancePresentIMI, 1991; UK CAB International, 1991; EPPO, 2014south
GermanyAbsent, formerly presentIMI, 1991; UK CAB International, 1991; EPPO, 2014
GreecePresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
GreecePresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
HungaryPresent, few occurrencesIntroduced Invasive IMI, 1991; UK CAB International, 1991; EPPO, 2014
IrelandPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
IrelandPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
ItalyPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
ItalyPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
LatviaPresentEPPO, 2014
LithuaniaPresentEPPO, 2014
NetherlandsPresentEPPO, 2014
NorwayPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
NorwayPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
PolandPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
PolandPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
PortugalPresent, few occurrencesIMI, 1991; UK CAB International, 1991; EPPO, 2014
RomaniaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
RomaniaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
Russian FederationPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
Russian FederationPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-Eastern SiberiaPresentEPPO, 2014
-Russia (Europe)PresentEPPO, 2014
-SiberiaPresentIMI, 1991; UK CAB International, 1991
-SiberiaPresentIMI, 1991; UK CAB International, 1991
-Western SiberiaPresentEPPO, 2014
SpainPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
SpainPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
SwedenPresent, few occurrencesIntroduced Invasive IMI, 1991; UK CAB International, 1991; EPPO, 2014
SwitzerlandPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
SwitzerlandPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
UKPresent, few occurrencesIntroduced Invasive IMI, 1991; UK CAB International, 1991; Sansford et al., 1998; EPPO, 2014First reported on wheat in 1998
UkrainePresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
UkrainePresentIMI, 1991; UK CAB International, 1991; EPPO, 2014

Oceania

AustraliaWidespreadMurray and Brown, 1987; IMI, 1991; UK CAB International, 1991; EPPO, 2014
-Australian Northern TerritoryPresent, few occurrencesMurray and Brown, 1987
-New South WalesPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-New South WalesPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-QueenslandPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-QueenslandPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-South AustraliaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-South AustraliaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-TasmaniaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-TasmaniaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-VictoriaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-VictoriaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-Western AustraliaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
-Western AustraliaPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
New ZealandPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014
New ZealandPresentIMI, 1991; UK CAB International, 1991; EPPO, 2014

Introductions

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Introduced toIntroduced fromYearReasonIntroduced byEstablished in wild throughReferencesNotes
Natural reproductionContinuous restocking
Mexico Australia 1945 Food (pathway cause) Yes Alvarez (1976); Alvarz (1976); Borlaug et al. (1946) Grain intended for food was planted

Risk of Introduction

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Rossman et al. (2006) placed U. agropyri in the category “Threat to Major Crop Plants” of <_st13a_place _w3a_st="on">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 <_st13a_place _w3a_st="on"><_st13a_country-region _w3a_st="on">Mexico (Borlaug et al., 1946) may be successful.

PHYTOSANITARY RISK

Risk Criteria Category

Economic Importance Low
Distribution Worldwide
Seedborne Incidence Low
Seed Transmitted Yes
Seed Treatment Yes

Overall Risk Low

Habitat List

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CategoryHabitatPresenceStatus
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 Affected

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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 Affected

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Growth Stages

Top of page Flowering stage, Fruiting stage, Pre-emergence, Seedling stage, Vegetative growing stage

Symptoms

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Infected leaves and leaf sheaths exhibit white to yellow streaks that turn grey and then black. Sori then appear in vegetative parts, most commonly in the leaves, as narrow elongated blisters between the leaf veins, some extending almost the entire length of the leaf lamina. Young sori are covered by the host epidermis, which later ruptures to expose the spore mass, splitting the leaves into ribbons (Mordue and Waller, 1981).
 
The leaves may droop and be thin and stunted before sporulation occurs. Black streaks may also occur on the stem, which is stunted and dwarfed at the internodes. Infected wheat plants are thus stunted and spindly, often bearing more tillers than healthy plants, which gives them a grass-like appearance. The inflorescence is stunted, distorted, and frequently sterile, the rachis bearing black streaks at maturity. Spike development usually stops before the head emerges from the leaf whorl, so that infected plants do not produce seeds. In cereals, especially in resistant varieties, only some tillers may show symptoms (Purdy, 1965).
 
Symptoms on turfgrasses are described by Smiley et al. (2005) as stunting, yellowing in cool weather, and stiffening of leaves, with streaks turning from yellow-green to dark grey. After the sori mature and release spores, the leaves turn brown, dry up and die.

List of Symptoms/Signs

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SignLife StagesType
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 Ecology

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Fischer and Holton (1957) and Purdy (1965) summarized the life cycle, mode of penetration and spread, and ecological relationships of U. agropyri and Urocystis tritici, respectively.

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.

Ecology

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).

Climate

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ClimateStatusDescriptionRemark
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 Aspects

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Incidence

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).

Seed Transmission

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).

Seed Treatments

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

Asaad and Abang (2009) report the standard methods they used to assess the level of seed infection. Seed testing methods for the detection of fungi are presented by Mathur and Kongsdal (2003).

Pathway Causes

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CauseNotesLong DistanceLocalReferences
Seed tradewheat and grass seed Yes Yes Asaad and Abang, 2009; Richardson, 1990

Plant Trade

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Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility 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
Flowers/Inflorescences/Cones/Calyx

Impact Summary

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CategoryImpact
Economic/livelihood Negative

Economic Impact

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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 Factors

Top 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
Impact outcomes
  • Host damage
  • Negatively impacts agriculture
  • Negatively impacts livelihoods
Impact mechanisms
  • Pathogenic
Likelihood of entry/control
  • Highly likely to be transported internationally accidentally
  • Difficult to identify/detect as a commodity contaminant
  • Difficult to identify/detect in the field

Uses

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Ibrahim (2007) suggests that an isolate of U. agropyri from Lolium multiflorum might be used for the control of that weed in wheat [Triticum aestivum]. In tests in Saudi Arabia, infestation of the soil with the fungus reduced the effect of L. multiflorum, in wheat fields sown with the weed, from a yield loss of 71% to one of 50%. Sampson and Watson (1985) suggested that a quackgrass (Elymus repens) isolate, which was shown not to infect wheat, other cereals or grasses, might be considered for use in control of the weed in Canada. Quackgrass is also a noxious weed in the USA (USDA-ARS, 2009).

Diagnosis

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No sets of DNA sequences have been made publicly available to identify and distinguish U. agropyri from Urocystis tritici or other species of the genus on the same or different hosts. The one sequence for the LSU region of rDNA deposited in GenBank for U. agropyri, (NCBI, 2009) is related to the report by McBeath et al. (2008) of flag smut on Festuca rubra growing as a turfgrass.

Detection and Inspection

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The appearance of whitish or yellowish to dark-grey longitudinal stripes between the veins of the leaves, formed by the smut sori, at the fourth- to fifth-leaf stage (about 6-10 weeks after planting) is the first reliable indicator of U. agropyri infection in wheat. Another early diagnostic symptom in susceptible grass plants is a large number of thin, stunted leaves in which sporulation will occur later (Thirumalachar and Dickson, 1949). Microscopic examination of the sorus contents is required to determine whether spore balls, rather than single spores, are present.

Similarities to Other Species/Conditions

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Within the genus Urocystis, there are a number of named species that attack grasses in the subfamily Pooideae; they can be distinguished with difficulty, if at all, by morphology. As they are described by Vánky (1994) and Vánky and Shivas (2008), these include at least Urocystis bolivarii, Urocystis bromi, Urocystis dactyli,Urocystis hispanica, Urocystisocculta, Urocystis poae, and Urocystis triseti, as well as Urocystis tritici and U. agropyri. Diagnostic key and taxonomic separations of species often relate largely to the host genus, thus identification of the fungus species may rely on correct identification of the grass genus, or even species. Nevertheless, the reported host ranges of different Urocystis species may extend to the same genus. Both U. tritici (Fischer and Holton, 1943) and U. agropyri are pathogens of Elymus repens. Urocystis hispanica (Vánky, 1994) and U. tritici (Vánky, 2007) can both infect species in the genus Aegilops. Urocystisulei is the species described on Festuca spp. (Vánky, 1994), but McBeath et al. (2008) found the description of U. agropyri a better fit for an isolate from Festuca rubra. Nevertheless, a key difference used by Vánky (1994) to distinguish U. tritici from U. agropyri, at least in Europe, is the primary host genus. A subtle morphological character noted for U. agropyri is the ridged appearance of spore balls due to the collapse of the sterile cells with age (Vánky, 1994).
 
Some species of smuts in the genera Ustilago and Tilletia, including the common stripe smut, Ustilago striiformis, also occur on the leaves of grasses, but the spores are single rather than in balls with sterile cells (Vánky, 1994). In the field, flag smut and stripe smut can be differentiated fairly reliably by the more brownish colour of the sori in U. agropyri and its earlier appearance in spring (Thirumalachar and Dickson, 1949).
 
The stripe rust, Puccinia striiformis on wheat [Triticum aestivum], barley [Hordeum vulgare], rye [Secale cereale], and other grasses within its limited distribution might be confused with a smut when its linear dark telial pustules appear on leaf sheathes, but the teliospores remain in place in the pustule, rather than dispersing as a powdery mass (Wiese, 1987). At an earlier stage, the interveinal yellowing on leaf blades is followed by the appearance of linear yellow uredinia (Smiley et al., 2005), not black sori. However, to complicate the situation further, as reported by Purdy and Holton (1963), both fungi can attack the same plant and be present together in the same leaves.

Prevention and Control

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Prevention

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).
 
Eradication 
 
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.
 
Control
 
Cultural Control
 
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.
 
Host-Plant Resistance
 
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).
 
Chemical Control

 
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 Needs

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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. 

References

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Allan RE, 1976. Flag smut reaction in wheat: its genetic control and associations with other traits. Crop Science, 16(5):685-687

Alvarez MG, 1976. Primer catalogo de enfermedades de plantas Mexicanas. Fitofilo, 71:1-169.

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.

Anon., 2005. Foreign quarantine notices. United States Federal Register, 70. 8231-8233. [7 CFR Part 319.]

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

Ballantyne B, 1993. Reactions of wheat cultivars to flag smut in southern New South Wales. Australasian Plant Pathology, 22(3):100-104

Bansandrai AK; Sood AK; Sud AK, 1993. Prevalence of flag smut of wheat (Urocystis agropyri) in Himachal Pradesh. Plant Disease Research, 8(1):85.

Beniwal MS, 1992. Effect of flag smut on yield and yield components of wheat varieties. Crop Research (Hisar), 5(2):348-351

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