Urocystis agropyri
(flag smut of wheat)

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.

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.

PHYTOSANITARY RISK

Risk Criteria Category

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

Overall Risk Low

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.

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).

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).

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.

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.

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. 

10/09/09 Updated by: