Tilletia controversa (dwarf bunt of wheat)
- 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
- Plant Trade
- Detection and Inspection
- Prevention and Control
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Tilletia controversa J. G. Kühn
Preferred Common Name
- dwarf bunt of wheat
Other Scientific Names
- Tilletia brevifaciens G. W. Fisch.
- Tilletia tritici-anifican F. Wagner (nom.inval.)
International Common Names
- English: dwarf: rye bunt; dwarf: wheat bunt
- Spanish: caries enana del trigo
- French: carie naine du blé; carie naine du seigle
Local Common Names
- Germany: Zwerg-: Roggen Brand; Zwerg-: Weizen Brand; Zwergstein-: Roggen Brand; Zwergstein-: Weizen Brand; Zwergsteinbrand
- TILLCO (Tilletia controversa)
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Fungi
- Phylum: Basidiomycota
- Subphylum: Ustilaginomycotina
- Class: Ustilaginomycetes
- Subclass: Exobasidiomycetidae
- Order: Tilletiales
- Family: Tilletiaceae
- Genus: Tilletia
- Species: Tilletia controversa
Notes on Taxonomy and NomenclatureTop of page
In a review of current literature, Mathre (1996) found evidence that three bunt pathogens, T. controversa, T. caries and T. foetida, are variants of a single species.
DescriptionTop of page
Teliospores are yellow-brown to red-brown (mature spores mostly much darker), globose or subglobose, mostly 19-24 µm (17-32 µm) diameter, mature spores are typically surrounded by a hyaline gelatinous sheath 1.5-5.5 µm thick. In median view, the exospore is reticulate, with relatively large, regular, polygonal areolae, 1.5-3 µm high and 3.5 µm diameter; areolae are occasionally irregular to subcerebriform.
Sterile cells are fewer and generally smaller than the spores, regularly globose, with smooth walls, hyaline or faintly greenish or brownish, sometimes encased in a hyaline, gelatinous sheath 2-4 µm thick; mostly 11-16 µm (9-22 µm) in diameter, including the sheath. For more information, see Duran and Fischer (1961).
DistributionTop of page
A record of T. controversa in Argentina (CABI/EPPO, 2012; EPPO, 2014) published in previous versions of the Compendium was based on original sources that are old or refer to in vitro trials. T. controversa has not been found in the wheat-growing region of Argentina in more than 30 years of surveys conducted by Instituto Fitotécnico Santa Catalina, and the environmental conditions in Argentina are not suitable for the establishment of the pathogen (M Astiz Gasso, Instituto Fitotécnico Santa Catalina, Argentina, personal communication, 2019).
See also CABI/EPPO (1998, No. 245).
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 Nov 2020
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Morocco||Absent, Unconfirmed presence record(s)|
|Azerbaijan||Absent, Unconfirmed presence record(s)|
|France||Absent, Formerly present|
|Lithuania||Absent, Intercepted only|
|Portugal||Absent, Intercepted only|
|Serbia||Absent, Unconfirmed presence record(s)|
|Spain||Absent, Invalid presence record(s)|
|-Alberta||Absent, Invalid presence record(s)|
|United States||Present, Localized|
|-California||Absent, Invalid presence record(s)|
|Australia||Absent, Invalid presence record(s)|
|-New South Wales||Absent, Invalid presence record(s)|
|-South Australia||Absent, Invalid presence record(s)|
|-Western Australia||Absent, Invalid presence record(s)||Original citation: Biosecurity Australia, 2010, personal communication|
|New Zealand||Absent, Unconfirmed presence record(s)|
|Argentina||Absent, Formerly present||M Astiz Gasso, Instituto Fitotécnico Santa Catalina, Argentina, personal communication, 2019|
|Uruguay||Absent, Invalid presence record(s)|
Risk of IntroductionTop of page
ECONOMIC IMPORTANCE Moderate
SEEDBORNE INCIDENCE Low
SEED TRANSMITTED Yes
SEED TREATMENT Yes
Notes on Phytosanitary Risk
None of 552 samples examined in 1983 had dwarf bunt infestation levels <1 g of teliospores/kg seed (equivalent to 20,000 teliospores/seed) necessary to result in bunted spikes when the seed is planted. Therefore, in areas where this disease is not known to occur, there seems to be minimal risk that the importation of US-produced wheat grain with low levels of infestation will result in significant disease development (Grey et al., 1986).
Very probably, T. controversa has reached the limits of its natural distribution in the EPPO region (Wagner, 1966). However, its introduction into areas where it does not occur would certainly create difficulties for the export of grain to other continents, even if direct damage was slight.
Since the main mode of dispersal is by seeds, seed crops of wheat from countries where the fungus occurs should be examined during the growing season and found free from T. controversa (OEPP/EPPO, 1990).
Habitat ListTop of page
|Terrestrial||Managed||Cultivated / agricultural land||Principal habitat||Harmful (pest or invasive)|
Hosts/Species AffectedTop of page
Occasionally other Poaceae (68 species) are attacked, such as Aegilops spp., Agropyron spp., Alopecurus myosuroides, Alopecurus agrestis, Arrhenatherum elatius, Bromus spp., Dactylis glomerata, Elymus spp., Festuca spp., Hordeum bulbosum, Hordeum leporinum, Hordeum vulgare, Koeleria macrantha, Lolium spp., Poa spp. and rye (see also Hardison et al., 1959).
Host Plants and Other Plants AffectedTop of page
Growth StagesTop of page
SymptomsTop of page
An infected plant shows no obvious sign of disease until the ears emerge, but its stem is usually shorter than in healthy plants and it may have more tillers. Bunted ears are somewhat narrower than healthy ones, but, as ripening proceeds, the glumes are pushed apart laterally so giving them a characteristic dishevelled appearance. Sori are spherical (elliptical in common bunt - T. caries) and contain a blackish powdery mass of teliospores surrounded by a thick grey-brown tegument. For more information, see Grassner and Niemann (1954), Baylis (1958), Purdy et al. (1963), Rapilly et al. (1966).
List of Symptoms/SignsTop of page
|Inflorescence / black fungal spores|
|Whole plant / dwarfing|
|Whole plant / unusual odour|
Biology and EcologyTop of page
In grass crops, infection is apparently confined to the secondary stem buds of grass seeded the previous spring. Lack of infection in grass plants over 1 year old is correlated with the absence of stem buds from many species during the winter/spring infection period and associated with the extensive development of basal leaves which protect the buds (Hordison, 1963).
Infection of winter wheat by T. controversa does not occur during seed germination to seedling emergence, but only after the seedling is well established. Following penetration, mycelium passes into the crown and keeps pace with the growth of the apex until the ear is formed. A smut ball (sorus) containing teliospores then forms in the ovaries.
A number of races differing in pathogenicity exist and continue to be distinguished (at least 15 in the northwestern USA alone; Hoffmann and Metzger, 1976). For more information, see Grassner and Niemann (1954), Baylis (1958), Tyler and Jensen (1958), Purdy et al. (1963).
The pathogen is mainly dispersed on infected wheat and grass seed, However, dispersal with soil or manure might be possible.
Seedborne AspectsTop of page
In a survey of 552 samples of wheat of for export from Pacific Northwest ports in 1983, 141 were free from T. controversa. The remaining samples, representing all classes of wheat, contained dwarf bunt teliospores, but none of these seed lots was heavily infested i.e. contained >1 g of teliospores/kg seed (equivalent to 20,000 teliospores/seed) (Grey et al., 1986).
Bechtel et al. (1999) showed that a high percentage of spores can be removed from wheat by mechanical cleaning but that it is not feasible to remove all of them.
Effect on Seed Quality
Teliospores released from sori adhere to the seed resulting in discolouration, due to blackening of the kernels, and a typical fishy odour of trimethylamine. The usefulness of the kernels for milling is reduced. Pirson (1978) estimated that 5 mg of bunt balls could contain as many as 1 million spores.
Spores adhering to the seed can contaminate uninfested soil and, under suitable conditions, germinate and penetrate the emerging seedling where infection becomes systemic (Neergaard, 1977). Field tests were conducted in five states of the USA over 2 years to determine if seedborne T. controversa teliospores could induce disease. Bunted spikes resulted only when heavily infested seed (>1 g teliospores/kg) was planted in disease-conducive locations (Grey et al., 1986).
The incidence of T. controversa as a function of inoculum density was studied at three disease-conducive locations in Montana, USA, for three seasons (1993-1996) (Goates and Peterson, 1999). In soil-inoculated plots, a minimum of 16 x 10³ teliospores/row was needed to cause trace amounts of disease (0.6% maximum). Only trace amounts or no disease occurred below the 16 x 10<(sup)5> rate. In the seed-inoculated plots, infection was rare and occurred only at inoculation rates of 2 x 10<(sup)5> teliospores/g or higher, with the highest disease incidence being 0.4%.
In a test of 22 formulations of fungicidal seed treatments, thiabendazole provided the highest level of control (Hoffman et al., 1983). Mathre et al. (1990) found that infection of healthy seed was reduced when seeds were treated with formulations containing carboxin or thiabendazole. All teliospores of T. controversa were destroyed when 0.13 M NaOCl was applied at 55°C for 30 seconds (Chastain, 1991). Although these seed treatments provide a means to control the spread of the disease to uninfected areas, Fushtey (1961) found that it was not effective in protecting the crop from infection by soilborne inoculum. The first completely effective control of the dwarf bunt fungus in susceptible wheat varieties was achieved with difenoconazole in 1994 (Sitton et al., 1993).
Treatment of winter wheat (Triticum aestivum) seeds with Dividend XL RTA (difenoconazole+metalaxyl-M), Vitaflo-280 (carbathiin+thiram), or bioagent ACM941, a strain of Clonostachys rosea, all significantly reduced seedborne instances of T. controversa. Dividend XL RTA was the most effective treatment, reducing pathogen instance by 98-99% relative to the control (Xue et al., 2007).
It has been suggested that although treatment in a chemosterilizer, that produces hydrogen peroxide vapour by a pulse-injection system, has insufficient activity for quarantine purposes if sori are present, it may be a practical seed-surface disinfestation process for nonhost seeds, such as barley, where contaminating teliospores from grain handling equipment are borne superficially on seed, and sori are rarely or not present (Smilanick et al., 1994).
Seed Health Tests
Wash method (Kietriber 1984).
- A quantity of seed is agitated in water to which a small amount of detergent has been added.
- The resultant suspension is decanted, centrifuged and resuspended.
- The resuspension is then either (a) filtered through a cellulose nitrate membrane which is then air dried, and examined under a microscope; or (b) placed on a haemocytometer and examined under a microscope.
- Spores of T. controversa are identified and counted.
PCR - Multiple Tilletia spp. (McDonald et al., 1999)
A simple technique of conducting PCR on single ungerminated teliospores of Tilletia species was developed. Teliospores were manually cracked under a stereo microscope prior to adding to the PCR reaction mixture. Amplification product was obtained using primers for either a portion of the nuclear ribosomal intergenic spacer region or a portion of the mitochondrial DNA. Collections of teliospores from T. indica, T. barclayana, T. controversa, T. tritici, T. laevis and an unidentified Tilletia sp. from Lolium varied in the proportion of spores from which amplification product could be detected, with the success rate ranging from 100 to 10%. This technique avoids the difficulty and time delay in having to germinate teliospores prior to extracting DNA from a mycelial matte and thus will be of great value in the application of PCR methods for regulatory testing and phylogenetic studies of Tilletia species.
Extracting spores T. controversa from bran (Zhang et al., 2002)
Methods of extracting spores of T. controversa from bran were studied. Three methods 'sieving-alpha-amylase degradation', 'sieving-density gradient centrifugation' and 'sieving-alpha-amylase degradation-density gradient centrifugation' were used to extract the spores. The number of T. controversa spores extracted depended on the use of sieving, alpha-amylase and density gradient centrifugation while the purity mainly on the density gradient centrifugation. Between 84 and 94% of bran could be removed by the method of double-layer gauze and five different combinations of sieving treatments. Between 95 and 99% of bran could be removed and 19 to 52% of T. controversa spores could be extracted by the method of sieving-alpha-amylase degradation. Using the sieving-density gradient centrifugation method, only a treatment of 60 meshes + 200 meshes + 300 meshes + 30 µm + 11 µm worked so that 7.2% pure spores were obtained after further density gradient centrifugation, which did not influence the reticulum height, autofluorescence and germination of spores. Using the sieving-alpha-amylase degradation-density gradient centrifugation method, a treatment of 60 meshes + 200 meshes + 300 meshes and 60 meshes + 200 meshes + 300 meshes + 30 µm + 11 µm was effective, and 18.8 and 12.2% of pure spores were obtained after further density gradient centrifugation, which did not influence the reticulum height of spores. The most effective condition for alpha-amylase to degrade insoluble starches was at 71°C and 350 r/min for 3 mins. These methods have been extensively applied in routine quarantine at ports.
Extraction of TCK spores from soil
A sucrose-centrifugation method was developed to extract teliospores of T. indica, T. controversa and T. barclayana from soil (Babadoost and Mathre, 1998).
Notes on methods
Where positive identification cannot be made from spore morphology alone, biological tests (spore germination on inoculation to differential hosts) may be necessary. Spores can be distinguished from those of Tilletia caries by fluorescence microscopy (Stockwell, 1986).
A rapid biochemical test was developed to indirectly assess the viability of teliospores of T. controversa that contaminate wheat grain. Lipase activity was detected consistently in extracts from viable teliospores by a fluorescein diacetate (FDA) assay (Chastain and King, 1990).
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|
|Flowers/Inflorescences/Cones/Calyx||hyphae; spores||Yes||Yes||Pest or symptoms usually visible to the naked eye|
|Stems (above ground)/Shoots/Trunks/Branches||hyphae||Yes||Pest or symptoms usually invisible|
|True seeds (inc. grain)||hyphae; spores||Yes||Yes||Pest or symptoms usually invisible|
|Plant parts not known to carry the pest in trade/transport|
|Fruits (inc. pods)|
ImpactTop of page
The possibility for establishment of T. controversa in winter wheat regions in China was assessed by simulation models and geographical information system (GIS) by Chen et al (2002). The winter wheat regions were divided into four areas, high, medium, low and basically no risk areas. In the high risk area, T. controversa occurs over nine times every eighteen years; the medium risk area, four to eight times every eighteen years; and the low risk area, one to three times every eighteen years. The percentage of areas with high and medium risk is 19.3% of the whole winter wheat regions of the country.
In Italy, epidemic outbreaks of dwarf bunt were reported in 1879, 1919, 1929 and 1946; however, in 1956, the disease was reported not to cause great concern. In Bavaria (Germany), up to 30% losses in wheat yield were recorded on crops grown more than once in a rotation of 5-6 years. In the 1970s, the disease was reported to be of great economic importance in the EPPO region in Austria, Poland and the former USSR and of less economic importance in the other countries in which it is established.
While the dwarf bunt fungus only affects a small portion of the total wheat production worldwide, presence of this disease has heightened economic importance due to the possibility of spread of the disease to uninfected areas (Mathre, 1996).
DiagnosisTop of page
T. controversa was identified in wheat plants using PCR (Kochanová et al., 2004). Both Yuan et al. (2009) and Nian et al. (2009) developed a TaqMan real-time PCR to successfully detect T. controversa in asymptomatic wheat tissue. Gao et al. (2010) designed specific primers using sequence characterised amplified region (SCAR) for use in PCR detection assays.
A different method of diagnosis, using amplified fragment length polymorphism (AFLP), is detailed in Liu et al. (2009). Alternatively, Cai et al. (2009) successfully diagnosed the pathogen during early stages of infestation in wheat using the hyper-branched rolling cycle amplification (HRCA).
Image analysis using disease micrographs has also been used to identify T. controversa (Deng et al., 2012). Overall recognition accuracy using this method was 82.9%.
Detection and InspectionTop of page
Teliospores are produced in large quantities when Tilletia controversa is grown at 15-18°C on a wheat-based medium. Vegetative hyphae of T. carries and T. controversa were not distinguishable on this media (Trione, 1974). For more information on the culture of T. controversa see Trione et al. (1989) or Trione (1964, 1974).
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.Host-Plant Resistance
Varietal resistance is the primary means of control. Several resistant wheat cultivars are available including Weston, Hansel and Winridge (Taylor et al., 1983; Johnsson, 1988).
Fungicides applied to the soil surface give control but are uneconomic (Hordison, 1963). Systemic fungicides have been used, for example, etaconazole has been used to provide good control after disease establishment in the plant (Hoffmann, 1971; Hoffman et al., 1983). Experiments in Sweden showed that seed treatments, in combination with the use of resistant cultivars, suppressed disease by up to 99.6% (Johnsson, 1991a). In a test of 22 formulations of fungicidal seed treatments, thiabendazole provided the highest level of control (Hoffman et al., 1983). Mathre et al. (1990) found that the infection of healthy seed was reduced when seeds were treated with formulations containing carboxin or thiabendazole. All teliospores of T. controversa are destroyed when 0.13 M of NaOCl are applied at 55°C for 30 s (Chastain, 1991). Although these seed treatments provide a means to control the spread of the disease to uninfected areas, Fushtey (1961) found that they were not effective in protecting the crop from infection by soil-borne inoculum. The first completely effective control of the dwarf bunt fungus in susceptible wheat varieties was achieved with difenoconazole in 1994 (Sitton et al., 1993).
ReferencesTop of page
Astiz Gasso, M., 2019. M Astiz Gasso, Instituto Fitotécnico Santa Catalina, Argentina, personal communication.
Baylis RJ, 1958. Studies of Tilletia contraversa, the cause of dwarf bunt of winter wheat. Canadian Journal of Botany, 36:17-32
Bechtel DB, Wilson JD, Eustace WD, Behnke KC, Whitaker T, Peterson GL, Sauer DB, 1999. Fate of dwarf bunt fungus teliospores during milling of wheat into flour. Cereal Chemistry, 76(2):270-275; 19 ref
Brennan J, Murray G, 1988. Australian wheat diseases - assessing their economic importance. Agricultural Science, 1(7):26-35
Brown JF, 1975. Diseases of wheat - their incidence and control. Australian field crops. Volume 1: wheat and other temperate cerals [ed. by Lazenby, A.\Matheson, E. M.]. Sydney, New South Wales, Australia: Angus and Robertson., 304-363
Cai Jun, Yin YouPing, Ge JianJun, Chen HongJun, Huang GuanJun, Zhang WenDi, Wang ZhongKang, 2009. Detection of Tilletia controversa with HRCA approach. Scientia Agricultura Sinica, 42(10):3493-3500. http://www.ChinaAgriSci.com
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Hardison JR, Meiners JP, Hoffmann JA, Waldher JT, 1959. Susceptibility of Graminae to Tilletia contraversa. Mycologica, 51:656-664
Hoffmann JA, 1971. Control of common and dwarf bunt of wheat with systemic fungicides. Plant Disease Reporter, 55:1132-1135
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Smilanick JL, Hartsell PL, Denis-Arrue R, Henson DJ, McKinney JD, Tebbets JC, Goates BJ, 1992. Survival of common and dwarf bunt teliospores and intact sori after fumigation of high and low moisture content winter wheat. Plant Disease, 76(3):293-296
Taylor GA, McGuire CF, Stewart VR, Dubbs AL, Baldridge DE, Kushnak GD, Bergmann JW, Mathre DE, Sharp EL, 1983. Registration of Winridge wheat. Crop Science, 23:1222
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Váňová, M., Matušinskyhacek˜, P., Benada, J., 2006. Survey of incidence of bunts (Tilletia caries and Tilletia controversa) in the Czech republic and susceptibility of winter wheat cultivars. Plant Protection Science, 42(1), 21-25. http://www.cazv.cz
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Xue AG, Tenuta A, Tian XL, Sparry E, Etienne M, Gaudet DA, Menzies JG, Graf RJ, Falk DE, Smid A, Pandeya RS, 2007. Evaluation of winter wheat genotypes and seed treatments for control of dwarf bunt in Ontario. Canadian Journal of Plant Pathology, 29(3):243-250. http://pubs.nrc-cnrc.gc.ca/tcjpp/plant.html
Yuan Qing, Nian Siji, Yin YouPing, Li MinHui, Cai Jun, Wang ZhongKang, 2009. Development of a PCR-based diagnostic tool specific to wheat dwarf bunt, caused by Tilletia controversa. European Journal of Plant Pathology, 124(4):585-594. http://springerlink.metapress.com/link.asp?id=100265
Zhang GM Lu J, Tian ZZ, Chen ZN, Deng Q, Li YN, 2002. Method of extracting spores of Tilletia controversa from bran. Acta-Phytopathologica-Sinica. 32: 4, 319-325
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DCA - Nationalt Center for Fødevarer og Jordbrug, Denmark, 2019. Update of pest status in Denmark for specific harmful organisms in relation to export of seeds - part 1. (Opdatering af skadegørerstatus i Danmark for specifikke skadegørere i relation til eksport af frø - del 1.). In: Opdatering af skadegørerstatus i Danmark for specifikke skadegørere i relation til eksport af frø - del 1. [ed. by Nicolaisen M, Justesen A F, Nielsen B J, Enkegaard A, Lövei G, Ravnskov S, Melander B, Jørgensen L N, Hovmøller M S, Skovgǻrd H, Kristensen M]. Tjele, Denmark: DCA - Nationalt Center for Fødevarer og Jordbrug, Aarhus University. 51 pp. https://pure.au.dk/portal/da/publications/opdatering-af-skadegoererstatus-i-danmark-for-specifikke-skadegoerere-i-relation-til-eksport-af-froe--del-1(0270de38-236d-4a8c-a8a5-98f5774b6b0d).html
Váňová M, Matušinskyhacek˜ P, Benada J, 2006. Survey of incidence of bunts (Tilletia caries and Tilletia controversa) in the Czech republic and susceptibility of winter wheat cultivars. Plant Protection Science. 42 (1), 21-25. http://www.cazv.cz
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