Claviceps sorghicola

Identity

Preferred Scientific Name

• Claviceps sorghicola Tsukib., Shiman. and T. Uematsu 1999

Summary of Invasiveness

C. sorghicola is an ergot pathogen of sorghum only found in Japan to date (2009). The risk of its spread and introduction is limited by the small amount of sorghum grown in Japan and by the lack of airborne secondary conidia. Sclerotia, which are known to germinate, are clearly distinct from, and larger than, seed and could be separated if necessary to prevent contamination of exports. The only alternate host identified to date is the closely related Sudangrass (Sorghum bicolor subsp. drummondii). The use of morphologically resistant cultivars of sorghum and Sudangrass, as well as early sowing, were found to control the disease.

Taxonomic Tree

• Domain: Eukaryota
•     Kingdom: Fungi
•         Phylum: Ascomycota
•             Subphylum: Pezizomycotina
•                 Class: Sordariomycetes
•                     Subclass: Hypocreomycetidae
•                         Order: Hypocreales
•                             Family: Clavicipitaceae
•                                 Genus: Claviceps
•                                     Species: Claviceps sorghicola

Description

C. sorghicola is an ergot fungus on sorghum flowers. Infection of the ovaries results in replacement of the plant tissue with fungal mycelium and the production of asexual spores (conidia) in a sugary liquid (honeydew). The fungus grows further to produce a hard survival structure (sclerotium) in the floret that may fall to the ground or become mixed with harvested seed. In the field, the following season, the sclerotium germinates to produce bodies (stromata) containing the perithecia, the sexual form of the fungus. Perithecia generate and eject ascospores that infect flowers.

Sclerotia cylindrical to conical, straight to curved, grooved longitudinally, purple black to black, 2.5-20 x 1.9-3.5 mm, with covering and small cap of white sphacelium. Stromata 1-4, with stipes brown to bronze-coloured, 3.5-17.0 mm, capitula globose-subglobose, dark-brown, papillate, 0.5-1.6 mm diameter. Ascomata in capitula ovoid to pyriform, 21-300 x 105-140 µm, ostioles erumpent. Asci cylindrical, 122-315 x 2.5-3.8 µm, with thickened apex. Ascospores hyaline, filiform, eight per ascus, 92-205 x 0.5-1.0 µm (Tsukiboshi et al., 1999).

Conidia in brownish honeydew and on sporulating sphacelium, ellipsoid to ovoid, hyaline, aseptate, 5.0-11.3 x 2.5-3.6 µm. No globose microconidia observed in nature (Tsukiboshi et al., 1999). No iteration to produce secondary conidia observed in planta or in vitro, but conidia will germinate and give rise to mycelial growth on culture media (Tsukiboshi et al., 1999; Pazoutova et al., 2004). Colonies white to cream, velutinous; growth range at least 10-34°C, with optimum growth at 25°C, on potato-dextrose agar (Tsukiboshi et al., 1999).

Distribution Table

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.

Hosts/Species Affected

Tsukiboshi et al. (1999) tested certain species of Poaceae (grasses) by inoculation and found infection of only Sorghum bicolor, and “Sorghumsudanense” (Sorghum bicolor subsp. drummondii) (USDA-ARS, 2009). Pearl millet (Pennisetum glaucum) was not affected. Wild species of Sorghum and related grass genera have been reported as hosts for the other sorghum ergots (Muthusubramanian et al., 2005), but cross-inoculation tests would be the best means of establishing their possible roles in epidemiology of C. sorghicola. Escaped plants and ratoon crops of the cultivated species can also have a significant role (Odvody et al., 2002).

Symptoms

Pale-brown honeydew is exuded from florets in mid-summer; this often becomes covered by the black growth of the fungus Cerebella andropogonis. Later, cylindrical to conical, grooved dark sclerotia, bearing remnant white sphacelial tissue, grow out from the infected florets (Tsukiboshi et al., 1999).

List of Symptoms/Signs

Biology and Ecology

Tsukiboshi et al. (1999) obtained germination of a large proportion of sclerotia to produce the perfect state (teleomorph), and observed sclerotia germinating under field conditions in July. Therefore, ascospores are presumed to be the primary inoculum for infection of florets. In other ergots, infection of ovaries requires the absence of fertilization (Bandyopadhyay et al., 1998). In South Africa, cool weather at certain times before and after anthesis, increases the incidence of sorghum ergot infection due to its effect on pollen viability and fertilization (McLaren and Wehner, 1990, 1992), and this effect may be involved for C. sorghicola infection as well. Tsukiboshi et al. (1999) observed infection of field varieties of sorghum (not male-sterile hybrid-breeding lines that are highly susceptible to ergot infection, Bandyopadhyay et al., 1998), and hypothesized that the temperate weather of Japan might be a factor enhancing susceptibility in the production cultivars.

Although Pazoutova et al. (2000) successfully inoculated a male-sterile line with an isolate of C.sorghicola, broader tests of virulence of the species on such varieties have not been reported. The same workers suggest that Claviceps africana, due to its greater epidemiological aggressiveness, may displace the Japanese ergot as it apparently displaced Claviceps sorghi in India (Pazoutova et al., 2000). In North America, C. africana has survived between cropping seasons on escaped, wild or weedy sorghum plants and varieties in wet southern areas and then spread northwards in warmer weather (Odvody et al., 2002). In Texas, it has also been shown to survive in honeydew on dry panicles on or above the ground in an infective condition long enough to provide inoculum the following season (Prom et al., 2005). Such means of survival in a temperate region might also be possible for C. sorghicola, but it lacks the production of airborne secondary conidia that facilitates rapid spread for C. africana. This means that, as suggested, the more fecund species may become predominant in Japan.

Climate

Means of Movement and Dispersal

Conidia in the sticky honeydew are transported from plant to plant by wind, rain splash and insects (Tsukiboshi et al., 1999). Insects are known to carry ergot conidia non-specifically on their bodies after feeding on honeydew (Prom et al., 2003).

If not cleaned or treated, sorghum seed containing sclerotia can be a means of local transport of the pathogen (Bandyopadhyay et al., 1998). If such seed were exported, this could be a means of introduction from Japan.

Seedborne Aspects

Tsukiboshi et al. (1999, 2001) do not provide any observations on seed-borne C. sorghicola.

Plant Trade

Impact Summary

Risk and Impact Factors

• Reproduces asexually

• Host damage
• Negatively impacts agriculture

• Pathogenic

Detection and Inspection

Pale-brown honeydew is produced in drops on infected florets, and may become covered by the black growth of another fungus. The hard bodies of sclerotia later grow out to project from between the glumes. These sclerotia, which may be harvested with the seed, are significantly bigger than the seed and of different colours.

Similarities to Other Species/Conditions

Two other ergot species, Claviceps africana (Frederickson et al., 1991) and Claviceps sorghi (Kulkarni et al., 1976) also infect sorghum, and one of them overlaps in distribution with C. sorghicola. C. africana is known to be present in most sorghum-growing regions worldwide, including Japan (Bandyopadhyay et al., 1998: Tsukiboshi et al., 2001). C. sorghi is found in India and possibly southeast Asia (Tonapi et al., 2003; Muthusubramanian et al., 2005). In describing the new species, Tsukiboshi et al. (1999) presented detailed comparison of its characteristics with those of the other ergots.

Both C. sorghi and C. sorghicola form elongate sphacelia and sclerotia, whereas those of C.africana are smaller, subglobose and project less beyond the glumes of the florets (Frederickson et al., 1991). This difference may not be apparent early in infection. For C. sorghicola and C. sorghi, honeydew appears early, before the sphacelia are visible (Frederickson and Mantle, 1988; Tsukiboshi et al., 1999). In C. africana, the sphacelium causes the glumes to bulge open before honeydew is produced (Frederickson et al., 1991).The conidia of C. sorghicola in the honeydew are significantly smaller than the macroconidia of the Indian and African ergots (see Description). Conidia of C. sorghicola, like those of C. sorghi, do not form secondary conidia in nature (Tsukiboshi et al., 1999), so the honeydew surface does not develop a superficial white layer under humid conditions.

Perithecia, asci and ascospores of C. sorghicola are significantly longer than those of the other two sorghum ergots. Most sclerotia of C. sorghicola and C. sorghi germinate readily to produce the teleomorph, but those of C. africana do not (Bandyopadhyay et al., 1998; Tsukiboshi et al., 1999).

In the absence of the teleomorph, one diagnostic test can be the identification of alkaloids in the sclerotia. C. africana uniquely produces the alkaloid dihydroergosine in sclerotial tissues (Frederickson et al., 1991; Mantle and Hassan, 1994). C. sorghicola and C. sorghi sclerotia contain caffeine (Bogo and Mantle, 2000; Bogo et al., 2003); those of C. sorghicola also contain paliclavine (Bogo and Mantle, 2000; Tsukiboshi et al., 1999). Sphacelia are not known to synthesize alkaloids in any species.

Various types of genetic analyses in the genus Claviceps have confirmed that C. sorghicola is a distinct species, but also show that the similarities in DNA sequences place it closer to the other ergot fungi on sorghum than to those that occur on other hosts (Tooley et al., 2000, 2001; Pazoutova et al., 2000, 2004). A DNA sequence technique was found that allowed for rapid identification of the species on sorghum, including C. sorghicola, in the presence of other fungi (Partridge et al., 2000).

The sori of covered kernel smut (Sphacelotheca sorghi) and long smut (Tolyposporium ehrenbergii) are sometimes confused with Claviceps sphacelia. However, in the smut fungi the sack-like sori consist of a smooth, cream to grey outer covering or peridium enclosing the black powdery teliospores (Frederiksen, 1986; Hilu, 1986). The sclerotia of C.sorghicola are hard, dark, grooved bodies without a peridium, but bearing a small cap and surface layer of white sphacelial tissue. Also, smuts do not produce honeydew. S. sorghi has been reported from China, Japan, Korea, Taiwan and The Philippines in eastern Asia, while T. ehrenbergii is reported from China (Farr at al., 2009).

Prevention and Control

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

C. sorghicola is not mentioned in quarantine lists of major sorghum-growing nations.

Eradication

Destruction of infected heads bearing honeydew may reduce spread of the fungus between plants, as well as preventing development of the sclerotia.

Control

Cultural control and sanitary measures

Early sowing has been shown to permit escape from infection by other sorghum ergots in other countries (Bandyopadhyay et al., 1998). This may be effective if it allows for flowering under weather conditions favourable for pollination and/or unfavourable for spore dispersal and infection. Tsukiboshi et al. (1998, 2001) reported that control by early sowing, so that flowering occurred in early to mid-summer, was feasible in Japan.

Where ascospores produced in or near the crop are the primary inoculum, crop rotation could allow for natural exhaustion of sclerotia as sources of the inoculum in a few growing seasons.

Physical/mechanical control

Due to the fact that ascospores are presumed to be the primary inoculum, burying sclerotia by ploughing them under will reduce inoculum from within a field.

Chemical control

Certain chemicals, when applied correctly and at the appropriate time, have been shown to be effective in preventing ergot caused by Claviceps africana, but their use may not be economical or practical (Prom and Isakeit, 2003).

Host resistance

Tsukiboshi et al. (1998, 2001) report reduced incidence in some sorghum and Sudangrass (Sorghum bicolor subsp. drummondii) cultivars that appears to be due to morphological and/or physiological aspects of their flowering, including short stigma excerption, greater coverage by glumes and high seed set. Use of these cultivars in combination with early planting could control disease; they could also be used in a breeding programme for newer lines.

Gaps in Knowledge/Research Needs

Research results for the more aggressive Claviceps africana can be applied.

References

Bandyopadhyay R; Frederickson DE; McLaren NW; Odvody GN; Ryley MJ, 1998. Ergot: a new disease threat to sorghum in the Americas and Australia. Plant Disease, 82(4):356-367; 54 ref.

Bogo A; Mantle PG, 2000. Caffeine: also a fungal metabolite. Phytochemistry, 54(8):937-939; 14 ref.

Bogo A; Mantle PG; Boff MIC; Amarante CVTdo, 2003. Production of caffeine alkaloid by Claviceps sorghi. Fitopatologia Brasileira, 28(4):446-448. http://www.scielo.br/pdf/fb/v28n4/17024.pdf

Farr DF; Rossman AY; Palm ME; McCray EB, 2009. Fungal Databases, Systematic Botany & Mycology Laboratory, ARS, USDA. USA: ARS, USDA. http://nt.ars-grin.gov/fungaldatabases/

Frederickson DE; Mantle PG, 1988. The path of infection of sorghum by Claviceps sorghi. Physiological and Molecular Plant Pathology, 33(2):221-234

Frederickson DE; Mantle PG; Milliano WAJde, 1991. Claviceps africana sp. nov.; the distinctive ergot pathogen of sorghum in Africa. Mycological Research, 95(9):1101-1107

Frederiksen RA, 1986. Covered kernel smut. In: Compendium of Sorghum Diseases [ed. by Frederiksen RA] St Paul, Minnesota, USA: American Phytopathological Society, 129 pp.

Hilu O, 1986. Long smut. In: Frederiksen RA, ed. Compendium of Sorghum Diseases. St Paul, Minnesota, USA: American Phytopathological Society.

Kulkarni BGP; Seshadri VS; Hegde RK, 1976. The perfect stage of Sphacelia sorghi McRp. Mysore Journal of Agricultural Sciences, 10(2):286-289

Mantle PG; Hassan HAG, 1994. Widening geographical distribution of Claviceps africana, an important ovary pathogen of grain sorghum. International Sorghum and Millets Newsletter, 35:97-98

McLaren NW; Wehner FC, 1990. Relationship between climatic variables during early flowering of sorghum and the incidence of sugary disease caused by Sphacelia sorghi. Journal of Phytopathology, 130(1):82-88

McLaren NW; Wehner FC, 1992. Pre-flowering low temperature predisposition of sorghum to sugary disease (Claviceps africana). Journal of Phytopathology, 135(4):328-334

Muthusubramanian V; Bandyopadhyay R; Tooley PW; Reddy DJ, 2005. Inoculated host range and effect of host on morphology and size of macroconidia produced by Claviceps africana and Claviceps sorghi. Journal of Phytopathology, 153(1):1-4. http://www.blackwell-synergy.com/rd.asp?code=EPI&goto=journal

Odvody GN; Frederickson DE; Isakeit T; Montes N; Dahlberg JA; Peterson GL, 2002. Quarantine issues arising from contamination of seed with ergot: an update. In: Sorghum and Millets Diseases [ed. by Leslie JF] Iowa, USA: Iowa State University Press, 123-129.

Partridge JE; Delserone LM; Jensen SG; Stack JP, 2000. A small subunit rDNA intron-based diagnostic for identification of Claviceps species. Phytopathology, 90:S59.

Pazoutová S; Kolarík M; Kolínská R, 2004. Pleomorphic conidiation in Claviceps. Mycological Research, 108(2):126-135.

Pazoutová S; Ranajit Bandyopadhyay; Frederickson DE; Mantle PG; Frederiksen RA, 2000. Relations among sorghum ergot isolates from the Americas, Africa, India, and Australia. Plant Disease, 84(4):437-442; 36 ref.

Prom LK; Isakeit T, 2003. Laboratory, greenhouse, and field assessment of fourteen fungicides for activity against Claviceps africana, causal agent of sorghum ergot. Plant Disease, 87(3):252-258.

Prom LK; Isakeit T; Odvody GN; Rush CM; Kaufman HW; Montes N, 2005. Survival of Claviceps africana within sorghum panicles at several Texas locations. Plant Disease, 89(1):39-43. http://www.apsnet.org

Prom LK; Lopez JD Jr; Latheef MA, 2003. Transmission of Claviceps africana spores from diseased to non-infected sorghum by corn earworm moths, Helicoverpa zea. Journal of Sustainable Agriculture, 21(4):49-58.

Tonapi VA; Wirojwattanakul K; Dang Van Vinh; Moung Moung Thein; Navi SS; Tooley PW, 2004. Prevalence of sorghum ergot in Southeast Asia. International Sorghum and Millets Newsletter, 44:95-97.

Tooley PW; Goley ED; Carras MM; Frederick RD; Weber EL; Kuldau GA, 2001. Characterization of Claviceps species pathogenic on sorghum by sequence analysis of the -tubulin gene intron 3 region and EF-1 gene intron 4. Mycologia, 93(3):541-551; 45 ref.

Tooley PW; O'Neill NR; Goley ED; Carras MM, 2000. Assessment of diversity in Claviceps africana and other Claviceps species by RAM and AFLP analyses. Phytopathology, 90(10):1126-1130.

Tsukiboshi T; Koga H; Uematsu T; Shimanuki T, 1998. Resistance of sorghum and sudangrass to ergot caused by Claviceps sp. and the cultural control of the disease. Sochi Shikenjo Kenkyu Hokoku = Bulletin of the National Grassland Research Institute, No. 56:28-35.

Tsukiboshi T; Shimanuki T; Koga H, 2001. Claviceps sorghicola and C. africana, the ergot pathogens of sorghum, and their cultural control in Japan. JARQ, Japan Agricultural Research Quarterly, 35(4):221-226.

Tsukiboshi T; Shimanuki T; Uematsu T, 1999. Claviceps sorghicola sp. nov., a destructive ergot pathogen of sorghum in Japan. Mycological Research, 103(11):1403-1408; 14 ref.

USDA-ARS, 2009. Germplasm Resources Information Network (GRIN). Online Database. Beltsville, Maryland, USA: National Germplasm Resources Laboratory. https://npgsweb.ars-grin.gov/gringlobal/taxon/taxonomysearch.aspx

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10/09/09 Updated by:

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