Analysis of the Fusarium graminearum species complex from wheat, barley and maize in South Africa provides evidence of species-specific differences in host preference

Fungal Genetics and Biology

Volumn 48, Issue 9, 2011, Pages 914-920

  Boutigny, Anne Laure ^a   Ward, Todd J ^b   Van Coller, Gert J ^a,c   Flett, Bradley ^d   Lamprecht, Sandra C ^e   O'Donnell, Kerry ^b   Viljoen, Altus ^a  

^a STELLENBOSCH UNIVERSITY   (South Africa)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c WESTERN CAPE DEPARTMENT OF AGRICULTURE   (South Africa)

^d ARC GRAIN CROPS INSTITUTE   (South Africa)

^e PLANT PROTECTION RESEARCH INSTITUTE   (South Africa)

Author keywords

Cereal; Chemotype; Fusarium; Fusarium head blight; Gibberella ear rot

Indexed keywords

TRICHOTHECENE;

ARTICLE; BARLEY; CONTROLLED STUDY; FUNGAL PLANT DISEASE; FUNGAL STRAIN; FUSARIUM; FUSARIUM BOOTHI; FUSARIUM GRAMINEARUM; FUSARIUM HEAD BLIGHT; GIBBERELLA EAR ROT; HOST SELECTION; INTERSPECIFIC HYBRID; MAIZE; MOLECULAR TYPING; MULTILOCUS GENOTYPING ASSAY; NONHUMAN; PLANT ROOT; PRIORITY JOURNAL; SOUTH AFRICA; SPECIES DIFFERENCE; SPECIES DIVERSITY; SPECIES DOMINANCE; SPECIES IDENTIFICATION; WHEAT;

FUSARIUM; GENETIC VARIATION; HORDEUM; HOST SPECIFICITY; MOLECULAR SEQUENCE DATA; PLANT DISEASES; SOUTH AFRICA; TRITICUM; ZEA MAYS;

FUSARIUM; FUSARIUM BOOTHII; GIBBERELLA; GIBBERELLA ZEAE; HORDEUM; TRITICUM AESTIVUM; ZEA MAYS;

EID: 79960615545     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2011.05.005     Document Type: Article

References (52)

1. Bennett J.W., Klich M. Mycotoxins. Clin. Microbiol. Rev. 2003, 16:497-516.
2. Chandler E.A., Simpson D.R., Thomsett M.A., Nicholson P. Development of PCR assays to Tri7 and Tri13 trichothecene biosynthetic genes, and characterization of chemotypes of Fusarium graminearum, Fusarium culmorum and Fusarium cerealis. Physiol. Mol. Plant Pathol. 2003, 62:355-367.
3. Desjardins A.E., Proctor R.H. Genetic diversity and trichothecene chemotypes of the Fusarium graminearum clade isolated from maize in Nepal and identification of a putative new lineage. Fungal Biol. 2011, 115:38-48.
4. Dowd P.F., Duvick J.P., Rood T. Comparative toxicity of allelochemicals and their enzymatic oxidation products to maize fungal pathogens, emphasizing Fusarium graminearum. Nat. Toxins 1997, 5:180-185.
5. Forsell J.H., Pestka J.J. Relation of 8-ketotrichothecene and zearalenone analog structure to inhibition of mitogen-induced human-lymphocyte blastogenesis. Appl. Environ. Microbiol. 1985, 50:1304-1307.
6. Friebe A., Vilich V., Hennig L., Kluge M., Sicker D. Detoxification of benzoxazolinone allelochemicals from wheat by Gaeumannomyces graminis var. tritici, G. graminis var. graminis, G. graminis var. avenae, and Fusarium culmorum. Appl. Environ. Microbiol. 1998, 64:2386-2391.
7. Gale L.R., Chen L.-F., Hernick C.A., Takamura K., Kistler H.C. Population analysis of Fusarium graminearum from wheat fields in Eastern China. Phytopathology 2002, 92:1315-1322.
8. Gale L.R., Harrison S.A., Ward T.J., O'Donnell K., Milus E.A., Gale S.W., Kistler H.C. Nivalenol-producing isolates of Fusarium graminearum and F. asiaticum are prevalent on wheat in southern Louisiana. Phytopathology 2011, 101:124-134.
9. Gilbert J., Clear R.M., Ward T.J., Gaba D., Tekauz A., Turkington T.K., Woods S.M., Nowicki T., O'Donnell K. Relative aggressiveness and mycotoxin accumulation of isolates of Fusarium graminearum producing either 3 or 15-acetyl deoxynivalenol in addition to deoxynivalenol. Can. J. Plant Pathol. 2010, 32:146-152.
10. Goswami R.S., Kistler H.C. Pathogenicity and in planta mycotoxin accumulation among members of the Fusarium graminearum species complex on wheat and rice. Phytopathology 2005, 95:1397-1404.
11. Jansen C., von Wettstein D., Schäfer W., Kogel K.-H., Felk A., Maier F.J. Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proc. Nat. Acad. Sci. USA 2005, 102:16892-16897.
12. Keyser Z., Vismer H.F., Klaasen J.A., Snijman P.W., Marasas W.F.O. The antifungal effect of fumonisin B1 on Fusarium and other fungal species. South Afr. J. Sci. 1999, 95:455-458.
13. Kimura M., Kaneko I., Komiyama M., Takatsuki A., Koshinoi H., Yoneyama K., Yamaguchi I. Trichothecene 3-O-acetyltransferase protects both the producing organism and transformed yeast from related mycotoxins. J. Biol. Chem. 1998, 273:1654-1661.
14. Láday M., Juhász Á., Mulè G., Moretti A., Szécsi Á., Logrieco A. Mitochondrial DNA diversity and lineage determination of European isolates of Fusarium graminearum (Gibberella zeae). Eur. J. Plant Pathol. 2004, 110:545-550.
15. Lee J., Chang I.Y., Kim H., Yun S.-H., Leslie J.F., Lee Y.-W. Genetic diversity and fitness of Fusarium graminearum populations from rice in Korea. Appl. Environ. Microbiol. 2009, 75:3289-3295.
16. Leslie J.F., Summerell B.A. The Fusarium Laboratory Manual 2006, Blackwell Publishing Professional, Ames, IA, USA.
17. Luongo D., Severino L., Bergamo P., D'Arienzo R., Rossi M. Trichothecenes NIV and DON modulate the maturation of murine dendritic cells. Toxicon 2010, 55:73-80.
18. Marasas W.F.O. Fumonisins: their implications for human and animal health. Nat. Toxins 1995, 3:193-198.
19. Marasas W.F.O., Kriek N.P.J., Wiggins V.M., Steyn P.S., Towers D.K., Hastie T.J. Incidence, geographic distribution, and toxigenicity of Fusarium species in South African corn. Phytopathology 1979, 69:1181-1185.
20. Marasas W.F.O., Voigt W.G.T., Lamprecht S.C., Van Wyk P.S. Crown rot and head blight of wheat caused by Fusarium graminearum Groups 1 and 2 in the Southern Cape Province. Phytophylactica 1988, 20:385-389.
21. Miller J.D., Greenalgh R., Wang Y., Lu M. Trichothecene chemotype of three Fusarium species. Mycologia 1991, 83:121-130.
22. Monds R.D., Cromey M.G., Lauren D.R., Di Menna M., Marshall J. Fusarium graminearum, F. cortaderiae and F. pseudograminearum in New Zealand: molecular phylogenetic analysis, mycotoxin chemotypes and co-existence of species. Mycol. Res. 2005, 109:410-420.
23. O'Donnell K., Kistler H.C., Tacke B.K., Casper H.H. Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum, the fungus causing wheat scab. Proc. Nat. Acad. Sci. USA 2000, 97:7905-7910.
24. O'Donnell K., Ward T.J., Geiser D.M., Kistler H.C., Aoki T. Genealogical concordance between the mating type locus and seven other nuclear genes supports formal recognition of nine phylogenetically distinct species within the Fusarium graminearum clade. Fungal Genet. Biol. 2004, 41:600-623.
25. O'Donnell K., Ward T.J., Aberra D., Kistler H.C., Aoki T., Orwig N., Kimura M., Bjørnstad Å., Klemsdal S.S. Multilocus genotyping and molecular phylogenetics resolve a novel head blight pathogen within the Fusarium graminearum species complex from Ethiopia. Fungal Genet. Biol. 2008, 45:1514-1522.
26. Pestka J.J. Deoxynivalenol: mechanisms of action, human exposure, and toxicological relevance. Arch. Toxicol. 2010, 84:663-679.
27. Placinta C.M., D'Mello J.P.F., MacDonald A.M.C. A review of worldwide contamination of cereal grains and animal feed with Fusarium mycotoxins. Anim. Feed Sci. Technol. 1999, 78:21-37.
28. Platt A.R., Woodhall R.W., George A.L. Improved DNA sequencing quality and efficiency using an optimized fast cycle sequencing protocol. Biotechniques 2007, 43:58.
29. Proctor R.H., Hohn T.M., McCormick S.P. Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Mol. Plant Microbe Interact. 1995, 8:593-601.
30. Ramirez M.L., Reynoso M.M., Farnochi M.C., Chulze S. Vegetative compatibility and mycotoxin chemotypes among Fusarium graminearum (Gibberella zeae) isolates from wheat in Argentina. Eur. J. Plant Pathol. 2006, 115:139-148.
31. Ramirez M.L., Reynoso M.M., Farnochi M.C., Torres A.M., Leslie J.F., Chulze S.N. Population genetic structure of Gibberella zeae isolated from wheat in Argentina. Food Addit. Contam. 2007, 24:1115-1120.
32. Reid L.M., Nicol R.W., Ouellet T., Savard M., Miller J.D., Young J.C., Stewart D.W., Schaafsma A.W. Interaction of Fusarium graminearum and F. moniliforme in maize ears: disease progress, fungal biomass, and mycotoxin accumulation. Phytopathology 1999, 89:1028-1037.
33. Rheeder J.P., Marasas W.F.O., Van Wyk P.S. Fungal associations in corn kernels and effects on germination. Phytopathology 1990, 80:131-134.
34. Rheeder J.P., Sydenham E.W., Marasas W.F.O., Thiel P.G., Shepard G.S., Schlechter M., Stockenstrom S., Cronje D.W., Viljoen J.H. Fungal infestation and mycotoxin contamination of South African commercial maize harvested in 1989 and 1990. South Afr. J. Sci. 1995, 91:127-131.
35. Sampietro D.A., Diaz C.G., Gonzalez V., Vattuone M.A., Polper L.D., Catalan C.A.N., Ward T.J. Species diversity and toxigenic potential of Fusarium graminearum complex isolates from maize fields in northwest Argentina. Int. J. Food Microbiol. 2011, 145:359-364.
36. Scott D.B., De Jager E.J.H., Van Wyk P.S. Head blight of irrigated wheat in South Africa. Phytophylactica 1988, 20:317-319.
37. Scoz L.B., Astolfi P., Reartes D.S., Schmale D.G., Moraes M.G., Del Ponte E.M. Trichothecene mycotoxin genotypes of Fusarium graminearum sensu stricto and Fusarium meridionale in wheat from southern Brazil. Plant Pathol. 2009, 58:344-351.
38. Simpson D.R., Rezanoor H.N., Parry D.W., Nicholson P. Evidence for differential host preference in Microdochium nivale var. majus and Microdochium nivale var. nivale. Plant Pathol. 2000, 49:261-268.
39. Starkey D.E., Ward T.J., Aoki T., Gale L.R., Kistler H.C., Geiser D.M., Suga H., Tóth B., Varga J., O'Donnell K. Global molecular surveillance reveals novel Fusarium head blight species and trichothecene toxin diversity. Fungal Genet. Biol. 2007, 44:1191-1204.
40. Suga H., Karugia G.W., Ward T., Gale L.R., Tomimura K., Nakajima T., Miyasaka A., Koizumi S., Kageyama K., Hyakumachi M. Molecular characterization of the Fusarium graminearum species complex in Japan. Phytopathology 2008, 98:159-166.
41. Sydenham E.W., Thiel P.G., Marasas W.F.O., Nieuwenhuis J.J. Occurrence of deoxynivalenol and nivalenol in Fusarium-graminearum infected undergrade wheat in South Africa. J. Agric. Food Chem. 1989, 37:921-926.
42. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
43. Thiel P.G., Meyer C.J., Marasas W.F.O. Natural occurrence of moniliformin together with deoxynivalenol and zearalenone in Transkeian corn. J. Agric. Food Chem. 1982, 30:308-312.
44. Tóth B., Mesterházy Á., Horváth Z., Bartók T., Varga M., Varga J. Genetic variability of central European isolates of the Fusarium graminearum species complex. Eur. J. Plant Pathol. 2005, 113:35-45.
45. Van Wyk P.S., Scholtz D.J., Marasas W.F.O. Protection of maize seedlings by Fusarium moniliforme against infection by Fusarium graminearum in the soil. Plant Soil 1988, 107:251-257.
46. von der Ohe C., Gauthier V., Tamburic-Ilincic L., Brule-Babel A., Fernando W.G.D., Clear R., Ward T.J., Miedaner T. A comparison of aggressiveness and deoxynivalenol production between Canadian Fusarium graminearum isolates with 3-acetyl and 15-acetyldeoxynivalenol chemotypes in field-grown spring wheat. Eur. J. Plant Pathol. 2010, 127:407-417.
47. Wagacha J.M., Steiner U., Dehne H.-W., Zuehlke S., Spiteller M., Muthomi J., Oerke E.-C. Diversity in mycotoxins and fungal species infecting wheat in Nakuru District, Kenya. J. Phytopathol. 2010, 158:527-535.
48. Ward T.J., Bielawski J.P., Kistler H.C., Sullivan E., O'Donnell K. Ancestral polymorphism and adaptive evolution in the trichothecene mycotoxin gene cluster of phytopathogenic Fusarium. Proc. Nat. Acad. Sci. USA 2002, 99:9278-9283.
49. Ward T.J., Clear R.M., Rooney A.P., O'Donnell K., Gaba D., Patrick S., Starkey D.E., Gilbert J., Geiser D.M., Nowicki T.W. An adaptive evolutionary shift in Fusarium head blight pathogen populations is driving the rapid spread of more toxigenic Fusarium graminearum in North America. Fungal Genet. Biol. 2008, 45:473-484.
50. Xu X., Nicholson P., Ritieni A. Effects of fungal interactions among Fusarium head blight pathogens on disease development and mycotoxin accumulation. Int. J. Food Microbiol. 2007, 119:67-71.
51. Yang L., van der Lee T., Yang X., Yu D., Waalwijk C. Fusarium populations on Chinese barley show a dramatic gradient in mycotoxin profiles. Phytopathology 2008, 98:719-727.
52. Yli-Mattila T., Gagkaeva T., Ward T.J., Aoki T., Kistler H.C., O'Donnell K. A novel Asian clade within the Fusarium graminearum species complex includes a newly discovered cereal head blight pathogen from the Russian Far East. Mycologia 2009, 101:841-852.