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Diversity in genetic structure and chemotype composition of Fusarium graminearum sensu stricto populations causing wheat head blight in individual fields in Germany

Abstract

Fusarium head blight (FHB) is one of the most destructive diseases of wheat. Twelve small commercial wheat fields (size 1–3 hectares) were sampled in Germany for Fusarium populations at three spots per field with 10 heads each. PCR assays using generic primers confirmed 338 isolates as F.graminearum sensu stricto (s.s.) (64.9%) out of 521 Fusarium spp. that were further analyzed. Populations of F. graminearum s.s. in Germany contain three types of trichothecenes with a dominancy of 15-acetyldeoxynivalenol chemotype (92%) followed by 3-acetyldeoxynivalenol chemotype (6.8%) and a few isolates of nivalenol chemotype (1.2%). All these isolates were genotyped using 19 microsatellite loci. The 12 populations showed a high genetic diversity within the small scale sampling areas resulting in 300 different haplotypes. Genetic diversity within populations (71.2%) was considerably higher than among populations (28.8%) as shown by analysis of molecular variance. Gene flow (Nm) between populations ranged from 0.76–3.16. Composition of haplotypes of one population followed over 2 years changed considerably. No correlation between genetic and geographical distance was found. In conclusion, populations of F. graminearum s.s. in Germany display a tremendous genetic variation on a local scale with a restricted diversity among populations.

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References

  • Agrios, G. N. (2004). Plant pathology (5th ed., 922 pp.). San Diego, USA: Elsevier Press.

  • Chandler, E. A., Duncan, R. S., Thomsett, M. A., & Nicholson, P. (2003). Development of PCR assays to Tri7 and Tri13 trichothecene biosynthetic genes and characterisation of chemotypes of Fusarium graminearum, Fusarium culmorum and Fusarium cerealis. Physiological and Molecular Plant Pathology, 62, 355–367.

    Article  CAS  Google Scholar 

  • Chen, Y., & Zhou, M. G. (2009). Sexual recombination of carbendazim resistance in Fusarium graminearum under field conditions. Pest Management Science, 65, 398–403.

    PubMed  Article  CAS  Google Scholar 

  • Demeke, T., Clear, R. M., Patrick, S. K., & Gaba, D. (2004). Species-specific PCR –based assays for the detection of Fusarium species and a comparison with the whole seed agar plate method and trichothecene analysis. International Journal of Food Microbiology, 103, 271–284.

    Article  Google Scholar 

  • Excoffier, L., & Lischer, H. E. L. (2010). Arlequin suite ver. 3.5: a new series of perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564–567.

    PubMed  Article  Google Scholar 

  • Gale, L. R., Bryant, J. D., Calvo, S., Giese, H., Katan, T., O’Donnell, K., et al. (2005). Chromosome complement of the fungal plant pathogen Fusarium graminearum based on genetic and physical mapping and cytological observations. Genetics, 171, 985–1001.

    PubMed  Article  CAS  Google Scholar 

  • Gale, L. R., Ward, T. J., Balmas, V., & Kistler, H. C. (2007). Population subdivision of Fusarium graminearum sensu stricto in the Upper Midwestern United States. Phytopathology, 97, 1434–1439.

    PubMed  Article  CAS  Google Scholar 

  • Gale, L. R., Harrison, S. A., Ward, T. J., O’Donnell, K., Milus, E. A., Gale, S. W., et al. (2011). Nivalenol type populations of Fusarium graminearum and F. asiaticum are prevalent on wheat in southern Louisiana. Phytopathology, 101, 124–134.

    PubMed  Article  CAS  Google Scholar 

  • Giraud, T., Fournier, E., Vautrin, D., Solignac, M., Vercken, E., Bakan, B., et al. (2002). Isolation of eight polymorphic microsatellite loci using an enrichment protocol, in the phytopathogenic fungus Fusarium culmorum. Molecular Ecology Notes, 2, 121–123.

    Article  CAS  Google Scholar 

  • Guo, X. W., Fernando, W. G. D., & Seow-Brock, H. Y. (2008). Population structure chemotype diversity and potential chemotype shifting of Fusarium graminearum in wheat fields of Manitoba. Plant Disease, 92, 756–762.

    Article  CAS  Google Scholar 

  • Hartl, D. L., & Clark, A. G. (2007). Principles of population genetics (4th ed., 652 pp.). Minnesota, USA: Sinauer Associates Press.

  • Hedrick, P. W. (2000). Genetics of populations (2nd ed.). Basic Book: Boston.

    Google Scholar 

  • Hoffman, C. S., & Winston, F. (1987). A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene, 57, 267–272.

    PubMed  Article  CAS  Google Scholar 

  • Jennings, P., Coates, M. E., Walsh, K., Turner, J. A., & Nicholson, P. (2004). Determination of deoxynivalenol and nivalenol producing chemotypes of Fusarium graminearum isolated from wheat crops in England and Wales. Plant Pathology, 53, 643–652.

    Article  CAS  Google Scholar 

  • Karugia, G. W., Suga, H., Gale, L. R., Nakajima, T., Tomimura, K., & Hyakumachi, M. (2009). Population structure of Fusarium graminearum species complex from a single Japanese wheat field sampled in two consecutive years. Plant Disease, 93, 170–174.

    Article  CAS  Google Scholar 

  • Knoll, S., Mulfinger, S., Niessen, L., & Vogel, F. (2002). Rapid preparation of Fusarium DNA from cereals for diagnostic PCR using sonification and an extraction kit. Plant Pathology, 51, 728–734.

    Article  CAS  Google Scholar 

  • Leslie, J. F., & Summerell, B. A. (2006). The Fusarium laboratory manual (388 pp.). Lowa, USA: Blackwell publishing.

  • Lowe, A., Harris, S., & Ashton, P. (2005). Ecological genetics. Design, analysis, and application (344 pp.). Minnesota, USA: Blackwell Publishing.

  • Mantel, N. (1967). The detection of disease clustering and a generalized regression approach. Cancer Research, 27, 209–220.

    PubMed  CAS  Google Scholar 

  • McDonald, B. A., & Linde, C. (2002). Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology, 40, 349–379.

    PubMed  Article  CAS  Google Scholar 

  • McDonald, M. V., & Chapman, R. (1997). The incidence of Fusarium moniliforme on maize from Central America, Africa and Asia during 1992–1995. Plant Pathology, 46, 112–125.

    Article  Google Scholar 

  • Miedaner, T., Reinbrecht, C., & Schilling, A. G. (2000). Association among aggressiveness, fungal colonization, and mycotoxin production of 26 isolates of Fusarium graminearum in winter rye head blight. Journal of Plant Disease and Production, 107, 124–134.

    CAS  Google Scholar 

  • Miedaner, T., Reinbrecht, C., Lauber, U., Schollenberger, M., & Geiger, H. H. (2001). Effects of genotype and genotype x environment on deoxynivalenol accumulation and resistance to Fusarium head blight in rye, triticale, and wheat. Plant Breeding, 120, 97–105.

    Article  CAS  Google Scholar 

  • Miedaner, T., Cumagun, C. J. R., & Chakraborty, S. (2008). Population genetics of three important head blight pathogens Fusarium graminearum, F. pseudograminearum and F. culmorum. Journal of Phytopathology, 156, 129–139.

    Article  Google Scholar 

  • Miller, J. D., Greenhalgh, R., Wang, Y. Z., & Lu, M. (1991). Trichothecene chemotypes of there Fusarium species. Mycologia, 82, 121–130.

    Article  Google Scholar 

  • Naef, A., & Défago, G. (2006). Population structure of plant-pathogenic Fusarium species in overwintered stalk residues from Bt-transformed and non-transformed maize crops. European Journal of Plant Pathology, 116, 129–143.

    Article  CAS  Google Scholar 

  • Nelson, P. E., Toussoun, T. A., & Marasas, W. F. O. (1983). Fusarium species: an illustrated manual for identification (193 pp.). Pennsylvania, USA: University Park, Pennsylvania State University.

    Google Scholar 

  • Nicholson, P., Simpson, D. R., Wilson, G., Rezanoor, H. N., Lees, A. K., Parry, D. W., et al. (1998). Detection and quantification of Fusarium culmorum and Fusarium graminearum in cereals using PCR assays. Physiological and Molecular Plant Pathology, 53, 17–37.

    Article  CAS  Google Scholar 

  • Nicholson, P., Chandler, E., Draeger, R. C., Gosman, N. E., Dimpson, D. R., Thomsett, M., et al. (2003). Molecular tools to study epidemiology and toxicology of fusarium head blight of cereals. European Journal of Plant Pathology, 109, 691–703.

    Article  CAS  Google Scholar 

  • O’Donnell, K., Ward, T. J., Geiser, D. M., Kistler, H. C., & Aoki, T. (2004). 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 Genetics and Biology, 41, 600–623.

    PubMed  Article  Google Scholar 

  • O’Donnell, K., Ward, T. J., Aberra, D., Kistler, H. C., Aoki, T., Orwig, N., et al. (2008). Multilocus genotyping and molecular phylogenetics resolve a novel head blight pathogen within the Fusarium graminearum species complex from Ethiopia. Fungal Genetics and Biology, 45, 1514–1522.

    PubMed  Article  Google Scholar 

  • Peakall, R., & Smouse, P. E. (2006). Genalex 6: genetic analysis in Excel. Population genetics software for teaching and research. Molecular Ecology Notes, 6, 288–295.

    Article  Google Scholar 

  • Schmale, D. G., Leslie, J. F., Zeller, K. A., Saleh, A. A., Shields, E. J., & Bergstrom, G. C. (2006). Genetic structure of atmospheric populations of Gibberella zeae. Phytopathology, 96, 1021–1026.

    Article  CAS  Google Scholar 

  • Shaner, G. (2003). Epidemiology of Fusarium Head Blight of small grain cereals in North America. (pp. 84–119). In K. J. Leonard, & W. R. Bushnell (Eds.), Fusarium Head Blight of Wheat and Barley (512 pp.). St. Paul, Minnesota, USA: APS Press.

  • Stack, R. W. (2003). History of Fusarium head blight with emphasis on North America. (pp. 1–34). In K. J. Leonard, & W. R. Bushnell (Eds.), Fusarium Head Blight of Wheat and Barley (512 pp.). St. Paul, Minnesota, USA: APS Press.

  • Suga, H., Gale, L. R., & Kistler, H. C. (2004). Development of VNTR markers for two Fusarium graminearum clade spcies. Molecular and Ecology Notes, 4, 468–470.

    Article  CAS  Google Scholar 

  • Suga, H., Karugia, G. W., Ward, T., Gale, L. R., Tominura, K., Nakajima, T., et al. (2008). Molecular characterization of the Fusarium graminearum species complex in Japan. Phytopathology, 98, 159–166.

    PubMed  Article  CAS  Google Scholar 

  • Sutton, J. C. (1982). Epidemiology of wheat head blight and maize ear rot caused by Fusarium graminearum. Canadian Journal of Plant Pathology, 4, 195–209.

    Article  Google Scholar 

  • Ward, T. J., Bielawski, J. P., Kistler, H. C., Sullivan, E., & O’Donnell, K. (2002). Ancestral polymorphism and adaptive evolution in the trichothecene mycotoxin gene cluster of phytopathogenic Fusarium. Proceedings of the National Academy of Sciences of the United States of America, 99, 9278–9283.

    PubMed  Article  CAS  Google Scholar 

  • Ward, T. J., Clear, R. M., Rooney, A. P., O’Donnell, K., Gaba, D., Patrick, S., et al. (2008). An adaptive evolutionary shift in Fusarium head blight pathogen populations is driving the rapid spread of more toxigenic Fusarium graminearum in North America. Fungal Genetics and Biology, 45, 473–484.

    PubMed  Article  Google Scholar 

  • Windels, C. E., & Kommedahl, T. (1984). Late season colonization and survival of Fusarium graminearum group II in cornstalks in Minnesota. Plant Disease, 68, 791–793.

    Google Scholar 

  • Xu, X. M., Nicholson, P., Thomsett, M. A., Simpson, D., Cooke, B. M., Doohan, F. M., et al. (2008). Relationship between the fungal complex causing Fusarium head blight of wheat and environmental conditions. Phytopathology, 98, 69–78.

    PubMed  Article  Google Scholar 

  • Yang, L., Van der Lee, T., Yang, X., Yu, D., & Waalwijk, C. (2008). Fusarium populations on Chinese barley show a dramatic gradient in mycotoxin profiles. Phytopathology, 98, 719–727.

    PubMed  Article  CAS  Google Scholar 

  • Yli-Mattila, T., Gagkeva, T., Ward, T., Aoki, T., Kistler, H. C., & O’Donnell, K. (2009). A novel Asian clade within the Fusarium graminearum species complex includes a newly discovered cereal head blight pathogen from Russian Far East. Mycologia, 101, 841–852.

    PubMed  Article  Google Scholar 

  • Zeller, K. A., Bowden, R. L., & Leslie, J. F. (2003). Diversity of epidemic populations of Gibberella zeae from small quadrants in Kansas and North Dakota. Phytopathology, 93, 874–880.

    PubMed  Article  Google Scholar 

  • Zeller, K. A., Bowden, R. L., & Leslie, J. F. (2004). Population differentiation and recombination in wheat scab populations of Gibberella zeae from the United States. Molecular Ecology, 13, 563–571.

    PubMed  Article  Google Scholar 

  • Zhang, Z., Zhang, H., Van der Lee, T., Chen, W. Q., Arens, P., Xu, J., et al. (2010). Geographical substructure of Fusarium asiaticum isolates collected from barley in China. European Journal of Plant Pathology, 127, 239–248.

    Article  Google Scholar 

  • Zhang, H., Zhang, Z., Van der Lee, T., Xu, J., Yang, L., Yu, D., et al. (2010). Population genetic analyses of Fusarium asiaticum populations from barley suggest a recent shift favoring 3ADON producers in southern China. Phytopathology, 100, 328–336.

    PubMed  Article  CAS  Google Scholar 

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Acknowledgments

This study was funded by the State Plant Breeding Institute, Universität Hohenheim, Germany, and German Academic Exchange Service (DAAD), Bonn, Germany. We thank Dr. Todd Ward, USDA-ARS, University St., Peoria, USA, for confirming the species identification for some isolates.

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Correspondence to Thomas Miedaner.

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Talas, F., Parzies, H.K. & Miedaner, T. Diversity in genetic structure and chemotype composition of Fusarium graminearum sensu stricto populations causing wheat head blight in individual fields in Germany. Eur J Plant Pathol 131, 39–48 (2011). https://doi.org/10.1007/s10658-011-9785-3

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Keywords

  • DON
  • Fusarium head blight
  • Mycotoxin
  • Gene flow
  • Population genetics