Advertisement

European Journal of Plant Pathology

, Volume 137, Issue 4, pp 743–752 | Cite as

Head-blighting populations of Fusarium culmorum from Germany, Russia, and Syria analyzed by microsatellite markers show a recombining structure

  • Thomas MiedanerEmail author
  • Franciele Caixeta
  • Firas Talas
Article

Abstract

Fusarium culmorum is a haploid, worldwide occurring phytopathogenic fungus causing seedling blight, foot rot, and head blight of cereals and producing the mycotoxins deoxynivalenol (DON) and nivalenol (NIV) associated with health hazards in human and animals. The fungus reproduces asexually by conidiospores, a teleomorph is not known. We analyzed for the first time naturally occurring F. culmorum populations collected randomly in the field from infected wheat heads. A total of 186 isolates, from three populations from Germany (GER), Russia (RUS), Syria (SYR), as well as an international collection (INT) for comparison, were genotyped by 10 microsatellite (SSR, single sequence repeat) markers. A high genetic diversity within the three natural populations and the INT population as well was detected. About 90 % of multi-locus haplotypes (MLH) were unique across populations. The largest part of variance (81 %) was found within populations. Accordingly, population subdivision was low, fixation indices were significant only in one out of six comparisons, while estimates of gene flow (N m ) ranged from 0.8–4.8. Linkage equilibrium was revealed by the index of multi-locus association and the quotient of observed and expected variance when two linked markers were deleted. DON and NIV chemotypes grouped closely together in a principle coordinate analysis. SYR isolates were partly separated from GER and RUS populations. All population-genetic parameters were in a similar range compared to those for the sexually propagating species F. graminearum. In conclusion, results support the hypothesis of a recombining structure in F. culmorum as revealed by the high genetic variation within populations, a low fixation index and low gametic phase disequilibrium within populations.

Keywords

Fungal populations Fusarium head blight Population structure Recombination 

Notes

Acknowledgments

This study was funded by the German Academic Exchange Service (DAAD), Bonn, Germany, by grants to FT and FC, and the State Plant Breeding Institute of the Universitaet Hohenheim, Germany. We thank Prof. Dr. M. Levitin and Dr. T. Yu. Gagkaeva (All-Russian Institute of Plant Protection, Saint-Petersburg, Russia) for generously sharing the RUS population with us.

Supplementary material

10658_2013_284_MOESM1_ESM.docx (30 kb)
Additional file 1 - Supplementary Table S1 Details of the isolates from the international collection (NA = not available) (DOCX 29 kb)
10658_2013_284_MOESM2_ESM.docx (27 kb)
Additional file 2 - Supplementary Table S2 Name, use and sequence of oligonucleotides and the product size (DOCX 27 kb)
10658_2013_284_MOESM3_ESM.docx (67 kb)
Additional file 3 - Supplementary Figure S1 Determination of the optimal number of clusters (K) among all isolates used in this study (DOCX 67.3 kb)
10658_2013_284_MOESM4_ESM.docx (22 kb)
Additional file 4 - Supplementary Table S3 Variation among (Va) and between (Vb) populations, fixation index (Fst) and gene flow (Nm) for the individual ten SSR loci (DOCX 21 kb)
10658_2013_284_Fig4_ESM.jpg (2.1 mb)
Additional file 5 - Supplementary Figure S2

Projection of the used primers on the draft genetic map of Fusarium graminearum (*Two primers F10 and F11 could not be assigned) (JPEG 2182 kb)

10658_2013_284_MOESM5_ESM.eps (709 kb)
High resolution image (EPS 709 kb)

References

  1. Abramson, D., Clear, R. M., Gaba, D., Smith, D., Patrick, S. K., & Saydak, D. (2001). Trichothecene and moniliformin production by Fusarium isolates from western Canadian wheat. Journal of Food Protection, 64, 1220–1225.PubMedGoogle Scholar
  2. Agapow, P.-M., & Burt, A. (2001). Indices of multilocus linkage disequilibrium. Molecular and Ecological Notes, 1, 101–102.CrossRefGoogle Scholar
  3. Audenaert, K., van Broeck, R., van Bekaert, B., de Witte, F., Heremans, B., Messens, K., et al. (2009). Fusarium head blight (FHB) in Flanders: population diversity, inter-species associations and DON contamination in commercial winter wheat varieties. European Journal of Plant Pathology, 125, 445–458.CrossRefGoogle Scholar
  4. Bakan, B., Pinson, L., Cahagnier, B., Melcion, D., Sémon, E., & Richard-Molard, D. (2001). Toxigenic potential of Fusarium culmorum strains isolated from French wheat. Food Additives and Contaminants, 18, 998–1003.PubMedCrossRefGoogle Scholar
  5. Çepni, E., Tunali, B., & Gürel, F. (2012). Genetic diversity and mating types of Fusarium culmorum and Fusarium graminearum originating from different agro-ecological regions in Turkey. Journal of Basic Microbiology, 52, 1–9.Google Scholar
  6. Demeke, T., Clear, R. M., Patrick, S. K., & Gaba, D. (2005). 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.PubMedCrossRefGoogle Scholar
  7. Evanno, G., Regnaut, S., & Goudet, J. (2005). Detection the number of clusters of individuals using the software STRUCTURE: A simulation study. Molecular Ecology, 14, 2611–2620.PubMedCrossRefGoogle Scholar
  8. Gang, G., Miedaner, T., Schuhmacher, U., Schollenberger, M., & Geiger, H. H. (1998). Deoxynivalenol and nivalenol production by Fusarium culmorum isolates differing in aggressiveness toward winter rye. Phytopathology, 88, 879–884.PubMedCrossRefGoogle Scholar
  9. Gargouri, S., Bernier, L., Hajlaoui, M. R., & Marrakchi, M. (2003). Genetic variability and population structure of the wheat foot rot fungus, Fusarium culmorum, in Tunisia. European Journal of Plant Pathology, 109, 807–815.CrossRefGoogle Scholar
  10. Gerlach, W., & Nirenberg, H. (1982). The Genus Fusarium — a Pictorial Atlas. Mitteilungen aus der Biologischen Bundesanstalt für Land- u. Forstwirtschaft, vol. 209.Google Scholar
  11. 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.CrossRefGoogle Scholar
  12. Gordon, D. M. (1997). The genetic structure of Escherichia coli populations in feral house mice. Microbiology, 143, 2039–2046.PubMedCrossRefGoogle Scholar
  13. Goswami, R. S., & Kistler, H. C. (2004). Heading for disaster: Fusarium graminearum on cereal crops. Molecular Plant Pathology, 5, 515–525.PubMedCrossRefGoogle Scholar
  14. Hartl, D. L., & Clark, A. G. (2007). Principles of population genetics (4th ed.). Minnesota: Sinauer Associates Press. 652 pp.Google Scholar
  15. Jennings, P., Coates, M. E., Turner, J. A., Chandler, E. A., & Nicholson, P. (2004). Determination of deoxynivalenol and nivalenol chemotypes of Fusarium culmorum isolates from England and Wales by PCR assay. Plant Pathology, 53, 182–190.CrossRefGoogle Scholar
  16. Kammoun, L. G., Gargouri, S., Barreau, C., Richard-Forget, F., & Hajlaoui, M. R. (2010). Trichothecene chemotypes of Fusarium culmorum infecting wheat in Tunisia. International Journal of Food Microbiology, 140, 84–89.PubMedCrossRefGoogle Scholar
  17. Kosiak, B., Skjerve, E., Thrane, U., & Torp, M. (2003). The prevalence and distribution of Fusarium species in Norwegian cereals: a survey. Acta Agriculturae Scandinavica, 53, 168–176.Google Scholar
  18. Langseth, W., Bernhoft, A., Rundberget, T., Kosiak, B., & Gareis, M. (1999). Mycotoxin production and cytotoxicity of Fusarium strains isolated from Norwegian cereals. Mycopathologia, 144, 103–113.CrossRefGoogle Scholar
  19. Leslie, J. F., & Summerell, B. A. (2006). The Fusarium laboratory manual. Iowa: Blackwell publishing. 388 pp.CrossRefGoogle Scholar
  20. Lienemann, K. (2002). Incidence of Fusarium species in winter wheat in the Rhineland and possibilities of control with special reference to wheat cultivars. Ph.D. Thesis, Universitaet Bonn, Germany.Google Scholar
  21. McDonald, B. A., & Linde, C. (2002). The population genetics of plant pathogens and breeding for durable resistance. Euphytica, 124, 163–180.CrossRefGoogle Scholar
  22. Miedaner, T., Gang, G., & Geiger, H. H. (1996). Quantitative-genetic basis of aggressiveness of 42 isolates of Fusarium culmorum for winter rye head blight. Plant Disease, 80, 500–504.CrossRefGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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.CrossRefGoogle Scholar
  25. Mirocha, C. J., Xie, W., Xu, Y., Wilcoxson, R. D., Woodward, R. P., Etebarian, R. H., et al. (1994). Production of trichothecene mycotoxins by Fusarium graminearum and Fusarium culmorum or barley and wheat. Mycopathologia, 128, 19–23.PubMedCrossRefGoogle Scholar
  26. Mishra, P. K., Fox, R. T. V., & Culham, A. (2002). Restriction analysis of PCR amplified nrDNA regions revealed intraspecific variation within populations of Fusarium culmorum. FEMS Microbiology Letters, 215, 291–296.PubMedCrossRefGoogle Scholar
  27. Mishra, P. K., Fox, R. T. V., & Culham, A. (2003). Inter-simple sequence repeat and aggressiveness analyses revealed high genetic diversity, recombination and long-range dispersal in Fusarium culmorum. Annals of Applied Biology, 143, 291–301.CrossRefGoogle Scholar
  28. Muthomi, J. W., Schütze, A., Dehne, H. W., Mutitu, E. W., & Oerke, E. C. (2000). Characterization of Fusarium culmorum isolates by mycotoxin production and aggressiveness to winter wheat. Journal of Plant Diseases and Protection, 107, 113–123.Google Scholar
  29. 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.CrossRefGoogle Scholar
  30. O’Donnell, K., Kistler, H. C., Tacke, B. K., & Casper, H. H. (2000). Gene genealogies reveal global phylogeographic structure and reproductive isolation among lineages of Fusarium graminearum, the fungus causing wheat scab. Proceedings of the National Academy of Sciences of the United States of America, 97, 7905–7910.PubMedCrossRefGoogle Scholar
  31. Obanor, F., Erginbas-Orakci, G., Tunali, B., Nicol, J. M., & Chakraborty, S. (2010). Fusarium culmorum is a single phylogenetic species based on multilocus sequence analysis. Fungal Biology, 114, 753–765.PubMedCrossRefGoogle Scholar
  32. Parry, D. W., Jenkinson, P., & McLeod, L. (1995). Fusarium ear blight (scab) in small grain cereals-a review. Plant Pathology, 44, 207–238.CrossRefGoogle Scholar
  33. 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.CrossRefGoogle Scholar
  34. Pritchard, J. K., Stephens, M., & Donnely, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.PubMedGoogle Scholar
  35. Puhalla, J. E. (1981). Genetic considerations of the genus Fusarium. In P. E. Nelson, T. A. Toussoun, & R. J. Cook (Eds.), Fusarium: diseases, biology and taxonomy (pp. 291–305). Pennsylvania: The Pennsylvania State University Press.Google Scholar
  36. Salamati, S., Zhan, J., Burdon, J. J., & McDonald, B. A. (2000). The genetic structure of field populations of Rhynchosporium secalis from three continents suggests moderate gene flow and regular recombination. Phytopathology, 90, 901–908.PubMedCrossRefGoogle Scholar
  37. Scherm, B., Balmas, V., Spanu, F., Pani, G., Delogu, G., Pasquali, M., et al. (2013). Fusarium culmorum: causal agent of foot and root rot and head blight on wheat. Molecular Plant Pathology, 14, 323–341.PubMedCrossRefGoogle Scholar
  38. Sokal, S. D., & Michener, C. D. (1958). A statistical method for evaluating systematic relationships. University of Kansas Science Bulletin, 38, 1409–1438.Google Scholar
  39. Suga, H., Gale, L. R., & Kistler, H. C. (2004). Development of VNTR markers for two Fusarium graminearum clade species. Molecular and Ecology Notes, 4, 468–470.CrossRefGoogle Scholar
  40. Talas, F., Parzies, H. K., & Miedaner, T. (2011). Diversity in genetic structure and chemotype composition of Fusarium graminearum sensu stricto populations causing wheat head blight in individual fields in Germany. European Journal of Plant Pathology, 131, 39–48.CrossRefGoogle Scholar
  41. Tóth, B., Mesterhazy, A., Nicholson, P., Teren, J., & Varga, J. (2004). Mycotoxin production and molecular variability of European and American isolates of Fusarium culmorum. European Journal of Plant Pathology, 110, 587–599.CrossRefGoogle Scholar
  42. Verstraete, F. (2008). European Union Legislation on mycotoxins in food and feed. Overview of the decision-making process and recent and future developments. In J. F. Leslie, R. Bandyopadhyay, & A. Visconti (Eds.), Mycotoxins: Detection methods, management, public health and agricultural trade (pp. 77–99). Wallingford: CABI Publishing.CrossRefGoogle Scholar
  43. Vigier, B., Reid, L. M., Seifert, K. A., Sterwert, D. W., & Hamilton, R. I. (1997). Distribution and prediction of Fusarium species associated with maize ear rot in Ontario. Canadian Journal of Plant Pathology, 19, 60–65.CrossRefGoogle Scholar
  44. Vogelgsang, S., Windmer, F., Jenny, E., & Enkerli, J. (2009). Characterisation of novel Fusarium graminearum microsatellite markers in different Fusarium species from various countries. European Journal of Plant Pathology, 123, 477–482.CrossRefGoogle Scholar
  45. Waalwijk, C., Kastelein, P., de Vries, I., Kerenyi, Z., Van der Lee, T., Hesselink, T., et al. (2003). Major changes in Fusarium spp. in wheat in the Netherlands. European Journal of Plant Pathology, 10, 743–754.CrossRefGoogle Scholar
  46. Wagacha, J. M., & Muthomi, J. W. (2007). Fusarium culmorum; infection process, mechanisms of mycotoxin production and their role in pathogenesis in wheat. Crop Protection, 26, 877–885.CrossRefGoogle Scholar
  47. Xu, X., Parry, D., Nicholson, P., Thomsett, M., Simpson, D., Edwards, S., et al. (2005). Predominance and association of pathogenic fungi causing Fusarium ear blight in wheat in four European countries. European Journal of Plant Pathology, 112, 143–154.CrossRefGoogle Scholar
  48. Yörük, E., & Albayrak, G. (2012). Chemotyping of Fusarium graminearum and F. culmorum isolates from Turkey by PCR assay. Mycopathologia, 173, 53–61.PubMedCrossRefGoogle Scholar
  49. 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.PubMedCrossRefGoogle Scholar

Copyright information

© KNPV 2013

Authors and Affiliations

  • Thomas Miedaner
    • 1
    Email author
  • Franciele Caixeta
    • 1
    • 2
  • Firas Talas
    • 1
    • 3
  1. 1.State Plant Breeding Institute (720)Universitaet HohenheimStuttgartGermany
  2. 2.Department of Agriculture, Central Seed LaboratoryUniversidade Federal de LavrasLavrasBrazil
  3. 3.ETH Zürich, Institute für Integrative BiologyZürichSwitzerland

Personalised recommendations