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Population genetic structure of Mycosphaerella graminicola and Quinone Outside Inhibitor (QoI) resistance in the Czech Republic

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Abstract

Damage caused by the wheat pathogen Mycosphaerella graminicola increased rapidly during the last two decades in the Czech Republic. We collected isolates from naturally infected fields in seven wheat-growing locations and analysed these using eight microsatellite markers. All markers were highly polymorphic. We found a high degree of genetic diversity and low clonality within all sampled Czech populations. We identified 158 unique multilocus haplotypes among 184 isolates. Field populations showed weak genetic structure but we detected more differentiation between climatic regions within the Czech Republic. We compared the Czech field populations to populations from the United Kingdom, Germany and Switzerland and found a marked differentiation between Czech populations and Western European populations. We hypothesize that decades of different agricultural practices, including the use of different wheat cultivars, may explain this genetic differentiation. We detected a rapid increase in QoI fungicide resistance during the sampling period from 2005 to 2011, coinciding with the widespread application of this class of fungicides in the Czech Republic. M. graminicola populations in the Czech Republic underwent a rapid adaptive evolution from sensitivity to resistance similar to what was described earlier in Western Europe.

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References

  • Abrinbana, M., Mozafari, J., Shams-bakhsh, M., & Mehrabi, R. (2010). Genetic structure of Mycosphaerella graminicola populations in Iran. Plant Pathology, 59, 829–838.

    Article  Google Scholar 

  • Banke, S., & McDonald, B. A. (2005). Migration patterns among global populations of the pathogenic fungus Mycosphaerella graminicola. Molecular Ecology, 14, 1881–1896.

    Article  PubMed  CAS  Google Scholar 

  • Barlett, D. W., Clough, J. M., Godwin, J. R., Hall, A. A., Hamer, M., & Parr-Dobrzanski, B. (2002). The strobilurin fungicides. Pest Management Science, 58, 649–662.

    Article  Google Scholar 

  • Beerli, P. (2011). Migrate-N, version 3.2.16. Retrieved on March 1, 2012, from http://popgen.sc.fsu.edu/Migrate.

  • Boukef, S., McDonald, B. A., Yahyaoui, A., Rezgui, S., & Brunner, P. C. (2012). Frequency of mutations associated with fungicide resistance and population structure of Mycosphaerella graminicola in Tunisia. European Journal of Plant Pathology, 132, 111–122.

    Article  CAS  Google Scholar 

  • Chen, R. S., & McDonald, B. A. (1996). Sexual reproduction plays a major role in the genetic structure of populations of the fungus Mycosphaerella graminicola. Genetics, 142, 1119–1127.

    PubMed  CAS  Google Scholar 

  • Cowger, C., Hoffer, M. E., & Mundt, C. C. (2000). Specific adaptation by Mycosphaerella graminicola to a resistant wheat cultivar. Plant Pathology, 49, 445–451.

    Article  Google Scholar 

  • Desmazières, J. B. H. (1842). Cryptogames nouvelles. Annales des Sciences Naturelles, 17, 91–118.

    Google Scholar 

  • El Chartouni, L., Tisserant, B., Siah, A., Duyme, F., Leducq, J.-B., Deweer, C., Fichter-Rosin, C., Sanssené, J., Durand, R., Halama, P., & Reignauld, P. (2011). Genetic diversity and population structure in French populations of Mycosphaerella graminicola. Mycologia, 103(4), 764–774.

    Article  PubMed  Google Scholar 

  • Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611–2620.

    Article  PubMed  CAS  Google Scholar 

  • Eyal, Z. (1999). The Septoria tritici and Stagonospora nodorum blotch diseases of wheat. European Journal of Plant Pathology, 105, 629–641.

    Article  Google Scholar 

  • Eyal, Z., Scharen, A. L., Huffman, M. D., & Prescott, J. M. (1985). Global insights into virulence frequencies of Mycosphaerella graminicola. Phytopathology, 75, 1456–1462.

    Article  Google Scholar 

  • FAOstat (2012). Resource document. http://faostat.fao.org Accessed on 2 August 2012.

  • Fraaije, B. A., Cools, H. J., Fountaine, J., Lovell, D. J., Motteram, J., West, J. S., & Lucas, J. A. (2005). Role of ascospores in further spread of QoI-resistant cytochrome b alleles (G143A) in field populations of Mycosphaerella graminicola. Phytopathology, 95(8), 933–941.

    Article  PubMed  CAS  Google Scholar 

  • Gisi, U., Sierotzki, H., Cook, A., & McCaffery, A. (2002). Mechanisms influencing the evolution of resistance to Qo inhibitor fungicides. Pest Management Science, 58, 859–867.

    Article  PubMed  CAS  Google Scholar 

  • Goodwin, S. B., van der Lee, T. A. J., Cavaletto, J. R., Hekkert, B., Crane, C. F., & Kema, G. H. J. (2007). Identification and genetic mapping of highly polymorphic microsatellite loci from an EST database of Septoria tritici blotch pathogen Mycosphaerella graminicola. Fungal Genetics and Biology, 44, 398–414.

    Article  PubMed  CAS  Google Scholar 

  • Gurung, S., Goodwin, S. B., Kabbage, M., Bockus, W. W., & Adhikari, T. B. (2011). Genetic differentiation at microsatellite loci among populations of Mycosphaerella graminicola from California, Indiana, Kansas, and North Dakota. Phytopathology, 101, 1251–1259.

    Article  PubMed  CAS  Google Scholar 

  • Haubold, H., & Hudson, R. R. (2000). LIAN 3.0: detecting linkage disequilibrium in multilocus data. Bioinformatics, 16, 847–848.

    Article  PubMed  CAS  Google Scholar 

  • Jürgens, T., Linde, C. C., & McDonald, B. A. (2006). Genetic structure of Mycosphaerella graminicola populations from Iran, Argentina and Australia. European Journal of Plant Pathology, 115, 223–233.

    Article  Google Scholar 

  • Kabbage, M., Leslie, J. F., Hulbert, S. H., & Bockus, W. W. (2009). Comparison of natural populations of Mycosphaerella graminicola from single fields in Kansas and California. Physiological and Molecular Plant Pathology, 74, 55–59.

    Article  CAS  Google Scholar 

  • Linde, C. C., Zhan, J., & McDonald, B. A. (2002). Population structure of Mycosphaerella graminicola: from lesions to continents. Phytopathology, 92, 946–955.

    Article  PubMed  CAS  Google Scholar 

  • McDonald, B. A., & Linde, C. (2002a). The population genetics of plant pathogens and breeding strategies for durable resistance. Euphytica, 124, 163–180.

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Meirmans, P. G., & Van Tienderen, P. H. (2004). GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Molecular Ecology Notes, 4, 792–794.

    Article  Google Scholar 

  • Moravec, D., & Votýpka, J. (1998). Klimatická regionalizace České republiky. Karolinum: Nakladateství Univerzity Karlovy.

    Google Scholar 

  • Nei, M. (1973). Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Sciences of the United States of America, 70, 3321–3323.

    Article  PubMed  CAS  Google Scholar 

  • Nybom, H. (2004). Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Molecular Ecology, 13, 1143–1155.

    Article  PubMed  CAS  Google Scholar 

  • Owen, P. G., Pei, M., Karp, A., Royle, D. J., & Edwards, K. J. (1998). Isolation and characterization of microsatellite loci in the wheat pathogen Mycosphaerella graminicola. Molecular Ecology, 7, 1611–1612.

    Article  PubMed  CAS  Google Scholar 

  • Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.

    PubMed  CAS  Google Scholar 

  • Quaedvlieg W., Kema G. H. J., Groenewald J. Z., Verkley G. J. M., Seifbarghi S., Razavi M., Mirzadi Gohari A., Mehrabi R. & Crous P. W. (2011) Zymoseptoria gen. nov.: a new genus to accommodate Septoria-like species occuring on graminicolous hosts. Persoonia, 26, 57–69.

  • Rannala, B., & Yang, Z. (2003). Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci. Genetics, 164, 1645–1656.

    PubMed  CAS  Google Scholar 

  • Razavi, M., & Hughes, G. R. (2004). Microsatellite markers provide evidence for sexual reproduction of Mycosphaerella graminicola in Saskatchewan. Genome, 47, 789–794.

    Article  PubMed  CAS  Google Scholar 

  • Risser, P., Ebmezer, E., Korzun, V., Hartl, L., & Miedaner, T. (2011). Quantitative trait loci for adult-plant resistance to Mycosphaerella graminicola in two winter wheat populations. Phytopathology, 101(10), 1209–1216.

    Article  PubMed  CAS  Google Scholar 

  • Sanderson, F. R. (1972). A Mycosphaerella species as the ascogenous state of Septoria tritici Rob. and Desm. New Zealand Journal of Botany, 10, 707–710.

    Article  Google Scholar 

  • Schilly, A., Risser, P., Ebmeyer, E., Hartl, L., Reif, J. C., Wuerschum, T., & Miedaner, T. (2011). Stability of adult-plant resistance to Septoria tritici blotch in 24 European winter wheat varieties across nine field environments. Journal of Phytopathology, 159, 411–416.

    Google Scholar 

  • Schnieder, F., Koch, G., Jung, C., & Vereet, J. A. (1998). The application of molecular markers for genetic characterization of Septoria tritici populations. Plant Diseases and Protection, 105, 452–461.

    Google Scholar 

  • Schnieder, F., Koch, G., Jung, C., & Verreet, J. A. (2001). Genotypic diversity of the wheat leaf blotch pathogen Mycosphaerella graminicola (anamorph) Septoria tritici in Germany. European Journal of Plant Pathology, 107, 285–290.

    Article  CAS  Google Scholar 

  • Siah, A., Tisserant, B., Chartouni, L. E., Duyme, F., Deweer, C., Roisin-Fichter, C., Sanssene, J., Durand, R., Reignault, P., & Halama, P. (2010). Mating type idiomorphs from a French population of the wheat pathogen Mycosphaerella graminicola: widespread equal distribution and low but distinct levels of molecular polymorphism. Plant Pathology, 59, 661–670.

    Article  Google Scholar 

  • Šíp, V. (2003). Breeding wheat for resistance to Septoria tritici blotch in the Czech Republic. In: G.H.J. Kema, M. van Ginkel, M. Harrabi (Eds.), Global insights into the Septoria and Stagonospora diseases of cereals. Proceedings of the 6th international symposium on septoria and stagonospora diseases in cereals, Tunis, Tunisia, 169–170.

  • State Phytosanitary Administration (2012). Resource document. http://www.srs.cz Accessed on 2 August 2012.

  • Stukenbrock, E. H., Banke, S., Javan-Nikkhah, & McDonald, B. A. (2007). Origin and domestication of the fungal wheat pathogen Mycosphaerella graminicola via sympatric speciation. Molecular Biology and Evolution, 24, 398–411.

    Article  PubMed  CAS  Google Scholar 

  • Swinnen J., van Herck K., & Vranken L. (2009). Agricultural productivity in transition economies. Resource document. http://www.choicesmagazine.org/magazine/article.php?article=93 Accessed on 2 August 2012.

  • Torriani, S. F. F., Bruner, P. C., McDonald, B. A., & Sierotzki, H. (2009). QoI resistance emerged independently at least 4 times in European populations of Mycosphaerella graminicola. Pest Management Science, 65, 155–162.

    Article  PubMed  CAS  Google Scholar 

  • Waalwijk, C., Mendes, O., Verstappen, E. C. P., Waard, M. A., & Kema, G. H. J. (2002). Isolation and characterization of the mating type idiomorphs from the wheat septoria leaf blotch fungus Mycosphaerella graminicola. Fungal Genetics and Biology, 35, 277–286.

    Article  PubMed  CAS  Google Scholar 

  • Wingen, L. U., Brown, J. K. M., & Shaw, M. W. (2007). The population genetic structure of clonal organisms generated by exponentially bounded and fat-tailed dispersal. Genetics, 177, 435–448.

    Article  PubMed  Google Scholar 

  • Zhan, J., Mundt, C. C., Hoffer, M. E., & McDonald, B. A. (2002a). Local adaptation and effect of host genotype on the rate of pathogen evolution: an experimental test in plant pathosystem. Journal of Evolutionary Biology, 15, 634–647.

    Article  Google Scholar 

  • Zhan, J., Kema, G. H. J., Waalwijk, C., & McDonald, B. A. (2002b). Distribution of mating type alleles in the wheat pathogen Mycosphaerella graminicola over spatial scales from lesions to continents. Fungal Genetics and Biology, 36, 128–136.

    Article  PubMed  CAS  Google Scholar 

  • Zhan, J., Pettway, R. E., & McDonald, B. A. (2003). The global genetic structure of the wheat pathogen Mycosphaerella graminicola is characterized by high nuclear diversity, low mitochondrial diversity, regular recombination, and gene flow. Fungal Genetics and Biology, 38, 286–297.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We would like to thank Lubomír Věchet for providing some of the isolates used in this study. This work was financially supported by a Ministry of Agriculture grant (QH 81284) from the Czech government. Data analyzed in this paper were partly generated in the Genetic Diversity Centre of ETH Zurich.

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Correspondence to Daniel Croll.

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Drabešová, J., Ryšánek, P., Brunner, P. et al. Population genetic structure of Mycosphaerella graminicola and Quinone Outside Inhibitor (QoI) resistance in the Czech Republic. Eur J Plant Pathol 135, 211–224 (2013). https://doi.org/10.1007/s10658-012-0080-8

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