Population structure and frequency differences of CYP51 mutations in Zymoseptoria tritici populations in the Nordic and Baltic regions
Septoria tritici blotch caused by the fungus Zymoseptoria tritici (formerly Mycosphaerella graminicola) is one of the most yield-reducing diseases worldwide. Effective disease management involves the use of resistant cultivars and application of fungicides. In this study, the population structure and genetic diversity of 183 Z. tritici isolates from Denmark, Sweden, Finland and the Baltic countries were analysed by molecular markers. In population structure analysis, isolates from Denmark and Sweden were grouped together, whereas isolates from the Baltics and Finland were grouped together. Analysis of genetic diversity and ϕ-values confirmed the division of Nordic and Baltic regions. Danish isolates sampled from different regions and different varieties were not genetically different. However, significant genetic differences were detected between isolates sampled from different years in Denmark and for isolates sampled from specific cultivars in different years. Additionally, the frequency of several known point mutations in the gene cyp51, conferring decreased sensitivity to DMI fungicides, was investigated. Several of the examined mutations were detected at a lower frequency in Baltic isolates compared to Danish and Swedish isolates. Analysis of the Danish population revealed a significant increase in specific mutations over the years. Lastly, some mutations were significantly more frequent in isolates derived from certain varieties. By using different resistance sources in breeding programmes and application of a wide range of fungicides, a sustainable and efficient disease management can be obtained.
KeywordsSeptoria leaf blotch Mycosphaerella graminicola Genetic diversity Genetic structure Fungicide resistance Mutations
This project is funded by the Danish Research Council and Pajbjerg Foundation. We appreciate the help from Vahid Edriss in genetic analysis. We thank laboratory technician Hanne Svenstrup from Nordic Seed, and laboratory technicians Birgitte Boyer Frederiksen and Hanne-Birgitte Christiansen from Aarhus Univeristy, Flakkebjerg for supporting laboratory work. We also appreciate the help from Kirsten Jensen for proofreading of the manuscript.
Compliance with ethical standards
Conflicts of interests
This study was done as cooperation. The authors are employees at the breeding company Nordic Seed A/S and Aarhus University. The authors declare that there are no conflicts of interests.
The work was funded by the Danish Research Council and Pajbjerg Foundation.
- Berraies, S., Salah Gharbi, M., Belzile, F., Yahyaoui, A., Hajlaoui, M. R., Trifi, M., et al. (2013). High genetic diversity of Mycospaherella graminicola (Zymoseptoria tritici) from a single wheat field in Tunisia as revealed by SSR markers. African Journal of Biotechnology, 12, 1344–1349. https://doi.org/10.5897/AJB12.2299.Google Scholar
- 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. https://doi.org/10.1007/s10658-011-9853-8.CrossRefGoogle Scholar
- Chen, R., & McDonald, B. A. (1996). Sexual reproduction plays a major role in the genetic structure of populations of the fungus Mycosphaerella graminicola. Genetics, 142(4), 1119–1127. http://www.genetics.org/content/142/4/1119%5Cn http://www.genetics.org/content/142/4/1119.full.pdf%5Cn http://www.genetics.org/content/142/4/1119.long%5Cn http://www.ncbi.nlm.nih.gov/pubmed/8846892
- Eyal, Z., Scharen, A. L., Prescott, J. M., & van Ginkel, M. (1987). The Septoria diseases of wheat: Concepts and methods of disease management. CIMMYT Mexico.Google Scholar
- FAOSTAT. 2016. Anonymous. http://www.fao.org/resources/infographics/infographics-details/en/c/240943/. Accessed April 2017
- 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. https://doi.org/10.1094/PHYTO-95-0933.CrossRefPubMedGoogle Scholar
- Ghaffary, S. M. T., Robert, O., Laurent, V., Lonnet, P., Margalé, E., van der Lee, T. J., et al. (2011). Genetic analysis of resistance to septoria tritici blotch in the French winter wheat cultivars balance and apache. TAG. Theoretical and applied genetics. Theoretische und angewandte Genetik, 123(5), 741–754. https://doi.org/10.1007/s00122-011-1623-7.CrossRefPubMedGoogle Scholar
- Ghaffary, S. M. T., Faris, J. D., Friesen, T. L., Visser, R. G. F., van der Lee, T. J., Robert, O., & Kema, G. H. J. (2012). New broad-spectrum resistance to septoria tritici blotch derived from synthetic hexaploid wheat. Theoretical and Applied Genetics, 124(1), 125–142. https://doi.org/10.1007/s00122-011-1692-7.CrossRefGoogle Scholar
- Heick, T., Jørgensen, L. N., Christiansen, H., & Olsen, B. (2017a). Fungicide resistance-related investigations. In: Applied crop protections 2016. DCA report, Markbrug. nr. 094.78–84.Google Scholar
- Jørgensen, L. N., Hovmøller, M. S., Hansen, J. G., Lassen, P., Clark, B., Bayles, R., Rodemann B., Flath K., Jahn M., Goral T., Jerzy Czembor J., Cheyron P., Maumene C., de Pope C., Ban R., Nielsen G. C., Berg G. (2014). IPM strategies and their dilemmas including an introduction to www.eurowheat.org. Journal of Integrative Agriculture, 13, 265–281 https://doi.org/10.1016/S2095-3119(13)60646-2.
- Kabbage, M., Leslie, J. F., Zeller, K. A., Hulbert, S. H., & Bockus, W. W. (2008). Genetic diversity of Mycosphaerella graminicola, the causal agent of Septoria tritici blotch, in Kansas winter wheat. Journal of Agricultural, Food, and Environmental Sciences, 2(1).Google Scholar
- Kildea, S., Mehenni-Ciz, J., Spink, J., & O’Sullivan, E. (2014). Changes in the frequency of Irish Mycosphaerella graminicola CYP51 variants 2006–2011. In: 17th international Teinhardsbrunn symposium (pp. 143–144).Google Scholar
- Leroux, P., Albertini, C., Gautier, A., Gredt, M., & Walker, A. S. (2007). Mutations in the CYP51 gene correlated with changes in sensitivity to sterol 14α-demethylation inhibitors in field isolates of Mycosphaerella graminicola. Pest Management Science, 63(7), 688–698. https://doi.org/10.1002/ps.1390.CrossRefPubMedGoogle Scholar
- Saghai-Maroof, M. A., Soliman, K. M., Jorgensen, R. A., & Allard, R. W. (1984). Ribosomal DNA spacer-length polymorphisms in barley: Mendelian inheritance, chromosomal location, and population dynamics. Proceedings of the National Academy of Sciences of the United States of America, 81(24), 8014–8018. https://doi.org/10.1073/pnas.81.24.8014.CrossRefPubMedPubMedCentralGoogle Scholar
- Shaw, M. W. (1990). Effects of temperature, leaf wetness and cultivar on the latent period of Mycosphaerella graminicola on winter wheat. Plant Pathology, 39(2), 255–268. https://doi.org/10.1111/j.1365-3059.1990.tb02501.x.CrossRefGoogle Scholar
- Shaw, M. W., & Royle, D. J. (1989). Airborne inoculum as a major source of Septoria tritici (Mycosphaerella graminicola) infections in winter wheat crops in the UK. Plant Pathology, 38(1), 35–43. https://doi.org/10.1111/j.1365-3059.1989.tb01425.x.CrossRefGoogle Scholar
- Wieczorek, T., Berg, G., Semaškienė, R., Mehl, A., Sierotzki, H., Stammler, G., et al. (2015). Impact of DMI and SDHI fungicides on disease control and CYP51 mutations in populations of Zymoseptoria tritici from northern Europe. European Journal of Plant Pathology, 143, 861–871. https://doi.org/10.1007/s10658-015-0737-1.CrossRefGoogle Scholar
- Zeller, K. A., Jurgenson, J. E., El-Assiuty, E. M., & Leslie, J. F. (2000). Isozyme and amplified fragment length polymorphisms from Cephalosporium maydis in Egypt. Phytoparasitica, 28(2), 121–130 http://www.phytoparasitica.org/phyto/pdfs/2000/issue2/zelly.pdf.CrossRefGoogle 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.CrossRefPubMedGoogle Scholar
- Zhan, J., Stefanato, F. L., & Mcdonald, B. A. (2006). Selection for increased cyproconazole tolerance in Mycosphaerella graminicola through local adaptation and in response to host resistance. Molecular Plant Pathology, 7(4), 259–268. https://doi.org/10.1111/j.1364-3703.2006.00336.x.CrossRefPubMedGoogle Scholar