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European Journal of Plant Pathology

, Volume 152, Issue 2, pp 327–341 | Cite as

Population structure and frequency differences of CYP51 mutations in Zymoseptoria tritici populations in the Nordic and Baltic regions

  • Nana Vagndorf
  • Thies Marten Heick
  • Annemarie Fejer Justesen
  • Jeppe Reitan Andersen
  • Ahmed Jahoor
  • Lise Nistrup Jørgensen
  • Jihad Orabi
Article

Abstract

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.

Keywords

Septoria leaf blotch Mycosphaerella graminicola Genetic diversity Genetic structure Fungicide resistance Mutations 

Notes

Acknowledgements

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.

Supplementary material

10658_2018_1478_MOESM1_ESM.docx (34 kb)
ESM 1 (DOCX 34 kb)

References

  1. Banke, S., Peschon, A., & McDonald, B. (2004). Phylogenetic analysis of globally distributed Mycosphaerella graminicola populations based on three DNA sequence loci. Fungal Genetics and Biology, 41(2), 226–238.  https://doi.org/10.1016/j.fgb.2003.09.006.CrossRefPubMedGoogle Scholar
  2. 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
  3. 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
  4. Brunner, P. C., Stefanato, F. L., & McDonald, B. (2008). Evolution of the CYP51 gene in Mycosphaerella graminicola: Evidence for intragenic recombination and selective replacement. Molecular Plant Pathology, 9, 305–316.  https://doi.org/10.1111/j.1364-3703.2007.00464.x.CrossRefPubMedGoogle Scholar
  5. 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
  6. Cools, H., & Fraaije, B. A. (2008). Are azole fungicides losing ground against Septoria wheat disease? Resistance mechanisms in Mycosphaerella graminicola. Pest Management Science, 64(7), 681–684.  https://doi.org/10.1002/ps.1568.CrossRefPubMedGoogle Scholar
  7. Cowger, C., Hoffer, M. E., & Mundt, C. C. (2000). Specific adaptation by Mycosphaerella graminicola to a resistant wheat cultivar. Plant Pathology, 49(4), 445–451.  https://doi.org/10.1046/j.1365-3059.2000.00472.x.CrossRefGoogle Scholar
  8. Dooley, H., Shaw, M. W., Mehenni-Ciz, J., Spink, J., & Kildea, S. (2016). Detection of Zymoseptoria tritici SDHI-insensitive field isolates carrying the SdhC-H152R and SdhD-R47W substitutions. Pest Management Science, 72(12), 2203–2207.  https://doi.org/10.1002/ps.4269.CrossRefPubMedGoogle Scholar
  9. El Chartouni, L., Tisserant, B., Siah, A., Duyme, F., Leducq, J.-B., Deweer, C., et al. (2011). Genetic diversity and population structure in French populations of Mycosphaerella graminicola. Mycologia, 103(4), 764–774.  https://doi.org/10.3852/10-184.CrossRefPubMedGoogle Scholar
  10. Eriksen, L., & Munk, L. (2003). The occurrence of Mycosphaerella graminicola and its anamorph Septoria tritici in winter wheat during the growing season. European Journal of Plant Pathology, 109(3), 253–259.  https://doi.org/10.1023/A:1022851502770.CrossRefGoogle Scholar
  11. Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Molecular Ecology, 14(8), 2611–2620.  https://doi.org/10.1111/j.1365-294X.2005.02553.x.CrossRefPubMedGoogle Scholar
  12. 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
  13. 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
  14. 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
  15. 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
  16. Grimmer, M. K., van den Bosch, F., Powers, S. J., & Paveley, N. D. (2014). Fungicide resistance risk assessment based on traits associated with the rate of pathogen evolution. Pest Management Science, 71(2), 207–215.  https://doi.org/10.1002/ps.3781.CrossRefPubMedGoogle Scholar
  17. 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
  18. Heick, T. M., Justesen, A. F., & Jørgensen, L. N. (2017b). Resistance of wheat pathogen Zymoseptoria tritici to DMI and QoI fungicides in the Nordic-Baltic region - a status. European Journal of Plant Pathology, 149(3), 669–682.  https://doi.org/10.1007/s10658-017-1216-7.CrossRefGoogle Scholar
  19. 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.
  20. Jørgensen, L. N., van den Bosch, F., Oliver, R. P., Heick, T. M., & Paveley, N. (2017). Targeting fungicide inputs according to need. Annual Review of Phytopathology, 55, 181–203.  https://doi.org/10.1146/annurev-phyto-080516.CrossRefPubMedGoogle Scholar
  21. 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
  22. 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
  23. 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
  24. Linde, C. C., Zhan, J., & McDonald, B. A. (2002). Population structure of Mycosphaerella graminicola: From lesions to continents. Phytopathology, 92(9), 946–955.  https://doi.org/10.1094/PHYTO.2002.92.9.946.CrossRefPubMedGoogle Scholar
  25. Lucas, J. A., Hawkins, N. J., & Fraaije, B. A. (2015). The evolution of fungicide resistance. Advances in Applied Microbiology, 90, 29–92.  https://doi.org/10.1016/bs.aambs.2014.09.001.CrossRefPubMedGoogle Scholar
  26. McDonald, B. A., & Mundt, C. C. (2016). How knowledge of pathogen population biology informs Management of Septoria Tritici Blotch. Phytopathology, 106(9), 948–955.  https://doi.org/10.1094/PHYTO-03-16-0131-RVW.CrossRefPubMedGoogle Scholar
  27. Naouari, M., Siah, A., Elgazzah, M., Reignault, P., & Halama, P. (2016). Mitochondrial DNA-based genetic diversity and population structure of Zymoseptoria tritici in Tunisia. European Journal of Plant Pathology, 146(2), 305–314.  https://doi.org/10.1007/s10658-016-0915-9.CrossRefGoogle Scholar
  28. Oerke, E. C. (2006). Crop losses to pests. The Journal of Agricultural Science, 144(1), 31.  https://doi.org/10.1017/S0021859605005708.CrossRefGoogle Scholar
  29. Orabi, J., Jahoor, A., & Backes, G. (2014). Changes in allelic frequency over time in European bread wheat (Triticum aestivum L.) varieties revealed using DArT and SSR markers. Euphytica, 197(3), 447–462.  https://doi.org/10.1007/s10681-014-1080-x.CrossRefGoogle Scholar
  30. Peakall, R., & Smouse, P. E. (2012). GenALEx 6.5: Genetic analysis in excel. Population genetic software for teaching and research-an update. Bioinformatics, 28(19), 2537–2539.  https://doi.org/10.1093/bioinformatics/bts460.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Pritchard, J. K. (2010). Documentation for structure software : Version 2 . 3. In Practice, 6(3), 321–326.  https://doi.org/10.1002/spe.4380060305.Google Scholar
  32. Raman, H., & Milgate, a. (2012). Molecular breeding for Septoria tritici blotch resistance in wheat. Cereal Research Communications, 40(4), 451–466.  https://doi.org/10.1556/CRC.40.2012.4.1.CrossRefGoogle Scholar
  33. Razavi, M., & Hughes, G. R. (2004). Microsatellite markers provide evidence for sexual reproduction of Mycosphaerella graminicola in Saskatchewan. Genome, 47(5), 789–794.  https://doi.org/10.1139/G04-036.CrossRefPubMedGoogle Scholar
  34. Rehfus, A., Strobel, D., Bryson, R., & Stammler, G. (2017). Mutations in sdh genes in field isolates of Zymoseptoria tritici and impact on the sensitivity to various succinate dehydrogenase inhibitors. Plant Pathology, 67, 175–180.  https://doi.org/10.1111/ppa.12715.CrossRefGoogle Scholar
  35. 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
  36. Schneider, F., Koch, G., Jung, C., & Verreet, J. A. (2001). Genotypic diversity of the wheat leaf blotch pathogen Mycospaerella graminicola (anamorph) Septoria tritici in Germany. European Journal of Plant Pathology, 107, 285–290.CrossRefGoogle Scholar
  37. 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
  38. 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
  39. Suffert, F., & Sache, I. (2011). Relative importance of different types of inoculum to the establishment of Mycosphaerella graminicola in wheat crops in north-West Europe. Plant Pathology, 60(5), 878–889.  https://doi.org/10.1111/j.1365-3059.2011.02455.x.CrossRefGoogle Scholar
  40. Torriani, S. F. F., Brunner, 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(2), 155–162.  https://doi.org/10.1002/ps.1662.CrossRefPubMedGoogle Scholar
  41. Vos, P., Hogers, R., Bleeker, M., Reijans, M., Van De Lee, T., Hornes, M., et al. (1995). AFLP: A new technique for DNA fingerprinting. Nucleic Acids Research, 23(21), 4407–4414.  https://doi.org/10.1093/nar/23.21.4407.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 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
  43. 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
  44. Zhan, J., & McDonald, B. A. (2004). The interaction among evolutionary forces in the pathogenic fungus Mycosphaerella graminicola. Fungal Genetics and Biology, 41, 590–599.  https://doi.org/10.1016/j.fgb.2004.01.006.CrossRefPubMedGoogle Scholar
  45. 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
  46. 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

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2018

Authors and Affiliations

  • Nana Vagndorf
    • 1
    • 2
  • Thies Marten Heick
    • 2
  • Annemarie Fejer Justesen
    • 2
  • Jeppe Reitan Andersen
    • 1
  • Ahmed Jahoor
    • 1
    • 3
  • Lise Nistrup Jørgensen
    • 2
  • Jihad Orabi
    • 1
  1. 1.Nordic Seed A/SOdderDenmark
  2. 2.Department of AgroecologyAarhus UniversitySlagelseDenmark
  3. 3.Department of Plant BreedingSwedish University of Agricultural SciencesAlnarpSweden

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