Abstract
Subpopulations of the wheat pathogen Zymoseptoria tritici (26 sample groups composed of 794 isolates) were collected in two nearby wheat fields in the Paris basin, during both epidemic and inter-epidemic periods of three successive years (2009–2013). In addition to the type of inoculum (ascospores vs. pycnidiospores), the alternative presence of wheat debris allowed taking into account its putative origin (local vs. distant). We used a molecular epidemiology approach, based on population genetic indices derived from SSR marker analysis, to describe putative changes in the structure and genotypic diversity of these subpopulations over 3 years, at a spatiotemporal scale consistent with epidemiological observations. Genetic structure was broadly stable over time (within and between years) and between fields, however with weak population differentiation over time. All subpopulations displayed very high diversity and the occurrence of regular sexual reproduction was confirmed in the two fields. A significant increase of the MAT1–1/MAT1–2 ratio was observed over the course of the epidemics. This original finding suggests a competitive advantage of MAT1–1 strains consistently with their greater pathogenicity reported in the literature and may reveal undescribed adaptation. Finally, we found that the period, the type of inoculum and its putative origin had little effect on the short term evolution of the local population of Z. tritici. Fungal population size and diversity are apparently large enough to prevent genetic drift at this fine spatiotemporal scale, and more likely short distance migration contributes strongly to the stabilization of genetic diversity among and within plots.
Similar content being viewed by others
References
Abang, M. M., Baum, M., Ceccarelli, S., Grando, S., Linde, C. C., Yahyaoui, A., Zhan, J., & McDonald, B. A. (2006). Differential selection on Rhynchosporium secalis during parasitic and saprophytic phases in the barley scald disease cycle. Phytopathology, 96, 1214–1222.
Abrinbana, M., Mozafari, J., Shams-Bakhsh, M., & Mehrabi, R. (2010). Genetic structure of Mycosphaerella graminicola populations in Iran. Plant Pathology, 59, 829–838.
Agapow, P. M., & Burt, A. (2001). Indices of multilocus linkage disequilibrium. Molecular Ecology Notes, 1, 101–102.
Ali, S., Gladieux, P., Rahman, H., Saqib, M. S., Fiaz, M., Ahmad, H., Leconte, M., Gautier, A., Justesen, A. F., Hovmøller, M. S., Enjalbert, J., & de Vallavieille-Pope, C. (2014). Inferring the contribution of sexual reproduction, migration and off-season survival to the temporal maintenance of microbial populations: A case study on the wheat fungal pathogen Puccinia striiformis f.sp. tritici. Molecular Ecology, 23, 603–617.
Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N., Bonhomme, F., (1996-2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171, Université de Montpellier II, Montpellier, France. http://www.genetix.univ-montp2.fr/genetix/intro.htm. Accessed 21 Jan 2019.
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.
Brunner, P. C., & McDonald, B. A. (2018). Evolutionary analyses of the avirulence effector AvrStb6 in global populations of Zymoseptoria tritici identify candidate amino acids involved in recognition. Molecular Plant Pathology, in press, 19, 1836–1846.
Chen, R. S., Boeger, J. M., & McDonald, B. A. (1994). Genetic stability in a population of a plant pathogenic fungus over time. Molecular Ecology, 3, 209–218.
Cools, H. J., Hawkins, N. J., & Fraaije, B. A. (2013). Constraints on the evolution of azole resistance in plant pathogenic fungi. Plant Pathology, 62, 36–42.
Cortesi, P., & Milgroom, M. G. (2001). Outcrossing and diversity of vegetative compatibility types in populations of Eutypa lata from grapevines. Journal of Plant Pathology, 83, 79–86.
Duvivier, M. (2015). Distribution of the airborne inoculum of wheat leaf rust and septoria tritici blotch. PhD thesis. Belgique: Université Catholique de Louvain.
Earl, D. A., & Vonholdt, B. M. (2012). STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4, 359–361.
El Chartouni, L., Tisserant, B., Siah, A., Duyme, F., Leducq, J. B., Deweer, C., Fichter-Roisin, C., Sanssené, J., Durand, R., Halama, P., & Reignault, P. (2011). Genetic diversity and population structure in French populations of Mycosphaerella graminicola. Mycologia, 103, 764–774.
El Chartouni, L., Tisserant, B., Siah, A., Duyme, F., Durand, R., Halama, P., & Reignault, P. (2012). Evolution of Mycosphaerella graminicola at the wheat leaf and field levels. Phytopathologia Mediterranea, 51, 332–339.
Eriksen, L., Shaw, M. W., & Østergård, H. (2001). A model of the effect of pseudothecia on genetic recombination and epidemic development in populations of Mycosphaerella graminicola. Phytopathology, 91, 240–248.
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.
Excoffier, L., & Lischer, H. E. L. (2010). ARLEQUIN suite v3.5: A new series of programs to perform population genetics analyses under Linux and windows. Molecular Ecology Resources, 10, 564–567.
Eyal, Z. (1999). The Septoria tritici and Stagonospora nodorum blotch diseases of wheat. European Journal of Plant Pathology, 105, 629–641.
Fones, H., & Gurr, S. (2015). The impact of Septoria tritici blotch disease on wheat: An EU perspective. Fungal Genetics and Biology, 79, 3–7.
Gautier, A., Marcel, T., Confais, J., Crane, C., Kema, G., Suffert, F., & Walker, A. S. (2014). Development of a rapid multiplex SSR genotyping method to study populations of the fungal plant pathogen Zymoseptoria tritici. BMC Research Notes, 7, 373.
Hayes, L. E., Sackett, K. E., Anderson, N. P., Flowers, M. D., & Mundt, C. C. (2016). Evidence of selection for fungicide resistance in Zymoseptoria tritici populations on wheat in western Oregon. Plant Disease, 100, 483–489.
Holderegger, R., Kamm, U., & Gurgerli, F. (2006). Adaptive vs. neutral genetic diversity: Implications for landscape genetics. Landscape Ecology, 21, 797–707.
Jürgens, T., Celeste, C., 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.
Linde, C. C., Zhan, J., & McDonald, B. A. (2002). Population structure of Mycosphaerella graminicola: From lesions to continents. Phytopathology, 92, 946–955.
McDonald, B. A., & Linde, C. (2002). Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology, 40, 349–379.
Milgroom, M. G., & Peever, T. L. (2003). Population biology of plant pathogens - the synthesis of plant disease epidemiology and population genetics. Plant Disease, 87, 608–617.
Morais, D., Sache, I., Suffert, F., & Laval, V. (2016a). Is onset of Septoria tritici blotch epidemics related to local availability of ascospores? Plant Pathology, 65, 250–260.
Morais, D., Laval, V., Sache, I., & Suffert, F. (2016b). Inferring the origin of primary inoculum of Zymoseptoria tritici from differential adaptation of resident and immigrant populations to wheat cultivars. European Journal of Plant Pathology, 145, 393–404.
Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.
Raymond, M., & Rousset, F. (1995). GENEPOP (VERSION-1.2) - population-genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248–249.
Razavi, M., & Hughes, G. R. (2004). Microsatellite markers provide evidence for sexual reproduction of Mycosphaerella graminicola in Saskatchewan. Genome, 47, 789–794.
Rehfus, A., Strobel, D., Bryson, R., & Stammler, G. (2018). Mutations in sdh genes in field isolates of Zymoseptoria tritici and impact on the sensitivity to various succinate dehydrogenase inhibitors. Plant Pathology, 67(1), 175–180.
Rieux, A., Soubeyrand, S., Bonnot, F., Klein, E. K., Ngando, J. E., Mehl, A., Ravigné, V., Carlier, J., & Lapeyre de Bellaire, L. (2014). Long-distance wind-dispersal of spores in a fungal plant pathogen: Estimation of anisotropic dispersal kernels from an extensive field experiment. PLoS One, 9, e103225.
Sanderson, F. R. (1972). A Mycosphaerella species as the ascogenous state of Septoria tritici rob. And Desm. New Zealand Journal of Botany, 10, 707–709.
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.
Shah, D. A., Bergstrom, G. C., & Ueng, P. P. (2001). Foci of Stagonospora nodorum blotch in winter wheat before canopy development. Phytopathology, 91, 642–647.
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, 35–43.
Siah, A., Tisserant, B., El Chartouni, L., Duyme, F., Deweer, C., Roisin-Fichter, C., Sanssené, 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. Fungal Biology, 114, 980–990.
Siah, A., Bomble, M., Tisserant, B., Cadalen, T., Holvoet, M., Hilbert, J.-L., Halama, P., & Reignault, P. L. (2018). Genetic structure of Zymoseptoria tritici in northern France at region, field, plant and leaf layer scales. Phytopathology, in press, 108, 1114–1123.
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, 878–889.
Suffert, F., Sache, I., & Lannou, C. (2011). Early stages of Septoria tritici blotch epidemics of winter wheat: Build-up, overseasoning, and release of primary inoculum. Plant Pathology, 60, 166–177.
Suffert, F., Ravigné, V., & Sache, I. (2015). Seasonal changes drive short-term selection for fitness traits in the wheat pathogen Zymoseptoria tritici. Applied and Environmental Microbiology, 81, 6367–6379.
Suffert, F., Goyeau, H., Sache, I., Carpentier, F., Gélisse, S., Morais, D., & Delestre, G. (2018). Epidemiological trade-off between intra- and inter-annual scales in the evolution of aggressiveness in a local plant pathogen population. Evolutionary Applications, 11, 768–780.
Waalwijk, C., Mendes, O., Verstappen, E. C. P., De 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.
Weir, B. S., & Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358–1370.
Welch, T., Feechan, A., & Kildea, S. (2018). Effect of host resistance on genetic structure of core and accessory chromosomes in Irish Zymoseptoria tritici populations. European Journal of Plant Pathology, 150, 139–148.
Zhan, J., Mundt, C. C., & McDonald, B. A. (1998). Measuring immigration and sexual reproduction in field populations of Mycosphaerella graminicola. Phytopathology, 88, 1330–1337.
Zhan, J., Mundt, C. C., & McDonald, B. A. (2001). Using restriction fragment length polymorphismsto assess temporal variation and estimate the number of ascospores that initiate epidemics in field populations of Mycosphaerella graminicola. Phytopathology, 91, 1011–1017.
Zhan, J., Kema, G. H. J., Waalwijk, C., & McDonald, B. A. (2002). 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.
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.
Zhan, J., Torriani, S. F. F., & McDonald, B. A. (2007). Significant difference in pathogenicity between MAT1-1 and MAT1-2 isolates in the wheat pathogen Mycosphaerella graminicola. Fungal Genetics and Biology, 44, 339–346.
Zhong, Z., Marcel, T. C., Hartmann, F. E., Ma, X., Plissonneau, C., Zala, M., Ducasse, A., Confais, J., Compain, J., Lapalu, N., Amselem, J., McDonald, B. A., Croll, D., & Palma-Guerrero, J. (2017). A small secreted protein in Zymoseptoria tritici is responsible for avirulence on wheat cultivars carrying the Stb6 resistance gene. New Phytologist, 214, 619–631.
Zwankhuizen, M. J., Govers, F., & Zadoks, J. C. (1998). Development of potato late blight epidemics: Disease foci, disease gradients, and infection sources. Phytopathology, 88, 754–763.
Acknowledgments
The authors thank Angélique Gautier (INRA BIOGER) and Christophe Montagnier (INRA Experimental Unit, Thiverval-Grignon) for technical assistance.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
This study was supported by a grant from the European Union Seventh Framework Program (Grant Agreement no. 261752, PLANTFOODSEC project) and a grant from the European Union Horizon Framework 2020 Program (Grant Agreement no. 634179, EMPHASIS project).
Conflict of interest
The authors declare that they have no conflict of interest.
Human and animal studies
This article does not contain any studies with human participants or animals performed by any of the authors.
Electronic supplementary material
ESM 1
(DOCX 47 kb)
Rights and permissions
About this article
Cite this article
Morais, D., Duplaix, C., Sache, I. et al. Overall stability in the genetic structure of a Zymoseptoria tritici population from epidemic to interepidemic stages at a small spatial scale. Eur J Plant Pathol 154, 423–436 (2019). https://doi.org/10.1007/s10658-018-01666-y
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-018-01666-y