Advertisement

European Journal of Plant Pathology

, Volume 146, Issue 2, pp 305–314 | Cite as

Mitochondrial DNA-based genetic diversity and population structure of Zymoseptoria tritici in Tunisia

  • Mouna Naouari
  • Ali Siah
  • Mohamed Elgazzah
  • Philippe Reignault
  • Patrice Halama
Article

Abstract

A total of 108 isolates of the wheat pathogen Zymoseptoria tritici were collected from four distinct locations of Tunisia and characterized for three mitochondrial DNA sequences to provide insight into the genetic diversity and population structure of the fungus in this country. The number of different alleles averaged over all loci within locations ranged from 3.33 to 5.67, with an average of 4.42 per location. Multilocus analysis identified 27 (25 %) distinct haplotypes among the 108 assessed isolates, revealing a high mtDNA-based clonality within the population. Three of the highlighted haplotypes occurred in all locations and nine of them covered at least two locations. Significant levels of genetic diversity were found for the whole population and within each of the sampled locations, as indicated by the Nei’s gene diversity (0.52), unbiased gene diversity (0.58) and allele richness (4.43) indices. Further analyzes using Bayesian and non-Bayesian statistical models, as well as AMOVA, showed a lack of mtDNA-based genetic structure (GST = 0.06), hence supporting previous reports on Z. tritici in Tunisia performed using nuclear-DNA markers. A high level of gene flow (Nm = 8.27) corroborates the lack of structure and suggests regular cycles of sexual reproduction, leading to allelic pool homogenization via wind-born ascospores in the Tunisian population of Z. tritici.

Keywords

Zymoseptoria tritici Mitochondrial DNA Genetic diversity Population structure SSCP 

Notes

Acknowledgments

This research was supported by financial supports from the University of El-Manar (Tunis, Tunisia) and the Higher Institute of Agriculture (Lille, France).

References

  1. Abrinbana, M., Mozafiri, J., Shams-bakhsh, M., & Mehrabi, R. (2010). Genetic structure of Mycosphaerella graminicola populations in Iran. Plant Pathology, 59, 829–838.CrossRefGoogle Scholar
  2. Aguileta, G., de Vienne, D. M., Ross, O. N., Hood, M. E., Giraud, T., Petit, E., & Gabaldón, T. (2014). High variability of mitochondrial gene order among fungi. Genome Biology and Evolution, 6, 451–465.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Anon, A. (1996). The evaluation of forensic DNA evidence. Washington: National Academy Press. 272 pages.Google Scholar
  4. Bassam, B. J., Gaetano-Anolles, G., & Gresshoff, P. M. (1991). Fast and sensitive silver staining of DNA in polyacrylamide gels. Analytical Biochemistry, 196, 80–83.CrossRefPubMedGoogle Scholar
  5. 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.CrossRefGoogle Scholar
  6. Boukef, S., Yahyaoui, A., & Rezgui, S. (2013). Geographical distribution of a specific mitochondrial haplotype of Zymoseptoria tritici. Phytopathologia Mediterranea, 52, 466–471.Google Scholar
  7. Carlisle, D. J., Cooke, L. R., & Brown, A. E. (2001). Phenotypic and genotypic characterization of Northern Ireland isolates of Phytophthora infestans. European Journal of Plant Pathology, 107, 291–303.CrossRefGoogle Scholar
  8. Correll, J. C., Harp, T. L., Guerber, J. C., Zeigler, R. S., Liu, B., Cartwright, R. D., & Lee, F. N. (2000). Characterization of Pyricularia grisea in the United States using independent genetic and molecular markers. Phytopathology, 90, 1396–1404.CrossRefPubMedGoogle Scholar
  9. Czembor, P. C., & Arseniuk, E. (1999). Study of variability among monopycnidial mononpycnidiospore isolates derived from single pycnidia of Stagonospora ssp. and Septoria tritici with the use of RAPD-PCR, MP-PCR and rep-PCR techniques. Journal of Phytopathology, 147, 539–546.CrossRefGoogle Scholar
  10. Drabešová, J., Ryšánek, P., Brunner, P., McDonald, B. A., & Croll, D. (2013). Population genetic structure of Mycosphaerella graminicola and quinone outside inhibitor (QoI) resistance in the Czech Republic. European Journal of Plant Pathology, 135, 211–224.CrossRefGoogle Scholar
  11. 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, 764–774.CrossRefPubMedGoogle Scholar
  12. 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.CrossRefPubMedGoogle Scholar
  13. Falush, D., Stephens, M., & Pritchard, J. K. (2003). Inference of population structure: extensions to linked loci and correlated allele frequencies. Genetics, 164, 1567–1587.PubMedPubMedCentralGoogle Scholar
  14. Goodwin, S. B., Cohen, B. A., & Fry, W. E. (1994). Panglobal distribution of a single clonal lineage of the Irish potato famine fungus. Proceedings of the National Academy of Sciences of the United States of America, 91, 11591–11595.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Goodwin, S. B., Ben M’Barek, S., Dhillon, B., Wittenberg, A. H. J., Crane, C. F., Hane, J. K., et al. (2011). Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genetics, 7(6), e1002070. doi: 10.1371/journal.pgen.1002070.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Goudet, J. (2001). FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3) (http://www2.unil.ch/popgen/softwares/fstat.htm).
  17. 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.CrossRefPubMedGoogle Scholar
  18. Hunter, R., Coker, R. R., & Royle, D. J. (1999). The teleomorph stage, Mycosphaerella graminicola, in epidemics of Septoria tritici blotch on winter wheat in UK. Plant Pathology, 48, 51–57.CrossRefGoogle Scholar
  19. Jost, L. (2008). GST and its relatives do not measure differentiation. Molecular Ecology, 17, 4015–4026.CrossRefPubMedGoogle Scholar
  20. 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, 1–9.Google Scholar
  21. Keller, S. M., McDermott, J. M., Pettway, R. E., Wolfe, M. S., & McDonald, B. A. (1997). Gene flow and sexual reproduction in the wheat glume blotch pathogen Phaeosphaeria nodorum (anamorph Stagonospora nodorum). Phytopathology, 87, 353–358.CrossRefPubMedGoogle Scholar
  22. Kudla, J., Albertazzi, F. J., Blazevic, D., Hermann, M., & Bock, R. (2002). Loss of the mitochondrial cox2 intron 1 in a family of monocotyledonous plants and utilization of mitochondrial intron sequences for the construction of a nuclear intron. Molecular Genetics and Genomics, 267, 223–230.CrossRefPubMedGoogle Scholar
  23. Kurdyla, T. M., Guthrie, P. A. I., McDonald, B. A., & Appel, D. N. (1995). RFLPs in mitochondrial and nuclear DNA indicate low levels of genetic diversity in the oak wilt pathogen Ceratocystis fagacearum. Current Genetics, 27, 373–378.CrossRefPubMedGoogle Scholar
  24. Linde, C., Zhan, J., & McDonald, B. A. (2002). Population structure of Mycosphaerella graminicola: from lesions to continents. Phytopathology, 92, 946–955.CrossRefPubMedGoogle Scholar
  25. Liu, Y. C., Cortesi, P., Double, M. L., MacDonald, W. L., & Milgroom, M. G. (1996). Diversity and multilocus genetic structure in populations of Cryphonectria parasitica. Phytopathology, 86, 1344–1351.Google Scholar
  26. McDonald, B. A., Zhan, J., Yarden, O., Hogan, K., Garton, J., & Pettway, R. E. (1999). The population genetics of Mycosphaerella graminicola and Phaeosphaeria nodorum. In J. A. Lucas, P. Bowyer, & H. M. Anderson (Eds.), Septoria on cereals: A study of pathosystems (pp. 44–69). Wallingford: CAB International.Google Scholar
  27. Meirmans, P. G., & Hedrick, P. W. (2011). Assessing population structure: FST and related measures. Molecular Ecology Resources, 11, 5–18.CrossRefPubMedGoogle Scholar
  28. Naouari, M., Siah, A., Elgazzah, M., Reignault, P., & Halama, P. (2013). Tunisian population of the wheat pathogen Mycosphaerella graminicola is still fully sensitive to strobilurin fungicides. Journal of Agricultural Science and Technology, 3, 955–959.Google Scholar
  29. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Orita, M., Iwahana, H., Kanazawa, H., Hayashi, K., & Sekiya, T. (1989). Detection of polymorphisms of human DNA by gel electrophoresis as single-strand conformation polymorphisms. Proceedings of the National Academy of Sciences of the United States of America, 86, 2766–2770.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Peakall, R., & Smouse, P. E. (2012). GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics, 28, 2537–2539.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Petit, R. J., El Mousadik, A., & Pons, O. (1998). Identifying populations for conservation on the basis of genetic markers. Conservation Biology, 12, 844–855.CrossRefGoogle Scholar
  33. Ponomarenko, A., Goodwin, S. B., & Kema, G. H. J. (2011). Septoria tritici blotch (STB) of wheat. Plant Health Instructor. doi: 10.1094/PHI-I-2011-0407-01.Google Scholar
  34. Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.PubMedPubMedCentralGoogle Scholar
  35. Razavi, M., & Hughes, G. R. (2004a). Molecular variability of Mycosphaerella graminicola as detected by RAPD markers. Journal of Phytopathology, 152, 543–548.CrossRefGoogle Scholar
  36. Razavi, M., & Hughes, G. R. (2004b). Microsatellite markers provide evidence for sexual reproduction of Mycosphaerella graminicola in Saskatchewan. Genome, 47, 789–794.CrossRefPubMedGoogle Scholar
  37. Sheedy, E. M., Van de Wouw, A. P., Howlett, B. J., & May, T. W. (2014). Mitochondrial microsatellite markers for the Australian ectomycorrhizal fungus Laccaria sp. A (Hydnangiaceae). Applications in Plant Sciences. doi: 10.3732/apps.1300086.PubMedPubMedCentralGoogle Scholar
  38. Siah, A., Tisserant, B., El Chartouni, L., Duyme, F., Deweer, C., 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.CrossRefGoogle Scholar
  39. Siah, A., Reignault, P., & Halama, P. (2013). Genetic diversity of Mycosphaerella graminicola isolates from a single field. Communications in Agricultural and Applied Biological Sciences, 78, 437–442.PubMedGoogle Scholar
  40. Siah, A., Elbekali, A. Y., Ramdani, A., Reignault, P., Torriani, S. F. F., Brunner, P. C., & Halama, P. (2014). QoI resistance and mitochondrial genetic structure of Zymoseptoria tritici in Morocco. Plant Disease, 98, 1138–1144.CrossRefGoogle Scholar
  41. Sun, X., Kang, S., Zhang, Y., Tan, X., Yu, Y., He, H., et al. (2013). Genetic diversity and population structure of rice pathogen Ustilaginoidea virens in China. PLoS ONE, 8(9), e76879.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Torriani, S. F. F., Goodwin, S. B., Kema, G. H. J., Pandilinan, J. L., & McDonald, B. A. (2008). Intraspecific comparison and annotation of two complete mitochondrial genome sequences from the plant pathogenic fungus Mycosphaerella graminicola. Fungal Genetics and Biology, 45, 628–637.CrossRefPubMedGoogle Scholar
  43. 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, 155–162.CrossRefPubMedGoogle Scholar
  44. Torriani, S. F. F., Brunner, P. C., & McDonald, B. A. (2011). Evolutionary history of the mitochondrial genome in Mycosphaerella populations infecting bread wheat, durum wheat and wild grasses. Molecular Phylogenetics and Evolution, 58, 192–197.CrossRefPubMedGoogle Scholar
  45. Xia, J. Q., Correll, J. C., Lee, F. N., Ross, W. J., & Rhoads, D. D. (2000). Regional population diversity of Pyricularia grisea in Arkansas and the influence of host selection. Plant Disease, 84, 877–884.CrossRefGoogle Scholar
  46. Xu, J., Kerrigan, R. W., Callac, P., Horgen, P. A., & Anderson, J. B. (1997). Genetic structure of natural populations of Agaricus bisporus, the commercial button mushroom. Journal of Heredity, 88, 482–488.CrossRefGoogle Scholar
  47. Xu, J., Kerrigan, R. W., Sonnenberg, A. S., Callac, P., Horgen, P. A., & Anderson, J. B. (1998). Mitochondrial DNA variation in natural populations of the mushroom Agaricus bisporus. Molecular Ecology, 7, 19–23.CrossRefGoogle Scholar
  48. Yeh, F. C., Yang, R., & Boyle, T. (2000). Popgene 1.32. The user-friendly software for population genetic analysis. Molecular Biology and Biotechnology Center, Univ Alberta, and CIFOR, Canada (https://www.ualberta.ca/~fyeh/index.html).
  49. Youssar, L., Grüning, B. A., Günther, S., & Hüttel, W. (2013). Characterization and phylogenetic analysis of the mitochondrial genome of Glarea lozoyensis indicates high diversity within the order Helotiales. PLoS ONE, 8(9), e74792. doi: 10.1371/journal.pone.0074792.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 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
  51. Zhan, J., Kema, G. H. J., & McDonald, B. A. (2004). Evidence for natural selection in the mitochondrial genome of Mycosphaerella graminicola. Phytopathology, 94, 261–267.CrossRefPubMedGoogle Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2016

Authors and Affiliations

  • Mouna Naouari
    • 1
  • Ali Siah
    • 2
  • Mohamed Elgazzah
    • 1
  • Philippe Reignault
    • 3
  • Patrice Halama
    • 2
  1. 1.Unité de Génétique des Populations et Ressources Biologiques, Faculté des Sciences de TunisCampus Universitaire El-ManarTunisTunisia
  2. 2.Equipe Biotechnologie et Gestion des Agents Pathogènes en agriculture, Laboratoire Charles Viollette, GIS PhyNoPi, Institut Supérieur d’AgricultureUniv. Lille-Nord de FranceLille CedexFrance
  3. 3.Unité de Chimie Environnementale et Interactions sur le Vivant, GIS PhyNoPiUniversité du Littoral Côte d’Opale, Univ. Lille-Nord de FranceCalais CedexFrance

Personalised recommendations