European Journal of Plant Pathology

, Volume 134, Issue 1, pp 167–180 | Cite as

The genetic diversity of Icelandic populations of two barley leaf pathogens, Rhynchosporium commune and Pyrenophora teres

  • Tryggvi S. Stefansson
  • Marjo Serenius
  • Jon Hallsteinn HallssonEmail author


Twelve species of fungi have been found growing on barley leaves in Icelandic fields. The study presented here on the population structure of two of these species, the pathogens Rhynchosporium commune and Pyrenophora teres f. teres, reveals high levels of genetic diversity, low levels of migration, and a significant differentiation from other European populations, despite the short history of continuous barley cultivation in Iceland. The gene diversity for R. commune in Iceland was 0.55 compared to a range of 0.43–0.73 for six European populations. The gene diversity for P. teres was higher in Iceland than in populations from Russia and Finland. The two mating types were found to overlap in distribution for both fungi making sexual reproduction a possibility, supported by the few clones and the gametic equilibrium within the Icelandic populations. When the high levels of diversity, low levels of migration, and the genetic differentiation observed between Icelandic and Scandinavian populations are put into context with the short history of barley cultivation in Iceland, it raises questions regarding the origin of the Icelandic fungal populations. It also underlines the importance of proper analysis of pathogens prior to starting resistance breeding projects. The findings are an addition to the ongoing analysis of the global diversity of barley fungal pathogens in general and an important input into future barley breeding projects in Iceland in particular.


Scald Net blotch Genetic differentiation AFLP Microsatellites Cultivation history 



The authors would like to thank Dr. Bruce A. McDonald for supplying R. commune samples for comparative purposes and for valuable comments on the manuscript. The authors would also like to thank Magnus Göranson, Dr. Áslaug Helgadóttir, and two anonymous reviewers for constructive criticism of the manuscript. Financial support for this study was provided by the Icelandic Agricultural Productivity Fund and the Technology Development Fund.


  1. Agapow, P. M., & Burt, A. (2001). Indices of multilocus linkage disequilibrium. Molecular Ecology Notes, 1(1–2), 101–102.CrossRefGoogle Scholar
  2. Arabi, M. I. E., Jawhar, M., & Al-Shehadah, E. (2008). Molecular and pathogenic variation identified among isolates of Rhynchosporium secalis from Syria. Journal of Plant Pathology, 90(2), 179–184.Google Scholar
  3. Badr, A., Muller, K., Schafer-Pregl, R., El Rabey, H., Effgen, S., Ibrahim, H. H., Pozzi, C., Rohde, W., & Salamini, F. (2000). On the origin and domestication history of barley (Hordeum vulgare). Molecular Biology and Evolution, 17(4), 499–510.PubMedCrossRefGoogle Scholar
  4. Bogucki, P. (2000). How agriculture came to north-central Europe. In: Europe’s First Farmers, 1st edn. Cambridge University Press. Cambridge, United Kingdom.Google Scholar
  5. Brown, A. H. D., Feldman, M. W., & Nevo, E. (1980). Multilocus structure of natural populations of Hordeum spontaneum. Genetics, 96(2), 523–536.PubMedGoogle Scholar
  6. Brown, M., Steffenson, B. J., & Webster, R. K. (1993). Host range of Pyrenophora teres f. teres isolates from California. Plant Disease, 77(9), 942.CrossRefGoogle Scholar
  7. Cavalli-Sforza, L. L., & Edwards, A. W. F. (1967). Phylogenetic analysis: models and estimation procedures. American Journal of Human Genetics, 19, 233–257.PubMedGoogle Scholar
  8. Conners, I. L. (1967). An annotated index of plant diseases in Canada and fungi recorded on plants in Alaska, Canada and Greenland. Canada: Dept. of Agriculture. Research Branch.Google Scholar
  9. Corander, J., & Marttinen, P. (2006). Bayesian identification of admixture events using multilocus molecular markers. Molecular Ecology, 15(10), 2833–2843.PubMedCrossRefGoogle Scholar
  10. Corander, J., Waldmann, P., Marttinen, P., & Sillanpaa, M. J. (2004). BAPS 2: Enhanced possibilities for the analysis of genetic population structure. Bioinformatics, 20(15), 2363–2369.PubMedCrossRefGoogle Scholar
  11. Cornuet, J. M., & Luikart, G. (1996). Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144(4), 2001–2014.PubMedGoogle Scholar
  12. Excoffier, L., Laval, G., & Schneider, S. (2005). Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47–50.Google Scholar
  13. Foister, C. E. (1961). The economic plant diseases of Scotland. Technical Bulletin of the Department of Agriculture and Fisheries Scotland, 1, 1–210.Google Scholar
  14. Fountaine, J. M., Shaw, M. W., Ward, E., & Fraaije, B. A. (2010). The role of seeds and airborne inoculum in the initiation of leaf blotch (Rhynchosporium secalis) epidemics in winter barley. Plant Pathology, 59(2), 330–337.CrossRefGoogle Scholar
  15. Ginns, J. H. (1986). Compendium of plant disease and decay fungi in Canada, 1960 1980. Ottawa: Canadian Government Publishing Centre.CrossRefGoogle Scholar
  16. Gordon, D. M. (1997). The genetic structure of Escherichia coli populations in feral house mice. Microbiology, 143(Pt 6), 2039–2046.PubMedCrossRefGoogle Scholar
  17. Goudet, J. (1995). FSTAT (Version 1.2): a computer program to calculate F-statistics. Journal of Heredity, 86(6), 485–486.Google Scholar
  18. Grand, L. F. (1985). North Carolina plant disease index. North Carolina Agricultural Research Service Technical Bulletin, 240, 1–157.Google Scholar
  19. Hermannsson, J. (1993). Kornrækt á Íslandi (in Icelandic). Ráðunautafundur, BÍ/LbhÍ, Reykjavik Iceland 178187.Google Scholar
  20. Jordan, V. W. L. (1981). Aetiology of barley net blotch caused by Pyrenophora teres and some effects on yield. Plant Pathology, 30(2), 77–87.CrossRefGoogle Scholar
  21. Jorgensen, J. (1977). Incidence of infections of barley seed by Pyrenophora graminea and Pyrenophora teres as revealed by freezing blotter method and disease counts in field. Seed Science and Technology, 5(1), 105–110.Google Scholar
  22. Karlsson, G. (2009). Lífsbjörg íslendinga frá 10. öld til 16. aldar (in Icelandic) (1st ed.). Reykjavik: University of Iceland Press.Google Scholar
  23. Khan, T. N., & Crosbie, G. B. (1988). Effect of scald (Rhynchosporium secalis (Oud.) J. Davis) infection on some quality characteristics of barley. Australian Journal of Experimental Agriculture, 28(6), 783–785.CrossRefGoogle Scholar
  24. Kumar, S., Nei, M., Dudley, J., & Tamura, K. (2008). MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Briefings in Bioinformatics, 9(4), 299–306.PubMedCrossRefGoogle Scholar
  25. Lee, H. K., Tewari, J. P., & Turkington, T. K. (1999). Histopathology and isolation of Rhynchosporium secalis from infected barley seed. Seed Science and Technology, 27(2), 477–482.Google Scholar
  26. Leisova, L., Minarikova, V., Kucera, L., & Ovesna, J. (2005). Genetic diversity of Pyrenophora teres isolates as detected by AFLP analysis. Journal of Phytopathology, 153(10), 569–578.CrossRefGoogle Scholar
  27. Linde, C. C., Zala, M., Ceccarelli, S., & McDonald, B. A. (2003). Further evidence for sexual reproduction in Rhynchosporium secalis based on distribution and frequency of mating-type alleles. Fungal Genetics and Biology, 40(2), 115–125.PubMedCrossRefGoogle Scholar
  28. Linde, C. C., Zala, M., & McDonald, B. A. (2005). Isolation and characterization of microsatellite loci from the barley scald pathogen, Rhynchosporium secalis. Molecular Ecology Notes, 5, 546–548.CrossRefGoogle Scholar
  29. Linde, C. C., Zala, M., & McDonald, B. A. (2009). Molecular evidence for recent founder populations and human-mediated migration in the barley scald pathogen Rhynchosporium secalis. Molecular Phylogenetics and Evolution, 51(3), 454–464.PubMedCrossRefGoogle Scholar
  30. Liu, K., & Muse, S. V. (2005). PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics Applications Note, 21(9), 2128–2129.Google Scholar
  31. Mäkelä, K. (1972). Rhynchosporium species on Finnish grasses. Karstenia, 13, 23–31.Google Scholar
  32. Maynard Smith, J., Smith, N. H., O’Rourke, M., & Spratt, B. G. (1993). How clonal are bacteria? Proceedings of the National Academy of Sciences of the United States of America, 90(10), 4384–4388.CrossRefGoogle Scholar
  33. McDonald, B. A., & Linde, C. C. (2002). Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology, 40, 349–379.PubMedCrossRefGoogle Scholar
  34. Nei, M. (1987). Molecular evolutionary genetics (1st ed.). New York: Columbia University Press.Google Scholar
  35. Nei, M., Tajima, F., & Tateno, Y. (1983). Accuracy of estimated phylogenetic trees from molecular data. Journal of Molecular Evolution, 19(2), 153–170.PubMedCrossRefGoogle Scholar
  36. Peakall, R., & Smouse, P. E. (2006). GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6, 288–295.CrossRefGoogle Scholar
  37. Peltonen, S., Jalli, M., Kammiovirta, K., & Karjalainen, R. (1996). Genetic variation in Drechslera teres populations as indicated by RAPD markers. Annals of Applied Biology, 128(3), 465–477.CrossRefGoogle Scholar
  38. Pennycook, S. R. (1989). Plant diseases recorded in New Zealand. Plant Diseases Division, DSIR. Auckland, New Zealand.Google Scholar
  39. Rannala, B., & Mountain, J. (1997). Detecting immigration by using multilocus genotypes. Proceedings of the National Academy of Sciences of the United States of America, 94(17), 9197–9201.PubMedCrossRefGoogle Scholar
  40. Rau, D., Brown, A. H. D., Brubaker, C. L., Attene, G., Balmas, V., Saba, E., & Papa, R. (2003). Population genetic structure of Pyrenophora teres Drechs. the causal agent of net blotch in Sardinian landraces of barley (Hordeum vulgare L.). Theoretical and Applied Genetics, 106(5), 947–959.PubMedGoogle Scholar
  41. Reynolds, J., Weir, B. S., & Cockerham, C. C. (1983). Estimation of the coancestry coefficient: Basis for a short-term genetic distance. Genetics, 105, 767–779.PubMedGoogle Scholar
  42. Richardson, M. J. (1990). An Annotated List of Seed-borne Diseases. 4th edn. International Seed Testing Association.Google Scholar
  43. Robbertse, B., van der Rijst, M., van Aarde, I. M. R., Lennox, C., & Crous, P. W. (2001). DMI sensitivity and cross-resistance patterns of Rhynchosporium secalis isolates from South Africa. Crop Protection, 20(2), 97–102.CrossRefGoogle Scholar
  44. Rostoks, N., Zale, J. M., Soule, J., Brueggeman, R., Druka, A., Kudrna, D., Steffenson, B., & Kleinhofs, A. (2002). A barley gene family homologous to the maize rust resistance gene Rp1-D. Theoretical and applied genetics, 104(8), 1298–1306.PubMedCrossRefGoogle Scholar
  45. Salamati, S., & Tronsmo, A. M. (1997). Pathogenicity of Rhynchosporium secalis isolates from Norway on 30 cultivars of barley. Plant Pathology, 46, 416–424.CrossRefGoogle Scholar
  46. Salamati, S., Zhan, J., Burdon, J. J., & McDonald, B. A. (2000). The genetic structure of field populations of Rhynchosporium secalis from three continents suggests moderate gene flow and regular recombination. Phytopathology, 90(8), 901–908.PubMedCrossRefGoogle Scholar
  47. Serenius, M., Mironenko, N., & Manninen, O. (2005). Genetic variation, occurrence of mating types and different forms of Pyrenophora teres causing net blotch of barley in Finland. Mycological Research, 109, 809–817.PubMedCrossRefGoogle Scholar
  48. Serenius, M., Manninen, O., Wallwork, H., & Williams, K. (2007). Genetic differentiation in Pyrenophora teres populations measured with AFLP markers. Mycological Research, 111, 213–223.PubMedCrossRefGoogle Scholar
  49. Shipton, W. A., Boyd, W. J. R., & Ali, S. M. (1974). Scald of barley. Review of Plant Pathology, 53, 840–861.Google Scholar
  50. Slatkin, M. (1995). A measure of population subdivision based on microsatellite allele frequencies. Genetics, 139(1), 457–462.PubMedGoogle Scholar
  51. Souza, V., Nguyen, T. T., Hudson, R. R., Piñero, D., & Lenski, R. E. (1992). Hierarchical analysis of linkage disequilibrium in Rhizobium populations: evidence for sex? Proceedings of the National Academy of Sciences of the United States of America, 89(17), 8389–8393.PubMedCrossRefGoogle Scholar
  52. Sprague, R. (1950). Diseases of cereals and grasses in North America (Fungi, except smuts and rusts). New York: The Ronald Press Company.Google Scholar
  53. Stefansson, T. S., & Hallsson, J. H. (2011). Analysis of the species diversity of leaf pathogens in Icelandic barley fields. Icelandic Agricultural Sciences, 24, 13–23.Google Scholar
  54. Taggart, P. J., Locke, T., Phillips, A. N., Pask, N., Hollomon, D. W., Kendall, S. J., Cooke, L. R., & Mercer, P. C. (1999). Benzimidazole resistance in Rhynchosporium secalis and its effect on barley leaf blotch control in the UK. Crop Protection, 18(4), 239–243.CrossRefGoogle Scholar
  55. Tajima, F. (1983). Evolutionary relationship of DNA-sequences in finite populations. Genetics, 105(2), 437–460.PubMedGoogle Scholar
  56. von Korff, M., Udupa, S. M., Yahyaoui, A., & Baum, M. (2004). Genetic variation among Rhynchosporium secalis populations of West Asia and North Africa as revealed by RAPD and AFLP analysis. Journal of Phytopathology, 152(2), 106–113.CrossRefGoogle Scholar
  57. Xi, K. N., Turkington, T., Meadus, J., Helm, J. H., & Tewari, J. (2003). Dynamics of Rhynchosporium secalis pathotypes in relation to barley cultivar resistance. Mycological Research, 107, 1485–1492.PubMedCrossRefGoogle Scholar
  58. Zaffarano, P. L., McDonald, B. A., & Linde, C. C. (2011). Two new species of Rhynchosporium. Mycologia, 103(1), 195–202.PubMedCrossRefGoogle Scholar
  59. Zhan, J., Fitt, B. D. L., Pinnschmidt, H. O., Oxley, S. J. P., & Newton, A. C. (2008). Resistance, epidemiology and sustainable management of Rhynchosporium secalis populations on barley. Plant Pathology, 57(1), 1–14.Google Scholar

Copyright information

© KNPV 2012

Authors and Affiliations

  • Tryggvi S. Stefansson
    • 1
    • 2
  • Marjo Serenius
    • 3
    • 4
  • Jon Hallsteinn Hallsson
    • 1
    Email author
  1. 1.Faculty of Land and Animal ResourcesAgricultural University of IcelandReykjavikIceland
  2. 2.ETH Zürich, Institute for Integrative BiologyZürichSwitzerland
  3. 3.MTT Agrifood Research, Biotechnology & Food ResearchJokioinenFinland
  4. 4.Agricultural Foundation of TradeK-maatalous Experimental FarmHauhoFinland

Personalised recommendations