European Journal of Plant Pathology

, Volume 141, Issue 1, pp 159–168 | Cite as

Sexual reproduction contributes to genotypic variation in the population of Puccinia graminis in Tajikistan

  • Anna Berlin
  • Mahbubjon Rahmatov
  • Hafiz Muminjanov
  • Jonathan Yuen
Article

Abstract

Stem rust, caused by Puccinia graminis, is a potential threat to wheat production in Central Asia. To investigate if sexual reproduction is important for the epidemiology of the disease, the population biology of the fungus was studied. Samples of P. graminis were collected from six wheat fields and from wild oats within two of the wheat fields during the growing season of 2010. The population structure of P. graminis was investigated by evaluating a total of 121 single uredinia collected from wheat and wild oats, using nine polymorphic simple sequence repeat (SSR) markers. The results presented in this study indicate that there is a selection process by the grass host, in particular wheat, that favours certain clones, which in turn affects the population structure of P. graminis in Tajikistan. The genotypic variation was large, both within and between the wheat fields and three populations were in linkage equilibrium, indicating that sexual reproduction within the P. graminis population takes place. This leads to the conclusion that the presence of Berberis spp. in Tajikistan has an important role in the population dynamics of P. graminis within the country, even if the fungus must reproduce primarily in a clonal manner during most of the year. Results also confirm that the two formae speciales, P. graminis f. sp. tritici and P. graminis f. sp. avenae, are genetically different even if they were collected in the same field.

Keywords

Avena fatua Triticum aestivum microsatellites alternate host Berberis spp Puccinia graminis f. sp. tritici Puccinia graminis f. sp. avenae 

Notes

Acknowledgments

The authors wish to thank Bernt Pett for assistance with sample collection, Annika Djurle for valuable comment on the manuscript and the Swedish University for Agricultural Sciences (SLU) for funding this research.

Supplementary material

10658_2014_534_MOESM1_ESM.docx (97 kb)
Supplementary Table 1BLASTn identity based on the Internal transcribed spacer (ITS) region (DOCX 97 kb)
10658_2014_534_Fig3_ESM.gif (121 kb)
Supplementary Figure 1

Structure output for K=5. Samples denominated as P. graminis f. sp. tritici are represented by yellow, green, pink and blue, and samples denominated as P. graminis f. sp. avenae are represented in red. (GIF 120 kb)

10658_2014_534_MOESM2_ESM.eps (768 kb)
High Resolution Image(EPS 768 kb)
10658_2014_534_Fig4_ESM.gif (9 kb)
Supplementary Figure 2

Neighbor-joining tree based on the ITS sequences of the collected samples with 1,000 bootstrap replications (GIF 8 kb)

10658_2014_534_MOESM3_ESM.eps (325 kb)
High Resolution Image(EPS 324 kb)

References

  1. Abbasi, M., Goodwin, S. B., & Scholler, M. (2005). Taxonomy, phylogeny, and distribution of Puccinia graminis, the black stem rust: new insights based on rDNA sequence data. Mycoscience, 46, 241–247.CrossRefGoogle Scholar
  2. Agapow, P. M., & Burt, A. (2001). Indices of multilocus linkage disequilibrium. Molecular Ecology Notes, 1, 101–102.CrossRefGoogle Scholar
  3. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research, 25(17), 3389–3402.PubMedCentralPubMedCrossRefGoogle Scholar
  4. Anonymous (2014). Rust susceptible Berberis, Mahoberberis, and Mahonia plants. USDA, Cereal disease laboaratory. http://www.ars.usda.gov/Main/docs.htm?docid=9751. Accessed 25 Aug 2014.
  5. Barnes, C. W., & Szabo, L. J. (2007). Detection and identification of four common rust pathogens of cereals and grasses using real-time polymerase chain reaction. Phytopathology, 97(6), 717–727.PubMedCrossRefGoogle Scholar
  6. Berlin, A., Djurle, A., Samils, B., & Yuen, J. (2012). Genetic variation in Puccinia graminis collected from oat, rye and barberry. Phytopathology, 102, 1006–1012.PubMedCrossRefGoogle Scholar
  7. Berlin, A., Samils, B., Djurle, A., Wirsén, H., Szabo, L., & Yuen, J. (2013). Disease development and genotypic diversity of Puccinia graminis f. sp. avenae in Swedish oat fields. Plant Pathology, 62(1), 32–40.CrossRefGoogle Scholar
  8. Davlatov, S.-K., & Baikova, E. V. (2011). Altitudinal limits of Berberis L. in Tajikistan. Contemporary Problems of Ecology, 4(2), 164–166.CrossRefGoogle Scholar
  9. Donish. (1982). Tajikistan: Priroda i prirodnye resursy (Tajikistan: Nature and Natural Resources). Dushanbe: Donish.Google Scholar
  10. Eriksson, J., & Henning, E. (1896). Die Getrideroste ihre Geschichte und Natur sowie Massregeln gegen dieselben. Stockholm: P. A. Nordstedt & Söner.Google Scholar
  11. Goudet, J. (1995). Fstat version 1.2: a computer program to calculate Fstatistics. Journal of Heredity, 86(6), 485–486.Google Scholar
  12. Gäumann, E. (1959). Die Rostpilze Mitteleuropas. Bern: Buchdruckeri Büchler & Co.Google Scholar
  13. Jin, Y. (2011). Role of Berberis spp. as alternate hosts in generating new races of Puccinia graminis and P. striiformis. Euphytica, 179(1), 105–108.CrossRefGoogle Scholar
  14. Jin, Y., Szabo, L. J., Rouse, M. N., Fetch, T., Pretorius, Z. A., Wanyera, R., & Njau, P. (2009). Detection of virulence to resistance gene Sr36 within the TTKS race lineage of Puccinia graminis f. sp. tritici. Plant Disease, 93, 367–370.CrossRefGoogle Scholar
  15. Johnson, T. (1949). Intervarietal crosses in Puccinia graminis. Canadian Journal of Research Section C, 27, 45–65.CrossRefGoogle Scholar
  16. Kolmer, J. A. (2005). Tracking wheat rust on a continental scale. Current Opinion in Plant Biology, 5, 411–449.Google Scholar
  17. Lehtinen, A., Andersson, B., Le, V. H., Naertad, R., Rastas, M., Ketoja, E., Hannukkala, A. O., Hermansen, A., Nielsen, B. J., Hansen, J. G., & Yuen, J. (2009). Aggressiveness of Phytophthora infestans on detached potato leaflets in four Nordic countries. Plant Pathology, 58, 690–702.CrossRefGoogle Scholar
  18. Leonard, K. J., & Szabo, L. J. (2005). Stem rust of small grains and grasses caused by Puccinia graminis. Molecular Plant Pathology, 6(2), 99–111.PubMedCrossRefGoogle Scholar
  19. McDonald, B. A., & Linde, C. (2002). Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology, 40, 349–379.PubMedCrossRefGoogle Scholar
  20. Peakall, R., & Smouse, P. E. (2006). GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6(1), 288–295.CrossRefGoogle Scholar
  21. Peterson, R. F., Campbell, A. B., & Hannah, A. E. (1948). A diagrammatic scale for estimating rust severity on leaves and stems of cereals. Canadian Journal of Research Section C, 26, 496–500.CrossRefGoogle Scholar
  22. Pett, B., Muminjanov, H., Morgunov, A., Rahmatov, M., & Sarkisova, T. (2005). Wheat diseases & pests observation for selection of resistant varieties in Tajikistan. Agromeridian, Theoretical and Applied Agricultural Research Journal (1) 83–87.Google Scholar
  23. Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.PubMedCentralPubMedGoogle Scholar
  24. Rahmatov, M., Husenov, B., Otambekova, M., Makhkamov, M., Eshonova, Z., Soliev, B., Karimov, M., Ibragimov, A., Hede, A., Morgounov, A., & Muminjanov, H. (2010). Results of investigations on wheat breeding in Tajikistan (In Russian). News of the Academy of Sciences of the Republic of Tajikistan, 172, 71–82. Dushanbe.Google Scholar
  25. Roelfs, A. P. (1982). Effects of barberry eradication on stem rust in the United States. Plant Disease, 66(2), 177–181.CrossRefGoogle Scholar
  26. Roelfs, A. P., Singh, R. P., & Saari, E. E. (1992). Rust diseases of wheat: Concepts and methods of disease management. Mexico: CIMMYT.Google Scholar
  27. Saitou, N., & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4(4), 406–425.PubMedGoogle Scholar
  28. Singh, R. P., Hodson, D. P., Huerta-Espino, J., Jin, Y., Bhavani, S., Njau, P., Herrera-Foessel, S., Singh, P. K., Singh, S., & Govindan, V. (2011). The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annual Review of Phytopathology, 49, 465–481.PubMedCrossRefGoogle Scholar
  29. Szabo, L. J. (2007). Development of simple sequence repeat markers for the plant pathogenic rust fungus. Puccinia graminis. Molecular Ecology Notes, 7, 92–94.CrossRefGoogle Scholar
  30. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kurmar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10), 2731–2739.PubMedCentralPubMedCrossRefGoogle Scholar
  31. Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680.PubMedCentralPubMedCrossRefGoogle Scholar
  32. Ul’anishchev, V. I. (1978). Opredelitel' rzhavchinnykh gribov SSSR. Chast 2 (Key to rust fungi of the USSR). Leningrad: Akademiya Nauk.Google Scholar
  33. Weir, B. S., & Cockerham, C. (1984). Estimating F-statistics for the analysis of population structure. Evolution, 38(6), 1358–1370.CrossRefGoogle Scholar
  34. Wingen, L. U., Shaw, M. W., & Brown, J. K. M. (2013). Long-distance dispersal and its influence on adaptation to host resistance in a heterogeneous landscape. Plant Pathology, 62(1), 9–20.CrossRefGoogle Scholar
  35. Zambino, P. J., & Szabo, L. J. (1993). Phylogenetic relationships of selected cereal and grass rusts based on rDNA sequence analysis. Mycologia, 85(3), 401–414.CrossRefGoogle Scholar
  36. Zhong, S., Leng, Y., Friesen, T. L., Faris, J. D., & Szabo, L. J. (2009). Development and characterization of expressed sequence tag-derived microsatellite markers for the wheat stem rust fungus Puccinia graminis f. sp. tritici. Phytopathology, 99(3), 282–289.PubMedCrossRefGoogle Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2014

Authors and Affiliations

  • Anna Berlin
    • 1
  • Mahbubjon Rahmatov
    • 2
    • 3
  • Hafiz Muminjanov
    • 2
  • Jonathan Yuen
    • 1
  1. 1.Department of Forest Mycology and Plant PathologySwedish University of Agricultural SciencesUppsalaSweden
  2. 2.Tajik Agrarian UniversityDushanbeTajikistan
  3. 3.Department of Plant BreedingSwedish University of Agricultural SciencesAlnarpSweden

Personalised recommendations