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

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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.

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References

  • 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.

    Article  CAS  Google Scholar 

  • Agapow, P. M., & Burt, A. (2001). Indices of multilocus linkage disequilibrium. Molecular Ecology Notes, 1, 101–102.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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.

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Berlin, A., Djurle, A., Samils, B., & Yuen, J. (2012). Genetic variation in Puccinia graminis collected from oat, rye and barberry. Phytopathology, 102, 1006–1012.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Davlatov, S.-K., & Baikova, E. V. (2011). Altitudinal limits of Berberis L. in Tajikistan. Contemporary Problems of Ecology, 4(2), 164–166.

    Article  Google Scholar 

  • Donish. (1982). Tajikistan: Priroda i prirodnye resursy (Tajikistan: Nature and Natural Resources). Dushanbe: Donish.

    Google Scholar 

  • Eriksson, J., & Henning, E. (1896). Die Getrideroste ihre Geschichte und Natur sowie Massregeln gegen dieselben. Stockholm: P. A. Nordstedt & Söner.

    Google Scholar 

  • Goudet, J. (1995). Fstat version 1.2: a computer program to calculate Fstatistics. Journal of Heredity, 86(6), 485–486.

    Google Scholar 

  • Gäumann, E. (1959). Die Rostpilze Mitteleuropas. Bern: Buchdruckeri Büchler & Co.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Johnson, T. (1949). Intervarietal crosses in Puccinia graminis. Canadian Journal of Research Section C, 27, 45–65.

    Article  Google Scholar 

  • Kolmer, J. A. (2005). Tracking wheat rust on a continental scale. Current Opinion in Plant Biology, 5, 411–449.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • McDonald, B. A., & Linde, C. (2002). Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology, 40, 349–379.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

  • Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 

  • Roelfs, A. P. (1982). Effects of barberry eradication on stem rust in the United States. Plant Disease, 66(2), 177–181.

    Article  Google Scholar 

  • Roelfs, A. P., Singh, R. P., & Saari, E. E. (1992). Rust diseases of wheat: Concepts and methods of disease management. Mexico: CIMMYT.

    Google Scholar 

  • Saitou, N., & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4(4), 406–425.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Szabo, L. J. (2007). Development of simple sequence repeat markers for the plant pathogenic rust fungus. Puccinia graminis. Molecular Ecology Notes, 7, 92–94.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ul’anishchev, V. I. (1978). Opredelitel' rzhavchinnykh gribov SSSR. Chast 2 (Key to rust fungi of the USSR). Leningrad: Akademiya Nauk.

  • Weir, B. S., & Cockerham, C. (1984). Estimating F-statistics for the analysis of population structure. Evolution, 38(6), 1358–1370.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

Download references

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.

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Authors and Affiliations

  1. Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences, Box 7026, SE-750 07, Uppsala, Sweden

    Anna Berlin & Jonathan Yuen

  2. Tajik Agrarian University, 146 Rudaki Avenue, 734017, Dushanbe, Tajikistan

    Mahbubjon Rahmatov & Hafiz Muminjanov

  3. Department of Plant Breeding, Swedish University of Agricultural Sciences, Box 101, SE-230 53, Alnarp, Sweden

    Mahbubjon Rahmatov

Authors
  1. Anna Berlin
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  2. Mahbubjon Rahmatov
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  3. Hafiz Muminjanov
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  4. Jonathan Yuen
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Corresponding author

Correspondence to Anna Berlin.

Electronic supplementary material

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Supplementary Table 1

BLASTn identity based on the Internal transcribed spacer (ITS) region (DOCX 97 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)

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(EPS 768 kb)

Supplementary Figure 2

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

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(EPS 324 kb)

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Berlin, A., Rahmatov, M., Muminjanov, H. et al. Sexual reproduction contributes to genotypic variation in the population of Puccinia graminis in Tajikistan. Eur J Plant Pathol 141, 159–168 (2015). https://doi.org/10.1007/s10658-014-0534-2

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