Abstract
Information on the pathogen virulence profile and diversity across locations is crucial for host germplasm improvement and deployment. The rapid acquisition of virulence to host resistance by the wheat yellow/stripe rust pathogen (Puccinia striiformis f.sp. tritici: PST), makes it crucial to know about its virulence and pathotype diversity. Recent studies have shown the plausible centre of origin of the pathogen in the Himalayan region, with Pakistan being the most ancestral to all other worldwide populations. To assess the status of virulence and pathotype diversity in the Himalayan region of Pakistan, a set of 127 PST infected wheat samples from eight locations were collected, multiplied and pathotyped using a set of 36 differential lines from the world set, European and Chinese sets, and 9 Avocet Yr isolines. Virulence (Vr) was recorded to 18 out of 24 tested yellow rust resistance (Yr) genes, while a total of 53 pathotypes were detected out of 127 isolates tested. Virulence was found to the resistance genes rarely deployed in Pakistan (Vr8) or even worldwide level (Vr5), while virulence to Vilmorin 23 (Yr3+) was absent in Pakistan, which is common in Europe. None of the pathotypes was dominant across all locations, however, no clear spatial structuring was observed for the studied locations. Our results suggested a high virulence and pathotype diversity in line with the previously proposed potential role of sexual recombination in the temporal maintenance of PST in the Himalayan region of Pakistan. This information should be useful in host resistance gene improvement and deployment.
Similar content being viewed by others
References
Afzal, S. N., Haque, M. I., & Ahmedani, M. S. (2008). Impact of stripe rust on kernel weight of wheat varieties sown in rainfed areas of Pakistan. Pakistan Journal of Botany, 40, 923–929.
Ahmad, S., Afzal, M., Noorka, I. R., Iqbal, Z., Akhtar, N., Iftkhar, Y., & Kamran, M. (2010). Prediction of yield losses in wheat (Triticum aestivum L.) caused by yellow rust in relation to epidemiological factors in Faisalabad. Pakistan Journal of Botany, 42, 401–407.
Ali, S. (2012) Population biology and invasion history of Puccinia striiformis f.sp. tritici at worldwide and local scale, Université Paris-Sud 11.
Ali, S., Shah, S. J. A., & Ibrahim, M. (2007). Assessment of wheat breeding lines for slow yellow rusting (Puccinia striiformis West. tritici). Pakistan Journal of Biological Science, 10, 3440–3444.
Ali, S., Shah, S. J. A., Khalil, I. H., Rahman, H., Maqbool, K., & Ullah, W. (2009a). Partial resistance to yellow rust in introduced winter wheat germplasm at the north of Pakistan. Australian Journal of Crop Science, 3, 37–43.
Ali, S., Shah, S. J. A., & Rahman, H. (2009b). Multi-locations variability in Pakistan for partial resistance in wheat to Puccinia striiformis West. tritici. Phytopathologia Mediterranea, 48, 269–279.
Ali, S., Shah, S. J. A., Rahman, H., Saqib, M. S., Ibrahim, M., & Sajjad, M. (2009c). Variability in wheat yield under yellow rust pressure in Pakistan. Turkish Journal of Agriculture and Forestry, 33, 537–546.
Ali, S., Leconte, M., Walker, A.-S., Enjalbert, J., & de Vallavieille-Pope, C. (2010). Reduction in the sex ability of worldwide clonal populations of Puccinia striiformis f.sp. tritici. Fungal Genetics and Biology, 47, 828–838.
Ali, S., Gladieux, P., Leconte, M., Gautier, A., Justesen, A. F., Hovmoller, M. S., Enjalbert, J., & De Vallavieille-Pope, C. (2014a). Origin, migration routes and worldwide population genetic structure of the wheat yellow rust pathogen Puccinia striiformis f.sp. tritici. PLoS Pathogens, 10, e1003903.
Ali, S., Gladieux, P., Rahman, H., Saqib, M. S., Fiaz, M., Ahmed, H., Leconte, M., Gautier, A., Justesen, A. F., Hovmøller, M. S., Enjalbert, J., & de Vallavieille-Pope, C. (2014b). 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.
Ali, S., Gladieux, P., Rahman, H., Saqib, M.S., Fiaz, M., Ahmed, H., Leconte, M., Gautier, A., Hovmøller, M.S., Enjalbert, J. & de Vallavieille-Pope, C. (2012) Population structure and temporal maintenance of Puccinia striiformis in the Himalayan region of Pakistan 13th International Cereal Rusts and Powdery Mildews Conference. Beiging, China.
Bahri, B., Leconte, M., Ouffroukh, A., de Vallavieille-Pope, C., & Enjalbert, J. (2009). Geographic limits of a clonal population of wheat yellow rust in the Mediterranean region. Molecular Ecology, 18, 4165–4179.
Bahri, B., Shah, S. J. A., Hussain, S., Leconte, M., Enjalbert, J., & de Vallavieille-Pope, C. (2011). Genetic diversity of wheat yellow rust population in Pakistan and its relationship with host resistance. Plant Pathology, 60, 649–660.
Chaves, M. S., Martinelli, J. A., Wesp-Guterres, C., Graichen, F. A. S., Brammer, S. P., Scagliusi, S. M., da Silva, W. P., Torres, G. A. M., Lau, E. Y., Consoli, L., & Chaves, A. L. S. (2013). The importance for food security of maintaining rust resistance in wheat. Food Security, 5, 157–176.
Chen, X. M. (2005). Epidemiology and control of stripe rust [Puccinia striiformis f. sp. tritici] on wheat. Canadian Journal of Plant Pathology, 27, 314–337.
Chen, X., Line, R. F., & Leung, H. (1993). Relationship between virulence variation and DNA polymorphism in Puccinia striiformis. Phytopathology, 83, 1489–1497.
de Vallavieille-Pope, C., & Line, R. F. (1990). Virulence of north american and european races of Puccinia striiformis on north american, world and european differentials. Plant Disease, 74, 739–743.
de Vallavieille-Pope, C., Huber, L., Leconte, M., & Goyeau, H. (1995). Comparative effects of temperature and interrupted wet periods on germination, penetration, and infection of Puccinia recondita f.sp. tritici and P. striiformis on wheat seedlings. Phytopathology, 85, 409–415.
de Vallavieille-Pope, C., Huber, L., Leconte, M., & Bethenod, O. (2002). Preinoculation effects of light quantity on infection efficiency of Puccinia striiformis and P. triticina on wheat seedlings. Phytopathology, 92, 1308–1314.
de Vallavieille-Pope, C., Ali, S., Leconte, M., Enjalbert, J., Delos, M., & Rouzet, J. (2012). Virulence dynamics and regional structuring of Puccinia striiformis f. sp. tritici in France between 1984 and 2009. Plant Disease, 96, 131–140.
Dedryver, F., Paillard, S., Mallard, S., Robert, O., Trottet, M., Nègre, S., Verplancke, G., & Jahier, J. (2009). Characterization of genetic components involved in durable resistance to stripe rust in the bread wheat ‘Renan’. Phytopathology, 99, 968–973.
Enjalbert, J., Duan, X., Leconte, M., Hovmøller, M. S., & de Vallavieille-Pope, C. (2005). Genetic evidence of local adaptation of wheat yellow rust (Puccinia striiformis f. sp. tritici) within France. Molecular Ecology, 14, 2065–2073.
Giraud, T., Villareal, L., Austerlitz, F., Le Cam, B., & Lavigne, C. (2006). Importance of the life cycle in host race formation and sympatric speciation in parasites. Phytopathology, 96, 280–287.
Giraud, T., Gladieux, P., & Gavrilets, S. (2010). Linking the emergence of fungal plant diseases with ecological speciation. Trends in Ecology & Evolution, 25, 387–395.
Gladieux, P., Byrnese, E., Fisher, M. C., Aguleta, G., Heitman, J., & Giraud, T. (2011). Epidemiology and evolution of fungal pathogens, in plants and animals. In M. Tibayrenc (Ed.), In: Genetics and Evolution of Infectious Diseases (pp. 59–106). USA: Elsevier Inc.
Hau, B., & de Vallavieille-Pope, C. (2006). Wind-dispersed diseases. In The Epidemiology of Plant Diseases (pp. 387–416). Netherlands: Springer Netherlands.
Hawkesford, M. J., Araus, J.-L., Park, R. F., Calderini, D., Mirralles, M., Shen, T., Zhang, J., & Parry, M. A. J. (2013). Prospects of doubling global wheat yields. Food and Energy Security, 2, 34–48.
Hovmøller, M. S. (2001). Disease severity and pathotype dynamics of Puccinia striiformis f.sp. tritici in Denmark. Plant Pathology, 50, 181–189.
Hovmøller, M. S., Justesen, A. F., & Brown, J. K. M. (2002). Clonality and long-distance migration of Puccinia striiformis f.sp. tritici in north-west Europe. Plant Pathology, 51, 24–32.
Hovmøller, M. S., Walter, S., & Justesen, A. F. (2010). Escalating threat of wheat rusts. Science, 329, 369.
Hovmøller, M. S., Sørensen, C. K., Walter, S., & Justesen, A. F. (2011). Diversity of Puccinia striiformis on cereals and grasses. Annual Review of Phytopathology, 49, 197–217.
Irfaq, M., Ajab, M., Khattak, G. S. S., Mohammad, T., & Shah, S. J. A. (2009). Genetic behavior of controlling area under disease progress curve for stripe rust (Puccinia striiformis f. sp. tritici) in two wheat (Triticum aestivum) crosses. Phytopathology, 99, 1265–1272.
Johnson, R. (1992). Reflection of a plant pathologist on breeding for disease resistance, with emphasis on yellow rust and eyespot of wheat. Plant Pathology, 41, 239–254.
Johnson, R., Stubbs, R. W., Fuchs, E., & Chamberlain, N. H. (1972). Nomenclature for physiologic races of Puccinia striiformis infecting wheat. Transactions of the British Mycological Society, 58, 475–480.
Jombart, T., Devillard, S. & Balloux, F. (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics 11, 95 http://www.biomedcentral.com/1471-2156/1411/1494.
Kisana, S.N., Mujahid, Y.M. & Mustafa, Z.S. (2003) Wheat production and productivity 2002–2003. A technical report to apprise the issues and future strategies, p. 19. Coordinated wheat, barley and triticale program, National Agricultural Research Center, PARC, Islamabad, Pakistan, Islamabad, Pakistan.
Line, R. F. (2002). Stripe rust of wheat and barley in north America: A retrospective hisotrical review. Annual Review of Phytopathology, 40, 75–118.
Mboup, M., Leconte, M., Gautier, A., Wan, A. M., Chen, W., de Vallavieille-Pope, C., & Enjalbert, J. (2009). Evidence of genetic recombination in wheat yellow rust populations of a Chinese oversummering area. Fungal Genetics and Biology, 46, 299–307.
Mboup, M., Bahri, B., Leconte, M., de Vallavieille-Pope, C., Kaltz, O., & Enjalbert, J. (2012). Genetic structure and local adaptation of European wheat yellow rust populations: the role of temperature-specific adaptation. Evolutionary Applications, 5, 341–352.
McDonald, B. A., & Linde, C. (2002). Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology, 40, 349–379.
McIntosh, R.A., Dubcovsky, J. & Rogers, W.J. (2010) Catalogue of gene symbols. KOMUGI Integrated Wheat Science Database, http://www.shigen.nig.ac.jp/wheat/komugi/genes/symbolClassList.jsp;jsessionid=689B192F53CED7CB561A9DC624FB9518.lb1,%202010.
Paillard, S., Trotoux-Verplancke, G., Perretant, M.-R., Mohamadi, F., Leconte, M., Coëdel, S., de Vallavieille-Pope, C., & Dedryver, F. (2012). Durable resistance to stripe rust is due to three specific resistance genes in French bread wheat cultivar Apache. Theoretical and Applied Genetics, 125, 955–965.
Pathan, A. K., & Park, R. F. (2007). Evaluation of seedling and adult plant resistance to stem rust in European wheat cultivars. Euphytica, 155, 87–105.
Peterson, R. F., Campbell, A. B., & Hannah, A. E. (1948). A diagrammatic scale for rust intensity on leaves and stems of cereals. Canadian Journal of Research, 26, 496–500.
Ray, R., Gururaja, K. V., & Ramchandra, T. V. (2011). Predictive distribution modeling for rare Himalayan medicinal plant Berberis aristata DC. Journal of Environmental Biology, 32, 725–730.
Rizwan, S., Iftikhar, A., Kazi, A. M., Sahi, G. M., Mirza, J. I., Rattu, A. R., & Ashraf, M. (2010). Virulence variation of Puccinia striiformis Westend. f. sp. tritici in Pakistan. Archives of Phytopathology and Plant Protection, 43, 875–882.
Saari, E. E., Prescott, J. M., & Roelfs, A. P. (1985). World distribution in relation to economic losses. In A. P. Roelfs (Ed.), In: The Cereal Rusts. Orlando: Academic.
Shah, S.J.A. (2010) Aerobiology, slow rusting resistance, gene postulation and virulence diversity of Puccinia striformis Westend. f. sp.tritici in NWFP, Pakistan. Department of Plant Pathology, Khyber pakhtunkhwa Agricultural University Peshawar, Pakistan. PhD thesis.
Shah, S. J. A., Imtiaz, M., & Hussain, S. (2009). Phenotypic and molecular characterization of wheat for slow rusting resistance against Puccinia striiformis Westend. f.sp. tritici. Journal of Phytopathology, 158, 393–402.
Sharma-Poudyal, D., Chen, X., Wan, A. M., Zhan, G. M., Kang, Z. S., Cao, S. Q., Jin, S. L., Morgounov, A., Akin, B., Mert, Z., Shah, S. J. A., Bux, H., Ashraf, M., Sharma, R. C., Madariaga, R., Puri, K. D., Wellings, C., Xi, K. Q., Wanyera, R., Manninger, K., Ganzález, M. I., Koyda, M., Sanin, S., & Patzek, L. J. S. (2013). Virulence characterization of international collections of the wheat stripe rust pathogen, Puccinia striiformis f. sp. tritici. Plant Disease, 97, 379–386.
Singh, R. P. (1993). Resistance to leaf rust in 26 Mexican wheat cultivars. Crop Science, 33, 633–637.
Singh, R.P., William, H.M., Huerta-Espino, J. & Rosewarne, G. (2004) Wheat rust in Asia: meeting the challenges with old and new technologies. In proceedings of the 4th International Crop Science Congress; 26 Sep - 1 Oct 2004; Brisbane, Australia. Available at: . http://www.cropscience.org.au/icsc2004/symposia/3/7/141_singhrp.htm .
Stubbs, R. W. (1985). Stripe rust. In A. P. Roelfs & W. R. Bushnell (Eds.), In: The Cereal Rusts, Diseases, Distribution, Epidemiology and Control (pp. 61–101). London: Academic.
Stubbs, R. W. (1988). Pathogenicity analysis of yellow (stripe) rust of wheat and its significance in a global context. In N. W. Simmonds & S. Rajaram (Eds.), In: Breeding strategies for resistance to the rusts of wheat. Mexico: CIMMYT D.F.
Stukenbrock, E. H., & McDonald, B. A. (2008). The origins of plant pathogens in agro-ecosystems. Annual Review of Phytopathology, 46, 75–100.
Ward, J. H. J. (1963). Hierarchical grouping to optimize an objective function. Journal of the American Statistical Association, 58, 236–244.
Wellings, C. R. (2007). Puccinia striiformis in Australia: a review of the incursion, evolution and adaptation of stripe rust in the period 1979–2006. Australian Journal of Agricultural Research, 58, 567–575.
Wellings, C., Singh, R.P., McIntosh, R.A. & Pretorius, Z.A. (2004) The development and application of near isogenic lines for the stripe (yellow) rust pathosystem. Cereal Rusts Powdery Mildews Bulliten http://www.crpmb.org/.
Acknowledgments
We are thankful to our colleagues from Pakistan for their facilitation during sampling, particularly, Muhammad Sartaj (NTRI, Mansehra, Pakistan), Muhammad Latif (ARS, Mansehra, Pakistan) and Abdul Hakim Khan (ARS, Mansehra, Pakistan). We are profoundly grateful to Laurent Gérard for his remarkable contribution to spore multiplication and pathotyping work in confined high security greenhouse. We are thankful to Nathalie Galet and Nicolas Lecutier for technical assistance. The present work was supported by the European Integrated Project BIOEXPLOIT, FOOD-CT-2005-513959 and the French project EMERFUNDIS, ANR 07-BDIV-003. Sajid Ali was financed by a grant from the Higher Education Commission, Pakistan and partially by the above mentioned projects.
Author information
Authors and Affiliations
Corresponding author
Additional information
Author contributions
SA, HR and MSS carried out field assessment and yellow rust sampling. SA, ML and CP did the spore multiplication and pathotyping. SA, PG, CP and JE prepared the manuscript. SA, JE, and CP conceived and designed the study. All authors read and approved the manuscript.
Rights and permissions
About this article
Cite this article
Ali, S., Leconte, M., Rahman, H. et al. A high virulence and pathotype diversity of Puccinia striiformis f.sp. tritici at its centre of diversity, the Himalayan region of Pakistan. Eur J Plant Pathol 140, 275–290 (2014). https://doi.org/10.1007/s10658-014-0461-2
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-014-0461-2