Diversity in Puccinia striiformis populations causing the 2013 yellow rust epidemics on major wheat cultivars of Pakistan

LITERATURE CITED

• Ali S, Gladieux P, Leconte M, Gautier A, Justesen AF, Hovmoller MS, 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.
   PubMed Web of Science ®Google Scholar
• Ali S, Gladieux P, Rahman H, Saqib MS, Fiaz M, Ahmed H, Leconte M, Gautier A, Justesen AF, Hovmøller MS, 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.
   PubMed Web of Science ®Google Scholar
• Ali S, Hodson D. 2017. Wheat rust surveillance; field disease scoring and sample collection for phenotyping and molecular genotyping In: Periyannan S, ed. Methods in molecular biology. Humana Press.
   Google Scholar
• Ali S, Hovmøller MS, Swati ZA, Hussain M, Bibi S, Justesen AF. 2015. Diversity of Puccinia spp. on wheat, grasses and Berberis spp. in the Himalayan center of diversity of Puccinia striiformis f. sp. tritici. Borlaug Global Rust Initiative. [cited 2020 Feb 15]. Available from: https://globalrust.org/content/diversity-puccinia-spp-wheat-grasses-and-berberis-spp-himalayan-center-diversity-puccinia
   Google Scholar
• Ali S, Khan MR, Gautier A, Swati ZA, Walter S. 2017a. Microsatellite genotyping of the wheat yellow rust pathogen Puccinia striiformis. In: Periyannan S, ed. Wheat rust disease. Methods in molecular biology. Vol. 1659. Humana Press. p. 59–70.
   Google Scholar
• Ali S, Leconte M, Rahman H, Saqib MS, Gladieux P, Enjalbert J, de Vallavieille-Pope C. 2014c. A high virulence and pathotype diversity of Puccinia striiformis f. sp. tritici at its centre of diversity, the Himalayan region of Pakistan. European Journal of Plant Pathology 140:275–290.
   Web of Science ®Google Scholar
• Ali S, Leconte M, Walker AS, 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.
   PubMed Web of Science ®Google Scholar
• Ali S, Rodriguez-Algaba J, Thach T, Sørensen C, Hansen JG, Lassen P, Kumarse N, Hodson D, Justesen AF, Hovmoller MS. 2017b. Yellow rust epidemics worldwide were caused by pathogen races from divergent genetic lineages. Frontiers in Plant Science 8:1057, doi:10.3389/fpls.2017.01057-1057
   Google Scholar
• Ali S, Sharma S, Leconte M, Shah SJA, Duveiller E, de Vallvieille-Pope C. 2018. Low pathotype diversity in a recombinant Puccinia striiformis population through convergent selection at the Eastern part of Himalayan centre of diversity (Nepal). Plant Pathology 67:810–820.
   Web of Science ®Google Scholar
• Beddow JM, Pardey PG, Chai Y, Hurley TM, Kriticos DJ, Braun JC, Park RF, Cuddy WS, Yonow T. 2015. Research investment implications of shifts in the global geography of wheat stripe rust. Nature Plants 1:15132.
   PubMed Web of Science ®Google Scholar
• Belkhir KBP, Chikhi L, Raufaste N, Bonhomme F. 2004. GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Montpellier, France: Laboratoire Génome, Populations, Interactions, CNRS UMR 5000: Université de Montpellier II. Available from: https://kimura.univ-montp2.fr/genetix/
   Google Scholar
• Brar GS, Ali S, Qutob D, Ambrose S, Lou K, Maclachlan R, Pozniak CJ, Fu YB, Sharpe AG, Kutcher HR. 2018. Genome resequencing and simple sequence repeat markers reveal the existence of divergent lineages in the Canadian Puccinia striiformis f. sp. tritici population with extensive DNA methylation. Environmental microbiology 20:1498–1515.
   PubMed Web of Science ®Google Scholar
• Brown JKM, Hovmøller MS. 2002. Aerial dispersal of fungi on the global and continental scales and its consequences for plant disease. Science 297:537–541.
   PubMed Web of Science ®Google Scholar
• Chen XM. 2005. Epidemiology and control of stripe rust [Puccinia striiformis f. sp. tritici] on wheat. Canadian Journal of Plant Pathology 27:314–337.
   Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Dean R, Van Kan J, Pretorius ZA, Hammond-Kosack KE, Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD. 2012. The top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology 13:414–430.
   PubMed Web of Science ®Google Scholar
• El Amil R. 2015. Effet de l’hôte et de la température sur la structure de la population de Puccinia striiformis f. sp. tritici, agent de la rouille jaune du blé au Moyen Orient [PhD dissertation]. Paris, France: Université Paris-Sud. 209 p.
   Google Scholar
• Ezzahiri B, Yahyaoui A, Hovmøller MS. 2009. An analysis of the 2009 epidemic of yellow rust on wheat in Morocco. In: The 4th Regional Yellow Rust Conference for Central and West Asia and North Africa, [Place], [Dates]. Antalya, Turkey: Turkish Ministry of Agriculture and Rural Affairs, International Center for Agricultural Research in the Dry Areas, International Maize and Wheat Improvement Center, Food and Agriculture Organization of the United Nations.
   Google Scholar
• Gladieux P, Byrnese E, Fisher MC, Aguleta G, Heitman J, Giraud T. 2011. Epidemiology and evolution of fungal pathogens, in plants and animals ed. M Tibayrenc. Genetics and Evolution of Infectious Diseases 59–106.
   Google Scholar
• Hovmøller MS, Sørensen CK, Walter S, Justesen AF. 2011. Diversity of Puccinia striiformis on cereals and grasses. Annual Review of Phytopathology 49:197–217.
   PubMed Web of Science ®Google Scholar
• Hovmøller MS, Walter S, Bayles R, Hubbard A, Flath K, Sommerfeldt N, Leconte, M. Rodriguez-Algaba J, Hansen JG, Lassen P, Justesen AF, Ali S, de Vallavieille-Pope C. 2016. Replacement of the European wheat yellow rust population by new races from the centre of diversity in the near-Himalayan region. Plant Pathology 65:402– 411.
   Web of Science ®Google Scholar
• Hovmøller MS, Yahyaoui AH, Milus EA, Justesen AF. 2008. Rapid global spread of two aggressive strains of a wheat rust fungus. Molecular Ecology 17:3818–3826.
   PubMed Web of Science ®Google Scholar
• Jin Y, Szabo LJ, Carson M. 2010. Century-old mystery of Puccinia striiformis life history solved with the identification of Berberis as an alternate host. Phytopathology 100:432–435.
   PubMed Web of Science ®Google Scholar
• 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/1471-2156/11/94
   Google Scholar
• Justesen AF, Ridoutb CJ, Hovmøller MS. 2002. The recent history of Puccinia striiformis f. sp. tritici in Denmark as revealed by disease incidence and AFLP markers. Plant Pathology 51:13–23.
   Web of Science ®Google Scholar
• Kamvar ZN, Tabima, JF, and Grünwald, NJ. 2014. Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281, doi:10.7717/peerj.281
   PubMed Web of Science ®Google Scholar
• Khan MR, Rehman Z-u, Nazir SN, Tshewang S, Baidya S, Hodson D, Imtiaz M, Ali S. 2019. Genetic divergence and diversity in Himalayan Puccinia striiformis populations from Bhutan, Nepal and Pakistan. Phytopathology 109:1793–1800.
   Web of Science ®Google Scholar
• Langella O. 2008. POPULATIONS 1.2.3, logiciel de génétique des populations. Gif-sur-Yvette, France: Laboratoire Populations, Génétique et évolution, CNRS.
   Google Scholar
• R Core Team. 2016. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
   Google Scholar
• Rahmatov M. 2016. Genetic characterisation of novel resistance alleles to stem rust and stripe rust in wheat-alien introgression lines. Alnarp, Sweden: Swedish University of Agricultural Sciences. 76 p.
   Google Scholar
• Raymond M, Rousset F. 1995. GENEPOP version 1.2: population genetics software for exact tests and ecumenicism. Journal of Heredity 86:248–249.
   Web of Science ®Google Scholar
• Rodriguez-Algaba J, Walter S, Sørensen CK, Hovmøller MS, Justesen AF. 2014. Sexual structures and recombination of the wheat rust fungus Puccinia striiformis on Berberis vulgaris. Fungal Genetics and Biology 70:77–85.
   Web of Science ®Google Scholar
• Shean M. 2010. Middle East: yellow rust epidemic affects regional wheat crops. Washington, DC: United States Department of Agriculture. [cited 2020 Feb 15]. Available from: https://ipad.fas.usda.gov/highlights/2010/06/Middle%20East/
   Google Scholar
• Simpson EH. 1949. Measurement of diversity. Nature 163:688, doi:10.1038/163688a0
   Web of Science ®Google Scholar
• Singh RP, Singh PK, Rutkoski J, Hodson DP, He X, Jorgensen LN, Hovmoller MS, Huerta- Espino J. 2016. Disease impact on wheat yield potential and prospects of genetic control. Annual Review of Phytopathology 54:303–322.
   PubMed Web of Science ®Google Scholar
• Singh RP, William HM, 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; Brisbane, Australia; 26 Sep–1 Oct 2004. [cited 2020 Feb 15]. Available from: http://www.cropscience.org.au/icsc2004/symposia/3/7/141_singhrp.htm
   Google Scholar
• Thach T, Ali S, de Vallavieille-Pope C, Justesen AF, Hovmøller MS. 2016. Worldwide population structure of the wheat rust fungus Puccinia striiformis in the past. Fungal Genetics and Biology 87:1–8, doi:10.1016/j.fgb.2015.12.014
   PubMed Web of Science ®Google Scholar
• Walter S, Ali S, Kemen E, Nazari K, Bahri B, Enjalbert J, Bochra A, Hansen JG, Brown JKM, Sicheritzé PT, Jones J. 2016. Molecular markers for tracking the origin and worldwide distribution of invasive strains of Puccinia striiformis. Ecology and Evolution 6:2790–2804.
   PubMed Web of Science ®Google Scholar