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Thesis Title: Population biology and invasion history of Puccinia striiformis f.sp. tritici at worldwide and local scale
PhD session: October 2009 - September 2012
Specialization: Genetics, Evolution, Population Biology, Epidemiology, Resistance Breeding
University: Doctoral School of Plant Sciences, UNIVERSITE PARIS-SUD – UFR des Sciences – France
Host Laboratory: UR BIOGER-CPP, INRA Versailles-Grignon, France
Scholarship: Overseas scholarship for MS/MPhil leading to PhD in selected field phase-II batch II - 2008, Higher Education Commission, Government of Pakistan
PhD Supervision:
Claude de Vallavieille-Pope, INRA UR 1290 BIOGER-CPP, BP01, F-78850 Thiverval-Grignon, France
Jerome Enjalbert, INRA UMR 320 Génétique Végétale, Ferme du Moulon, F-91190 Gif sur Yvette, France
Mogens S. Hovmøller, Department of Agroecology, Aarhus University, Flakkebjerg, DK-4200 Slagelse, Denmark
Pierre Gladieux, Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720-3102
Date of PhD defense: 10 September 2012
Jury for PhD defense:
Jacqui Shykoff DR, CNRS-Université Paris-Sud 11, Orsay, France – Président
James K.M. Brown Professor, John Innes Centre, UK – Rapporteurs
Didier Tharreau DR, UMR BGPI, CIRAD, France – Rapporteurs
Tatiana Giraud DR, CNRS-Université Paris-Sud 11, Orsay, France – Examinateur
Kumarse Nazari Senior Cereal Pathologist, ICARDA, Syria – Examinateur
Mogens S. Hovmøller Professor, Aarhus University, Denmark – Examinateur
Claude de Vallavieille-Pope DR, UR BIOGER-CPP, INRA Grignon, France – Directrice de thèse
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POPULATION BIOLOGY AND INVASION HISTORY OF PUCCINIA STRIIFORMIS F.SP. TRITICI AT WORLDWIDE AND LOCAL SCALE
Analyses of the large-scale population structure of pathogens enable the identification of migration patterns, diversity reservoirs or longevity of populations, the understanding of current evolutionary trajectories and the anticipation of future ones. Once identified, a detailed analysis of populations in centre of diversity, with emphasis on demographic and reproductive parameters should enable to infer the adaptive capacity of the pathogen and identify potential sources for new invasions. Puccinia striiformis f.sp. tritici (PST) is the causal agent of wheat yellow/stripe rust, and despite a worldwide distribution, this fungus remains a model species for invasion studies, due to its long-distance migration capacity and recurrent local emergence of new strains. Little is known about the ancestral relationship of the worldwide PST population, while its center of origin is still unknown. We used multilocus microsatellite genotyping to infer the worldwide population structure of PST and the origin of new invasions, analysing a set of isolates representative of sampling performed over six continents. Bayesian and multivariate clustering methods partitioned the isolates into six distinct genetic groups, corresponding to distinct geographic areas. The assignment analysis confirmed the Middle East-Red Sea Area as the most likely source of newly spreading, high-temperature-adapted strains; Europe as the source of South American, North American and Australian populations; and Mediterranean-Central Asian populations as the origin of South African populations. The existence of strong population subdivision at worldwide level shows that major genetic groups are not markedly affected by recent dispersal events. However, the sources for recent invasions and the migration routes identified emphasize the importance of human activities on the recent long-distance spread of the disease. The analyses of linkage disequilibrium and genotypic diversity indicated a strong regional heterogeneity in levels of recombination, with clear signatures of recombination in the Himalayan (Nepal and Pakistan) and near-Himalayan (China) regions and a predominant clonal population structure in other regions. To explain the variability in diversity and recombination of worldwide PST populations, we assessed their sex ability in terms of telial production, the sex-specific structures that are obligatory for PST sexual cycle, in a set of 56 isolates representative of these worldwide geographical origins. We confirmed that the variability in genotypic diversity/ recombination was linked with the sex ability, pinpointing the Himalayan region as the possible center of origin of PST, from where it then spread worldwide. The reduced sex ability in clonal populations certainly reflects a loss of sexual function, associated to migration in areas where sexual alternate host is lacking, or not necessary for the completion of epidemic cycle. Approximate Bayesian computation analyses confirmed an out of Himalaya spread of PST, with Pakistan and China being the most ancestral population. An in-depth study was made in the Himalayan region (Pakistan) and Near Himalayan region (Gansu, China) to better describe the population maintenance in two areas of high diversity. Analyses of Pakistani population at regional level revealed the existence of a strong population subdivision, a high genotypic diversity and the existence of recombination signature at each location reflecting the role of sexual recombination in the temporal maintenance at local level. A time spaced sampling of PST in the valley of Tianshui (China) inspired the development of a new estimator, allowing to quantify the relative contribution of sexual reproduction and effective population size on the basis of clonal resampling within and between years. A sexual reproduction rate of 74% (95% confidence interval [CI]: 38-95%) and effective population size of 1735 (95% CI: 675-2800) was quantified in Chinese PST population. The description of the origin and migration routes of PST populations worldwide and at its centre of diversity contributes to our understanding of PST evolutionary potential, and is helpful to build disease management strategies.
PhD publications media coverage:
http://www.versailles-grignon.inra.fr/Toutes-les-actualites/201407-Rouille-jaune-du-ble
Articles published from PhD work:
Ali, S, Gladieux P, Leconte M, Gautier A, Justesen AF, Hovmoller MS, Enjalbert J, De Vallavieille-Pope C. 2014. Origin, migration routes and genetic structure of worldwide populations of the wheat yellow rust pathogen, Puccinia striiformis f.sp. tritici. PLOS Pathogens. 10: e1003903. DOI: 10.1371/journal.ppat.1003903.http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1003903
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. 2014. 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. DOI: 10.1111/mec.12629. http://onlinelibrary.wiley.com/doi/10.1111/mec.12629/abstract
Ali, S., A. Gautier, M. Leconte, J. Enjalbert, and C. De Vallavieille-Pope. 2011. A rapid genotyping method for an obligate fungal pathogen, Puccinia striiformis f.sp. tritici, based on DNA extraction from infected leaf and Multiplex PCR genotyping. BMC Research Notes. 4: 240. http://www.biomedcentral.com/1756-0500/4/240/abstract
Ali, S., M. Leconte, A.-S. Walker, J. Enjalbert, and C. De Vallavieille-Pope. 2010. Reduction in the sex ability of worldwide clonal populations of Puccinia striiformis f.sp. tritici. Fungal Genetics and Biology. 47: 828-838. http://www.sciencedirect.com/science/article/pii/S1087184510001283
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.http://apsjournals.apsnet.org/doi/abs/10.1094/PDIS-02-11-0078
Link to download the thesis: http://tel.archives-ouvertes.fr/tel-00806507/
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