Analyses of 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. This is particularly important for long-distance migrating fungal pathogens such as Puccinia striiformis f.sp. tritici (PST), capable of rapid spread to new regions and crop varieties. Although a range of recent PST invasions at continental scales are well documented, the worldwide population structure and the center of origin of the pathogen were still unknown. In this study, we used multilocus microsatellite genotyping to infer worldwide population structure of PST and the origin of new invasions based on 409 isolates representative of distribution of the fungus on six continents. Bayesian and multivariate clustering methods partitioned the set of multilocus genotypes into six distinct genetic groups associated with their geographical origin. 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 regions (China) and a predominant clonal population structure in other regions. The higher genotypic diversity, recombinant population structure and high sexual reproduction ability in the Himalayan and neighboring regions suggests this area as the putative center of origin of PST. We used clustering methods and approximate Bayesian computation (ABC) to compare different competing scenarios describing ancestral relationship among ancestral populations and more recently founded populations. Our analyses confirmed the Middle East-East Africa 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. Although most geographic populations are not markedly affected by recent dispersal events, this study emphasizes the influence of human activities on recent long-distance spread of the pathogen.

Isolates of recently spreading races of yellow rust from wheat and triticale in Europe were analysed using virulence phenotypic data of 2605 isolates sampled in 12 countries between 2000 and 2014. A subset of 239 isolates was investigated by microsatellite markers. At least three races of non-European origin, termed 'Warrior', 'Kranich' and 'Triticale aggressive', were identified in the post-2011 population. The Warrior race was already present in high frequencies in the first year of detection in most European countries and to a large extent it replaced the pre-2011 European population. In contrast, the two other exotic races were localized to certain regions and/or crop type. The presence already of at least six multilocus genotypes of the Warrior race and five genotypes of the Kranich race in the first year of detection and across large areas is consistent with a hypothesis of aerial spread from genetically diverse source populations. A comparison with reference isolates sampled from six continents suggested that the Warrior and Kranich races originated from sexually recombining populations in the centre of diversity of the yellow rust fungus in the near-Himalayan region of Asia. However, the Triticale aggressive race was most similar to populations in the Middle East/Central Asia. The study illustrated the potential role of sexual Puccinia striiformis populations as a reservoir for new races replacing distant clonal populations.