Population genomics wheat stripe rust fungi in China. Puccinia striiformis

Plant pathogens are notorious for their ability to quickly evolve in response to the changing host and environment, resulting in destructive epidemics, particularly in agriculture. The fungus Puccinia striiformis f. sp. tritici (Pst), causing wheat stripe rust disease worldwide, is one such pathogen. In the arms race between pathogens and hosts, changes in host populations exerted continuous selective forces on the dynamics of pathogens. However, the footprints of these selection forces and the demography of Pst remain poorly explored. Exploring the footprints of selection forces and demography can enable us to better understand the evolutionary processes that shape the spread and evolution of pathogens, and further to provide insights into the prediction of pathogen population changes when host resistance is utilized to control the disease in modern agriculture. In this study, we revealed several features of worldwide Pst populations through population genomic analyses. Firstly, there might be limited gene flow between Pst populations from China and other countries. A slower rate of linkage disequilibrium decay was detected comparing to rust fungi with known sexual reproduction. Furthermore, we shown that the pervasive hard and soft sweeps were associated with Pst adaptation. Genes within the selective sweeps were enriched in secreted proteins and effectors and showed functions related to pathogenicity or virulence, temperature tolerance, and fungicide resistance implying that Chinese Pst populations suffered positive selection pressures from host and abiotic factors. Moreover, demographic history indicated Pst populations experienced strong bottlenecks at the beginning of the wheat domestication around 10,000 years ago and during modern agriculture around 100 years ago, suggesting that the crop domestication and breeding programs could continuously contribute to the decline of pathogen effective population sizes. Our results provided insights into the evolution of the Pst genome and highlighted the role of modern agriculture on pathogen demography.