Population genomic analyses reveal extensive genomic regions within selective sweeps associated with adaptation and demographic history of a wheat fungal pathogen

Abstract Plant pathogens rapidly evolve in response to changes in their hosts and environments, resulting in destructive epidemics. The fungus Puccinia striiformis f. sp. tritici ( Pst ), responsible for wheat stripe rust disease, exemplifies such evolutionary dynamics. Host population changes impose selective pressures on pathogens; however, the selection footprints and demographic patterns of Pst are not well understood. In this study, we performed whole‐genome sequencing of 69 Pst isolates collected from diverse regions across China to investigate genome‐wide patterns of gene flow and divergence. Our findings reveal significant gene flow within China but limited exchange between Chinese and international Pst populations, characterized by a slower decay of linkage disequilibrium compared to fungi with known sexual reproduction. We identified extensive hard and soft sweeps associated with Pst adaptation. The genes involved in these sweeps are enriched for secreted proteins and effectors, with functions related to pathogenicity, temperature tolerance, and fungicide resistance, indicating positive selection driven by both host and abiotic pressures. Demographic reconstruction shows strong bottlenecks in Pst populations during the domestication of wheat approximately 10,000 years ago and the advent of modern agriculture 100 years ago, suggesting that crop domestication and breeding programs have significantly influenced pathogen population dynamics. Our study provides valuable insights into the genomic evolution of Pst in China and highlights the impact of modern agricultural practices on pathogen demography.