Global rise of a wheat pathogen through two-stage evolutionary emergence coupled with aerial dispersal

The rise of plant pathogens following crop domestication and their subsequent global spread pose persistent threats to food security, yet the mechanisms underlying host jumps and rapid adaptation in obligate biotrophs remain unclear. Using 319 Puccinia striiformis f. sp. tritici (Pst) genomes and virulence phenotypes of 234 isolates across six continents, we construct its origin and global dissemination. Our analyses support a two-stage emergence model: P. striiformis sensu stricto originated and diversified in the Himalayan region, subsequently a P. striiformis s. str. lineage jumped to domesticated wheat in the Fertile Crescent, giving rise to epidemic lineage (Pst) and spreading worldwide with wheat cultivation. This host jump triggered demographic expansion and selective sweeps, while GWAS identified region-specific virulence loci shaped by resistant cultivars. Overlay of air trajectory and dispersal simulations identified atmospheric corridors consistent with genomic migration patterns, supporting a historical role for long-distance aerial transport in the pathogen’s global spread.