Two Ancient Nuclear Lineages and Divergent Reproductive Strategies Drive Global Success of the Wheat Stripe Rust Pathogen.

Plant pathogen evolution is driven by complex biological and ecological processes with major consequences for food security. Understanding how genetic diversity arises and is maintained is critical for predicting disease emergence. The wheat stripe rust fungus Puccinia striiformis f. sp. tritici is among the world's most destructive crop pathogens. As a dikaryotic fungus harboring two distinct haploid nuclei, Puccinia striiformis f. sp. tritici offers an excellent model to investigate nuclear-level evolution. Here, using population genomics of 507 global isolates and haplotype-phased genomes, we reconstruct the evolutionary history of Puccinia striiformis f. sp. tritici and its two nuclei. We show that two ancient nuclear lineages, nuclA and nuclB, originated from a common ancestor and diverged approximately 10,000 years ago, predating modern agriculture. Their differentiation was reinforced during wheat domestication and early agricultural expansion, which imposed new ecological and selective pressures. Subsequent wheat dispersal and regional adaptation promoted the emergence of two allopatric homozygous populations: nuclA-nuclA, which is predominant in south Asia/east Africa, while nuclB-nuclB is predominant in China, with both undergoing sexual recombination. In contrast, later agricultural intensification favored clonal propagation and facilitated recurrent somatic nuclear exchange, giving rise to a globally dominant heterokaryotic population (nuclA-nuclB) with high heterozygosity and broad adaptability. Notably, similar virulence traits can arise independently in clonal populations and sexual populations, resulting in convergent evolutionary outcomes. Together, our results establish a unified evolutionary framework in which host domestication, reproductive strategy, and nuclear-lineage dynamics jointly shape the origin, diversification, and global success of a major crop pathogen.