Two divergent haploid nuclei shaped the landscape of population diversity in wheat stripe rust Puccinia striiformis f. sp. tritici

Heterozygosity is a measure of allelic diversity within individuals. Puccinia striiformis f. sp. tritici (Pst) is a highly heterozygous dikaryotic crop pathogen. The source of heterozygosity variation and the contribution to adaptability are still unknown. By analyzing resequencing data of 266 worldwide Pst isolates, we find that two predominant nuclear haplotypes, A and B, exist in Pst population. Strains with different combinations of these nuclear haplotypes exhibit divergent levels of heterozygosity. Between the A/B two haploid genomes, 16% of the genome is divergent, scattered as mosaic blocks within the genome. These regions are enriched with genes displaying critical roles during infection of the plant host, and exhibit higher expression level in publicly available transcriptome samples. In these regions, 8.0 Mb shows recombination fingerprints associated with virulence, while 4.9 Mb displays linkage across the entire genome. We demonstrate that sexual recombination in Pst is extensive and significant. Pst can gain genetic diversity and adaptability due to intra- and inter-species hybridization. Our study resolves the debate over the sources of individual allele diversity in Pst and expands the understanding of pathogen virulence evolution. These findings also suggest that interrupting the sexual reproduction of pathogens can be an effective strategy for controlling wheat stripe rust. Analysis of resequencing data from the dikaryotic fungus Puccinia striiformis f. sp. tritici identified two predominant nuclear haplotypes in the global pathogen population. Genomic evidence confirmed hybridization events within the population, which contributed to genetic diversity and provided new insights into the evolution of virulence.