Global Patterns of Genetic Variation and Population Structure in Grapevine Powdery Mildew (Erysiphe necator)

Erysiphe necator, the causal agent of grapevine powdery mildew, is the most damaging pathogen in global viticulture. To characterize its population structure, genetic diversity, and dispersal patterns, we analyzed 410 isolates collected from major viticultural regions across Europe, the Americas, China, and Australia between 2012 and 2017. Genotyping employed 20 simple sequence repeat (SSR) markers, including 16 newly developed for this study, together with three nuclear loci (Tub2, EF1-α, IGS), enabling high resolution inference of global population structure, lineage connectivity, and diversity. The combined dataset revealed high genetic diversity and two major clusters with continental differentiation. Hierarchical analyses resolved additional substructure corresponding to geographic origin and regional adaptation. A distinct Australian cluster was recovered, consistent with geographic isolation and restricted gene flow. In the United States, Western populations displayed multilocus genotype richness comparable to Eastern populations but slightly lower allelic richness and the highest number of private alleles, a pattern consistent with regional diversification potentially on native Vitis hosts rather than recent European introduction. Fine‑scale structure in California, Oregon, and Australia indicated contributions from repeated introductions, environmental heterogeneity, and region‑specific selective pressures. Contrasting patterns of multilocus linkage disequilibrium revealed mixed reproductive modes, with some lineages dominated by clonality and others showing signatures of recombination and admixture. Collectively, these findings refine the global population landscape of E. necator, identify regions of elevated pathogen diversity, and underscore the need for regionally tailored surveillance and integrated management strategies as human mediated movement continues to shape global pathogen population structure.