Host-mediated demographic filtering drives rapid lineage turnover in the wheat stripe rust pathogen population
Stripe rust, caused by the fungal pathogen Puccinia striiformis f. sp. tritici (Pst), remains a major threat to wheat production in Central Asia. This study investigates how host genetic composition and environmental factors drive demographic filtering and shape the temporal turnover of pathogen lineages in Uzbekistan. From 2023 to 2025, a total of 793 paired host-pathogen samples were collected across diverse agroecological zones and genotyped using high-resolution GenoBaits panels (20K for Pst and 100K for wheat). Population genomic analyses revealed pronounced temporal and spatial shifts in Pst genetic structure. Predominant lineages (AD, HB_25, G2) declined, replaced by G5 and G7 by 2025. In contrast, the wheat population showed low genetic diversity, with repeated cultivation of highly similar cultivars across multiple regions and years, likely facilitating recurrent epidemics driven by dominant Pst lineages. Host-pathogen association analysis identified lineage-specific virulence patterns, with the AD group infecting most major cultivars except Krasnadar, while G2 showed strong virulence against Krasnadar. HB_25 was highly virulent to Vexa and Velena. Climatic association analysis indicated significant environmental adaptation among Pst lineages, with G2 prevailing under broader temperature and higher rainfall conditions, whereas G7 was associated with warmer environments and moderate rainfall. Spore dispersal analysis identified Tashkent as the principal regional hub for pathogen spread, whereas Surkhandarya emerged as a potential gateway for the introduction of new lineages from neighboring Afghanistan and Tajikistan. Notably, G5 and G7 lineages, which became predominant in 2025, were first detected in the region during their initial incursion in 2023. These findings highlight the combined roles of host genetic uniformity, pathogen adaptation, and regional dispersal in shaping stripe rust epidemics, demonstrating how host-mediated demographic filtering drives rapid lineage turnover.