Deciphering a pathogen's evolution: a two-decade longitudinal study reveals virulence shifts and identifies durable Pm genes against Himalayan Blumeria graminis f. sp. tritici populations.

Wheat powdery mildew, caused by the obligate biotrophic fungus Blumeria graminis f. sp. tritici (Bgt), is a devastating disease responsible for substantial global yield reductions. Host resistance offers the most sustainable management strategy, yet its durability is continually undermined by high evolutionary potential of the pathogen, driven by sexual recombination and rapid mutation. To decipher long-term virulence dynamics, we conducted a comparative analysis of Bgt populations in the Northwestern Himalayas over two decades (1994-1998 and 2015-2019). Pathotype profiling of 285 isolates on a common set of nine differential lines revealed a significant shift in virulence structure over time. While the mean virulence complexity per isolate increased in the contemporary population, indicating enhanced pathogenic capability, overall pathotype diversity decreased, suggesting a selective sweep toward fewer, more aggressive lineages. Marked changes in virulence frequency were observed with severe efficacy erosion for Pm1a (virulence increased from 6 to 63%) and Pm8, while virulence against Pm2, Pm3a, and Pm3b declined significantly. Notably, genes Pm2 and Pm4a demonstrated complete and durable effectiveness throughout the study period. Our results identify these as stable resistance donors and underscores the continuous adaptation of Bgt populations. This study provides critical insights for designing durable resistance gene pyramids and underscores the necessity of continuous virulence surveillance to sustain wheat production in the face of evolving pathogen threats.