Genomic surveillance and molecular evolution of fungicide resistance in European populations of wheat powdery mildew

Fungicides are used in agriculture to manage fungal infections and maintain crop yield and quality. In Europe, their application on cereals increased drastically starting from the mid 1970s, contributing to a significant improvement in yields. However, extensive usage has led to the rapid evolution of resistant pathogen populations within just a few years of fungicide deployment. Here we focus on wheat powdery mildew, a disease caused by the ascomycete fungus Blumeria graminis forma specialis tritici (Bgt). Previous research on Bgt documented the emergence of resistance to different fungicides and identified various resistance mechanisms. Yet, the frequency, distribution, and evolutionary dynamics of fungicide resistance in Bgt populations remain largely unexplored. In this study we leveraged extensive sampling and whole-genome sequencing of Bgt populations in Europe and the Mediterranean to investigate the population genetics and molecular epidemiology of fungicide resistance towards five major fungicide classes. We analyzed gene sequences and copy number variation of eight known fungicide target genes in 415 Bgt isolates sampled between 1980 and 2023. We observed that mutations conferring resistance to various fungicides increased in frequency over time, and had distinct geographic distributions, likely due to diverse deployment of fungicides across different regions. For demethylation inhibitor fungicides we identified multiple independent events of resistance emergence with distinct mutational profiles, and we tracked their rapid spread in the last decades. Overall, we revealed the evolutionary and epidemiological dynamics of fungicide resistance mutations in European Bgt populations. These results underscore the potential of genomic surveillance and population genetics to enhance our understanding of fungicide resistance.