Genomic Insights into Historical Adaptation of Three Key Fungal Plant Pathogens

Fungal culture collections hold a wealth of historical isolates that could be used to study fungal evolution over the past decades, an era that coincided with agricultural industrialization. We performed population structure and temporal association analysis on three major fungal crop pathogens, Verticillium nonalfalfae, Fusarium culmorum, and Botrytis cinerea, collected between 1956 and 2023. Population structure analysis indicated predominantly sexual reproduction in F. culmorum and B. cinerea, whereas V. nonalfalfae was shown to be largely asexual. Single nucleotide polymorphisms (SNPs) of the recombining species F. culmorum and B. cinerea that showed major temporal changes fell within or close to coding genes, whereas time-variant SNPs in V. nonalfalfae were located within or close to transposable elements (TEs) and a Starship element. This is consistent with the hypothesis that rare-sex fungal species often rely on TE-mediated genomic diversification rather than sexual recombination. Across all three species, rapidly evolving SNPs were associated with genes encoding Major Facilitator Superfamily transporters, which are frequently implicated in fungicide resistance, and Zn2Cys6 fungal-type transcription factors, which play key roles in stress responses and pathogenesis. Our findings demonstrate the value of temporal association analysis as an untargeted approach for exploring fungal evolution since the advent of the green revolution. Applying this method across a broader range of fungal crop pathogens could provide deeper insights into their evolution and adaptation.