Botrytis cinerea identifies host plants via the recognition of antifungal capsidiol to induce expression of a specific detoxification gene

The gray mold pathogen has a broad host range, causing disease in >400 plant species, but it is not known how this pathogen evolved this polyxenous nature. can metabolize a wide range of phytoalexins, including the stilbenoid resveratrol in grape, and the sesquiterpenoids capsidiol in tobacco and rishitin in potato and tomato. In this study, we analyzed the metabolism of sesquiterpenoid phytoalexins by . Capsidiol was dehydrogenated to capsenone, which was then further oxidized, while rishitin was directly oxidized to epoxy- or hydroxyrishitins, indicating that has separate mechanisms to detoxify structurally similar sesquiterpenoid phytoalexins. RNA-seq analysis revealed that a distinct set of genes were induced in when treated with capsidiol or rishitin, suggesting that can distinguish structurally similar phytoalexins to activate appropriate detoxification mechanisms. The gene most highly upregulated by capsidiol treatment encoded a dehydrogenase, designated . Heterologous expression of in a capsidiol-sensitive plant symbiotic fungus, , resulted in an acquired tolerance of capsidiol and the ability to metabolize capsidiol to capsenone, while mutants became relatively sensitive to capsidiol. The mutant showed reduced virulence on the capsidiol producing and species but remained fully pathogenic on potato and tomato. Homologs of are found in taxonomically distant Ascomycota fungi but not in related Leotiomycetes species, suggesting that acquired the ancestral by horizontal gene transfer, thereby extending the pathogenic host range of this polyxenous pathogen to capsidiol-producing plant species.