Botrytis cinereadetoxifies the sesquiterpenoid phytoalexin rishitin through multiple metabolizing pathways

Abstract

ABSTRACTBotrytis cinereais a necrotrophic pathogen that infects across a broad range of plant hosts, including high-impact crop species. Its generalist necrotrophic behavior stems from its ability to detoxify structurally diverse phytoalexins. The current study aims to provide evidence of the ability ofB. cinereato tolerate the sesquiterpenoid phytoalexin rishitin, which is produced by potato and tomato. While the growth of potato pathogensPhytophthora infestans(late blight) andAlternaria solani(early blight) was severely inhibited by rishitin,B. cinereawas tolerant to rishitin. After incubation of rishitin with the mycelia ofB. cinerea, it was metabolized to at least six oxidized forms. Structural analysis of these purified rishitin metabolites revealed a variety of oxidative metabolism including hydroxylation at C7 or C12, ketone formation at C5, and dihydroxylation at the 10,11-olefin. Six rishitin metabolites showed reduced toxicity toP. infestansandA. solani, indicating thatB. cinereahas at least 5 distinct enzymatic reactions to detoxify rishitin. Four host-specialized phytopathogenicBotrytisspecies, namelyB. elliptica, B. allii, B. squamosa,andB. tulipaealso had at least a partial ability to metabolize rishitin asB. cinerea, but their metabolic capacity was significantly weaker than that ofB. cinerea. These results suggest that the ability ofB. cinereato rapidly metabolize rishitin through multiple detoxification mechanisms could be critical for its pathogenicity in potato and tomato.