The grey mould Botrytis cinerea employs multiple mechanisms to protect itself from antifungal plant metabolites

Abstract

Saponins are plant secondary metabolites comprising glycosylated triterpenoids, steroids or steroidal alkaloids with a broad spectrum of toxicity to microbial pathogens and pest organisms that contribute to basal plant defence to biotic attack. Secretion of glycosyl hydrolases that enzymatically convert saponins into less toxic products was thus far the only mechanism reported to enable fungal pathogens to colonize their saponin-containing host plant(s). We studied the mechanisms that the fungus Botrytis cinerea utilizes to be tolerant to well-characterized, structurally related saponins from tomato and Digitalis purpurea. By gene expression studies, comparative genomics, enzyme assays and testing a large panel of fungal (knockout and complemented) mutants, we unraveled four distinct cellular mechanisms that participate in mitigation of the toxic activity of these saponins. The enzymatic deglycosylation is novel and unique to this fungus-saponin combination, while the genes involved in other tolerance mechanisms have orthologs that are widely distributed in the fungal kingdom. We present a spatial and temporal model on how these mechanisms jointly confer tolerance to α- tomatine and we discuss the repercussions for other fungi and different saponins.