Botrytis cinerea combines four molecular strategies to tolerate membrane-permeating plant compounds and to increase virulence

Yaohua You, H.M. Suraj, Linda Matz, A.L. Herrera Valderrama, Paul Ruigrok, Xiaoqian Shi-Kunne, Frank P.J. Pieterse, Anne Oostlander, Henriek G. Beenen, Edgar A. Chavarro-Carrero, Si Qin, Francel W.A. Verstappen, Iris F. Kappers, André Fleißner, Jan A.L. van Kan*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

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 defense 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 the mitigation of the toxic activity of these saponins and in virulence on saponin-producing host plants. The enzymatic deglycosylation that we identified is novel and unique to this fungus-saponin combination. The other three tolerance mechanisms operate in the fungal membrane and are mediated by protein families that are widely distributed in the fungal kingdom. We present a spatial and temporal model on how these mechanisms jointly confer tolerance to saponins and discuss the repercussions of these findings for other plant pathogenic fungi, as well as human pathogens.

Original languageEnglish
Article number6448
JournalNature Communications
Volume15
DOIs
Publication statusPublished - 31 Jul 2024

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