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

Yaohua You, H. M. Suraj, Linda Matz, A. Lorena 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 and Jan A. L. Kan ()
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Yaohua You: Wageningen University
H. M. Suraj: Wageningen University
Linda Matz: Technische Universität Braunschweig
A. Lorena Herrera Valderrama: Wageningen University
Paul Ruigrok: Wageningen University
Xiaoqian Shi-Kunne: Wageningen University
Frank P. J. Pieterse: Wageningen University
Anne Oostlander: Technische Universität Braunschweig
Henriek G. Beenen: Wageningen University
Edgar A. Chavarro-Carrero: Wageningen University
Si Qin: Wageningen University
Francel W. A. Verstappen: Wageningen University
Iris F. Kappers: Wageningen University
André Fleißner: Technische Universität Braunschweig
Jan A. L. Kan: Wageningen University

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-50748-5

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