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

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.

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Main Authors: You, Yaohua, Suraj, H.M., Matz, Linda, Herrera Valderrama, A.L., Ruigrok, Paul, Shi-Kunne, Xiaoqian, Pieterse, Frank P.J., Oostlander, Anne, Beenen, Henriek G., Chavarro-Carrero, Edgar A., Qin, Si, Verstappen, Francel W.A., Kappers, Iris F., Fleißner, André, van Kan, Jan A.L.
Format: Article/Letter to editor biblioteca
Language:English
Subjects:Life Science,
Online Access:https://research.wur.nl/en/publications/botrytis-cinerea-combines-four-molecular-strategies-to-tolerate-m
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spelling dig-wur-nl-wurpubs-6330272024-12-04 You, Yaohua Suraj, H.M. Matz, Linda Herrera Valderrama, A.L. Ruigrok, Paul Shi-Kunne, Xiaoqian Pieterse, Frank P.J. Oostlander, Anne Beenen, Henriek G. Chavarro-Carrero, Edgar A. Qin, Si Verstappen, Francel W.A. Kappers, Iris F. Fleißner, André van Kan, Jan A.L. Article/Letter to editor Nature Communications 15 (2024) ISSN: 2041-1723 Botrytis cinerea combines four molecular strategies to tolerate membrane-permeating plant compounds and to increase virulence 2024 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. en application/pdf https://research.wur.nl/en/publications/botrytis-cinerea-combines-four-molecular-strategies-to-tolerate-m 10.1038/s41467-024-50748-5 https://edepot.wur.nl/670880 Life Science https://creativecommons.org/licenses/by-nc-nd/4.0/ https://creativecommons.org/licenses/by-nc-nd/4.0/ Wageningen University & Research
institution WUR NL
collection DSpace
country Países bajos
countrycode NL
component Bibliográfico
access En linea
databasecode dig-wur-nl
tag biblioteca
region Europa del Oeste
libraryname WUR Library Netherlands
language English
topic Life Science
Life Science
spellingShingle Life Science
Life Science
You, Yaohua
Suraj, H.M.
Matz, Linda
Herrera Valderrama, A.L.
Ruigrok, Paul
Shi-Kunne, Xiaoqian
Pieterse, Frank P.J.
Oostlander, Anne
Beenen, Henriek G.
Chavarro-Carrero, Edgar A.
Qin, Si
Verstappen, Francel W.A.
Kappers, Iris F.
Fleißner, André
van Kan, Jan A.L.
Botrytis cinerea combines four molecular strategies to tolerate membrane-permeating plant compounds and to increase virulence
description 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.
format Article/Letter to editor
topic_facet Life Science
author You, Yaohua
Suraj, H.M.
Matz, Linda
Herrera Valderrama, A.L.
Ruigrok, Paul
Shi-Kunne, Xiaoqian
Pieterse, Frank P.J.
Oostlander, Anne
Beenen, Henriek G.
Chavarro-Carrero, Edgar A.
Qin, Si
Verstappen, Francel W.A.
Kappers, Iris F.
Fleißner, André
van Kan, Jan A.L.
author_facet You, Yaohua
Suraj, H.M.
Matz, Linda
Herrera Valderrama, A.L.
Ruigrok, Paul
Shi-Kunne, Xiaoqian
Pieterse, Frank P.J.
Oostlander, Anne
Beenen, Henriek G.
Chavarro-Carrero, Edgar A.
Qin, Si
Verstappen, Francel W.A.
Kappers, Iris F.
Fleißner, André
van Kan, Jan A.L.
author_sort You, Yaohua
title Botrytis cinerea combines four molecular strategies to tolerate membrane-permeating plant compounds and to increase virulence
title_short Botrytis cinerea combines four molecular strategies to tolerate membrane-permeating plant compounds and to increase virulence
title_full Botrytis cinerea combines four molecular strategies to tolerate membrane-permeating plant compounds and to increase virulence
title_fullStr Botrytis cinerea combines four molecular strategies to tolerate membrane-permeating plant compounds and to increase virulence
title_full_unstemmed Botrytis cinerea combines four molecular strategies to tolerate membrane-permeating plant compounds and to increase virulence
title_sort botrytis cinerea combines four molecular strategies to tolerate membrane-permeating plant compounds and to increase virulence
url https://research.wur.nl/en/publications/botrytis-cinerea-combines-four-molecular-strategies-to-tolerate-m
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