Plant triterpenoid saponins function as susceptibility factors to promote the pathogenicity of Botrytis cinerea

Autores
Escaray, Francisco José; Felipo Benavent, Amelia; Antonelli, Cristian Javier; Balaguer, Begoña; Lopez Gresa, Maria Pilar; Vera, Pablo
Año de publicación
2024
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The gray mold fungus Botrytis cinerea is a necrotrophic pathogen that causes diseases in hundreds of plant species, including high-value crops. Its polyxenous nature and pathogenic success are due to its ability to perceive host signals in its favor. In this study, we found that laticifer cells of Euphorbia lathyris are a source of susceptibility factors required by B. cinerea to cause disease. Consequently, poor-in-latex (pil) mutants, which lack laticifer cells, show full resistance to this pathogen, whereas lot-of-latex mutants, which produce more laticifer cells, are hypersusceptible. These S factors are triterpenoid saponins, which are widely distributed natural products of vast structural diversity. The downregulation of laticifer-specific oxydosqualene cyclase genes, which encode the first committed step enzymes for triterpene and, therefore, saponin biosynthesis, conferred disease resistance to B. cinerea. Likewise, the Medicago truncatula lha-1 mutant, compromised in triterpenoid saponin biosynthesis, showed enhanced resistance. Interestingly, the application of different purified triterpenoid saponins pharmacologically complemented the disease-resistant phenotype of pil and hla-1 mutants and enhanced disease susceptibility in different plant species. We found that triterpenoid saponins function as plant cues that signal transcriptional reprogramming in B. cinerea, leading to a change in its growth habit and infection strategy, culminating in the abundant formation of infection cushions, the multicellular appressoria apparatus dedicated to plant penetration and biomass destruction in B. cinerea. Taken together, these results provide an explanation for how plant triterpenoid saponins function as disease susceptibility factors to promote B. cinerea pathogenicity.
Fil: Escaray, Francisco José. Universidad Politécnica de Valencia; España. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Felipo Benavent, Amelia. Universidad Politécnica de Valencia; España
Fil: Antonelli, Cristian Javier. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Fisiología Vegetal. Universidad Nacional de La Plata. Facultad de Ciencias Naturales y Museo. Instituto de Fisiología Vegetal; Argentina
Fil: Balaguer, Begoña. Universidad Politécnica de Valencia; España
Fil: Lopez Gresa, Maria Pilar. Universidad Politécnica de Valencia; España
Fil: Vera, Pablo. Universidad Politécnica de Valencia; España
Materia
EUPHORBIA LATHYRIS
LATICIFER CELL
LATEX
APPRESSORIUM
INFECTION CUSHION
NECROTROPHIC FUNGI
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/262529
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/262529
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Plant triterpenoid saponins function as susceptibility factors to promote the pathogenicity of Botrytis cinereaEscaray, Francisco JoséFelipo Benavent, AmeliaAntonelli, Cristian JavierBalaguer, BegoñaLopez Gresa, Maria PilarVera, PabloEUPHORBIA LATHYRISLATICIFER CELLLATEXAPPRESSORIUMINFECTION CUSHIONNECROTROPHIC FUNGIhttps://purl.org/becyt/ford/4.4https://purl.org/becyt/ford/4The gray mold fungus Botrytis cinerea is a necrotrophic pathogen that causes diseases in hundreds of plant species, including high-value crops. Its polyxenous nature and pathogenic success are due to its ability to perceive host signals in its favor. In this study, we found that laticifer cells of Euphorbia lathyris are a source of susceptibility factors required by B. cinerea to cause disease. Consequently, poor-in-latex (pil) mutants, which lack laticifer cells, show full resistance to this pathogen, whereas lot-of-latex mutants, which produce more laticifer cells, are hypersusceptible. These S factors are triterpenoid saponins, which are widely distributed natural products of vast structural diversity. The downregulation of laticifer-specific oxydosqualene cyclase genes, which encode the first committed step enzymes for triterpene and, therefore, saponin biosynthesis, conferred disease resistance to B. cinerea. Likewise, the Medicago truncatula lha-1 mutant, compromised in triterpenoid saponin biosynthesis, showed enhanced resistance. Interestingly, the application of different purified triterpenoid saponins pharmacologically complemented the disease-resistant phenotype of pil and hla-1 mutants and enhanced disease susceptibility in different plant species. We found that triterpenoid saponins function as plant cues that signal transcriptional reprogramming in B. cinerea, leading to a change in its growth habit and infection strategy, culminating in the abundant formation of infection cushions, the multicellular appressoria apparatus dedicated to plant penetration and biomass destruction in B. cinerea. Taken together, these results provide an explanation for how plant triterpenoid saponins function as disease susceptibility factors to promote B. cinerea pathogenicity.Fil: Escaray, Francisco José. Universidad Politécnica de Valencia; España. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Felipo Benavent, Amelia. Universidad Politécnica de Valencia; EspañaFil: Antonelli, Cristian Javier. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Fisiología Vegetal. Universidad Nacional de La Plata. Facultad de Ciencias Naturales y Museo. Instituto de Fisiología Vegetal; ArgentinaFil: Balaguer, Begoña. Universidad Politécnica de Valencia; EspañaFil: Lopez Gresa, Maria Pilar. Universidad Politécnica de Valencia; EspañaFil: Vera, Pablo. Universidad Politécnica de Valencia; EspañaOxford University Press2024-07info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/262529Escaray, Francisco José; Felipo Benavent, Amelia; Antonelli, Cristian Javier; Balaguer, Begoña; Lopez Gresa, Maria Pilar; et al.; Plant triterpenoid saponins function as susceptibility factors to promote the pathogenicity of Botrytis cinerea; Oxford University Press; Molecular Plant; 17; 7; 7-2024; 1073-10891674-2052CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://linkinghub.elsevier.com/retrieve/pii/S1674205224001564info:eu-repo/semantics/altIdentifier/doi/10.1016/j.molp.2024.05.008info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:30:45Zoai:ri.conicet.gov.ar:11336/262529instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 10:30:45.773CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Plant triterpenoid saponins function as susceptibility factors to promote the pathogenicity of Botrytis cinerea
title Plant triterpenoid saponins function as susceptibility factors to promote the pathogenicity of Botrytis cinerea
spellingShingle Plant triterpenoid saponins function as susceptibility factors to promote the pathogenicity of Botrytis cinerea
Escaray, Francisco José
EUPHORBIA LATHYRIS
LATICIFER CELL
LATEX
APPRESSORIUM
INFECTION CUSHION
NECROTROPHIC FUNGI
title_short Plant triterpenoid saponins function as susceptibility factors to promote the pathogenicity of Botrytis cinerea
title_full Plant triterpenoid saponins function as susceptibility factors to promote the pathogenicity of Botrytis cinerea
title_fullStr Plant triterpenoid saponins function as susceptibility factors to promote the pathogenicity of Botrytis cinerea
title_full_unstemmed Plant triterpenoid saponins function as susceptibility factors to promote the pathogenicity of Botrytis cinerea
title_sort Plant triterpenoid saponins function as susceptibility factors to promote the pathogenicity of Botrytis cinerea
dc.creator.none.fl_str_mv Escaray, Francisco José
Felipo Benavent, Amelia
Antonelli, Cristian Javier
Balaguer, Begoña
Lopez Gresa, Maria Pilar
Vera, Pablo
author Escaray, Francisco José
author_facet Escaray, Francisco José
Felipo Benavent, Amelia
Antonelli, Cristian Javier
Balaguer, Begoña
Lopez Gresa, Maria Pilar
Vera, Pablo
author_role author
author2 Felipo Benavent, Amelia
Antonelli, Cristian Javier
Balaguer, Begoña
Lopez Gresa, Maria Pilar
Vera, Pablo
author2_role author
author
author
author
author
dc.subject.none.fl_str_mv EUPHORBIA LATHYRIS
LATICIFER CELL
LATEX
APPRESSORIUM
INFECTION CUSHION
NECROTROPHIC FUNGI
topic EUPHORBIA LATHYRIS
LATICIFER CELL
LATEX
APPRESSORIUM
INFECTION CUSHION
NECROTROPHIC FUNGI
purl_subject.fl_str_mv https://purl.org/becyt/ford/4.4
https://purl.org/becyt/ford/4
dc.description.none.fl_txt_mv The gray mold fungus Botrytis cinerea is a necrotrophic pathogen that causes diseases in hundreds of plant species, including high-value crops. Its polyxenous nature and pathogenic success are due to its ability to perceive host signals in its favor. In this study, we found that laticifer cells of Euphorbia lathyris are a source of susceptibility factors required by B. cinerea to cause disease. Consequently, poor-in-latex (pil) mutants, which lack laticifer cells, show full resistance to this pathogen, whereas lot-of-latex mutants, which produce more laticifer cells, are hypersusceptible. These S factors are triterpenoid saponins, which are widely distributed natural products of vast structural diversity. The downregulation of laticifer-specific oxydosqualene cyclase genes, which encode the first committed step enzymes for triterpene and, therefore, saponin biosynthesis, conferred disease resistance to B. cinerea. Likewise, the Medicago truncatula lha-1 mutant, compromised in triterpenoid saponin biosynthesis, showed enhanced resistance. Interestingly, the application of different purified triterpenoid saponins pharmacologically complemented the disease-resistant phenotype of pil and hla-1 mutants and enhanced disease susceptibility in different plant species. We found that triterpenoid saponins function as plant cues that signal transcriptional reprogramming in B. cinerea, leading to a change in its growth habit and infection strategy, culminating in the abundant formation of infection cushions, the multicellular appressoria apparatus dedicated to plant penetration and biomass destruction in B. cinerea. Taken together, these results provide an explanation for how plant triterpenoid saponins function as disease susceptibility factors to promote B. cinerea pathogenicity.
Fil: Escaray, Francisco José. Universidad Politécnica de Valencia; España. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Felipo Benavent, Amelia. Universidad Politécnica de Valencia; España
Fil: Antonelli, Cristian Javier. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - La Plata. Instituto de Fisiología Vegetal. Universidad Nacional de La Plata. Facultad de Ciencias Naturales y Museo. Instituto de Fisiología Vegetal; Argentina
Fil: Balaguer, Begoña. Universidad Politécnica de Valencia; España
Fil: Lopez Gresa, Maria Pilar. Universidad Politécnica de Valencia; España
Fil: Vera, Pablo. Universidad Politécnica de Valencia; España
description The gray mold fungus Botrytis cinerea is a necrotrophic pathogen that causes diseases in hundreds of plant species, including high-value crops. Its polyxenous nature and pathogenic success are due to its ability to perceive host signals in its favor. In this study, we found that laticifer cells of Euphorbia lathyris are a source of susceptibility factors required by B. cinerea to cause disease. Consequently, poor-in-latex (pil) mutants, which lack laticifer cells, show full resistance to this pathogen, whereas lot-of-latex mutants, which produce more laticifer cells, are hypersusceptible. These S factors are triterpenoid saponins, which are widely distributed natural products of vast structural diversity. The downregulation of laticifer-specific oxydosqualene cyclase genes, which encode the first committed step enzymes for triterpene and, therefore, saponin biosynthesis, conferred disease resistance to B. cinerea. Likewise, the Medicago truncatula lha-1 mutant, compromised in triterpenoid saponin biosynthesis, showed enhanced resistance. Interestingly, the application of different purified triterpenoid saponins pharmacologically complemented the disease-resistant phenotype of pil and hla-1 mutants and enhanced disease susceptibility in different plant species. We found that triterpenoid saponins function as plant cues that signal transcriptional reprogramming in B. cinerea, leading to a change in its growth habit and infection strategy, culminating in the abundant formation of infection cushions, the multicellular appressoria apparatus dedicated to plant penetration and biomass destruction in B. cinerea. Taken together, these results provide an explanation for how plant triterpenoid saponins function as disease susceptibility factors to promote B. cinerea pathogenicity.
publishDate 2024
dc.date.none.fl_str_mv 2024-07
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/262529
Escaray, Francisco José; Felipo Benavent, Amelia; Antonelli, Cristian Javier; Balaguer, Begoña; Lopez Gresa, Maria Pilar; et al.; Plant triterpenoid saponins function as susceptibility factors to promote the pathogenicity of Botrytis cinerea; Oxford University Press; Molecular Plant; 17; 7; 7-2024; 1073-1089
1674-2052
CONICET Digital
CONICET
url http://hdl.handle.net/11336/262529
identifier_str_mv Escaray, Francisco José; Felipo Benavent, Amelia; Antonelli, Cristian Javier; Balaguer, Begoña; Lopez Gresa, Maria Pilar; et al.; Plant triterpenoid saponins function as susceptibility factors to promote the pathogenicity of Botrytis cinerea; Oxford University Press; Molecular Plant; 17; 7; 7-2024; 1073-1089
1674-2052
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://linkinghub.elsevier.com/retrieve/pii/S1674205224001564
info:eu-repo/semantics/altIdentifier/doi/10.1016/j.molp.2024.05.008
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.069144

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