Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorhizal plant species

Autores
Chabaud, Mireille; Fournier, Joëlle; Brichet, Lukas; Abdou Pavy, Iltaf; Imanishi, Leandro Ezequiel; Brottier, Laurent; Pirolles, Elodie; Hocher, Valérie; Franche, Claudine; Bogusz, Didier; Wall, Luis Gabriel; Svistoonoff, Sergio; Gherbi, Hassen; Barker, David G.
Año de publicación
2019
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Mutualistic plant-microbe associations are widespread in natural ecosystems and have made major contributions throughout the evolutionary history of terrestrial plants. Amongst the most remarkable of these are the so-called root endosymbioses, resulting from the intracellular colonization of host tissues by either arbuscular mycorrhizal (AM) fungi or nitrogen-fixing bacteria that both provide key nutrients to the host in exchange for energy-rich photosynthates. Actinorhizal host plants, members of the Eurosid 1 clade, are able to associate with both AM fungi and nitrogen-fixing actinomycetes known as Frankia. Currently, little is known about the molecular signaling that allows these plants to recognize their fungal and bacterial partners. In this article, we describe the use of an in vivo Ca2+ reporter to identify symbiotic signaling responses to AM fungi in roots of both Casuarina glauca and Discaria trinervis, actinorhizal species with contrasting modes of Frankia colonization. This approach has revealed that, for both actinorhizal hosts, the short-chain chitin oligomer chitotetraose is able to mimic AM fungal exudates in activating the conserved symbiosis signaling pathway (CSSP) in epidermal root cells targeted by AM fungi. These results mirror findings in other AM host plants including legumes and the monocot rice. In addition, we show that chitotetraose is a more efficient elicitor of CSSP activation compared to AM fungal lipo-chitooligosaccharides. These findings reinforce the likely role of short-chain chitin oligomers during the initial stages of the AM association, and are discussed in relation to both our current knowledge about molecular signaling during Frankia recognition as well as the different microsymbiont root colonization mechanisms employed by actinorhizal hosts.
Fil: Chabaud, Mireille. University of Toulouse; Francia. Centre National de la Recherche Scientifique; Francia
Fil: Fournier, Joëlle. University of Toulouse; Francia. Centre National de la Recherche Scientifique; Francia
Fil: Brichet, Lukas. University of Toulouse; Francia. Centre National de la Recherche Scientifique; Francia
Fil: Abdou Pavy, Iltaf. University of Toulouse; Francia. Centre National de la Recherche Scientifique; Francia
Fil: Imanishi, Leandro Ezequiel. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Brottier, Laurent. University of Montpellier; Francia. University of Montpellier SupAgro; Francia
Fil: Pirolles, Elodie. University of Montpellier SupAgro; Francia
Fil: Hocher, Valérie. University of Montpellier SupAgro; Francia
Fil: Franche, Claudine. University of Montpellier; Francia
Fil: Bogusz, Didier. University of Montpellier; Francia
Fil: Wall, Luis Gabriel. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Svistoonoff, Sergio. University of Montpellier SupAgro; Francia
Fil: Gherbi, Hassen. University of Montpellier SupAgro; Francia
Fil: Barker, David G.. University of Toulouse; Francia. Centre National de la Recherche Scientifique; Francia
Materia
SYMBIOSIS
MICORRHIZA
FRANKIA
ACTINORHIZA
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:11336/159502
Acceder
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network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorhizal plant speciesChabaud, MireilleFournier, JoëlleBrichet, LukasAbdou Pavy, IltafImanishi, Leandro EzequielBrottier, LaurentPirolles, ElodieHocher, ValérieFranche, ClaudineBogusz, DidierWall, Luis GabrielSvistoonoff, SergioGherbi, HassenBarker, David G.SYMBIOSISMICORRHIZAFRANKIAACTINORHIZAhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Mutualistic plant-microbe associations are widespread in natural ecosystems and have made major contributions throughout the evolutionary history of terrestrial plants. Amongst the most remarkable of these are the so-called root endosymbioses, resulting from the intracellular colonization of host tissues by either arbuscular mycorrhizal (AM) fungi or nitrogen-fixing bacteria that both provide key nutrients to the host in exchange for energy-rich photosynthates. Actinorhizal host plants, members of the Eurosid 1 clade, are able to associate with both AM fungi and nitrogen-fixing actinomycetes known as Frankia. Currently, little is known about the molecular signaling that allows these plants to recognize their fungal and bacterial partners. In this article, we describe the use of an in vivo Ca2+ reporter to identify symbiotic signaling responses to AM fungi in roots of both Casuarina glauca and Discaria trinervis, actinorhizal species with contrasting modes of Frankia colonization. This approach has revealed that, for both actinorhizal hosts, the short-chain chitin oligomer chitotetraose is able to mimic AM fungal exudates in activating the conserved symbiosis signaling pathway (CSSP) in epidermal root cells targeted by AM fungi. These results mirror findings in other AM host plants including legumes and the monocot rice. In addition, we show that chitotetraose is a more efficient elicitor of CSSP activation compared to AM fungal lipo-chitooligosaccharides. These findings reinforce the likely role of short-chain chitin oligomers during the initial stages of the AM association, and are discussed in relation to both our current knowledge about molecular signaling during Frankia recognition as well as the different microsymbiont root colonization mechanisms employed by actinorhizal hosts.Fil: Chabaud, Mireille. University of Toulouse; Francia. Centre National de la Recherche Scientifique; FranciaFil: Fournier, Joëlle. University of Toulouse; Francia. Centre National de la Recherche Scientifique; FranciaFil: Brichet, Lukas. University of Toulouse; Francia. Centre National de la Recherche Scientifique; FranciaFil: Abdou Pavy, Iltaf. University of Toulouse; Francia. Centre National de la Recherche Scientifique; FranciaFil: Imanishi, Leandro Ezequiel. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Brottier, Laurent. University of Montpellier; Francia. University of Montpellier SupAgro; FranciaFil: Pirolles, Elodie. University of Montpellier SupAgro; FranciaFil: Hocher, Valérie. University of Montpellier SupAgro; FranciaFil: Franche, Claudine. University of Montpellier; FranciaFil: Bogusz, Didier. University of Montpellier; FranciaFil: Wall, Luis Gabriel. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Svistoonoff, Sergio. University of Montpellier SupAgro; FranciaFil: Gherbi, Hassen. University of Montpellier SupAgro; FranciaFil: Barker, David G.. University of Toulouse; Francia. Centre National de la Recherche Scientifique; FranciaPublic Library of Science2019-10info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/159502Chabaud, Mireille; Fournier, Joëlle; Brichet, Lukas; Abdou Pavy, Iltaf; Imanishi, Leandro Ezequiel; et al.; Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorhizal plant species; Public Library of Science; Plos One; 14; 10; 10-2019; 1-13; e02231491932-6203CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0223149info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0223149info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-22T11:29:08Zoai:ri.conicet.gov.ar:11336/159502instacron: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:34982025-10-22 11:29:08.984CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorhizal plant species
title Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorhizal plant species
spellingShingle Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorhizal plant species
Chabaud, Mireille
SYMBIOSIS
MICORRHIZA
FRANKIA
ACTINORHIZA
title_short Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorhizal plant species
title_full Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorhizal plant species
title_fullStr Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorhizal plant species
title_full_unstemmed Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorhizal plant species
title_sort Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorhizal plant species
dc.creator.none.fl_str_mv Chabaud, Mireille
Fournier, Joëlle
Brichet, Lukas
Abdou Pavy, Iltaf
Imanishi, Leandro Ezequiel
Brottier, Laurent
Pirolles, Elodie
Hocher, Valérie
Franche, Claudine
Bogusz, Didier
Wall, Luis Gabriel
Svistoonoff, Sergio
Gherbi, Hassen
Barker, David G.
author Chabaud, Mireille
author_facet Chabaud, Mireille
Fournier, Joëlle
Brichet, Lukas
Abdou Pavy, Iltaf
Imanishi, Leandro Ezequiel
Brottier, Laurent
Pirolles, Elodie
Hocher, Valérie
Franche, Claudine
Bogusz, Didier
Wall, Luis Gabriel
Svistoonoff, Sergio
Gherbi, Hassen
Barker, David G.
author_role author
author2 Fournier, Joëlle
Brichet, Lukas
Abdou Pavy, Iltaf
Imanishi, Leandro Ezequiel
Brottier, Laurent
Pirolles, Elodie
Hocher, Valérie
Franche, Claudine
Bogusz, Didier
Wall, Luis Gabriel
Svistoonoff, Sergio
Gherbi, Hassen
Barker, David G.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv SYMBIOSIS
MICORRHIZA
FRANKIA
ACTINORHIZA
topic SYMBIOSIS
MICORRHIZA
FRANKIA
ACTINORHIZA
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Mutualistic plant-microbe associations are widespread in natural ecosystems and have made major contributions throughout the evolutionary history of terrestrial plants. Amongst the most remarkable of these are the so-called root endosymbioses, resulting from the intracellular colonization of host tissues by either arbuscular mycorrhizal (AM) fungi or nitrogen-fixing bacteria that both provide key nutrients to the host in exchange for energy-rich photosynthates. Actinorhizal host plants, members of the Eurosid 1 clade, are able to associate with both AM fungi and nitrogen-fixing actinomycetes known as Frankia. Currently, little is known about the molecular signaling that allows these plants to recognize their fungal and bacterial partners. In this article, we describe the use of an in vivo Ca2+ reporter to identify symbiotic signaling responses to AM fungi in roots of both Casuarina glauca and Discaria trinervis, actinorhizal species with contrasting modes of Frankia colonization. This approach has revealed that, for both actinorhizal hosts, the short-chain chitin oligomer chitotetraose is able to mimic AM fungal exudates in activating the conserved symbiosis signaling pathway (CSSP) in epidermal root cells targeted by AM fungi. These results mirror findings in other AM host plants including legumes and the monocot rice. In addition, we show that chitotetraose is a more efficient elicitor of CSSP activation compared to AM fungal lipo-chitooligosaccharides. These findings reinforce the likely role of short-chain chitin oligomers during the initial stages of the AM association, and are discussed in relation to both our current knowledge about molecular signaling during Frankia recognition as well as the different microsymbiont root colonization mechanisms employed by actinorhizal hosts.
Fil: Chabaud, Mireille. University of Toulouse; Francia. Centre National de la Recherche Scientifique; Francia
Fil: Fournier, Joëlle. University of Toulouse; Francia. Centre National de la Recherche Scientifique; Francia
Fil: Brichet, Lukas. University of Toulouse; Francia. Centre National de la Recherche Scientifique; Francia
Fil: Abdou Pavy, Iltaf. University of Toulouse; Francia. Centre National de la Recherche Scientifique; Francia
Fil: Imanishi, Leandro Ezequiel. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Brottier, Laurent. University of Montpellier; Francia. University of Montpellier SupAgro; Francia
Fil: Pirolles, Elodie. University of Montpellier SupAgro; Francia
Fil: Hocher, Valérie. University of Montpellier SupAgro; Francia
Fil: Franche, Claudine. University of Montpellier; Francia
Fil: Bogusz, Didier. University of Montpellier; Francia
Fil: Wall, Luis Gabriel. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Svistoonoff, Sergio. University of Montpellier SupAgro; Francia
Fil: Gherbi, Hassen. University of Montpellier SupAgro; Francia
Fil: Barker, David G.. University of Toulouse; Francia. Centre National de la Recherche Scientifique; Francia
description Mutualistic plant-microbe associations are widespread in natural ecosystems and have made major contributions throughout the evolutionary history of terrestrial plants. Amongst the most remarkable of these are the so-called root endosymbioses, resulting from the intracellular colonization of host tissues by either arbuscular mycorrhizal (AM) fungi or nitrogen-fixing bacteria that both provide key nutrients to the host in exchange for energy-rich photosynthates. Actinorhizal host plants, members of the Eurosid 1 clade, are able to associate with both AM fungi and nitrogen-fixing actinomycetes known as Frankia. Currently, little is known about the molecular signaling that allows these plants to recognize their fungal and bacterial partners. In this article, we describe the use of an in vivo Ca2+ reporter to identify symbiotic signaling responses to AM fungi in roots of both Casuarina glauca and Discaria trinervis, actinorhizal species with contrasting modes of Frankia colonization. This approach has revealed that, for both actinorhizal hosts, the short-chain chitin oligomer chitotetraose is able to mimic AM fungal exudates in activating the conserved symbiosis signaling pathway (CSSP) in epidermal root cells targeted by AM fungi. These results mirror findings in other AM host plants including legumes and the monocot rice. In addition, we show that chitotetraose is a more efficient elicitor of CSSP activation compared to AM fungal lipo-chitooligosaccharides. These findings reinforce the likely role of short-chain chitin oligomers during the initial stages of the AM association, and are discussed in relation to both our current knowledge about molecular signaling during Frankia recognition as well as the different microsymbiont root colonization mechanisms employed by actinorhizal hosts.
publishDate 2019
dc.date.none.fl_str_mv 2019-10
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/11336/159502
Chabaud, Mireille; Fournier, Joëlle; Brichet, Lukas; Abdou Pavy, Iltaf; Imanishi, Leandro Ezequiel; et al.; Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorhizal plant species; Public Library of Science; Plos One; 14; 10; 10-2019; 1-13; e0223149
1932-6203
CONICET Digital
CONICET
url http://hdl.handle.net/11336/159502
identifier_str_mv Chabaud, Mireille; Fournier, Joëlle; Brichet, Lukas; Abdou Pavy, Iltaf; Imanishi, Leandro Ezequiel; et al.; Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorhizal plant species; Public Library of Science; Plos One; 14; 10; 10-2019; 1-13; e0223149
1932-6203
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://journals.plos.org/plosone/article?id=10.1371/journal.pone.0223149
info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0223149
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 Public Library of Science
publisher.none.fl_str_mv Public Library of Science
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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