Cell remodeling and subtilase gene expression in the actinorhizal plant Discaria trinervis highlight host orchestration of intercellular Frankia colonization

Autores
Fournier, Joëlle; Imanishi, Leandro Ezequiel; Chabaud, Mireille; Abdou‐Pavy, Iltaf; Genre, Andrea; Brichet, Lukas; Lascano, Hernan Ramiro; Muñoz, Nacira Belen; Vayssières, Alice; Pirolles, Elodie; Brottier, Laurent; Gherbi, Hassen; Hocher, Valérie; Svistoonoff, Sergio; Barker, David G.; Wall, Luis Gabriel
Año de publicación
2018
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Nitrogen‐fixing filamentous Frankia colonize the root tissues of its actinorhizal host Discaria trinervis via an exclusively intercellular pathway. Here we present studies aimed at uncovering mechanisms associated with this little‐researched mode of root entry, and in particular the extent to which the host plant is an active partner during this process. Detailed characterization of the expression patterns of infection‐associated actinorhizal host genes has provided valuable tools to identify intercellular infection sites, thus allowing in vivo confocal microscopic studies of the early stages of Frankia colonization. The subtilisin‐like serine protease gene Dt12, as well as its Casuarina glauca homolog Cg12, are specifically expressed at sites of Frankia intercellular colonization of D. trinervis outer root tissues. This is accompanied by nucleo‐cytoplasmic reorganization in the adjacent host cells and major remodeling of the intercellular apoplastic compartment. These findings lead us to propose that the actinorhizal host plays a major role in modifying both the size and composition of the intercellular apoplast in order to accommodate the filamentous microsymbiont. The implications of these findings are discussed in the light of the analogies that can be made with the orchestrating role of host legumes during intracellular root hair colonization by nitrogen‐fixing rhizobia.
Instituto de Fisiología y Recursos Genéticos Vegetales
Fil: Fournier, Joëlle. Université de Toulouse. LIPM; Francia. INRA-CNRS; Francia
Fil: Imanishi, Leandro Ezequiel. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología. Laboratorio de Bioquímica, Microbiología e Interacciones Biológicas en el Suelo; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Chabaud, Mireille. Université de Toulouse. LIPM; Francia. INRA-CNRS; Francia
Fil: Abdou‐Pavy, Iltaf. Université de Toulouse. LIPM; Francia. INRA-CNRS; Francia
Fil: Genre, Andrea. University of Torino. Department of Life Sciences and Systems Biology; Italia
Fil: Brichet, Lukas. Université de Toulouse. LIPM; Francia. INRA-CNRS; Francia
Fil: Lascano, Hernan Ramiro. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Fisiología y Recursos Genéticos Vegetales; Argentina
Fil: Muñoz, Nacira Belen. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Fisiología y Recursos Genéticos Vegetales; Argentina
Fil: Vayssières, Alice. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; Francia
Fil: Pirolles, Elodie. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; Francia
Fil: Brottier, Laurent. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; Francia
Fil: Gherbi, Hassen. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; Francia
Fil: Hocher, Valérie. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; Francia
Fil: Svistoonoff, Sergio. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; Francia. Centre de Recherche de Bel Air. Laboratoire Mixte International Adaptation des Plantes et Microorganismes Associés aux Stress Environnementaux; Senegal. Institut de Recherche pour le Développement-Institut Sénégalais des Recherches Agricoles-Université Cheikh Anta Diop. Laboratoire Commun de Microbiologie; Senegal
Fil: Barker, David G. Université de Toulouse. LIPM; Francia. INRA-CNRS; Francia
Fil: Wall, Luis Gabriel. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología. Laboratorio de Bioquímica, Microbiología e Interacciones Biológicas en el Suelo; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fuente
New Phytologist 219 (3) : 1018-1030 (August 2018)
Materia
Frankia
Bacteria
Bacteria Fijadora del Nitrógeno
Expresión Génica
Huéspedes
Fijación Biológica del Nitrógeno
Suelo
Nitrogen Fixing Bacteria
Gene Expression
Hosts
Biological Nitrogen Fixation
Soil
Discaria trinervis
Nivel de accesibilidad
acceso restringido
Condiciones de uso
Repositorio
INTA Digital (INTA)
Institución
Instituto Nacional de Tecnología Agropecuaria
OAI Identificador
oai:localhost:20.500.12123/3693
Acceder
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oai_identifier_str oai:localhost:20.500.12123/3693
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network_name_str INTA Digital (INTA)
spelling Cell remodeling and subtilase gene expression in the actinorhizal plant Discaria trinervis highlight host orchestration of intercellular Frankia colonizationFournier, JoëlleImanishi, Leandro EzequielChabaud, MireilleAbdou‐Pavy, IltafGenre, AndreaBrichet, LukasLascano, Hernan RamiroMuñoz, Nacira BelenVayssières, AlicePirolles, ElodieBrottier, LaurentGherbi, HassenHocher, ValérieSvistoonoff, SergioBarker, David G.Wall, Luis GabrielFrankiaBacteriaBacteria Fijadora del NitrógenoExpresión GénicaHuéspedesFijación Biológica del NitrógenoSueloNitrogen Fixing BacteriaGene ExpressionHostsBiological Nitrogen FixationSoilDiscaria trinervisNitrogen‐fixing filamentous Frankia colonize the root tissues of its actinorhizal host Discaria trinervis via an exclusively intercellular pathway. Here we present studies aimed at uncovering mechanisms associated with this little‐researched mode of root entry, and in particular the extent to which the host plant is an active partner during this process. Detailed characterization of the expression patterns of infection‐associated actinorhizal host genes has provided valuable tools to identify intercellular infection sites, thus allowing in vivo confocal microscopic studies of the early stages of Frankia colonization. The subtilisin‐like serine protease gene Dt12, as well as its Casuarina glauca homolog Cg12, are specifically expressed at sites of Frankia intercellular colonization of D. trinervis outer root tissues. This is accompanied by nucleo‐cytoplasmic reorganization in the adjacent host cells and major remodeling of the intercellular apoplastic compartment. These findings lead us to propose that the actinorhizal host plays a major role in modifying both the size and composition of the intercellular apoplast in order to accommodate the filamentous microsymbiont. The implications of these findings are discussed in the light of the analogies that can be made with the orchestrating role of host legumes during intracellular root hair colonization by nitrogen‐fixing rhizobia.Instituto de Fisiología y Recursos Genéticos VegetalesFil: Fournier, Joëlle. Université de Toulouse. LIPM; Francia. INRA-CNRS; FranciaFil: Imanishi, Leandro Ezequiel. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología. Laboratorio de Bioquímica, Microbiología e Interacciones Biológicas en el Suelo; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Chabaud, Mireille. Université de Toulouse. LIPM; Francia. INRA-CNRS; FranciaFil: Abdou‐Pavy, Iltaf. Université de Toulouse. LIPM; Francia. INRA-CNRS; FranciaFil: Genre, Andrea. University of Torino. Department of Life Sciences and Systems Biology; ItaliaFil: Brichet, Lukas. Université de Toulouse. LIPM; Francia. INRA-CNRS; FranciaFil: Lascano, Hernan Ramiro. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Fisiología y Recursos Genéticos Vegetales; ArgentinaFil: Muñoz, Nacira Belen. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Fisiología y Recursos Genéticos Vegetales; ArgentinaFil: Vayssières, Alice. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; FranciaFil: Pirolles, Elodie. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; FranciaFil: Brottier, Laurent. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; FranciaFil: Gherbi, Hassen. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; FranciaFil: Hocher, Valérie. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; FranciaFil: Svistoonoff, Sergio. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; Francia. Centre de Recherche de Bel Air. Laboratoire Mixte International Adaptation des Plantes et Microorganismes Associés aux Stress Environnementaux; Senegal. Institut de Recherche pour le Développement-Institut Sénégalais des Recherches Agricoles-Université Cheikh Anta Diop. Laboratoire Commun de Microbiologie; SenegalFil: Barker, David G. Université de Toulouse. LIPM; Francia. INRA-CNRS; FranciaFil: Wall, Luis Gabriel. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología. Laboratorio de Bioquímica, Microbiología e Interacciones Biológicas en el Suelo; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina2018-10-24T14:10:15Z2018-10-24T14:10:15Z2018-08info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfhttp://hdl.handle.net/20.500.12123/3693https://nph.onlinelibrary.wiley.com/doi/full/10.1111/nph.152160028-646X1469-8137https://doi.org/10.1111/nph.15216New Phytologist 219 (3) : 1018-1030 (August 2018)reponame:INTA Digital (INTA)instname:Instituto Nacional de Tecnología Agropecuariaenginfo:eu-repo/semantics/restrictedAccess2025-10-23T11:16:42Zoai:localhost:20.500.12123/3693instacron:INTAInstitucionalhttp://repositorio.inta.gob.ar/Organismo científico-tecnológicoNo correspondehttp://repositorio.inta.gob.ar/oai/requesttripaldi.nicolas@inta.gob.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:l2025-10-23 11:16:42.699INTA Digital (INTA) - Instituto Nacional de Tecnología Agropecuariafalse
dc.title.none.fl_str_mv Cell remodeling and subtilase gene expression in the actinorhizal plant Discaria trinervis highlight host orchestration of intercellular Frankia colonization
title Cell remodeling and subtilase gene expression in the actinorhizal plant Discaria trinervis highlight host orchestration of intercellular Frankia colonization
spellingShingle Cell remodeling and subtilase gene expression in the actinorhizal plant Discaria trinervis highlight host orchestration of intercellular Frankia colonization
Fournier, Joëlle
Frankia
Bacteria
Bacteria Fijadora del Nitrógeno
Expresión Génica
Huéspedes
Fijación Biológica del Nitrógeno
Suelo
Nitrogen Fixing Bacteria
Gene Expression
Hosts
Biological Nitrogen Fixation
Soil
Discaria trinervis
title_short Cell remodeling and subtilase gene expression in the actinorhizal plant Discaria trinervis highlight host orchestration of intercellular Frankia colonization
title_full Cell remodeling and subtilase gene expression in the actinorhizal plant Discaria trinervis highlight host orchestration of intercellular Frankia colonization
title_fullStr Cell remodeling and subtilase gene expression in the actinorhizal plant Discaria trinervis highlight host orchestration of intercellular Frankia colonization
title_full_unstemmed Cell remodeling and subtilase gene expression in the actinorhizal plant Discaria trinervis highlight host orchestration of intercellular Frankia colonization
title_sort Cell remodeling and subtilase gene expression in the actinorhizal plant Discaria trinervis highlight host orchestration of intercellular Frankia colonization
dc.creator.none.fl_str_mv Fournier, Joëlle
Imanishi, Leandro Ezequiel
Chabaud, Mireille
Abdou‐Pavy, Iltaf
Genre, Andrea
Brichet, Lukas
Lascano, Hernan Ramiro
Muñoz, Nacira Belen
Vayssières, Alice
Pirolles, Elodie
Brottier, Laurent
Gherbi, Hassen
Hocher, Valérie
Svistoonoff, Sergio
Barker, David G.
Wall, Luis Gabriel
author Fournier, Joëlle
author_facet Fournier, Joëlle
Imanishi, Leandro Ezequiel
Chabaud, Mireille
Abdou‐Pavy, Iltaf
Genre, Andrea
Brichet, Lukas
Lascano, Hernan Ramiro
Muñoz, Nacira Belen
Vayssières, Alice
Pirolles, Elodie
Brottier, Laurent
Gherbi, Hassen
Hocher, Valérie
Svistoonoff, Sergio
Barker, David G.
Wall, Luis Gabriel
author_role author
author2 Imanishi, Leandro Ezequiel
Chabaud, Mireille
Abdou‐Pavy, Iltaf
Genre, Andrea
Brichet, Lukas
Lascano, Hernan Ramiro
Muñoz, Nacira Belen
Vayssières, Alice
Pirolles, Elodie
Brottier, Laurent
Gherbi, Hassen
Hocher, Valérie
Svistoonoff, Sergio
Barker, David G.
Wall, Luis Gabriel
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Frankia
Bacteria
Bacteria Fijadora del Nitrógeno
Expresión Génica
Huéspedes
Fijación Biológica del Nitrógeno
Suelo
Nitrogen Fixing Bacteria
Gene Expression
Hosts
Biological Nitrogen Fixation
Soil
Discaria trinervis
topic Frankia
Bacteria
Bacteria Fijadora del Nitrógeno
Expresión Génica
Huéspedes
Fijación Biológica del Nitrógeno
Suelo
Nitrogen Fixing Bacteria
Gene Expression
Hosts
Biological Nitrogen Fixation
Soil
Discaria trinervis
dc.description.none.fl_txt_mv Nitrogen‐fixing filamentous Frankia colonize the root tissues of its actinorhizal host Discaria trinervis via an exclusively intercellular pathway. Here we present studies aimed at uncovering mechanisms associated with this little‐researched mode of root entry, and in particular the extent to which the host plant is an active partner during this process. Detailed characterization of the expression patterns of infection‐associated actinorhizal host genes has provided valuable tools to identify intercellular infection sites, thus allowing in vivo confocal microscopic studies of the early stages of Frankia colonization. The subtilisin‐like serine protease gene Dt12, as well as its Casuarina glauca homolog Cg12, are specifically expressed at sites of Frankia intercellular colonization of D. trinervis outer root tissues. This is accompanied by nucleo‐cytoplasmic reorganization in the adjacent host cells and major remodeling of the intercellular apoplastic compartment. These findings lead us to propose that the actinorhizal host plays a major role in modifying both the size and composition of the intercellular apoplast in order to accommodate the filamentous microsymbiont. The implications of these findings are discussed in the light of the analogies that can be made with the orchestrating role of host legumes during intracellular root hair colonization by nitrogen‐fixing rhizobia.
Instituto de Fisiología y Recursos Genéticos Vegetales
Fil: Fournier, Joëlle. Université de Toulouse. LIPM; Francia. INRA-CNRS; Francia
Fil: Imanishi, Leandro Ezequiel. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología. Laboratorio de Bioquímica, Microbiología e Interacciones Biológicas en el Suelo; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Chabaud, Mireille. Université de Toulouse. LIPM; Francia. INRA-CNRS; Francia
Fil: Abdou‐Pavy, Iltaf. Université de Toulouse. LIPM; Francia. INRA-CNRS; Francia
Fil: Genre, Andrea. University of Torino. Department of Life Sciences and Systems Biology; Italia
Fil: Brichet, Lukas. Université de Toulouse. LIPM; Francia. INRA-CNRS; Francia
Fil: Lascano, Hernan Ramiro. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Fisiología y Recursos Genéticos Vegetales; Argentina
Fil: Muñoz, Nacira Belen. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Fisiología y Recursos Genéticos Vegetales; Argentina
Fil: Vayssières, Alice. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; Francia
Fil: Pirolles, Elodie. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; Francia
Fil: Brottier, Laurent. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; Francia
Fil: Gherbi, Hassen. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; Francia
Fil: Hocher, Valérie. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; Francia
Fil: Svistoonoff, Sergio. IRD-INRA-CIRAD-Université de Montpellier-Supagro. Laboratoire des Symbioses Tropicales et Méditerranéennes; Francia. Centre de Recherche de Bel Air. Laboratoire Mixte International Adaptation des Plantes et Microorganismes Associés aux Stress Environnementaux; Senegal. Institut de Recherche pour le Développement-Institut Sénégalais des Recherches Agricoles-Université Cheikh Anta Diop. Laboratoire Commun de Microbiologie; Senegal
Fil: Barker, David G. Université de Toulouse. LIPM; Francia. INRA-CNRS; Francia
Fil: Wall, Luis Gabriel. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología. Laboratorio de Bioquímica, Microbiología e Interacciones Biológicas en el Suelo; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
description Nitrogen‐fixing filamentous Frankia colonize the root tissues of its actinorhizal host Discaria trinervis via an exclusively intercellular pathway. Here we present studies aimed at uncovering mechanisms associated with this little‐researched mode of root entry, and in particular the extent to which the host plant is an active partner during this process. Detailed characterization of the expression patterns of infection‐associated actinorhizal host genes has provided valuable tools to identify intercellular infection sites, thus allowing in vivo confocal microscopic studies of the early stages of Frankia colonization. The subtilisin‐like serine protease gene Dt12, as well as its Casuarina glauca homolog Cg12, are specifically expressed at sites of Frankia intercellular colonization of D. trinervis outer root tissues. This is accompanied by nucleo‐cytoplasmic reorganization in the adjacent host cells and major remodeling of the intercellular apoplastic compartment. These findings lead us to propose that the actinorhizal host plays a major role in modifying both the size and composition of the intercellular apoplast in order to accommodate the filamentous microsymbiont. The implications of these findings are discussed in the light of the analogies that can be made with the orchestrating role of host legumes during intracellular root hair colonization by nitrogen‐fixing rhizobia.
publishDate 2018
dc.date.none.fl_str_mv 2018-10-24T14:10:15Z
2018-10-24T14:10:15Z
2018-08
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
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info:ar-repo/semantics/articulo
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status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/20.500.12123/3693
https://nph.onlinelibrary.wiley.com/doi/full/10.1111/nph.15216
0028-646X
1469-8137
https://doi.org/10.1111/nph.15216
url http://hdl.handle.net/20.500.12123/3693
https://nph.onlinelibrary.wiley.com/doi/full/10.1111/nph.15216
https://doi.org/10.1111/nph.15216
identifier_str_mv 0028-646X
1469-8137
dc.language.none.fl_str_mv eng
language eng
dc.rights.none.fl_str_mv info:eu-repo/semantics/restrictedAccess
eu_rights_str_mv restrictedAccess
dc.format.none.fl_str_mv application/pdf
dc.source.none.fl_str_mv New Phytologist 219 (3) : 1018-1030 (August 2018)
reponame:INTA Digital (INTA)
instname:Instituto Nacional de Tecnología Agropecuaria
reponame_str INTA Digital (INTA)
collection INTA Digital (INTA)
instname_str Instituto Nacional de Tecnología Agropecuaria
repository.name.fl_str_mv INTA Digital (INTA) - Instituto Nacional de Tecnología Agropecuaria
repository.mail.fl_str_mv tripaldi.nicolas@inta.gob.ar
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