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

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...

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Main Authors: 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
Format: info:ar-repo/semantics/artículo
Language:Inglés
Published: 2018
Subjects:
Online Access: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
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author 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_browse Abdou‐Pavy, Iltaf
Barker, David G.
Brichet, Lukas
Brottier, Laurent
Chabaud, Mireille
Fournier, Joëlle
Genre, Andrea
Gherbi, Hassen
Hocher, Valérie
Imanishi, Leandro Ezequiel
Lascano, Hernan Ramiro
Muñoz, Nacira Belen
Pirolles, Elodie
Svistoonoff, Sergio
Vayssières, Alice
Wall, Luis Gabriel
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_sort Fournier, Joëlle
collection INTA Digital
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.
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spelling INTA36932024-08-23T12:10:44Z Cell remodeling and subtilase gene expression in the actinorhizal plant Discaria trinervis highlight host orchestration of intercellular Frankia colonization 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 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 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 2018-10-24T14:10:15Z 2018-10-24T14:10:15Z 2018-08 info:ar-repo/semantics/artículo info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion 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 eng info:eu-repo/semantics/restrictedAccess application/pdf New Phytologist 219 (3) : 1018-1030 (August 2018)
spellingShingle 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
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
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
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_short 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
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
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
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