The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis

Autores
Svistoonoff, Sergio; Benabdoun, Faiza Meriem; Nambiar Veetil, Mathish; Imanishi, Leandro Ezequiel; Vaissayre, Virginie; Cesari, Stella; Diagne, Nathalie; Hocher, Valérie; de Billy, Françoise; Wall, Luis Gabriel; Ykhlef, Nadia; Rossemberg, Charles; Bogusz, Didier; Franche, Claudine; Gherbi, Hassen
Año de publicación
2013
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Only species belonging to the Fabid clade, limited to four classes and ten families of Angiosperms, are able to form nitrogen-fixing root nodule symbioses (RNS) with soil bacteria. This concerns plants of the legume family (Fabaceae) and Parasponia (Cannabaceae) associated with the Gram-negative proteobacteria collectively called rhizobia and actinorhizal plants associated with the Gram-positive actinomycetes of the genus Frankia. Calcium and calmodulin-dependent protein kinase (CCaMK) is a key component of the common signaling pathway leading to both rhizobial and arbuscular mycorrhizal symbioses (AM) and plays a central role in cross-signaling between root nodule organogenesis and infection processes. Here, we show that CCaMK is also needed for successful actinorhiza formation and interaction with AM fungi in the actinorhizal tree Casuarina glauca and is also able to restore both nodulation and AM symbioses in a Medicago truncately ccamk mutant. Besides, we expressed auto-active CgCCaMK lacking the auto-inhibitory/CaM domain in two actinorhizal species: C. glauca (Casuarinaceae), which develops an intracellular infection pathway, and Discaria trinervis (Rhamnaceae) which is characterized by an ancestral intercellular infection mechanism. In both species, we found induction of nodulation independent of Frankia similar to response to the activation of CCaMK in the rhizobia-legume symbiosis and conclude that the regulation of actinorhiza organogenesis is conserved regardless of the infection mode. It has been suggested that rhizobial and actinorhizal symbioses originated from a common ancestor with several independent evolutionary origins. Our findings are consistent with the recruitment of a similar genetic pathway governing rhizobial and Frankia nodule organogenesis.
Fil: Svistoonoff, Sergio. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia
Fil: Benabdoun, Faiza Meriem. Mentouri University. Departement of Biology and Ecology; Argelia. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia
Fil: Nambiar Veetil, Mathish. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia
Fil: Imanishi, Leandro Ezequiel. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Vaissayre, Virginie. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia
Fil: Cesari, Stella. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia. Institut National de la Recherche Agronomique; Francia
Fil: Diagne, Nathalie. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia. Institut National de la Recherche Agronomique; Francia
Fil: Hocher, Valérie. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia
Fil: de Billy, Françoise. Centre National de la Recherche Scientifique; Francia. Institut National de la Recherche Agronomique; Francia
Fil: Wall, Luis Gabriel. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Ykhlef, Nadia. Mentouri University. Departement of Biology and Ecology; Argelia
Fil: Rossemberg, Charles. Centre National de la Recherche Scientifique; Francia. Institut National de la Recherche Agronomique; Francia
Fil: Bogusz, Didier. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia
Fil: Franche, Claudine. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia
Fil: Gherbi, Hassen. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia
Materia
Frankia
Actinorrizas
Symbiosis
Discaria
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:11336/23861
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/23861
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesisSvistoonoff, SergioBenabdoun, Faiza MeriemNambiar Veetil, MathishImanishi, Leandro EzequielVaissayre, VirginieCesari, StellaDiagne, NathalieHocher, Valériede Billy, FrançoiseWall, Luis GabrielYkhlef, NadiaRossemberg, CharlesBogusz, DidierFranche, ClaudineGherbi, HassenFrankiaActinorrizasSymbiosisDiscariahttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Only species belonging to the Fabid clade, limited to four classes and ten families of Angiosperms, are able to form nitrogen-fixing root nodule symbioses (RNS) with soil bacteria. This concerns plants of the legume family (Fabaceae) and Parasponia (Cannabaceae) associated with the Gram-negative proteobacteria collectively called rhizobia and actinorhizal plants associated with the Gram-positive actinomycetes of the genus Frankia. Calcium and calmodulin-dependent protein kinase (CCaMK) is a key component of the common signaling pathway leading to both rhizobial and arbuscular mycorrhizal symbioses (AM) and plays a central role in cross-signaling between root nodule organogenesis and infection processes. Here, we show that CCaMK is also needed for successful actinorhiza formation and interaction with AM fungi in the actinorhizal tree Casuarina glauca and is also able to restore both nodulation and AM symbioses in a Medicago truncately ccamk mutant. Besides, we expressed auto-active CgCCaMK lacking the auto-inhibitory/CaM domain in two actinorhizal species: C. glauca (Casuarinaceae), which develops an intracellular infection pathway, and Discaria trinervis (Rhamnaceae) which is characterized by an ancestral intercellular infection mechanism. In both species, we found induction of nodulation independent of Frankia similar to response to the activation of CCaMK in the rhizobia-legume symbiosis and conclude that the regulation of actinorhiza organogenesis is conserved regardless of the infection mode. It has been suggested that rhizobial and actinorhizal symbioses originated from a common ancestor with several independent evolutionary origins. Our findings are consistent with the recruitment of a similar genetic pathway governing rhizobial and Frankia nodule organogenesis.Fil: Svistoonoff, Sergio. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; FranciaFil: Benabdoun, Faiza Meriem. Mentouri University. Departement of Biology and Ecology; Argelia. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; FranciaFil: Nambiar Veetil, Mathish. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; FranciaFil: Imanishi, Leandro Ezequiel. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Vaissayre, Virginie. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; FranciaFil: Cesari, Stella. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia. Institut National de la Recherche Agronomique; FranciaFil: Diagne, Nathalie. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia. Institut National de la Recherche Agronomique; FranciaFil: Hocher, Valérie. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; FranciaFil: de Billy, Françoise. Centre National de la Recherche Scientifique; Francia. Institut National de la Recherche Agronomique; FranciaFil: Wall, Luis Gabriel. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Ykhlef, Nadia. Mentouri University. Departement of Biology and Ecology; ArgeliaFil: Rossemberg, Charles. Centre National de la Recherche Scientifique; Francia. Institut National de la Recherche Agronomique; FranciaFil: Bogusz, Didier. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; FranciaFil: Franche, Claudine. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; FranciaFil: Gherbi, Hassen. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; FranciaPublic Library of Science2013-05info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/23861Svistoonoff, Sergio; Benabdoun, Faiza Meriem; Nambiar Veetil, Mathish; Imanishi, Leandro Ezequiel; Vaissayre, Virginie; et al.; The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis; Public Library of Science; Plos One; 8; 5; 5-2013; 1-10; e645151932-6203CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0064515info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0064515info:eu-repo/semantics/altIdentifier/url/https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3669324/info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:14:27Zoai:ri.conicet.gov.ar:11336/23861instacron: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 10:14:28.112CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis
title The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis
spellingShingle The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis
Svistoonoff, Sergio
Frankia
Actinorrizas
Symbiosis
Discaria
title_short The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis
title_full The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis
title_fullStr The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis
title_full_unstemmed The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis
title_sort The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis
dc.creator.none.fl_str_mv Svistoonoff, Sergio
Benabdoun, Faiza Meriem
Nambiar Veetil, Mathish
Imanishi, Leandro Ezequiel
Vaissayre, Virginie
Cesari, Stella
Diagne, Nathalie
Hocher, Valérie
de Billy, Françoise
Wall, Luis Gabriel
Ykhlef, Nadia
Rossemberg, Charles
Bogusz, Didier
Franche, Claudine
Gherbi, Hassen
author Svistoonoff, Sergio
author_facet Svistoonoff, Sergio
Benabdoun, Faiza Meriem
Nambiar Veetil, Mathish
Imanishi, Leandro Ezequiel
Vaissayre, Virginie
Cesari, Stella
Diagne, Nathalie
Hocher, Valérie
de Billy, Françoise
Wall, Luis Gabriel
Ykhlef, Nadia
Rossemberg, Charles
Bogusz, Didier
Franche, Claudine
Gherbi, Hassen
author_role author
author2 Benabdoun, Faiza Meriem
Nambiar Veetil, Mathish
Imanishi, Leandro Ezequiel
Vaissayre, Virginie
Cesari, Stella
Diagne, Nathalie
Hocher, Valérie
de Billy, Françoise
Wall, Luis Gabriel
Ykhlef, Nadia
Rossemberg, Charles
Bogusz, Didier
Franche, Claudine
Gherbi, Hassen
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Frankia
Actinorrizas
Symbiosis
Discaria
topic Frankia
Actinorrizas
Symbiosis
Discaria
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Only species belonging to the Fabid clade, limited to four classes and ten families of Angiosperms, are able to form nitrogen-fixing root nodule symbioses (RNS) with soil bacteria. This concerns plants of the legume family (Fabaceae) and Parasponia (Cannabaceae) associated with the Gram-negative proteobacteria collectively called rhizobia and actinorhizal plants associated with the Gram-positive actinomycetes of the genus Frankia. Calcium and calmodulin-dependent protein kinase (CCaMK) is a key component of the common signaling pathway leading to both rhizobial and arbuscular mycorrhizal symbioses (AM) and plays a central role in cross-signaling between root nodule organogenesis and infection processes. Here, we show that CCaMK is also needed for successful actinorhiza formation and interaction with AM fungi in the actinorhizal tree Casuarina glauca and is also able to restore both nodulation and AM symbioses in a Medicago truncately ccamk mutant. Besides, we expressed auto-active CgCCaMK lacking the auto-inhibitory/CaM domain in two actinorhizal species: C. glauca (Casuarinaceae), which develops an intracellular infection pathway, and Discaria trinervis (Rhamnaceae) which is characterized by an ancestral intercellular infection mechanism. In both species, we found induction of nodulation independent of Frankia similar to response to the activation of CCaMK in the rhizobia-legume symbiosis and conclude that the regulation of actinorhiza organogenesis is conserved regardless of the infection mode. It has been suggested that rhizobial and actinorhizal symbioses originated from a common ancestor with several independent evolutionary origins. Our findings are consistent with the recruitment of a similar genetic pathway governing rhizobial and Frankia nodule organogenesis.
Fil: Svistoonoff, Sergio. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia
Fil: Benabdoun, Faiza Meriem. Mentouri University. Departement of Biology and Ecology; Argelia. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia
Fil: Nambiar Veetil, Mathish. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia
Fil: Imanishi, Leandro Ezequiel. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Vaissayre, Virginie. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia
Fil: Cesari, Stella. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia. Institut National de la Recherche Agronomique; Francia
Fil: Diagne, Nathalie. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia. Institut National de la Recherche Agronomique; Francia
Fil: Hocher, Valérie. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia
Fil: de Billy, Françoise. Centre National de la Recherche Scientifique; Francia. Institut National de la Recherche Agronomique; Francia
Fil: Wall, Luis Gabriel. Universidad Nacional de Quilmes. Departamento de Ciencia y Tecnología; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Ykhlef, Nadia. Mentouri University. Departement of Biology and Ecology; Argelia
Fil: Rossemberg, Charles. Centre National de la Recherche Scientifique; Francia. Institut National de la Recherche Agronomique; Francia
Fil: Bogusz, Didier. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia
Fil: Franche, Claudine. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia
Fil: Gherbi, Hassen. Centre National de la Recherche Scientifique. Institut de Recherche pour le Développement; Francia
description Only species belonging to the Fabid clade, limited to four classes and ten families of Angiosperms, are able to form nitrogen-fixing root nodule symbioses (RNS) with soil bacteria. This concerns plants of the legume family (Fabaceae) and Parasponia (Cannabaceae) associated with the Gram-negative proteobacteria collectively called rhizobia and actinorhizal plants associated with the Gram-positive actinomycetes of the genus Frankia. Calcium and calmodulin-dependent protein kinase (CCaMK) is a key component of the common signaling pathway leading to both rhizobial and arbuscular mycorrhizal symbioses (AM) and plays a central role in cross-signaling between root nodule organogenesis and infection processes. Here, we show that CCaMK is also needed for successful actinorhiza formation and interaction with AM fungi in the actinorhizal tree Casuarina glauca and is also able to restore both nodulation and AM symbioses in a Medicago truncately ccamk mutant. Besides, we expressed auto-active CgCCaMK lacking the auto-inhibitory/CaM domain in two actinorhizal species: C. glauca (Casuarinaceae), which develops an intracellular infection pathway, and Discaria trinervis (Rhamnaceae) which is characterized by an ancestral intercellular infection mechanism. In both species, we found induction of nodulation independent of Frankia similar to response to the activation of CCaMK in the rhizobia-legume symbiosis and conclude that the regulation of actinorhiza organogenesis is conserved regardless of the infection mode. It has been suggested that rhizobial and actinorhizal symbioses originated from a common ancestor with several independent evolutionary origins. Our findings are consistent with the recruitment of a similar genetic pathway governing rhizobial and Frankia nodule organogenesis.
publishDate 2013
dc.date.none.fl_str_mv 2013-05
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/11336/23861
Svistoonoff, Sergio; Benabdoun, Faiza Meriem; Nambiar Veetil, Mathish; Imanishi, Leandro Ezequiel; Vaissayre, Virginie; et al.; The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis; Public Library of Science; Plos One; 8; 5; 5-2013; 1-10; e64515
1932-6203
CONICET Digital
CONICET
url http://hdl.handle.net/11336/23861
identifier_str_mv Svistoonoff, Sergio; Benabdoun, Faiza Meriem; Nambiar Veetil, Mathish; Imanishi, Leandro Ezequiel; Vaissayre, Virginie; et al.; The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis; Public Library of Science; Plos One; 8; 5; 5-2013; 1-10; e64515
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/http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0064515
info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pone.0064515
info:eu-repo/semantics/altIdentifier/url/https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3669324/
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)
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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 13.070432

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