The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis.
Identifieur interne : 001C01 ( Main/Curation ); précédent : 001C00; suivant : 001C02The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis.
Auteurs : Sergio Svistoonoff [France] ; Faiza Meriem Benabdoun ; Mathish Nambiar-Veetil ; Leandro Imanishi ; Virginie Vaissayre ; Stella Cesari ; Nathalie Diagne ; Valérie Hocher ; Françoise De Billy ; Jocelyne Bonneau ; Luis Wall ; Nadia Ykhlef ; Charles Rosenberg ; Didier Bogusz ; Claudine Franche ; Hassen GherbiSource :
- PloS one [ 1932-6203 ] ; 2013.
Descripteurs français
- KwdFr :
- Calcium-Calmodulin-Dependent Protein Kinase Kinase (génétique), Calcium-Calmodulin-Dependent Protein Kinase Kinase (métabolisme), Cannabaceae (enzymologie), Cannabaceae (génétique), Données de séquences moléculaires (MeSH), Expression des gènes (MeSH), Fabaceae (enzymologie), Fabaceae (génétique), Fixation de l'azote (physiologie), Frankia (enzymologie), Frankia (génétique), Mutation (MeSH), Mycorhizes (enzymologie), Mycorhizes (génétique), Nodulation racinaire (physiologie), Protéines bactériennes (génétique), Protéines bactériennes (métabolisme), Protéines végétales (génétique), Protéines végétales (métabolisme), Rhizobium (enzymologie), Rhizobium (génétique), Symbiose (MeSH), Séquence d'acides aminés (MeSH), Test de complémentation (MeSH), Transduction du signal (MeSH), Transduction génétique (MeSH), Évolution biologique (MeSH).
- MESH :
- enzymologie : Cannabaceae, Fabaceae, Frankia, Mycorhizes, Rhizobium.
- génétique : Calcium-Calmodulin-Dependent Protein Kinase Kinase, Cannabaceae, Fabaceae, Frankia, Mycorhizes, Protéines bactériennes, Protéines végétales, Rhizobium.
- métabolisme : Calcium-Calmodulin-Dependent Protein Kinase Kinase, Protéines bactériennes, Protéines végétales.
- physiologie : Fixation de l'azote, Nodulation racinaire.
- Données de séquences moléculaires, Expression des gènes, Mutation, Symbiose, Séquence d'acides aminés, Test de complémentation, Transduction du signal, Transduction génétique, Évolution biologique.
English descriptors
- KwdEn :
- Amino Acid Sequence (MeSH), Bacterial Proteins (genetics), Bacterial Proteins (metabolism), Biological Evolution (MeSH), Calcium-Calmodulin-Dependent Protein Kinase Kinase (genetics), Calcium-Calmodulin-Dependent Protein Kinase Kinase (metabolism), Cannabaceae (enzymology), Cannabaceae (genetics), Fabaceae (enzymology), Fabaceae (genetics), Frankia (enzymology), Frankia (genetics), Gene Expression (MeSH), Genetic Complementation Test (MeSH), Molecular Sequence Data (MeSH), Mutation (MeSH), Mycorrhizae (enzymology), Mycorrhizae (genetics), Nitrogen Fixation (physiology), Plant Proteins (genetics), Plant Proteins (metabolism), Plant Root Nodulation (physiology), Rhizobium (enzymology), Rhizobium (genetics), Signal Transduction (MeSH), Symbiosis (MeSH), Transduction, Genetic (MeSH).
- MESH :
- chemical , genetics : Bacterial Proteins, Calcium-Calmodulin-Dependent Protein Kinase Kinase, Plant Proteins.
- chemical , metabolism : Bacterial Proteins, Calcium-Calmodulin-Dependent Protein Kinase Kinase, Plant Proteins.
- enzymology : Cannabaceae, Fabaceae, Frankia, Mycorrhizae, Rhizobium.
- genetics : Cannabaceae, Fabaceae, Frankia, Mycorrhizae, Rhizobium.
- physiology : Nitrogen Fixation, Plant Root Nodulation.
- Amino Acid Sequence, Biological Evolution, Gene Expression, Genetic Complementation Test, Molecular Sequence Data, Mutation, Signal Transduction, Symbiosis, Transduction, Genetic.
Abstract
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 truncatula 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.
DOI: 10.1371/journal.pone.0064515
PubMed: 23741336
PubMed Central: PMC3669324
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pubmed:23741336Le document en format XML
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(MeSH)</term><term>Calcium-Calmodulin-Dependent Protein Kinase Kinase (genetics)</term><term>Calcium-Calmodulin-Dependent Protein Kinase Kinase (metabolism)</term><term>Cannabaceae (enzymology)</term><term>Cannabaceae (genetics)</term><term>Fabaceae (enzymology)</term><term>Fabaceae (genetics)</term><term>Frankia (enzymology)</term><term>Frankia (genetics)</term><term>Gene Expression (MeSH)</term><term>Genetic Complementation Test (MeSH)</term><term>Molecular Sequence Data (MeSH)</term><term>Mutation (MeSH)</term><term>Mycorrhizae (enzymology)</term><term>Mycorrhizae (genetics)</term><term>Nitrogen Fixation (physiology)</term><term>Plant Proteins (genetics)</term><term>Plant Proteins (metabolism)</term><term>Plant Root Nodulation (physiology)</term><term>Rhizobium (enzymology)</term><term>Rhizobium (genetics)</term><term>Signal Transduction (MeSH)</term><term>Symbiosis (MeSH)</term><term>Transduction, Genetic (MeSH)</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Calcium-Calmodulin-Dependent Protein Kinase Kinase (génétique)</term><term>Calcium-Calmodulin-Dependent Protein Kinase Kinase (métabolisme)</term><term>Cannabaceae (enzymologie)</term><term>Cannabaceae (génétique)</term><term>Données de séquences moléculaires (MeSH)</term><term>Expression des gènes (MeSH)</term><term>Fabaceae (enzymologie)</term><term>Fabaceae (génétique)</term><term>Fixation de l'azote (physiologie)</term><term>Frankia (enzymologie)</term><term>Frankia (génétique)</term><term>Mutation (MeSH)</term><term>Mycorhizes (enzymologie)</term><term>Mycorhizes (génétique)</term><term>Nodulation racinaire (physiologie)</term><term>Protéines bactériennes (génétique)</term><term>Protéines bactériennes (métabolisme)</term><term>Protéines végétales (génétique)</term><term>Protéines végétales (métabolisme)</term><term>Rhizobium (enzymologie)</term><term>Rhizobium (génétique)</term><term>Symbiose (MeSH)</term><term>Séquence d'acides aminés (MeSH)</term><term>Test de complémentation (MeSH)</term><term>Transduction du signal (MeSH)</term><term>Transduction génétique (MeSH)</term><term>Évolution biologique (MeSH)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Bacterial Proteins</term><term>Calcium-Calmodulin-Dependent Protein Kinase Kinase</term><term>Plant Proteins</term></keywords><keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Bacterial Proteins</term><term>Calcium-Calmodulin-Dependent Protein Kinase Kinase</term><term>Plant Proteins</term></keywords><keywords scheme="MESH" qualifier="enzymologie" xml:lang="fr"><term>Cannabaceae</term><term>Fabaceae</term><term>Frankia</term><term>Mycorhizes</term><term>Rhizobium</term></keywords><keywords scheme="MESH" qualifier="enzymology" xml:lang="en"><term>Cannabaceae</term><term>Fabaceae</term><term>Frankia</term><term>Mycorrhizae</term><term>Rhizobium</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Cannabaceae</term><term>Fabaceae</term><term>Frankia</term><term>Mycorrhizae</term><term>Rhizobium</term></keywords><keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>Calcium-Calmodulin-Dependent Protein Kinase Kinase</term><term>Cannabaceae</term><term>Fabaceae</term><term>Frankia</term><term>Mycorhizes</term><term>Protéines bactériennes</term><term>Protéines végétales</term><term>Rhizobium</term></keywords><keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>Calcium-Calmodulin-Dependent Protein Kinase Kinase</term><term>Protéines bactériennes</term><term>Protéines végétales</term></keywords><keywords scheme="MESH" qualifier="physiologie" xml:lang="fr"><term>Fixation de l'azote</term><term>Nodulation racinaire</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Nitrogen Fixation</term><term>Plant Root Nodulation</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Amino Acid Sequence</term><term>Biological Evolution</term><term>Gene Expression</term><term>Genetic Complementation Test</term><term>Molecular Sequence Data</term><term>Mutation</term><term>Signal Transduction</term><term>Symbiosis</term><term>Transduction, Genetic</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Données de séquences moléculaires</term><term>Expression des gènes</term><term>Mutation</term><term>Symbiose</term><term>Séquence d'acides aminés</term><term>Test de complémentation</term><term>Transduction du signal</term><term>Transduction génétique</term><term>Évolution biologique</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">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 truncatula 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.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">23741336</PMID><DateCompleted><Year>2014</Year><Month>02</Month><Day>18</Day></DateCompleted><DateRevised><Year>2020</Year><Month>03</Month><Day>05</Day></DateRevised><Article PubModel="Electronic-Print"><Journal><ISSN IssnType="Electronic">1932-6203</ISSN><JournalIssue CitedMedium="Internet"><Volume>8</Volume><Issue>5</Issue><PubDate><Year>2013</Year></PubDate></JournalIssue><Title>PloS one</Title><ISOAbbreviation>PLoS One</ISOAbbreviation></Journal><ArticleTitle>The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis.</ArticleTitle><Pagination><MedlinePgn>e64515</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1371/journal.pone.0064515</ELocationID><Abstract><AbstractText>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 truncatula 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.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Svistoonoff</LastName><ForeName>Sergio</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Equipe Rhizogenèse, UMR DIADE (IRD, UM2), Institut de Recherche pour le Développement, Montpellier, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Benabdoun</LastName><ForeName>Faiza Meriem</ForeName><Initials>FM</Initials></Author><Author ValidYN="Y"><LastName>Nambiar-Veetil</LastName><ForeName>Mathish</ForeName><Initials>M</Initials></Author><Author ValidYN="Y"><LastName>Imanishi</LastName><ForeName>Leandro</ForeName><Initials>L</Initials></Author><Author ValidYN="Y"><LastName>Vaissayre</LastName><ForeName>Virginie</ForeName><Initials>V</Initials></Author><Author ValidYN="Y"><LastName>Cesari</LastName><ForeName>Stella</ForeName><Initials>S</Initials></Author><Author ValidYN="Y"><LastName>Diagne</LastName><ForeName>Nathalie</ForeName><Initials>N</Initials></Author><Author ValidYN="Y"><LastName>Hocher</LastName><ForeName>Valérie</ForeName><Initials>V</Initials></Author><Author ValidYN="Y"><LastName>de Billy</LastName><ForeName>Françoise</ForeName><Initials>F</Initials></Author><Author ValidYN="Y"><LastName>Bonneau</LastName><ForeName>Jocelyne</ForeName><Initials>J</Initials></Author><Author ValidYN="Y"><LastName>Wall</LastName><ForeName>Luis</ForeName><Initials>L</Initials></Author><Author ValidYN="Y"><LastName>Ykhlef</LastName><ForeName>Nadia</ForeName><Initials>N</Initials></Author><Author ValidYN="Y"><LastName>Rosenberg</LastName><ForeName>Charles</ForeName><Initials>C</Initials></Author><Author ValidYN="Y"><LastName>Bogusz</LastName><ForeName>Didier</ForeName><Initials>D</Initials></Author><Author ValidYN="Y"><LastName>Franche</LastName><ForeName>Claudine</ForeName><Initials>C</Initials></Author><Author ValidYN="Y"><LastName>Gherbi</LastName><ForeName>Hassen</ForeName><Initials>H</Initials></Author></AuthorList><Language>eng</Language><DataBankList CompleteYN="Y"><DataBank><DataBankName>GENBANK</DataBankName><AccessionNumberList><AccessionNumber>HF952923</AccessionNumber><AccessionNumber>HF952924</AccessionNumber></AccessionNumberList></DataBank></DataBankList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2013</Year><Month>05</Month><Day>31</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>PLoS 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