The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis.
Identifieur interne : 001C01 ( Main/Corpus ); 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 ; 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.
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
Links to Exploration step
pubmed:23741336Le document en format XML
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<author><name sortKey="Benabdoun, Faiza Meriem" sort="Benabdoun, Faiza Meriem" uniqKey="Benabdoun F" first="Faiza Meriem" last="Benabdoun">Faiza Meriem Benabdoun</name>
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<author><name sortKey="Vaissayre, Virginie" sort="Vaissayre, Virginie" uniqKey="Vaissayre V" first="Virginie" last="Vaissayre">Virginie Vaissayre</name>
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<author><name sortKey="Bogusz, Didier" sort="Bogusz, Didier" uniqKey="Bogusz D" first="Didier" last="Bogusz">Didier Bogusz</name>
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<author><name sortKey="Franche, Claudine" sort="Franche, Claudine" uniqKey="Franche C" first="Claudine" last="Franche">Claudine Franche</name>
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<imprint><date when="2013" type="published">2013</date>
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<profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Amino Acid Sequence (MeSH)</term>
<term>Bacterial Proteins (genetics)</term>
<term>Bacterial Proteins (metabolism)</term>
<term>Biological Evolution (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="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="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="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>
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<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>
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<ArticleTitle>The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis.</ArticleTitle>
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<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>
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<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>
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<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>
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<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>
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<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>
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<ForeName>Charles</ForeName>
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<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>
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<Language>eng</Language>
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</MeshHeading>
<MeshHeading><DescriptorName UI="D001426" MajorTopicYN="N">Bacterial Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
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<MeshHeading><DescriptorName UI="D005075" MajorTopicYN="N">Biological Evolution</DescriptorName>
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<MeshHeading><DescriptorName UI="D027581" MajorTopicYN="N">Cannabaceae</DescriptorName>
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<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D007887" MajorTopicYN="N">Fabaceae</DescriptorName>
<QualifierName UI="Q000201" MajorTopicYN="N">enzymology</QualifierName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
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</MeshHeading>
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<MeshHeading><DescriptorName UI="D005816" MajorTopicYN="N">Genetic Complementation Test</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D008969" MajorTopicYN="N">Molecular Sequence Data</DescriptorName>
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<MeshHeading><DescriptorName UI="D009154" MajorTopicYN="N">Mutation</DescriptorName>
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<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
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<MeshHeading><DescriptorName UI="D009586" MajorTopicYN="N">Nitrogen Fixation</DescriptorName>
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<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
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<MeshHeading><DescriptorName UI="D055170" MajorTopicYN="N">Plant Root Nodulation</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
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<MeshHeading><DescriptorName UI="D012231" MajorTopicYN="N">Rhizobium</DescriptorName>
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<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D015398" MajorTopicYN="N">Signal Transduction</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D013559" MajorTopicYN="N">Symbiosis</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D014161" MajorTopicYN="N">Transduction, Genetic</DescriptorName>
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<PubmedData><History><PubMedPubDate PubStatus="received"><Year>2013</Year>
<Month>01</Month>
<Day>18</Day>
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<PubMedPubDate PubStatus="accepted"><Year>2013</Year>
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