The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis.
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 pro...
Guardado en:
| Autores principales: | , , , , , , , , , , , , , , , |
|---|---|
| Formato: | article |
| Lenguaje: | EN |
| Publicado: |
Public Library of Science (PLoS)
2013
|
| Materias: | |
| Acceso en línea: | https://doaj.org/article/04f6142d865e47439ecd2efb39eebb25 |
| Etiquetas: |
Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
|
| id |
oai:doaj.org-article:04f6142d865e47439ecd2efb39eebb25 |
|---|---|
| record_format |
dspace |
| spelling |
oai:doaj.org-article:04f6142d865e47439ecd2efb39eebb252021-11-18T07:43:38ZThe independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis.1932-620310.1371/journal.pone.0064515https://doaj.org/article/04f6142d865e47439ecd2efb39eebb252013-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23741336/pdf/?tool=EBIhttps://doaj.org/toc/1932-6203Only 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.Sergio SvistoonoffFaiza Meriem BenabdounMathish Nambiar-VeetilLeandro ImanishiVirginie VaissayreStella CesariNathalie DiagneValérie HocherFrançoise de BillyJocelyne BonneauLuis WallNadia YkhlefCharles RosenbergDidier BoguszClaudine FrancheHassen GherbiPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 8, Iss 5, p e64515 (2013) |
| institution |
DOAJ |
| collection |
DOAJ |
| language |
EN |
| topic |
Medicine R Science Q |
| spellingShingle |
Medicine R Science Q 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 Gherbi The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis. |
| 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 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. |
| format |
article |
| author |
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 Gherbi |
| author_facet |
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 Gherbi |
| author_sort |
Sergio Svistoonoff |
| title |
The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis. |
| 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 |
independent acquisition of plant root nitrogen-fixing symbiosis in fabids recruited the same genetic pathway for nodule organogenesis. |
| publisher |
Public Library of Science (PLoS) |
| publishDate |
2013 |
| url |
https://doaj.org/article/04f6142d865e47439ecd2efb39eebb25 |
| work_keys_str_mv |
AT sergiosvistoonoff theindependentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT faizameriembenabdoun theindependentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT mathishnambiarveetil theindependentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT leandroimanishi theindependentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT virginievaissayre theindependentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT stellacesari theindependentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT nathaliediagne theindependentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT valeriehocher theindependentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT francoisedebilly theindependentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT jocelynebonneau theindependentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT luiswall theindependentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT nadiaykhlef theindependentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT charlesrosenberg theindependentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT didierbogusz theindependentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT claudinefranche theindependentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT hassengherbi theindependentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT sergiosvistoonoff independentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT faizameriembenabdoun independentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT mathishnambiarveetil independentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT leandroimanishi independentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT virginievaissayre independentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT stellacesari independentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT nathaliediagne independentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT valeriehocher independentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT francoisedebilly independentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT jocelynebonneau independentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT luiswall independentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT nadiaykhlef independentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT charlesrosenberg independentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT didierbogusz independentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT claudinefranche independentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis AT hassengherbi independentacquisitionofplantrootnitrogenfixingsymbiosisinfabidsrecruitedthesamegeneticpathwayfornoduleorganogenesis |
| _version_ |
1718423013761744896 |