title: The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis.
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.
authors.affiliation: Equipe Rhizogenèse, UMR DIADE (IRD, UM2), Institut de Recherche pour le Développement, Montpellier, France.
authors.forename: Sergio
authors.initials: S
authors.lastname: Svistoonoff
authors.forename: Faiza Meriem
authors.initials: FM
authors.lastname: Benabdoun
authors.forename: Mathish
authors.initials: M
authors.lastname: Nambiar-Veetil
authors.forename: Leandro
authors.initials: L
authors.lastname: Imanishi
authors.forename: Virginie
authors.initials: V
authors.lastname: Vaissayre
authors.forename: Stella
authors.initials: S
authors.lastname: Cesari
authors.forename: Nathalie
authors.initials: N
authors.lastname: Diagne
authors.forename: Valérie
authors.initials: V
authors.lastname: Hocher
authors.forename: Françoise
authors.initials: F
authors.lastname: de Billy
authors.forename: Jocelyne
authors.initials: J
authors.lastname: Bonneau
authors.forename: Luis
authors.initials: L
authors.lastname: Wall
authors.forename: Nadia
authors.initials: N
authors.lastname: Ykhlef
authors.forename: Charles
authors.initials: C
authors.lastname: Rosenberg
authors.forename: Didier
authors.initials: D
authors.lastname: Bogusz
authors.forename: Claudine
authors.initials: C
authors.lastname: Franche
authors.forename: Hassen
authors.initials: H
authors.lastname: Gherbi
mesh_terms: D000595:Amino Acid Sequence; D001426:Bacterial Proteins / Q000235:genetics* / Q000378:metabolism; D005075:Biological Evolution; D054737:Calcium-Calmodulin-Dependent Protein Kinase Kinase / Q000235:genetics* / Q000378:metabolism; D027581:Cannabaceae / Q000201:enzymology / Q000235:genetics*; D007887:Fabaceae / Q000201:enzymology / Q000235:genetics*; D040161:Frankia / Q000201:enzymology / Q000235:genetics*; D015870:Gene Expression; D005816:Genetic Complementation Test; D008969:Molecular Sequence Data; D009154:Mutation; D038821:Mycorrhizae / Q000201:enzymology / Q000235:genetics*; D009586:Nitrogen Fixation / Q000502:physiology; D010940:Plant Proteins / Q000235:genetics* / Q000378:metabolism; D055170:Plant Root Nodulation / Q000502:physiology; D012231:Rhizobium / Q000201:enzymology / Q000235:genetics*; D015398:Signal Transduction; D013559:Symbiosis; D014161:Transduction, Genetic
chemical_list: D001426:Bacterial Proteins; D010940:Plant Proteins; D054737:Calcium-Calmodulin-Dependent Protein Kinase Kinase