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.
Highlights
While more than 80% of land plants can establish root endosymbioses with Glomeromycota fungi through the arbuscular mycorrhizal (AM) association, only a small group of plants limited to four orders (Fagales, Fabales, Rosales and Cucurbitales) are able to form nitrogen-fixing root nodule symbiosis (RNS) in association with soil bacteria
We demonstrate that constitutive activation of Calcium and calmodulin-dependent protein kinase (CCaMK) is sufficient to trigger nodule organogenesis in the absence of Frankia in C. glauca and in Discaria trinervis (Rosales), a species characterized by an ancestral intercellular infection mechanism, suggesting that every independent acquisition of nodulation recruited the whole pathway beyond SYMRK
By cloning its full-length cDNA and the corresponding genomic fragment, we found that CgCCaMK encodes a 520 aa putative protein and has similar gene and protein structures compared to legume CCaMKs
Summary
While more than 80% of land plants can establish root endosymbioses with Glomeromycota fungi through the arbuscular mycorrhizal (AM) association, only a small group of plants limited to four orders (Fagales, Fabales, Rosales and Cucurbitales) are able to form nitrogen-fixing root nodule symbiosis (RNS) in association with soil bacteria This group comprises (i) most of the ,20.000 legume species and a few species of Parasponia (Cannabaceae) able to interact with Gram-negative proteobacteria, collectively called rhizobia; and (ii) actinorhizal plants, ,280 species able to interact with Gram-positive filamentous actinobacteria Frankia [1,2]. Nod factors (NFs), lipo-chito-oligosaccharides synthesized by rhizobia, are the key molecular determinants that enable the specific recognition of bacterial symbionts by the plant [6] Their perception is mediated by LysM receptors and elicits several host cellular responses, notably intracellular calcium oscillations and the activation of a signaling cascade involving a specific set of genes [7]. In Parasponia andersonii (Rosales) the interaction with rhizobia depends on NFP (a LysM receptor kinase) and CCaMK [12]
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