Evolution of a symbiotic receptor through gene duplications in the legume-rhizobium mutualism

Stéphane de Mita (1, 2) , Arend Streng (2) , Ton Bisseling (3) , Rene Geurts (3)

1 IAM - Interactions Arbres-Microorganismes
2 Laboratory of Molecular Biology, Department of Plant Science
3 Laboratory of Molecular Biology, Department of Plant Science

The symbiosis between legumes and nitrogen-fixing rhizobia co-opted pre-existing end-omycorrhizal features. In particular, both symbionts release lipo-chitooligosaccharides (LCOs) that are recognized by LysM-type receptor kinases. We investigated the evolutionary history of rhizobial LCO receptor genes MtLYK3-LjNFR1 to gain insight into the evolutionary origin of the rhizobial symbiosis. We performed a phylogenetic analysis integrating gene copies from nonlegumes and legumes, including the non-nodulating, phylogenetically basal legume Cercis chinensis. Signatures of differentiation between copies were investigated through patterns of molecular evolution. We show that two rounds of duplication preceded the evolution of the rhizobial symbiosis in legumes. Molecular evolution patterns indicate that the resulting three paralogous gene copies experienced different selective constraints. In particular, one copy maintained the ancestral function, and another specialized into perception of rhizobial LCOs. It has been suggested that legume LCO receptors evolved from a putative ancestral defense-related chitin receptor through the acquisition of two kinase motifs. However, the phylogenetic analysis shows that these domains are actually ancestral, suggesting that this scenario is unlikely. Our study underlines the evolutionary significance of gene duplication and subsequent neo-functionalization in MtLYK3-LjNFR1 genes. We hypothesize that their ancestor was more likely a mycorrhizal LCO receptor, than a defense-related receptor kinase.

Mots clés: coevolution; duplication; legume-rhizobium symbiosis; lipo-chitooligosaccharides (LCOs); molecular evolution; neofunctionalization; Nod factors; AMINO-ACSITES; MEDICAGO-TRUNCATULA; PHYLOGENETIC PERSPECTIVES; MYCORRHIZAL SYMBIOSIS; ARBUSCULAR MYCORRHIZA; POPULUS-TRICHOCARPA; MAXIMUM-LIKELIHOOD; DRAFT GENOME; LAND PLANTS; NODULATION

Domaines: Sciences du Vivant [q-bio]

Stéphane de Mita, Arend Streng, Ton Bisseling, Rene Geurts. Evolution of a symbiotic receptor through gene duplications in the legume-rhizobium mutualism. New Phytologist, 2014, 201 (3), pp.961 - 972. ⟨10.1111/nph.12549⟩. ⟨hal-01268605⟩