Duplication of Symbiotic Lysin Motif Receptors Predates the Evolution of Nitrogen-Fixing Nodule Symbiosis. Issue 2 (15th July 2020)

• Record Type: Journal Article
• Authors: Rutten, Luuk; Miyata, Kana; Roswanjaya, Yuda Purwana; Huisman, Rik; Bu, Fengjiao; Hartog, Marijke; Linders, Sidney; van Velzen, Robin; van Zeijl, Arjan; Bisseling, Ton; Kohlen, Wouter; Geurts, Rene
• Is Part Of: Plant physiology. Volume 184:Issue 2(2020)
• Page Start: 1004
• Page End: 1023
• Publication Date: 2020-07-15
• Subjects: Plant physiology -- Periodicals; Botany -- Periodicals; Periodicals; Electronic journals; 571.2
• DOI: 10.1104/pp.19.01420
• Languages: English
• ISSNs: 0032-0889

Abstract

Abstract : Four lysin motif receptor kinases controlling rhizobium nodule formation in the nonlegume Parasponia evolved after two ancient duplications. Abstract: Rhizobium nitrogen-fixing nodule symbiosis occurs in two taxonomic lineages: legumes (Fabaceae) and the genus Parasponia (Cannabaceae). Both symbioses are initiated upon the perception of rhizobium-secreted lipochitooligosaccharides (LCOs), called Nod factors. Studies in the model legumes Lotus japonicus and Medicago truncatula showed that rhizobium LCOs are perceived by a heteromeric receptor complex of distinct Lys motif (LysM)-type transmembrane receptors named NOD FACTOR RECEPTOR1 (LjNFR1) and LjNFR5 ( L. japonicus ) and LYSM DOMAIN CONTAINING RECEPTOR KINASE3 (MtLYK3)-NOD FACTOR PERCEPTION (MtNFP; M. truncatula ). Recent phylogenomic comparative analyses indicated that the nodulation traits of legumes, Parasponia spp., as well as so-called actinorhizal plants that establish a symbiosis with diazotrophic Frankia spp. bacteria share an evolutionary origin about 110 million years ago. However, the evolutionary trajectory of LysM-type LCO receptors remains elusive. By conducting phylogenetic analysis, transcomplementation studies, and CRISPR-Cas9 mutagenesis in Parasponia andersonii, we obtained insight into the origin of LCO receptors essential for nodulation. We identified four LysM-type receptors controlling nodulation in P. andersonii : PanLYK1, PanLYK3, PanNFP1, and PanNFP2 . These genes evolved from ancient duplication events predating and coinciding with the origin of nodulation. Phylogenetic and functional analyses associated the occurrence of a functional NFP2-orthologous receptor to LCO-driven nodulation. Legumes and Parasponia spp. use orthologous LysM-type receptors to perceive rhizobium LCOs, suggesting a shared evolutionary origin of LCO-driven nodulation. Furthermore, we found that both PanLYK1 and PanLYK3 are essential for intracellular arbuscule formation of mutualistic endomycorrhizal fungi. PanLYK3 also acts as a chitin oligomer receptor essential for innate immune signaling, demonstrating functional analogy to CHITIN ELECITOR RECEPTOR KINASE-type receptors.