From defense to symbiosis: limited alterations in the kinase domain of LysM receptor‐like kinases are crucial for evolution of legume–Rhizobium symbiosis

Abstract

SUMMARYNitrogen-fixing symbiosis between legumes and rhizobia is initiated by the recognition of rhizobial Nod factors (NFs) by host plants. NFs are diversely modified derivatives of chitin oligosaccharide, a fungal elicitor that induces defense responses in plants. Recent evidence has shown that both NFs and chitin elicitors are recognized by structurally related LysM receptor kinases. Transcriptome analyses of Lotus japonicus roots indicated that NFs not only activate symbiosis genes but also transiently activate defense-related genes through NF receptors. Conversely, chitin oligosaccharides were able to activate symbiosis genes independently of NF receptors. Analyses using chimeric genes consisting of the LysM receptor domain of a Lotus japonicus NF receptor, NFR1, and the kinase domain of an Arabidopsis chitin receptor, CERK1, demonstrated that substitution of a portion of the aEF helix in CERK1 with the amino acid sequence YAQ from the corresponding region of NFR1 enables L. japonicus nfr1 mutants to establish symbiosis with Mesorhizobium loti. We also showed that the kinase domains of two Lotus japonicus LysM receptor kinases, Lys6 and Lys7, which also possess the YAQ sequence, suppress the symbiotic defect of nfr1. These results strongly suggest that, in addition to adaptation of extracellular LysM domains to NFs, limited alterations in the kinase domain of chitin receptors have played a crucial role in shifting the intracellular signaling to symbiosis from defense responses, thus constituting one of the key genetic events in the evolution of root nodule symbiosis in legume plants.

Hijacking of leguminous nodulation signaling by the rhizobial type III secretion system

“…of LysM-RKs than nonleguminous plants (18,29). Together, these results suggest that rhizobial NFs are perceived by additional receptors in soybean roots, and that the derived signal and that from NFRs synergistically activate nodulation signaling.…”

“…To investigate further the importance of NFs and NFRs in the expression of these symbiosis genes, we compared their expression in the roots of Enrei and En1282 inoculated with T3SS and nodC mutants using realtime RT-PCR. Two well-characterized symbiosis genes, ENOD40 (15) and NIN (16), were selected as marker genes because their expression is induced early after NF perception (17,18). In both Enrei and En1282 roots, relative expression levels of ENOD40 and NIN were significantly induced by the inoculation of USDA61 (Fig.…”

Complexity of miRNA-dependent regulation in root symbiosis

“…The accumulation of reactive oxygen species leads to cell death and the necrosis of the area of infection, which prevents bacterial progression in the plant tissue. These observations suggest that Nod factors may also be important in the evasion of the plant immune response and the protection of cells from reactive oxygen species [10,15]. However, other components, such as receptor-like kinase with leucine-rich repeat (LRR) domains, have been identified to be essential for nodulation signalling in addition to the perception of pathogen signals [16,17].…”

The <i>Lotus</i> intrinsic ethylene receptor regulates both symbiotic and non-symbiotic responses

“…These M2 seeds were germinated and grown on half-strength Gamborg's B5 medium (Wako) including 10 µM ACC and grown in an artificially-lit growth cabinet at 24°C for 16 h (light) and 22°C for 8 h (dark). The method for nodulation analysis has been previously described (Nakagawa et al 2011).…”

“…Experimental methods for total RNA extraction and real-time PT-PCR analysis were described previously (Nakagawa et al 2011). The gene specific primers used for LjETR1 were 5′-TTG CTC TTA CGG GAA ACA CC-3′ and 5′-CAC CCC TCA TTT TGT CAA CAG-3′.…”