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Symbiosis receptor kinase (SYMRK) is a cell membrane-localized protein kinase containing extracellular malectin-like domain (MLD) and leucine-rich repeat (LRR) domains, which is critically required for both root nodule symbiosis (RNS) and arbuscular mycorrhizal symbiosis (AMS). SYMRK is widely distributed in the genomes of different plant species; however, the contribution of different domains of SYMRK and its homologs from other plant species to RNS is largely unclear. In this study, SYMRK and its homologs from three typical plant species including  Medicago truncatula  (for both RNS and AMS),  Oryza sativa  (for AMS but not RNS), and  Arabidopsis thaliana  (for neither RNS or AMS) were investigated using domain swap approach in response to rhizobia in  Lotus japonicus . Full-length SYMRK from rice and  Medicago  but not from  Arabidopsis  could complement  Lotus symrk-409  mutant plants to contribute RNS. The chimeric protein with the extracellular domain (ED) of LjSYMRK and cytoplasmic domains (CD) of SYMRK from both  Medicago  and rice but not  Arabidopsis  could contribute to RNS in  Lotus , suggesting that the CD of SYMRK is required for symbiotic signaling. The chimeric receptors containing the CD of LjSYMRK (SYMRK CD ) and the EDs of MtDMI2 (MtDMI2 ED ), OsSYMRK (OsSYMRK ED ), AtSYMRK (AtSYMRK ED ), NFR1 (NFR1 ED ), and NFR5 (NFR5 ED ) could complement  Lotus symrk-409  mutant plants to develop nodules. However, MtDMI2 could partially complement  Lotus symrk-409  mutants to form both effective nodules and ineffective bumps, which is similar to the complementation results from MtDMI2 ED -LjSYMRK CD  and LjSYMRK GDLC  in  Lotus symrk-409  mutants, suggesting that ED of SYMRK has a very fine-tune regulation for RNS in  Lotus . The deletion of either MLD or LRR on SYMRK GDLC  (a mutant version of SYMRK with GDPC motif replaced by GDLC) could contribute to RNS when overexpressed in  Lotus symrk-409  mutants, suggesting that MLD and LRR domains might work together to be involved in symbiotic signaling and the LRR domain might play a negative role in LjSYMRK GDLC -mediated RNS. By mutagenizing the conserved amino acids on LRR domain, five serine residues were found to be required for the function of LjSYMRK GDLC  in RNS. These finding precisely refine the molecular mechanisms of SYMRK function in symbiotic signaling in  L. japonicus .

Domain Swap Approach Reveals the Critical Roles of Different Domains of SYMRK in Root Nodule Symbiosis in Lotus japonicus