Conserved hinge regions in SYMRK enable release of malectin-like domain for symbiont passage during rhizobia-legume symbiosis

Symbiosis receptor kinase (SYMRK), a malectin-like-domain/leucine-rich-repeat receptor-like-kinase (MLD-LRR-RLK), is the upstream-most component in the common-symbiosis-signaling-pathway. We highlight 2 proline residues that were distinctly acquired by SYMRK orthologs in its hinge regions to constitute a signaling module for allowing progress of symbionts across transcellular barriers during rhizobia-legume symbiosis. Within the ectodomain hinge (EctoD-hinge), all MLD-LRR-RLKs have a conserved W1xnGDPCxnW2×4C motif, where SYMRK orthologs within legumes have a distinct signature with a proline preceding W2 enabling cleavage of SYMRK ectodomain for releasing MLD. Within the kinase hinge (KD-hinge) at gatekeeper + 1 position, a conserved glutamate in MLD-LRR-RLKs is replaced by proline in all SYMRK orthologs that enabled its dual-specific kinase activity for ensuring ectodomain cleavage. Substitution of either proline restricted cortical progression of symbionts, forming infection patches in the nodule apex without affecting epidermal invasion and nodule organogenesis. This halt was entirely overcome by ectopic expression of free MLD, demonstrating the released MLD has an active role in progress of symbionts. Overall, we show that conservation of distinct prolines in hinge regions of SYMRK orthologs in legumes generates a signaling module involving dimerization and optimal phosphorylation of SYMRK for releasing MLD as an active transducer of symbiosis signaling.