Receptor-like kinases (RLKs) are key cell signaling components. The rice ARBUSCULAR RECEPTOR-LIKE KINASE 1 (OsARK1) regulates the arbuscular mycorrhizal (AM) association postarbuscule development and belongs to an undefined subfamily of RLKs. Our phylogenetic analysis revealed that ARK1 has an ancient paralogue in spermatophytes, ARK2 . Single ark2 and ark1/ark2 double mutants in rice showed a nonredundant AM symbiotic function for OsARK2 . Global transcriptomics identified a set of genes coregulated by the two RLKs, suggesting that OsARK1 and OsARK2 orchestrate symbiosis in a common pathway. ARK lineage proteins harbor a newly identified SPARK domain in their extracellular regions, which underwent parallel losses in ARK1 and ARK2 in monocots. This protein domain has ancient origins in streptophyte algae and defines additional overlooked groups of putative cell surface receptors.