Competitive binding of small antagonistic peptides to the OsER1 receptor optimizes rice panicle architecture.

Abstract

Rice panicle architecture is a pivotal trait that strongly contributes to grain yield. Small peptide ligands from the OsEPF/EPFL family synergistically control panicle architecture by recognition of the OsER1 receptor and subsequent activation of the OsMKKK10-OsMKK4-OsMPK6 cascade, indicating that specific ligand-receptor pairs orchestrate rice panicle development. However, how small homologous peptides fine-tune organ morphogenesis by targeting a common receptor remains elusive. Here, we report that the small peptide OsEPFL5 acts as a ligand of the OsER1 receptor that inactivates the OsMKKK10-OsMKK4-OsMPK6 cascade, suggesting that OsEPFL5 plays the opposite role to that of the OsEPFL6/7/8/9 subfamily in regulating spikelet number per panicle and grain size. Notably, OsEPFL5 competitively replaces the OsEPFL6, OsEPFL7, OsEPFL8, or OsEPFL9 binding to the OsER1 receptor, exposing antagonistic competition between small homologous peptides. Specifically enhancing expression of OsEPFL5 significantly improves grain yield by suppressing functions of the ligand-receptor pairs of OsEPFL6-OsER1, OsEPFL7-OsER1, OsEPFL8-OsER1, and OsEPFL9-OsER1, suggesting that competitive binding to the OsER1 receptor by small antagonistic peptides can optimize rice panicle architecture. Our findings elucidate how a receptor agonist and antagonist define inductive and inhibitory cues to shape rice panicle architecture, thus providing a new method of rationally breaking yield trait coupling by manipulating small antagonistic peptides.