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

Tao Guo,Fuyan Si,Fei Lu,Lianlian Yang,Ke Chen,Xiaopan Wang,Guanglin Li,Zi-Qi Lu,Hong-Xuan Lin

Published 2024 in Plant Communications

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 to be clarified. 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 a role opposite to that of the OsEPFL6/7/8/9 subfamily in regulating spikelet number per panicle and grain size. Notably, OsEPFL5 competitively replaces binding of OsEPFL6, OsEPFL7, OsEPFL8, or OsEPFL9 to the OsER1 receptor, revealing antagonistic competition between these small homologous peptides. Specifically enhancing the expression of OsEPFL5 can significantly improve grain yield by suppressing functions of the ligand–receptor pairs 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 clarify how a receptor agonist and antagonist define inductive and inhibitory cues to shape rice panicle architecture, thus providing a new method for rationally breaking yield-trait coupling by manipulating small antagonistic peptides.

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