Rice Ethylene Receptors Function as Ca2+-Permeable Ion Channels to Orchestrate Calcium-Dependent Antagonism of Ethylene Responses in Roots

Abstract

The gaseous phytohormone ethylene governs essential plant processes spanning development, productivity, and stress resistance. As an essential nutrient and second messenger, calcium (Ca2+) is widely implicated in diverse plant physiological activities; however, its role in the ethylene signal transduction pathway remains elusive. Here, we identified a calcium-dependent antagonism of ethylene response (CAER) specifically modulates root elongation in the model cereal rice (Oryza sativa). Interestingly, we demonstrate that the ethylene receptors OsERS1 and OsERS2 both function as Ca2+-permeable channels, with OsERS1 further acting as a non-selective cation channel capable of permeating both monovalent and divalent cations. Mutagenesis analysis reveals that OsERS1 channel activity relies on homomeric assembly sites (C4/C6) rather than its ethylene-binding site (C65), indicating a clear decoupling of the molecular modules governing receptor signaling and ion channel function. The loss-of-function mutant Osers1/2 does not exhibit the CAER phenotype of the wild type (WT), confirm that this calcium-dependent regulatory mechanism is dependent on both OsERS1 and OsERS2. These findings uncover an unexpected ion-channel function of ethylene receptors, redefining their molecular identity beyond canonical signaling proteins and establishing the novel "hormone receptor-type ion channel (HRIC)" paradigm--one that fundamentally expands our understanding of how plant hormones transduce signals at the membrane.