Rice ethylene receptors OsERS1/2 function as Ca2+-permeable channels mediating calcium-dependent antagonism of ethylene-induced root growth inhibition

Rice (Oryza sativa), a staple food for over half of the global population and a model cereal, has evolved unique physiological mechanisms to adapt to its semi-aquatic environment, in which root development is critical for nutrient acquisition, stress tolerance, and grain yield. Ethylene, a gaseous phytohormone, plays a key role in regulating root elongation in rice. Calcium (Ca²⁺) is an essential nutrient and universal second messenger that mediates diverse physiological processes in plants. However, the molecular link between ethylene signaling and Ca²⁺ dynamics in rice particularly in the regulation of root growth that impacts agricultural productivity remains unclear. Here, we identify a Ca^2+-dependent antagonism of the ethylene-induced response (CAER) that specifically modulates root elongation in rice. Notably, we demonstrate that ethylene receptors OsERS1/2 function as Ca²⁺-permeable channels. OsERS1, in particular, exhibits permeability to both monovalent and divalent cations. Mutagenesis analyses further reveal that OsERS1 channel activity depends on homomeric assembly sites (Cys4 and Cys6), rather than on its ethylene-binding site (Cys65), indicating a clear functional decoupling between receptor signaling and ion channel activity. Loss-of-function mutants Osers1 and Osers2 fail to exhibit the CAER phenotype observed in wild-type plants, confirming that this Ca^2+-dependent regulatory mechanism requires OsERS1/2. Collectively, these findings uncover an unexpected ion channel function of ethylene receptors, redefining their molecular identity beyond canonical hormone signaling receptors. Moreover, our work introduces the concept of "hormone receptor-type ion channels (HRICs)" as a new functional category, expanding our understanding of how plant hormones transduce signals at the molecular level.