FERONIA signaling maintains cell wall integrity during brassinosteroid-induced cell expansion in Arabidopsis.

Abstract

Plant cell expansion is regulated by hormones and driven by turgor pressure, which stretches the cell wall and can potentially cause wall damage or rupture. How plant cells avoid cell wall rupture during hormone-induced rapid cell expansion remains poorly understood. Here, we show that the wall-sensing receptor kinase FERONIA (FER) plays an essential role in maintaining cell wall integrity during brassinosteroid (BR)-induced cell elongation. Compared to the wild type, the BR-treated fer mutants display an increased initial acceleration of cell elongation, increased cell wall damage and rupture, reduced production of reactive oxygen species (ROS), and enhanced cell wall acidification. Long-term treatments of fer with high concentrations of BR cause stress responses and reduce growth, whereas osmolytes, reducing turgor, alleviate the defects. These results show that BR-induced cell elongation causes damage to cell walls and the release of cell wall fragments that activate FER, which promotes ROS production, attenuates apoplastic acidification, and slows cell elongation, thereby preventing further cell wall damage and rupture. Furthermore, we show that BR signaling promotes FER accumulation at the plasma membrane (PM). When the BR level is low, the GSK3-like kinase BIN2 phosphorylates FER to reduce FER accumulation and translocation from the endoplasmic reticulum to PM. BR-induced inactivation of BIN2 leads to dephosphorylation and PM accumulation of FER. Thus, BR signaling enhances FER-mediated cell wall integrity surveillance while promoting cell expansion, whereas FER acts as a brake to maintain a safe cell elongation rate. Our study reveals a vital signaling circuit that coordinates hormone signaling with mechanical sensing to prevent cell rupture during hormone-induced cell expansion.