Distinct nanoscale dynamics of growth receptor complexes link hormone perception to rapid cell wall remodeling

Abstract

Cell elongation is a fundamental process allowing plants to change size and shape, a process governed by several growth promoting hormones. While hormones such as brassinosteroids (BRs) and phytosulfokines (PSKs) have been shown to play important roles in elongation growth, the early steps of signal perception remains elusive, especially with regard to PSK. Here we report a rapid mechanism by which PSK alter cell wall mechanical properties in elongating hypocotyls. Notably, this mode of action differs from that of BR. Making use of atomic force microscopy and fluorescence lifetime imaging microscopy we demonstrate how hallmarks of growing plant cells such as mechanical wall properties, porosity and apoplastic pH are differentially affected by PSK compared to BR. Using super-resolution microscopy, we show that the receptor complex components for BR and PSK display individual spatiotemporal movement and organization patterns. The BR receptor BRI1 transitions to a faster diffusive state upon ligand perception, while the PSK receptor PSKR1 associates in tighter clusters. The shared co-receptor BAK1 displays a selective decrease in cluster density after PSK treatment. We found that the putative cell wall state sensor RLP44 is required for the observed changes, however the spatiotemporal dynamics of RLP44 are not altered during signaling. We propose a model of how cell walls are specifically tuned by BRI1- and PSKR1-centered signaling hubs as potential prerequisites for and during cell elongation initiation.