Rhamnogalacturonan-II dimerization deficiency impairs the coordination between growth and adhesion maintenance in plants

Abstract

Cell adhesion is a fundamental feature of multicellular organisms. In plants, cell adhesion is mediated by the cell wall, but the control and maintenance of cell adhesion during growth and development remains poorly understood. Here we uncover the role of a component of the cell wall, rhamnogalacturonan-II (RG-II) and its capacity to crosslink in the presence of Boron, as a key regulator of plant cell adhesion maintenance. We show that RG-II dimerization deficiency leads to cell adhesion defects. Importantly, the analysis of mur1 mutants with RG-II dimerization defects uncovers a cell adhesion pathway that is distinct from that identified by the analysis of pectin deficient mutants. We found that mutations in two cell wall integrity sensors, RESISTANCE TO FUSARIUM OXYSPORUM 1 and RECEPTOR-LIKE PROTEIN 44, as well as supplementation with the hormone brassinosteroid can partially rescue the adhesion defects associated with RG-II dimerization deficiency. We also show that adhesion defects associated with RG-II dimerization deficiency are related to increased epidermal tension as well as decreased homogalacturonan levels in the cell wall, which can also be rescued by supplementation with brassinosteroid. Overall, we propose that RG-II dimerization defects alter cell adhesion directly (reduced crosslinks) but also indirectly through cell wall integrity sensing, brassinosteroid signalling, cell wall remodelling and cell layer growth coordination. Thus, our results uncover the involvement of cell wall integrity sensors and hormonal signalling in the coordination between growth and adhesion maintenance in plants, which is a key feature for complex multicellularity.