Mechano-transduction via the pectin-FERONIA complex activates ROP6 GTPase signaling in Arabidopsis pavement cell morphogenesis

During growth and morphogenesis, plant cells respond to mechanical stresses resulting from spatiotemporal changes in the cell wall that bear high internal turgor pressure. Microtubule (MT) arrays are reorganized to align in the direction of maximal tensile stress, presumably reinforcing the local cell wall by guiding the synthesis of cellulose. However, how mechanical forces regulate MT reorganization remains largely unknown. Here, we demonstrate that mechanical signaling that is based on the Catharanthus roseus RLK1-like kinase (CrRLK1L) subfamily receptor kinase FERONIA (FER) regulates the reorganization of cortical MT in cotyledon epidermal pavement cells (PCs) in Arabidopsis. Recessive mutations in FER compromised MT responses to mechanical perturbations, such as single-cell ablation, compression, and isoxaben treatment, in these PCs. These perturbations promoted the activation of ROP6 guanosine triphosphatase (GTPase) that acts directly downstream of FER. Furthermore, defects in the ROP6 signaling pathway negated the reorganization of cortical MTs induced by these stresses. Finally, reduction in highly demethylesterified pectin, which binds the extracellular malectin domains of FER and is required for FER-mediated ROP6 activation, also impacted mechanical induction of cortical MT reorganization. Taken together, our results suggest that the FER-pectin complex senses and/or transduces mechanical forces to regulate MT organization through activating the ROP6 signaling pathway in Arabidopsis.

Automated summary

Mechanical signaling, based on the FER kinase, regulates cortical MT reorganization in Arabidopsis. FER mutations impair cell response to mechanical perturbations and ROP6 activation. Reduction in pectin content also impacts mechanical induction of MT reorganization.