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

Abstract

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.

Arabidopsis pavement cell morphogenesis requires FERONIA binding to pectin for activation of ROP GTPase signaling

“…19,61 Finally, pectin binding to FER and other CrRLK1Ls appears to provide an important mechanism for Article sensing mechanical stress to feedback regulate cell growth, morphogenesis, and cell wall integrity maintenance in plants. 46,62 Therefore, the pectin-FER-ROP system may provide a paradigm for our understanding of how plant cells monitor the cell wall status and mechanical stresses to feedback regulate a plethora of important processes, such as cell expansion, cell shape formation, cell wall integrity maintenance, and stress responses.…”

“…Increasing studies show that FER, and other CrRLK1L family members, also participate in sensing and/or transducing the mechanical signals of either internal or external origin via their linkage with the structural cell wall components, such as pectin in Arabidopsis. 36,46,47,56,62 Coupling the sensing and signaling of extracellular matrices with mechanical sensing and signaling by a cell surface receptor is also common in animals and fungi. 67,68 In short, our findings here, together with recent studies showing CrRLK1Ls in RALF perception and their involvement in mechanical sensing and signaling, 35,36,45,47,56,63 suggest that FER and its relatives act as integrators of external signals.…”

Root Hairs Matter at Field Scale for Maize Shoot Growth and Nutrient Uptake, But Root Trait Plasticity is Primarily Triggered by Texture and Drought

“…Roots can show responses to touch or impermeable mechanical barriers by changes in cell division patterns, growth direction, cell differentiation and gene expression. Changes in pressure at the plant cell surface are signalled by mechanosensitive ion channels and kinases to the microtubule cytoskeleton, and lead to altered cytoskeletal architecture and reinforcement of the cell wall (Hamilton et al 2015;Tang et al 2021). Dupuy et al (2018) recently suggested re-visiting micromechanics of rooting development in soil by considering recent advances in granular matter physics.…”

Edge-based growth control inArabidopsisinvolves two cell wall-associated Receptor-Like Proteins

“…It has been reported that inhibition of ARF-GEF function can lead to reduced internalisation of PM-localised proteins through inhibition of endocytosis (Irani et al, 2012;Naramoto et al, 2010;Teh and Moore, 2007). We therefore hypothesised that secRFP:RLP4sΔECD undergo constitutive secretion, but are rapidly endocytosed under standard growth conditions and therefore do not accumulate at detectable levels at the PM The extracellular domain of RLP4s contains an MLD, a domain which is also found in RLKs of the CrRLK-L1 family, where it has been shown to bind pectins in vivo (Lin et al, 2022;Tang et al, 2022). To test whether RLP4s can also associate with the cell wall via their ECD, we expressed RLP4s variants that comprised solely of their ECD fused to RFP, while lacking their intracellular and transmembrane domains (pUBQ10::RLP4s-ECD:RFP).…”