The Plasma Membrane-An Integrating Compartment for Mechano-Signaling

Abstract

Plants are able to sense their mechanical environment. This mechanical signal is used by the plant to determine its phenotypic features. This is true also at a smaller scale. Morphogenesis, both at the cell and tissue level, involves mechanical signals that influence specific patterns of gene expression and trigger signaling pathways. How a mechanical stress is perceived and how this signal is transduced into the cell remains a challenging question in the plant community. Among the structural components of plant cells, the plasma membrane has received very little attention. Yet, its position at the interface between the cell wall and the interior of the cell makes it a key factor at the nexus between biochemical and mechanical cues. So far, most of the key players that are described to perceive and maintain mechanical cell status and to respond to a mechanical stress are localized at or close to the plasma membrane. In this review, we will focus on the importance of the plasma membrane in mechano-sensing and try to illustrate how the composition of this dynamic compartment is involved in the regulatory processes of a cell to respond to mechanical stress.

Keywords: Arabidopsis; cell wall integrity; mechanical stress; mechanosensitive signaling pathways; plasma membrane; receptor-like kinase.

Figure 1

A putative network for plasma membrane derived signaling molecules.

Figure 2

Role of the plasma membrane in mechano-sensing. Mechanical stress can modify the composition and/or organization of the cell wall. This may be perceived by transmembrane receptor kinases such as FERONIA (FER), THESEUS1 (THE1), WALL-ASSOCIATED KINASE (WAK) and FEI1 - FEI2 receptor-like kinases. Localization of FER in membrane domains may be done thanks to the interaction with LLG1, a glycosyl-phosphatidylinositol-anchored protein synthetized in the endoplasmic reticulum and localized in membrane domains in the Golgi. Selective opening of stretch-activated channels can open when a mechanical tension is pulling them (this implies they have to be anchored outside and/or outside the cell by an unknown mechanism represented by a spring) or by a modification of the membrane tension, that may be regulated by the membrane curvature and a specific lipid composition of the plasma membrane. Another hypothesis is that long decoration present in complex lipids such as Glycosyl Inositol Phospho Ceramides (GIPC) that can be formed by up to 14 sugars will interact with the cell wall and create a physical link between the lipid bilayer and the cell wall. Turgor pressure may potentially be perceived by ARABIDOPSIS HISTIDINE KINASEs (AHK) 1. Channel opening leads to an increase of calcium concentration ([Ca²⁺]) that activates respiratory burst oxidase homologues (RBOH) that will produce reactive oxygen species (ROS). Ca²⁺ is also needed for PIN1 relocalization in response to mechanical stress. Accumulation at the plasma membrane of RHO OF PLANT (ROP) 6 is activated by ROP-GEF that interacted with FER. ROP6 localization into membrane domains is driven by positive stretch that interact with the negatively charged signaling lipids. ROP6 can activate ROP-interactive CRIB motif-containing protein 1 (RIC1) and promotes KATANIN1 (KTN1) dependent parallel ordering of cMT. Cellulose synthase interactive protein 1 (CSI1) acts as a linker protein between CESA complexes and microtubules. Plasma membrane localization of the CESA and PINs is at least partially regulated by actin cytoskeleton.