The Role of Mechanoperception in Plant Cell Wall Integrity Maintenance

Abstract

The plant cell walls surrounding all plant cells are highly dynamic structures, which change their composition and organization in response to chemical and physical stimuli originating both in the environment and in plants themselves. They are intricately involved in all interactions between plants and their environment while also providing adaptive structural support during plant growth and development. A key mechanism contributing to these adaptive changes is the cell wall integrity (CWI) maintenance mechanism. It monitors and maintains the functional integrity of cell walls by initiating adaptive changes in cellular and cell wall metabolism. Despite its importance, both our understanding of its mode of action and knowledge regarding the molecular components that form it are limited. Intriguingly, the available evidence implicates mechanosensing in the mechanism. Here, we provide an overview of the knowledge available regarding the molecular mechanisms involved in and discuss how mechanoperception and signal transduction may contribute to plant CWI maintenance.

Keywords: cell wall; cell wall integrity; mechanoperception; mechanosensing; plant defense; plant environment interaction.

Figure 1

Comparison between cell wall integrity (CWI) maintenance mechanisms in (A) Saccharomyces cerevisiae and (B) Arabidopsis thaliana. In both organisms, mechanosensitive ion channels and receptors trigger signal transduction processes involving Ca²⁺ influx into the cytoplasm and the activation of cascades including calcium-dependent protein kinases (CDPKs), guanosine nucleotide exchange factors (GEFs) and mitogen-activated protein kinases (MAPKs) that eventually activate transcription factors. In A. thaliana, the processes are regulated in a more intricate manner, exemplified by the complex interconnected networks regulated by jasmonic acid (JA), salicylic acid (SA), and abscisic acid (ABA). The processes enable the regulation of gene expression in a tightly controlled and highly adaptive manner, allowing specific changes in cell wall and cellular metabolism to maintain cell wall integrity. Arrows are connecting elements belonging to the same pathway. ROS: reactive oxygen species; PTI: PAMP-triggered immunity; CRD: cysteine-rich domain; NGN: N-glycosilated asparagine; TM: transmembrane domain; GPI: glycosylphosphatidylinositol; STR: serine-/threonine-rich; STE: signal transduction element; LRR: leucine-rich repeat domain; LysM: lysin-motif-containing ectodomain; RALF: rapid alkalinization factor peptide; OGs: oligogalacturonides; TF: transcription factor; EGF-like: epidermal-growth-factor-like ectodomain.

Figure 2

Different stimuli could indicate alterations in cell wall integrity (CWI) in Arabidopsis thaliana, and are perceived through different signaling pathways. (A) Release of cell wall fragments, also known as damage-associated molecular patterns (DAMPs), is interpreted by the plant as the result of cell wall damage (CWD) that can derive from biotic and abiotic stresses as well as endogenous processes. DAMP perception by pattern-recognition receptors activates typical immunity responses including increases in cytoplasmic [Ca²⁺], phosphorylation of mitogen-activated protein kinases (MAPKs), production of jasmonic acid(JA)/salicylic acid (SA), reactive oxygen species (ROS), and lignin, and callose deposition. (B) Distortion of the cell wall–plasma membrane continuum occurs in response to plasma membrane shrinkage during hyperosmotic stress (drought). Mechanosensitive ion channels mediate Ca²⁺ influx into the cytoplasm, leading to the activation of signal transduction pathways. Moreover, interactions between abscisic acid (ABA) and FER modulate growth in response to the state of turgor pressure. (C) If the plasma membrane is stretched, either by a weakened cell wall or as result of hypoosmotic stress, mechanosensitive ion channels are activated and [Ca²⁺] in the cytoplasm is increased. Several of these channels are also required for the production of ROS. Moreover, THE1-mediated signaling modulates CWD-induced lignin and JA/SA production, and together with FER leads to growth arrest until CWI is recovered. The pathways in A, B, and C eventually lead to a series of changes in cell wall composition and cellular metabolism, enabling the plant to maintain CWI in response to different challenges.