Plant cell mechanobiology: Greater than the sum of its parts

Abstract

The ability to sense and respond to physical forces is critical for the proper function of cells, tissues, and organisms across the evolutionary tree. Plants sense gravity, osmotic conditions, pathogen invasion, wind, and the presence of barriers in the soil, and dynamically integrate internal and external stimuli during every stage of growth and development. While the field of plant mechanobiology is growing, much is still poorly understood-including the interplay between mechanical and biochemical information at the single-cell level. In this review, we provide an overview of the mechanical properties of three main components of the plant cell and the mechanoperceptive pathways that link them, with an emphasis on areas of complexity and interaction. We discuss the concept of mechanical homeostasis, or "mechanostasis," and examine the ways in which cellular structures and pathways serve to maintain it. We argue that viewing mechanics and mechanotransduction as emergent properties of the plant cell can be a useful conceptual framework for synthesizing current knowledge and driving future research.

Figure 1

Restoration of cellular mechanostasis after hypo-osmotic swelling. Hypo-osmotic cell swelling is caused by an increase in turgor pressure (inner arrows), which disrupts the homeostatic balance between turgor and the cell wall. The cell could regain balance between turgor and cell wall stiffness by returning to its previous size through osmoregulation, by undergoing expansion, or by stiffening the cell wall to counter the increased turgor.

Figure 2

Activation through membrane flattening and potential signaling outputs of MS ion channels. Once opened by membrane tension, MS ion channels mediate ion movement according to their electrochemical gradient. Some MS channels allow Ca²⁺ to enter the cytoplasm from the apoplast which could serve as a secondary messenger for mechanotransduction signaling cascades. Other MS channels release anions which could theoretically depolarize the membrane and/or function in osmoregulation by reducing cytoplasmic ion concentrations. Nonselective MS channels conduct both cations and anions. Some channels may have nonconducing functions, such as interacting with and activating other signaling partners.

Figure 3

Possible activators and signaling outputs of RLKs. A, Expected changes in cell wall–PM proximity in response to mechanical signals. Some RLKs are required for responses to hypo-osmotic shock, indentation, and bending (FER) and to cell wall weakening (FER and THE1). They might respond to the altered distance between the PM and certain cell wall components during these manipulations, and/or the compression of the PM against the cell wall. Lowering turgor pressure using osmolytes, which would be predicted to relieve the PM compression or displacement that occurs when cell walls are impaired, suppresses RLK signaling. B, PM-localized CrRLK1Ls are hypothesized to be activated by cell wall mechanics through their interaction with cell wall components, although this is less well-understood than their activation by RALF peptide ligands. RALFs mediate the interaction of CrRLK1Ls with LORELEI-like glycophosphatidylinositol-anchored protein co-receptors (LLGs) and Leucine-Rich-Repeat Extensins (LRXs) (Mecchia et al., 2017; Xiao et al., 2019). Activated CrRLK1Ls promote apoplastic alkalinization (perhaps by inhibiting the activity of H⁺-ATPases), the opening of unknown Ca²⁺ channel(s), cytoplasmic kinase cascades, and ROPGEF signaling, which activates ROS production through NADPH oxidases and is thought to promote exocytosis of cell wall components (Zhou et al., 2021). CrRLK1L kinase activity is not required for all signaling outputs and may depend on the stimulus. Components are not drawn to scale.