Life behind the wall: sensing mechanical cues in plants

Abstract

There is increasing evidence that all cells sense mechanical forces in order to perform their functions. In animals, mechanotransduction has been studied during the establishment of cell polarity, fate, and division in single cells, and increasingly is studied in the context of a multicellular tissue. What about plant systems? Our goal in this review is to summarize what is known about the perception of mechanical cues in plants, and to provide a brief comparison with animals.

Fig. 1.

Plants are pre-stressed structures and, in turn, plant cells respond to mechanical cues. a Pre-stressed structures are more resilient to mechanical fluctuations and are also energy efficient: a suspension bridge, in which beams are under compression and threads under tension, provides a response to the weak ability of concrete to resist compression, while better allowing swinging and dilatation than an arched bridge. A balloon, with an envelope under tension and a gas under compression, is a pre-stressed structure. When exhibiting a cylindrical shape, such an inflated balloon would display an anisotropic stress pattern, with tension being twice as high in the circumferential direction as in the axial direction. b The epidermis of plant aerial organs is under tension, while inner tissues are under compression. Therefore, in the cylindrical stem, tensile stress is predicted to be twice higher transversely than axially. At the apex of the stem, the hemispherical shape of shoot meristem prescribes isotropic tensile stress patterns. Local mechanical conflicts thus arise from cell shape or local differences in growth between adjacent cells. c At the shoot apical meristem, as cells are advected away from the meristem center, cells become exposed to varying degrees and direction of mechanical stresses; in turn, such cues can affect cell division plane orientation, gene expression (for example, STM expression in green) or cell polarity (for example, PIN1 recruitment to the plasma membrane in red)

Fig. 2.

Families of likely plant mechanosensitive ion channels. From left to right: MscS-like (MSL), Mid1-Complementing Activity (MCA), Two Pore Potassium (TPK), Reduced hyperosmolality-induced [Ca²⁺] increase (OSCA), and Piezo channel families, with their proposed primary ion permeability. The presence of homologs in bacterial, plant, and/or animal genomes is indicated with a checkmark. The predominant ion flux is shown for each channel, but for simplicity no directionality nor specificity is shown

Fig. 3.

Mechanoreceptors can operate at several distinct scales. a Mechanosensitive ion channels provide a clever mechanism to transduce physical force (in the form of lateral membrane tension, red arrows) into a change in cellular state (in the form of ion flux). b Trichomes, uniquely shaped cells of the plant leaf and stem epidermis, serve as cellular mechanoreceptors by focusing force applied anywhere along the length (red arrows) into a buckling movement only at the base (shown in purple). c Utricularia suction traps may be triggered through a purely mechanical mechanism that relies on a biomechanically bistable structure. Displacement of hairs on the trapdoor leads to rapid opening and closing (not shown) of the trapdoor and any nearby prey is aspirated into the trap