The stomatal flexoskeleton: how the biomechanics of guard cell walls animate an elastic pressure vessel

Abstract

In plants, stomatal guard cells are one of the most dynamic cell types, rapidly changing their shape and size in response to environmental and intrinsic signals to control gas exchange at the plant surface. Quantitative and systematic knowledge of the biomechanical underpinnings of stomatal dynamics will enable strategies to optimize stomatal responsiveness and improve plant productivity by enhancing the efficiency of photosynthesis and water use. Recent developments in microscopy, mechanical measurements, and computational modeling have revealed new insights into the biomechanics of stomatal regulation and the genetic, biochemical, and structural origins of how plants achieve rapid and reliable stomatal function by tuning the mechanical properties of their guard cell walls. This review compares historical and recent experimental and modeling studies of the biomechanics of stomatal complexes, highlighting commonalities and contrasts between older and newer studies. Key gaps in our understanding of stomatal functionality are also presented, along with assessments of potential methods that could bridge those gaps.

Cellular Heterogeneity in Pressure and Growth Emerges from Tissue Topology and Geometry

“…To test our predictions and deduce pressure in the SAM, we combined a recently developed indentation-based approach [41] with FEM-based realistic mechanical models of indentation [47]. We found values of turgor in the 1-3 MPa range, higher than the range 0.2-1 MPa typically measured in plant tissues [19], though values of up to 5 MPa were measured in guard cells [58]. For instance, the Arabidopsis root epidermis has a turgor of about 0.4 MPa, as measured with the pressure probe [59]; the Arabidopsis leaf epidermis has a turgor of about 1 to 2 MPa, as deduced from indentation and mechanical modeling [60].…”

COBL7 is required for stomatal formation via regulation of cellulose deposition in Arabidopsis

“…The initiation of stomatal pore formation is facilitated by the degradation of pectin, especially the HG, and inhibiting HG de‐methyl‐esterification delays pore initiation, whereas pore size is attributed to both pectin chemistry and GC pressurization (Amsbury et al ., 2016; Carter et al ., 2017; Rui et al ., 2017, 2019; Yi et al ., 2019). These studies not only represent a huge leap forward in understanding stomatal biology, as they experimentally confirmed the importance of the enzymatic breakdown of middle lamella pectin during stomatal pore formation, but also brought the importance of GC ventral wall modifications that give rise to the structural basis of maintaining cell wall integrity (and/or containing the mechanical forces) during pore initiation and enlargement driven by GC pressurization into the forefront again.…”

Plant biomechanics in the 21st century

“…Their controlled swelling and relaxation regulate the gas exchange between the internal leaf tissues and the outside, and thus influence photosynthesis, respiration, and transpiration. How the architecture and mechanical properties of individual guard cells ensure efficiency in this motor function is elaborated in detail by Yi et al (2019).…”