A computational approach for inferring the cell wall properties that govern guard cell dynamics

Abstract

SummaryGuard cells dynamically adjust their shape in order to regulate photosynthetic gas exchange, respiration rates and defend against pathogen entry. Cell shape changes are determined by the interplay of cell wall material properties and turgor pressure. To investigate this relationship between turgor pressure, cell wall properties and cell shape, we focused on kidney‐shaped stomata and developed a biomechanical model of a guard cell pair. Treating the cell wall as a composite of the pectin‐rich cell wall matrix embedded with cellulose microfibrils, we show that strong, circumferentially oriented fibres are critical for opening. We find that the opening dynamics are dictated by the mechanical stress response of the cell wall matrix, and as the turgor rises, the pectinaceous matrix stiffens. We validate these predictions with stomatal opening experiments in selected Arabidopsis cell wall mutants. Thus, using a computational framework that combines a 3D biomechanical model with parameter optimization, we demonstrate how to exploit subtle shape changes to infer cell wall material properties. Our findings reveal that proper stomatal dynamics are built on two key properties of the cell wall, namely anisotropy in the form of hoop reinforcement and strain stiffening.

Finite Element Modeling of Shape Changes in Plant Cells

“…This would entail an initial turgor-induced change in geometry from elliptical to circular (inflation), followed by an accommodation of any further increase in pressure by cell wall stretching, a process that requires higher turgor differentials to produce visible results. Therefore, the matrix strain-stiffening conjecture proffered by Woolfenden et al (2017), while consistent with polymer chemistry (Bidhendi and Geitmann, 2016), could be a secondary mechanism responsible for the apparent low sensitivity of aperture opening at high pressures. These concepts certainly merit further validation.…”

“…The role of cellulose orientation and cell wall anisotropy was reassessed in a recent study by Woolfenden et al (2017), who used nonlinear elasticity with a transversely isotropic material behavior to represent the guard cell wall, similar to studies by Cooke et al (1976). The authors observed that, using isotropic material properties, increasing the turgor pressure causes the stomatal pore to close rather than open.…”

“…The further increase in cell volume is attributed to stretching of the cell wall accompanied by its thinning and expansion at the poles (Sharpe and Wu, 1978). How the swelling of the two guard cells, their specific design, and their wall mechanics enable pore opening has been the subject of multiple studies with somewhat antithetical outcomes (DeMichele and Sharpe, 1973;Raschke, 1975;Cooke et al, 1976Cooke et al, , 2008Sharpe and Wu, 1978;Amsbury et al, 2016;Carter et al, 2017;Woolfenden et al, 2017). Several cell features have been hypothesized to be critical for pore opening when guard cell pressure rises: (1) the increased thickness of the ventral walls of guard cells (Fig.…”

“…5A). While Woolfenden et al (2017) did simulate this situation as well, they stated that, at higher 'correct' pressures, the pore closes in the absence of anisotropic properties. The study does not explicitly state a caveat that cannot be neglected, however.…”

“…This led Woolfenden et al (2017) to conclude that a strain stiffening must occur in the cell wall matrix. While this explanation is reasonable, it may not be the only one.…”