Architecture and functions of stomatal cell walls in eudicots and grasses

Abstract

Background: Like all plant cells, the guard cells of stomatal complexes are encased in cell walls that are composed of diverse, interacting networks of polysaccharide polymers. The properties of these cell walls underpin the dynamic deformations that occur in guard cells as they expand and contract to drive the opening and closing of the stomatal pore, the regulation of which is crucial for photosynthesis and water transport in plants.

Scope: Our understanding of how cell wall mechanics are influenced by the nanoscale assembly of cell wall polymers in guard cell walls, how this architecture changes over stomatal development, maturation and ageing and how the cell walls of stomatal guard cells might be tuned to optimize stomatal responses to dynamic environmental stimuli is still in its infancy.

Conclusion: In this review, we discuss advances in our ability to probe experimentally and to model the structure and dynamics of guard cell walls quantitatively across a range of plant species, highlighting new ideas and exciting opportunities for further research into these actively moving plant cells.

Keywords: Arabidopsis thaliana; Brachypodium distachyon; biomechanics; cellulose; guard cells; hemicellulose; pectin; plant cell wall; stomatal complex.

Fig. 1.

Differentiation and maturation of eudicot and grass stomatal complexes. In eudicots, e.g. Arabidopsis thaliana, a guard mother cell (left panel) divides symmetrically to give rise to two young kidney-shaped guard cells that separate in the middle to form the stomatal pore. Young stomatal complexes then grow and elongate to form mature complexes. Young and mature stomatal complexes can respond to opening and closing cues such as light and dark, respectively. In grasses, e.g. Brachypodium distachyon, the rectangular guard mother cell is flanked by two subsidiary cells (right panel). The guard mother cell divides symmetrically to give rise to two young guard cells and form a young stomatal complex. After pore formation and maturation via elongation of guard and subsidiary cells, the mature stomatal complex becomes responsive to environmental stimuli such as light and dark conditions.

Fig. 2.

Models of the dynamics of cellulose and pectin organization during stomatal function in kidney-shaped and dumbbell-shaped guard cells. In kidney-shaped guard cells, such as those of Arabidopsis thaliana, cellulose wraps around the circumference of the cell. In response to pore-closing stimuli (e.g. dark), cellulose forms bundles. Conversely, in response to an opening stimulus (e.g. light), cellulose bundles separate to allow for the guard cell elongation. The poles of kidney-shaped guard cells are rich in low-methyl-esterified pectin that provides stiffness to pin down and constrain the overall elongation of the complex, leading to the lateral bending of the guard cells and the opening of the pore. Stomatal complexes of grasses, such as Brachypodium distachyon, contain dumbbell-shaped guard cells that are flanked by two subsidiary cells. In opening conditions, guard cells expand asymmetrically at the ventral wall, leading to the bulbous end bulging and opening the pore (Gkolemis et al., 2023). We hypothesize that, in response to opening conditions (e.g. light), in which subsidiary cells compress to accommodate the guard cells, longitudinally arranged cellulose in subsidiary cells coalesces to form bundles; conversely, in response to closing conditions (e.g. dark), cellulose bundles separate to allow for subsidiary cell expansion and closing of the pore. We also hypothesize that longitudinally arranged cellulose in the central canal of the dumbbell-shaped guard cells, which is rich in low-methyl-esterified pectin, might not undergo reorganization owing to the stiffness of this region.

Fig. 3.

Cell wall architecture in kidney-shaped guard cells of Arabidopsis thaliana. In coronal (top row) and transverse (middle row) cross-sections of kidney-shaped guard cells of A. thaliana, low-methyl-esterified pectin is present at the poles and the ventral walls, whereas high-methyl-esterified pectin is evenly distributed at the dorsal wall. Cellulose is circumferentially arranged, and the hemicellulose, xyloglucan, occupies the ventral wall. A close-up model of the cell wall (lower panel) shows crosslinking of circumferentially arranged cellulose by xyloglucan and its spacing via pectin.