Formation of the Stomatal Outer Cuticular Ledge Requires a Guard Cell Wall Proline-Rich Protein

Abstract

(K.S.); 0000-0002-6438-9188 (R.S.); 0000-0002-9703-0745 (A.J.F.); 0000-0001-9972-5156 (J.E.G.).Stomata are formed by a pair of guard cells which have thickened, elastic cell walls to withstand the large increases in turgor pressure that have to be generated to open the pore that they surround. We have characterized FOCL1, a guard cell-expressed, secreted protein with homology to Hyp-rich cell wall proteins. FOCL1-GFP localizes to the guard cell outer cuticular ledge and plants lacking FOCL1 produce stomata without a cuticular ledge. Instead the majority of stomatal pores are entirely covered over by a continuous fusion of the cuticle, and consequently plants have decreased levels of transpiration and display drought tolerance. The focl1 guard cells are larger and less able to reduce the aperture of their stomatal pore in response to closure signals suggesting that the flexibility of guard cell walls is impaired. FOCL1 is also expressed in lateral root initials where it aids lateral root emergence. We propose that FOCL1 acts in these highly specialized cells of the stomata and root to impart cell wall strength at high turgor and/or to facilitate interactions between the cell wall and the cuticle.

POLYGALACTURONASE INVOLVED IN EXPANSION3 Functions in Seedling Development, Rosette Growth, and Stomatal Dynamics in Arabidopsis thaliana

“…In summary, the data presented here provide new insights into how guard cell walls are constructed to confer their specific biomechanical properties and meet their functional requirements: Along with cellulose and xyloglucan, which help control the anisotropic expansion of guard cells (Rui and Anderson, 2016;Woolfenden et al, 2017), and structural glycoproteins, which also influence guard cell flexibility (Hunt et al, 2017), characterization of PGX3 highlights its key function as a pectinase in guard cell walls that regulates the dynamics of guard cells, allowing them to maintain high integrity and flexibility during stomatal movements in Arabidopsis. Further understanding of the synthesis, composition, architecture, modifications, and dynamics of guard cell walls will have promising applications across many fields, including the design of biomaterials with useful mechanical properties and the production of plants with desirable stomatal traits.…”

“…These cycles can occur many thousands of times over the lifetime of a plant. In dicots, guard cell walls contain cellulose, hemicelluloses, pectins, and structural glycoproteins (Amsbury et al, 2016;Hunt et al, 2017;Majewska-Sawka et al, 2002;Rui and Anderson, 2016), and they are differentially thickened around their circumference (Zhao and Sack, 1999). Cellulose and xyloglucan function in the assembly and structural anisotropy of guard cell walls and influence stomatal opening and closure (Rui and Anderson, 2016;Woolfenden et al, 2017).…”

Small Pores with a Big Impact

“…de Marcos et al (2017) uncover an unexpected interaction between brassinosteroid signaling and transcriptional control behind cell fates leading to stomatal development. Related articles that bridge the gap between the development of the stomatal cell wall and stomatal function Hunt et al, 2017) will also be of interest in this context.…”

The Cell Wall PAC (Proline-Rich, Arabinogalactan Proteins, Conserved Cysteines) Domain-Proteins Are Conserved in the Green Lineage

“…PRPL1 (Proline-Rich Protein-Like, At5g05500) has a trichoblast-specific expression and plays roles in root hair elongation, as shown by the reduction in length of root hairs in the prpl1 mutant [20]. Plants lacking FOCL1 (Fused Outer Cutiular Ledge 1, At2g16630) produce stomata without a cuticular ledge, and thus, focl1 mutants display drought tolerance [21]. AtAGP30 (At2g33790) is involved in root regeneration in vitro and in the timing of seed germination [13].…”