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1. Stomatal opening efficiency is controlled by cell wall organization in Arabidopsis thaliana

   https://doi.org/10.1093/pnasnexus/pgad294  

   Keynia, Sedighe; Jaafar, Leila; Zhou, You; Anderson, Charles T; Turner, Joseph A (September 2023, PNAS Nexus)

   Bayer, Edward (Ed.)

   Abstract Stomatal function in plants is regulated by the nanoscale architecture of the cell wall and turgor pressure, which together control stomatal pore size to facilitate gas exchange and photosynthesis. The mechanical properties of the cell wall and cell geometry are critical determinants of stomatal dynamics. However, the specific biomechanical functions of wall constituents, for example, cellulose and pectins, and their impact on the work required to open or close the stomatal pore are unclear. Here, we use nanoindentation in normal and lateral directions, computational modeling, and microscopic imaging of cells from the model plant Arabidopsis thaliana to investigate the precise influences of wall architecture and turgor pressure on stomatal biomechanics. This approach allows us to quantify and compare the unique anisotropic properties of guard cells with normal composition, lower cellulose content, or alterations in pectin molecular weight. Using these data to calculate the work required to open the stomata reveals that the wild type, with a circumferential-to-longitudinal modulus ratio of 3:1, is the most energy-efficient of those studied. In addition, the tested genotypes displayed similar changes in their pore size despite large differences in wall thickness and biomechanical properties. These findings imply that homeostasis in stomatal function is maintained in the face of varying wall compositions and biomechanics by tuning wall thickness. 

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2. Protocol for mapping the variability in cell wall mechanical bending behavior in living leaf pavement cells

   https://doi.org/10.1093/plphys/kiab588  

   Li, Wenlong; Keynia, Sedighe; Belteton, Samuel A; Afshar-Hatam, Faezeh; Szymanski, Daniel B; Turner, Joseph A (December 2021, Plant Physiology)

   Abstract Mechanical properties, size and geometry of cells, and internal turgor pressure greatly influence cell morphogenesis. Computational models of cell growth require values for wall elastic modulus and turgor pressure, but very few experiments have been designed to validate the results using measurements that deform the entire thickness of the cell wall. New wall material is synthesized at the inner surface of the cell such that full-thickness deformations are needed to quantify relevant changes associated with cell development. Here, we present an integrated, experimental–computational approach to analyze quantitatively the variation of elastic bending behavior in the primary cell wall of living Arabidopsis (Arabidopsis thaliana) pavement cells and to measure turgor pressure within cells under different osmotic conditions. This approach used laser scanning confocal microscopy to measure the 3D geometry of single pavement cells and indentation experiments to probe the local mechanical responses across the periclinal wall. The experimental results were matched iteratively using a finite element model of the experiment to determine the local mechanical properties and turgor pressure. The resulting modulus distribution along the periclinal wall was nonuniform across the leaf cells studied. These results were consistent with the characteristics of plant cell walls which have a heterogeneous organization. The results and model allowed the magnitude and orientation of cell wall stress to be predicted quantitatively. The methods also serve as a reference for future work to analyze the morphogenetic behaviors of plant cells in terms of the heterogeneity and anisotropy of cell walls. 

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3. Architecture and functions of stomatal cell walls in eudicots and grasses

   https://doi.org/10.1093/aob/mcae078  

   Jaafar, Leila; Anderson, Charles_T (May 2024, Annals of Botany)

   Abstract BackgroundLike 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. ScopeOur 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. ConclusionIn 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. 

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4. Young guard cells function dynamically despite low mechanical anisotropy but gain efficiency during stomatal maturation in Arabidopsis thaliana

   https://doi.org/10.1111/tpj.16756  

   Jaafar, Leila; Chen, Yintong; Keynia, Sedighe; Turner, Joseph_A; Anderson, Charles_T (April 2024, The Plant Journal)

   SUMMARY Stomata are pores at the leaf surface that enable gas exchange and transpiration. The signaling pathways that regulate the differentiation of stomatal guard cells and the mechanisms of stomatal pore formation have been characterized inArabidopsis thaliana. However, the process by which stomatal complexes develop after pore formation into fully mature complexes is poorly understood. We tracked the morphogenesis of young stomatal complexes over time to establish characteristic geometric milestones along the path of stomatal maturation. Using 3D‐nanoindentation coupled with finite element modeling of young and mature stomata, we found that despite having thicker cell walls than young guard cells, mature guard cells are more energy efficient with respect to stomatal opening, potentially attributable to the increased mechanical anisotropy of their cell walls and smaller changes in turgor pressure between the closed and open states. Comparing geometric changes in young and mature guard cells of wild‐type and cellulose‐deficient plants revealed that although cellulose is required for normal stomatal maturation, mechanical anisotropy appears to be achieved by the collective influence of cellulose and additional wall components. Together, these data elucidate the dynamic geometric and biomechanical mechanisms underlying the development process of stomatal maturation. 

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5. Bottom-up multiscale modelling of guard cell walls reveals molecular mechanisms of stomatal biomechanics

   https://doi.org/10.1093/insilicoplants/diad017  

   Yi, Hojae; Anderson, Charles T (July 2023, in silico Plants)

   Zhu, Xin-Guang (Ed.)

   Abstract Stomata are dynamic pores on plant surfaces that regulate photosynthesis and are thus of critical importance for understanding and leveraging the carbon-capturing and food-producing capabilities of plants. However, our understanding of the molecular underpinnings of stomatal kinetics and the biomechanical properties of the cell walls of stomatal guard cells that enable their dynamic responses to environmental and intrinsic stimuli is limited. Here, we built multiscale models that simulate regions of the guard cell wall, representing cellulose fibrils and matrix polysaccharides as discrete, interacting units, and used these models to help explain how molecular changes in wall composition and underlying architecture alter guard wall biomechanics that gives rise to stomatal responses in mutants with altered wall synthesis and modification. These results point to strategies for engineering guard cell walls to enhance stomatal response times and efficiency. 

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