A computational approach for inferring the cell wall properties that govern guard cell dynamics. (23rd August 2017)

• Record Type: Journal Article
• Authors: Woolfenden, Hugh C.; Bourdais, Gildas; Kopischke, Michaela; Miedes, Eva; Molina, Antonio; Robatzek, Silke; Morris, Richard J.
• Is Part Of: Plant journal. Volume 92:Number 1(2017)
• Page Start: 5
• Page End: 18
• Publication Date: 2017-08-23
• Subjects: guard cells -- cell wall -- computational modelling -- biomechanics -- stomata -- Vicia faba -- Arabidopsis thaliana; Plant molecular biology -- Periodicals; Plant cells and tissues -- Periodicals; Botany -- Periodicals; 580
• DOI: 10.1111/tpj.13640
• Languages: English
• ISSNs: 0960-7412

Abstract

Significance Statement: We describe a computational approach for investigating guard cell dynamics, focusing on the link between turgor pressure, geometry and the material properties of the cell walls. Our results show that radially‐arranged fibers are critical for stomatal opening and that the cell wall matrix stiffens as turgor rises. Summary: Guard 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.