Dual mechanisms give rise to biphasic stomatal opening in onion

Stomata are controllable micropores on the leaf surface that regulate gas exchange and water loss. Pore aperture adjustment is a mechanical process whereby changes in guard cell turgor drive changes in cell shape, resulting in stomatal opening or closure. Previous computational models of kidney-shaped stomata primarily relied on guard cells elongating upon turgor increase, a process dependent on cell wall properties, such as anisotropy in stiffness, strain-stiffening, and polar fixing. Finite element method simulations using experimentally derived 3D meshes from confocal imaging of Allium cepa (onion) suggest an alternative mechanism for opening that is largely due to changes in guard cell cross-sectional shape. This mechanism does not rely on the assumptions for cell wall parameters required in previous models based on idealised geometries. We propose that mechanical responsiveness of guard cells to turgor changes is determined by a combination of two processes: one dependent on shape and the other on wall material properties. This suggests the parameters governing guard cell dynamics can be viewed abstractly as a two-dimensional (shape and material properties) 'morphospace', allowing multiple routes of shape adaptation to optimise gas exchange.