A constraint–relaxation–recovery mechanism for stomatal dynamics. (26th May 2019)

• Record Type: Journal Article
• Authors: Jezek, Mareike; Hills, Adrian; Blatt, Michael R.; Lew, Virgilio L.
• Is Part Of: Plant, cell and environment. Volume 42:Number 8(2019)
• Page Start: 2399
• Page End: 2410
• Publication Date: 2019-05-26
• Subjects: Plant physiology -- Periodicals; Plant cells and tissues -- Periodicals; Plant communities -- Periodicals; 581.105
• DOI: 10.1111/pce.13568
• Languages: English
• ISSNs: 0140-7791

Abstract

Abstract: Models of guard cell dynamics, built on the OnGuard platform, have provided quantitative insights into stomatal function, demonstrating substantial predictive power. However, the kinetics of stomatal opening predicted by OnGuard models were threefold to fivefold slower than observed in vivo. No manipulations of parameters within physiological ranges yielded model kinetics substantially closer to these data, thus highlighting a missing component in model construction. One well‐documented process influencing stomata is the constraining effect of the surrounding epidermal cells on guard cell volume and stomatal aperture. Here, we introduce a mechanism to describe this effect in OnGuard2 constructed around solute release and a decline in turgor of the surrounding cells and its subsequent recovery during stomatal opening. The results show that this constraint–relaxation–recovery mechanism in OnGuard2 yields dynamics that are consistent with experimental observations in wild‐type Arabidopsis, and it predicts the altered opening kinetics of ost2 H + ‐ATPase and slac1 Cl − channel mutants. Thus, incorporating solute flux of the surrounding cells implicitly through their constraint on guard cell expansion provides a satisfactory representation of stomatal kinetics, and it predicts a substantial and dynamic role for solute flux across the apoplastic space between the guard cells and surrounding cells in accelerating stomatal kinetics. Abstract : Models of stomatal function build on the OnGuard platform and our deep knowledge of guard cell transport and metabolism have provided quantitative insights into stomatal function. However, the kinetics of stomatal opening predicted by OnGuard models have consistently failed to match the accelerated opening observed in vivo, thus highlighting a missing component in model construction. Incorporating explicitly a solute flux‐based mechanism of constraint relaxation and recovery between cells surrounding the stoma and the stomatal guard cells accommodates the accelerated stomatal opening kinetics observed in vivo and accurately predicts the slowed kinetics of stomatal opening in guard cell transport mutants.