A constraint-relaxation-recovery mechanism for stomatal dynamics

Jezek, M., Hills, A., Blatt, M. R. and Lew, V. L. (2020) A constraint-relaxation-recovery mechanism for stomatal dynamics. Plant, Cell and Environment, 42(8), pp. 2399-2410. (doi: 10.1111/pce.13568) (PMID:31032976) (PMCID:PMC6771799)

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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.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Hills, Mr Adrian and Jezek, Mareike and Blatt, Professor Michael
Authors: Jezek, M., Hills, A., Blatt, M. R., and Lew, V. L.
College/School:College of Medical Veterinary and Life Sciences > Institute of Molecular Cell and Systems Biology
Journal Name:Plant, Cell and Environment
Publisher:Wiley
ISSN:0140-7791
ISSN (Online):1365-3040
Published Online:29 April 2019
Copyright Holders:Copyright © 2019 The Authors
First Published:First published in Plant, Cell and Environment 42(8):2399-2410
Publisher Policy:Reproduced under a Creative Commons License

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
650621Developing a synthetic approach to manipulating guard cell membrane transport and stomatal controlMichael BlattBiotechnology and Biological Sciences Research Council (BBSRC)BB/L019205/1RI MOLECULAR CELL & SYSTEMS BIOLOGY
656891Analysing GORK clustering for enhanced stomatal controlMichael BlattBiotechnology and Biological Sciences Research Council (BBSRC)BB/M001601/1RI MOLECULAR CELL & SYSTEMS BIOLOGY
626121Stomatal-based systems analysis of water use efficiencyMichael BlattBiotechnology and Biological Sciences Research Council (BBSRC)BB/L001276/1RI MOLECULAR CELL & SYSTEMS BIOLOGY