An optimal frequency in Ca2+ oscillations for stomatal closure is an emergent property of ion transport in guard cells

Minguet-Parramona, C., Wang, Y., Hills, A., Vialet-Chabrand, S., Griffiths, H., Rogers, S., Lawson, T., Lew, V. L. and Blatt, M. R. (2016) An optimal frequency in Ca2+ oscillations for stomatal closure is an emergent property of ion transport in guard cells. Plant Physiology, 170(1), pp. 33-42. (doi:10.1104/pp.15.01607) (PMID:26628748) (PMCID:PMC4704601)

[img]
Preview
Text
121182.pdf - Published Version
Available under License Creative Commons Attribution.

755kB

Abstract

Oscillations in cytosolic-free Ca2+ concentration ([Ca2+]i) have been proposed to encode information that controls stomatal closure. [Ca2+]i oscillations with a period near 10 min were previously shown to be optimal for stomatal closure in Arabidopsis (Arabidopsis thaliana), but the studies offered no insight into their origins or mechanisms of encoding to validate a role in signaling. We have used a proven systems modeling platform to investigate these [Ca2+]i oscillations and analyze their origins in guard cell homeostasis and membrane transport. The model faithfully reproduced differences in stomatal closure as a function of oscillation frequency with an optimum period near 10 min under standard conditions. Analysis showed that this optimum was one of a range of frequencies that accelerated closure, each arising from a balance of transport and the prevailing ion gradients across the plasma membrane and tonoplast. These interactions emerge from the experimentally derived kinetics encoded in the model for each of the relevant transporters, without the need of any additional signaling component. The resulting frequencies are of sufficient duration to permit substantial changes in [Ca2+]i and, with the accompanying oscillations in voltage, drive the K+ and anion efflux for stomatal closure. Thus, the frequency optima arise from emergent interactions of transport across the membrane system of the guard cell. Rather than encoding information for ion flux, these oscillations are a by-product of the transport activities that determine stomatal aperture.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Hills, Mr Adrian and Blatt, Professor Michael and Minguet, Miss Carla and Wang, Dr Yizhou
Authors: Minguet-Parramona, C., Wang, Y., Hills, A., Vialet-Chabrand, S., Griffiths, H., Rogers, S., Lawson, T., Lew, V. L., and Blatt, M. R.
College/School:College of Medical Veterinary and Life Sciences > Institute of Molecular Cell and Systems Biology
Journal Name:Plant Physiology
Publisher:American Society of Plant Biologists
ISSN:0032-0889
ISSN (Online):1532-2548
Published Online:01 December 2015
Copyright Holders:Copyright © 2016 The Authors
First Published:First published in Plant Physiology 170(1):33-42
Publisher Policy:Reproduced under a creative commons license

University Staff: Request a correction | Enlighten Editors: Update this record

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