Unexpected connections between humidity and ion transport discovered using a model to bridge guard cell-to-leaf scales

Wang, Y., Hills, A., Vialet-Chabrand, S., Papanatsiou, M., Griffiths, H., Rogers, S. , Lawson, T., Lew, V. L. and Blatt, M. R. (2017) Unexpected connections between humidity and ion transport discovered using a model to bridge guard cell-to-leaf scales. Plant Cell, 29(11), pp. 2921-2939. (doi:10.1105/tpc.17.00694) (PMID:29093213)

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Abstract

Stomatal movements depend on the transport and metabolism of osmotic solutes that drive reversible changes in guard cell volume and turgor. These processes are defined by a deep knowledge of the identities of the key transporters and of their biophysical and regulatory properties, and have been modelled successfully with quantitative kinetic detail at the cellular level. Transpiration of the leaf and canopy, by contrast, is described by quasi-linear, empirical relations for the inputs of atmospheric humidity, CO2, and light, but without connection to guard cell mechanics. Until now, no framework has been available to bridge this gap and provide an understanding of their connections. Here we introduce OnGuard2, a quantitative systems platform that utilizes the molecular mechanics of ion transport, metabolism and signalling of the guard cell to define the water relations and transpiration of the leaf. We show that OnGuard2 faithfully reproduces the kinetics of stomatal conductance in Arabidopsis, its dependence on vapor pressure difference (VPD) and on water feed to the leaf. OnGuard2 also predicted with VPD unexpected alterations in K+ channel activities, and changes in stomatal conductance of the slac1 Cl- channel and ost2 H+-ATPase mutants which we verified experimentally. OnGuard2 thus bridges the micro-macro divide, offering a powerful tool with which to explore the links between guard cell homeostasis, stomatal dynamics and foliar transpiration.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Papanatsiou, Miss Maria and Hills, Mr Adrian and Blatt, Professor Michael and Rogers, Dr Simon and Wang, Dr Yizhou
Authors: Wang, Y., Hills, A., Vialet-Chabrand, S., Papanatsiou, M., 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
College of Science and Engineering > School of Computing Science
Journal Name:Plant Cell
Publisher:American Society of Plant Biologists
ISSN:1040-4651
ISSN (Online):1532-298X
Published Online:01 November 2017
Copyright Holders:Copyright © 2017 American Society of Plant Biologists
First Published:First published in Plant Cell 29(11):2921-2939
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