Systems dynamic modeling of a guard cell Cl- channel mutant uncovers an emergent homeostatic network regulating stomatal transpiration

Wang, Y., Papanatsiou, M., Eisenach, C., Karnik, R., Williams, M., Hills, A., Lew, V.L. and Blatt, M.R. (2012) Systems dynamic modeling of a guard cell Cl- channel mutant uncovers an emergent homeostatic network regulating stomatal transpiration. Plant Physiology, 160(4), pp. 1956-1967. (doi:10.1104/pp.112.207704)

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Abstract

Stomata account for much of the 70% of global water usage associated with agriculture and have a profound impact on the water and carbon cycles of the world. Stomata have long been modeled mathematically, but until now, no systems analysis of a plant cell has yielded detail sufficient to guide phenotypic and mutational analysis. Here, we demonstrate the predictive power of a systems dynamic model in Arabidopsis (Arabidopsis thaliana) to explain the paradoxical suppression of channels that facilitate K+ uptake, slowing stomatal opening, by mutation of the SLAC1 anion channel, which mediates solute loss for closure. The model showed how anion accumulation in the mutant suppressed the H+ load on the cytosol and promoted Ca2+ influx to elevate cytosolic pH (pHi) and free cytosolic Ca2+ concentration ([Ca2+]i), in turn regulating the K+ channels. We have confirmed these predictions, measuring pHi and [Ca2+]i in vivo, and report that experimental manipulation of pHi and [Ca2+]i is sufficient to recover K+ channel activities and accelerate stomatal opening in the slac1 mutant. Thus, we uncover a previously unrecognized signaling network that ameliorates the effects of the slac1 mutant on transpiration by regulating the K+ channels. Additionally, these findings underscore the importance of H+-coupled anion transport for pHi homeostasis.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Hills, Mr Adrian and Blatt, Professor Michael and Karnik, Dr Rucha and Williams, Professor Mary and Papanatsiou, Miss Maria and Eisenach, Ms Cornelia
Authors: Wang, Y., Papanatsiou, M., Eisenach, C., Karnik, R., Williams, M., Hills, A., Lew, V.L., and Blatt, M.R.
College/School:College of Medical Veterinary and Life Sciences
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
Published Online:01 October 2012
Copyright Holders:Copyright © 2012 American Society of Plant Biologists
First Published:First published in Plant Physiology 160(4):1956-1967
Publisher Policy:Reproduced in accordance with the copyright policy of the publisher

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