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)

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, Dr 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 > School of Molecular Biosciences
• 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