Systems dynamic modelling of a guard cell Cl− channel mutant uncovers an emergent homeostatic network regulating stomatal transpiration
by Wang Y., Papanatsiou M., Eisenach C., Karnik R., Williams M., Hills A., Lew V. L., Blatt M. R. (2012)
- Yizhou Wang,
- Maria Papanatsiou,
- Cornelia Eisenach,
- Rucha Karnik,
- Mary Williams,
- Adrian Hills,
- Virgilio L. Lew
- Michael R. Blatt
Laboratory of Plant Physiology and Biophysics, Institute of Molecular, Cell, and Systems Biology, University of Glasgow, Glasgow G12 8QQ, United Kingdom (Y.W., M.P., C.E., R.K., M.W., A.H., M.R.B.); American Society of Plant Biologists, Rockville, Maryland 20855 (M.W.); and Physiological Laboratory, University of Cambridge, Cambridge CB2 3EG, United Kingdom (V.L.L.)
in Plant Physiol, 160 (2012), pp. 1956–1972. – doi: http://dx.doi.org/10.1104/pp.112.207704 –
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.