title: Systems dynamic modeling of a guard cell Cl- channel mutant uncovers an emergent homeostatic network regulating stomatal transpiration.
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 Ca(2+) influx to elevate cytosolic pH (pH(i)) and free cytosolic Ca(2+) concentration ([Ca(2+)](i)), in turn regulating the K(+) channels. We have confirmed these predictions, measuring pH(i) and [Ca(2+)](i) in vivo, and report that experimental manipulation of pH(i) and [Ca(2+)](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 pH(i) homeostasis.
authors.affiliation: Laboratory of Plant Physiology and Biophysics, Institute of Molecular, Cell, and Systems Biology, University of Glasgow, Glasgow G12 8QQ, United Kingdom.
authors.forename: Yizhou
authors.initials: Y
authors.lastname: Wang
authors.forename: Maria
authors.initials: M
authors.lastname: Papanatsiou
authors.forename: Cornelia
authors.initials: C
authors.lastname: Eisenach
authors.forename: Rucha
authors.initials: R
authors.lastname: Karnik
authors.forename: Mary
authors.initials: M
authors.lastname: Williams
authors.forename: Adrian
authors.initials: A
authors.lastname: Hills
authors.forename: Virgilio L
authors.initials: VL
authors.lastname: Lew
authors.forename: Michael R
authors.initials: MR
authors.lastname: Blatt
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000502:physiology / Q000528:radiation effects; D029681:Arabidopsis Proteins / Q000235:genetics*; D002118:Calcium / Q000378:metabolism; D002462:Cell Membrane / Q000378:metabolism / Q000528:radiation effects; D018118:Chloride Channels / Q000235:genetics; D018506:Gene Expression Regulation, Plant / Q000528:radiation effects; D006706:Homeostasis / Q000528:radiation effects; D006863:Hydrogen-Ion Concentration; D015640:Ion Channel Gating / Q000528:radiation effects; D008027:Light; D008565:Membrane Proteins / Q000235:genetics*; D008954:Models, Biological; D009154:Mutation / Q000235:genetics*; D054046:Plant Stomata / Q000166:cytology* / Q000235:genetics / Q000502:physiology* / Q000528:radiation effects; D018526:Plant Transpiration / Q000235:genetics / Q000502:physiology* / Q000528:radiation effects; D015221:Potassium Channels / Q000378:metabolism; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D015203:Reproducibility of Results; D015398:Signal Transduction / Q000235:genetics / Q000528:radiation effects; D049490:Systems Biology; D014158:Transcription, Genetic / Q000528:radiation effects
chemical_list: D029681:Arabidopsis Proteins; D018118:Chloride Channels; D008565:Membrane Proteins; D015221:Potassium Channels; D012333:RNA, Messenger; C528438:SLAC1 protein, Arabidopsis; D002118:Calcium