title: An Optimal Frequency in Ca2+ Oscillations for Stomatal Closure Is an Emergent Property of Ion Transport in Guard Cells.
abstract: Oscillations in cytosolic-free Ca(2+) concentration ([Ca(2+)]i) have been proposed to encode information that controls stomatal closure. [Ca(2+)]i oscillations with a period near 10 min were previously shown to be optimal for stomatal closure in Arabidopsis (Arabidopsis thaliana), but the studies offered no insight into their origins or mechanisms of encoding to validate a role in signaling. We have used a proven systems modeling platform to investigate these [Ca(2+)]i oscillations and analyze their origins in guard cell homeostasis and membrane transport. The model faithfully reproduced differences in stomatal closure as a function of oscillation frequency with an optimum period near 10 min under standard conditions. Analysis showed that this optimum was one of a range of frequencies that accelerated closure, each arising from a balance of transport and the prevailing ion gradients across the plasma membrane and tonoplast. These interactions emerge from the experimentally derived kinetics encoded in the model for each of the relevant transporters, without the need of any additional signaling component. The resulting frequencies are of sufficient duration to permit substantial changes in [Ca(2+)]i and, with the accompanying oscillations in voltage, drive the K(+) and anion efflux for stomatal closure. Thus, the frequency optima arise from emergent interactions of transport across the membrane system of the guard cell. Rather than encoding information for ion flux, these oscillations are a by-product of the transport activities that determine stomatal aperture.
authors.affiliation: Laboratory of Plant Physiology and Biophysics, University of Glasgow, Bower Building, Glasgow G12 8QQ, United Kingdom (C.M.-P., Y.W., A.H., M.R.B.);Biological Sciences, University of Essex, Wivenhoe Park, Colchester CO4 3SQ, United Kingdom (S.V.-C., T.L.);Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, United Kingdom (H.G.);Computing Science, University of Glasgow, Alwyn Williams Building, Glasgow G12 8QQ, United Kingdom (S.R.); andPhysiological Laboratory, University of Cambridge, Downing Street, Cambridge CB2 3EG, United Kingdom (V.L.L.).
authors.forename: Carla
authors.initials: C
authors.lastname: Minguet-Parramona
authors.affiliation: Laboratory of Plant Physiology and Biophysics, University of Glasgow, Bower Building, Glasgow G12 8QQ, United Kingdom (C.M.-P., Y.W., A.H., M.R.B.);Biological Sciences, University of Essex, Wivenhoe Park, Colchester CO4 3SQ, United Kingdom (S.V.-C., T.L.);Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, United Kingdom (H.G.);Computing Science, University of Glasgow, Alwyn Williams Building, Glasgow G12 8QQ, United Kingdom (S.R.); andPhysiological Laboratory, University of Cambridge, Downing Street, Cambridge CB2 3EG, United Kingdom (V.L.L.).
authors.forename: Yizhou
authors.identifier: http://orcid.org/0000-0002-2188-383X
authors.initials: Y
authors.lastname: Wang
authors.affiliation: Laboratory of Plant Physiology and Biophysics, University of Glasgow, Bower Building, Glasgow G12 8QQ, United Kingdom (C.M.-P., Y.W., A.H., M.R.B.);Biological Sciences, University of Essex, Wivenhoe Park, Colchester CO4 3SQ, United Kingdom (S.V.-C., T.L.);Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, United Kingdom (H.G.);Computing Science, University of Glasgow, Alwyn Williams Building, Glasgow G12 8QQ, United Kingdom (S.R.); andPhysiological Laboratory, University of Cambridge, Downing Street, Cambridge CB2 3EG, United Kingdom (V.L.L.).
authors.forename: Adrian
authors.initials: A
authors.lastname: Hills
authors.affiliation: Laboratory of Plant Physiology and Biophysics, University of Glasgow, Bower Building, Glasgow G12 8QQ, United Kingdom (C.M.-P., Y.W., A.H., M.R.B.);Biological Sciences, University of Essex, Wivenhoe Park, Colchester CO4 3SQ, United Kingdom (S.V.-C., T.L.);Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, United Kingdom (H.G.);Computing Science, University of Glasgow, Alwyn Williams Building, Glasgow G12 8QQ, United Kingdom (S.R.); andPhysiological Laboratory, University of Cambridge, Downing Street, Cambridge CB2 3EG, United Kingdom (V.L.L.).
authors.forename: Silvere
authors.initials: S
authors.lastname: Vialet-Chabrand
authors.affiliation: Laboratory of Plant Physiology and Biophysics, University of Glasgow, Bower Building, Glasgow G12 8QQ, United Kingdom (C.M.-P., Y.W., A.H., M.R.B.);Biological Sciences, University of Essex, Wivenhoe Park, Colchester CO4 3SQ, United Kingdom (S.V.-C., T.L.);Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, United Kingdom (H.G.);Computing Science, University of Glasgow, Alwyn Williams Building, Glasgow G12 8QQ, United Kingdom (S.R.); andPhysiological Laboratory, University of Cambridge, Downing Street, Cambridge CB2 3EG, United Kingdom (V.L.L.).
authors.forename: Howard
authors.initials: H
authors.lastname: Griffiths
authors.affiliation: Laboratory of Plant Physiology and Biophysics, University of Glasgow, Bower Building, Glasgow G12 8QQ, United Kingdom (C.M.-P., Y.W., A.H., M.R.B.);Biological Sciences, University of Essex, Wivenhoe Park, Colchester CO4 3SQ, United Kingdom (S.V.-C., T.L.);Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, United Kingdom (H.G.);Computing Science, University of Glasgow, Alwyn Williams Building, Glasgow G12 8QQ, United Kingdom (S.R.); andPhysiological Laboratory, University of Cambridge, Downing Street, Cambridge CB2 3EG, United Kingdom (V.L.L.).
authors.forename: Simon
authors.identifier: http://orcid.org/0000-0003-3578-4477
authors.initials: S
authors.lastname: Rogers
authors.affiliation: Laboratory of Plant Physiology and Biophysics, University of Glasgow, Bower Building, Glasgow G12 8QQ, United Kingdom (C.M.-P., Y.W., A.H., M.R.B.);Biological Sciences, University of Essex, Wivenhoe Park, Colchester CO4 3SQ, United Kingdom (S.V.-C., T.L.);Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, United Kingdom (H.G.);Computing Science, University of Glasgow, Alwyn Williams Building, Glasgow G12 8QQ, United Kingdom (S.R.); andPhysiological Laboratory, University of Cambridge, Downing Street, Cambridge CB2 3EG, United Kingdom (V.L.L.).
authors.forename: Tracy
authors.initials: T
authors.lastname: Lawson
authors.affiliation: Laboratory of Plant Physiology and Biophysics, University of Glasgow, Bower Building, Glasgow G12 8QQ, United Kingdom (C.M.-P., Y.W., A.H., M.R.B.);Biological Sciences, University of Essex, Wivenhoe Park, Colchester CO4 3SQ, United Kingdom (S.V.-C., T.L.);Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, United Kingdom (H.G.);Computing Science, University of Glasgow, Alwyn Williams Building, Glasgow G12 8QQ, United Kingdom (S.R.); andPhysiological Laboratory, University of Cambridge, Downing Street, Cambridge CB2 3EG, United Kingdom (V.L.L.) michael.blatt@glasgow.ac.uk vll1@cam.ac.uk.
authors.forename: Virgilio L
authors.initials: VL
authors.lastname: Lew
authors.affiliation: Laboratory of Plant Physiology and Biophysics, University of Glasgow, Bower Building, Glasgow G12 8QQ, United Kingdom (C.M.-P., Y.W., A.H., M.R.B.);Biological Sciences, University of Essex, Wivenhoe Park, Colchester CO4 3SQ, United Kingdom (S.V.-C., T.L.);Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, United Kingdom (H.G.);Computing Science, University of Glasgow, Alwyn Williams Building, Glasgow G12 8QQ, United Kingdom (S.R.); andPhysiological Laboratory, University of Cambridge, Downing Street, Cambridge CB2 3EG, United Kingdom (V.L.L.) michael.blatt@glasgow.ac.uk vll1@cam.ac.uk.
authors.forename: Michael R
authors.initials: MR
authors.lastname: Blatt
mesh_terms: D000251:Adenosine Triphosphatases / Q000378:metabolism; D017360:Arabidopsis / Q000166:cytology / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000378:metabolism; D001692:Biological Transport; D020013:Calcium Signaling / Q000502:physiology*; D002462:Cell Membrane / Q000378:metabolism; D003600:Cytosol / Q000378:metabolism; D008954:Models, Biological; D059828:Plant Cells / Q000378:metabolism; D054046:Plant Stomata / Q000378:metabolism*
chemical_list: D029681:Arabidopsis Proteins; D000251:Adenosine Triphosphatases