Calcium ions as second messengers in guard cell signal transduction

Ca2+ is a ubiquitous second messenger in plant cell signalling. In this review we consider the role of Ca2+-based signal transduction in stomatal guard cells focusing on three important areas: (1) the regulation of guard cell turgor relations and the control of gene expression in guard cells, (2) the control of specificity in Ca2+ signalling, (3) emerging technologies and new approaches for studying intracellular signalling. Stomatal apertures alter in response to a wide array of environmental stimuli as a result of changes in guard cell turgor. For example, the plant hormone abscisic acid (ABA) stimulates a reduction in stomatal aperture through a decrease in guard cell turgor. Furthermore, guard cells have been shown to be competent to relay an ABA signal from its site of perception to the nucleus. An increase in the concentration of cytosolic free Ca2+ ([Ca2+]1) is central to the mechanisms underlying ABA-induced changes in guard cell turgor. We describe a possible model of Ca2+-based ABA signal transduction during stomatal closure and discuss recent evidence which suggests that Ca2+ is also involved in ABA nuclear signal transduction. Many other environmental stimuli which affect stomatal apertures, in addition to ABA, induce an increase in guard cell [Ca2+]1) This raises questions regarding how increases in [Ca2+]1) can be a common component in the signal transduction pathways by which stimuli cause both stomatal opening and closure. We discuss several mechanisms of increasing the amount of information contained within the Ca2+ signal, including encoding information in a stimulus-specific Ca2+ signal or Ca2+ signature', the concept of the 'physiological address' of the cell, and the use of other second messengers. We conclude by addressing the emerging technologies and new approaches which can be used in conjunction with guard cells to dissect further the molecular mechanisms of Ca2+-mediated signalling in plants.

[1]  C. Gehring,et al.  Changes in cytosolic pH and calcium of guard cells precede stomatal movements. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[2]  J. Giraudat.  Abscisic acid signaling. , 1995, Current opinion in cell biology.

[3]  Roles of Ion Channels in Initiation of Signal Transduction in Higher Plants. , 1995 .

[4]  M. Berridge.  Inositol trisphosphate and calcium signalling , 1993, Nature.

[5]  M. C. Edwards,et al.  Guard Cells Extrude Protons Prior to Stomatal Opening—A Study using Fluorescence Microscopy and pH Micro-electrodes , 1988 .

[6]  K Raschke,et al.  Voltage dependence of K channels in guard-cell protoplasts. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[7]  S. Assmann.  Guard cell G proteins , 1996 .

[8]  J. Giraudat,et al.  Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. , 1994, Science.

[9]  J. Schroeder.  K+ transport properties of K+ channels in the plasma membrane of Vicia faba guard cells , 1988, The Journal of general physiology.

[10]  M. Iino,et al.  Outward-Rectifying K+ Channels in Stomatal Guard Cell Protoplasts , 1988 .

[11]  J. Giraudat,et al.  Protein phosphatase activity of abscisic acid insensitive 1 (ABI1) protein from Arabidopsis thaliana. , 1996, European journal of biochemistry.

[12]  E. Neher,et al.  Cytoplasmic calcium regulates voltage-dependent ion channels in plant vacuoles , 1987, Nature.

[13]  Peter A Lawrence,et al.  Morphogens, Compartments, and Pattern: Lessons from Drosophila? , 1996, Cell.

[14]  M. Blatt,et al.  Reversible inactivation of K+ channels of Vcia stomatal guard cells following the photolysis of caged inositol 1,4,5-trisphosphate , 1990, Nature.

[15]  C. Gehring,et al.  Rat natriuretic peptide binds specifically to plant membranes and induces stomatal opening. , 1996, Biochemical and biophysical research communications.

[16]  S. Schreiber,et al.  Immunosuppressants implicate protein phosphatase regulation of K+ channels in guard cells. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[17]  M. Sakata,et al.  Light-Induced Changes of Membrane Potential in Guard Cells of Vicia faba , 1983 .

[18]  E. Macrobbie.  Effects of ABA in ‘Isolated’ Guard Cells of Commelina communis L. , 1981 .

[19]  Two types of anion channel currents in guard cells with distinct voltage regulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[20]  J. Ward,et al.  Evidence for an Extracellular Reception Site for Abscisic Acid in Commelina Guard Cells , 1994, Plant physiology.

[21]  Klaus Raschke,et al.  Voltage-dependent anion channels in the plasma membrane of guard cells , 1989, Nature.

[22]  D. Sanders,et al.  Two Voltage-Gated, Calcium Release Channels Coreside in the Vacuolar Membrane of Broad Bean Guard Cells. , 1994, The Plant cell.

[23]  A. Trewavas,et al.  Elevation of cytoplasmic calcium by caged calcium or caged inositol trisphosphate initiates stomatal closure , 1990, Nature.

[24]  C. M. Karssen,et al.  The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana , 1984 .

[25]  H. C. Lee.  Cyclic ADP-ribose: a new member of a super family of signalling cyclic nucleotides. , 1994, Cellular signalling.

[26]  A. Trewavas,et al.  Cell wall oligogalacturonides increase cytosolic free calcium in carrot protoplasts , 1993 .

[27]  D. Ehrhardt,et al.  Calcium Spiking in Plant Root Hairs Responding to Rhizobium Nodulation Signals , 1996, Cell.

[28]  S. Assmann,et al.  Inhibition of inward K+ channels and stomatal response by abscisic acid: an intracellular locus of phytohormone action. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[29]  R. Hedrich,et al.  GCAC1 recognizes the pH gradient across the plasma membrane: a pH‐sensitive and ATP‐dependent anion channel links guard cell membrane potential to acid and energy metabolism , 1996 .

[30]  A. Webb,et al.  ABA-regulated promoter activity in stomatal guard cells. , 1995, The Plant journal : for cell and molecular biology.

[31]  S. Delmastro,et al.  Effect of two cAMP analogues on stomatal opening in Vicia faba. Possible relationship with cytosolic calcium concentration , 1994 .

[32]  A. Hetherington,et al.  Abscisic acid-induced elevation of guard cell cytosolic Ca2+ precedes stomatal closure , 1990, Nature.

[33]  M. Fricker,et al.  Two Transduction Pathways Mediate Rapid Effects of Abscisic Acid in Commelina Guard Cells. , 1994, The Plant cell.

[34]  A. Hetherington,et al.  Partial inhibition of ABA-induced stomatal closure by calcium-channel blockers , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[35]  W. Boss,et al.  Mastoparan-Induced Intracellular Ca2+ Fluxes May Regulate Cell-to-Cell Communication in Plants , 1996, Plant physiology.

[36]  J. Giraudat,et al.  Sensitivity to abscisic acid of guard-cell K+ channels is suppressed by abi1-1, a mutant Arabidopsis gene encoding a putative protein phosphatase. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[37]  R. Hedrich,et al.  [22] Patch clamp measurements on isolated guard cell protoplasts and vacuoles , 1989 .

[38]  A. Hetherington,et al.  SYNERGISM BETWEEN CALCIUM IONS AND ABSCISIC ACID IN PREVENTING STOMATAL OPENING , 1985 .

[39]  T. Kinoshita,et al.  Cytosolic Concentration of Ca2+ Regulates the Plasma Membrane H+-ATPase in Guard Cells of Fava Bean. , 1995, The Plant cell.

[40]  R. Quatrano,et al.  Fucus Embryogenesis: A Model to Study the Establishment of Polarity. , 1993, The Plant cell.

[41]  T. Kinoshita,et al.  Evidence for Ca2+-dependent protein phosphorylation in vitro in guard cells from Vicia faba L. , 1995 .

[42]  A. Hetherington,et al.  Some current aspects of stomatal physiology. , 1990 .

[43]  D. S. Bush.  Calcium Regulation in Plant Cells and its Role in Signaling , 1995 .

[44]  C. Brownlee,et al.  Localized Patch Clamping of Plasma Membrane of a Polarized Plant Cell : Laser Microsurgery of the Fucus spiralis Rhizoid Cell Wall. , 1992, Plant physiology.

[45]  C. Brearley,et al.  Metabolism of 3‐ and 4‐phosphorylated phosphatidylinositols in stomatal guard cells of Commelina communis L. , 1995 .

[46]  J. Rossier,et al.  AMPA receptor subunits expressed by single purkinje cells , 1992, Neuron.

[47]  K. Kasamo.  Effect of Abscisic Acid on the K+ Efflux and Membrane Potential of Nicotiana tabacum L. Leaf Cells , 1981 .

[48]  M. Berridge,et al.  Spatial and temporal aspects of cell signalling. , 1988, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[49]  S. Assmann.  Cyclic AMP as a Second Messenger in Higher Plants (Status and Future Prospects) , 1995, Plant physiology.

[50]  S. Hagiwara,et al.  Repetitive increases in cytosolic Ca2+ of guard cells by abscisic acid activation of nonselective Ca2+ permeable channels. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[51]  S. Assmann,et al.  A membrane-delimited pathway of G-protein regulation of the guard-cell inward K+ channel. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[52]  M. Blatt,et al.  Hormonal Control of Ion Channel Gating , 1993 .

[53]  S. Hagiwara,et al.  Cytosolic calcium regulates ion channels in the plasma membrane of Vicia faba guard cells , 1989, Nature.

[54]  L. M. Epstein,et al.  Expression of an mRNA with sequence similarity to pea dehydrin (Psdhn 1) in guard cells of Vicia faba in response to exogenous abscisic acid , 1995 .

[55]  J. R. Wood,et al.  Spatial Organization of Calcium Signaling Involved in Cell Volume Control in the Fucus Rhizoid. , 1996, The Plant cell.

[56]  M. Fricker,et al.  Role of Calcium in Signal Transduction of Commelina Guard Cells. , 1991, The Plant cell.

[57]  Stuart L. Schreiber,et al.  Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes , 1991, Cell.

[58]  A. Trewavas,et al.  Growth of Pollen Tubes of Papaver rhoeas Is Regulated by a Slow-Moving Calcium Wave Propagated by Inositol 1,4,5-Trisphosphate. , 1996, The Plant cell.

[59]  K. Raschke,et al.  A slow anion channel in guard cells, activating at large hyperpolarization, may be principal for stomatal closing , 1992, FEBS letters.

[60]  C. Somerville,et al.  Three Classes of Abscisic Acid (ABA)-Insensitive Mutations of Arabidopsis Define Genes that Control Overlapping Subsets of ABA Responses. , 1990, Plant physiology.

[61]  W. Davies,et al.  Control of water loss by delphinium plants cultured in vitro , 1994 .

[62]  K. Raschke,et al.  Abscisic Acid Content and Stomatal Sensitivity to CO(2) in Leaves of Xanthium strumarium L. after Pretreatments in Warm and Cold Growth Chambers. , 1976, Plant physiology.

[63]  A. Galione,et al.  Redundant mechanisms of calcium-induced calcium release underlying calcium waves during fertilization of sea urchin eggs. , 1993, Science.

[64]  A Goldbeter,et al.  Minimal model for signal-induced Ca2+ oscillations and for their frequency encoding through protein phosphorylation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[65]  A. Webb,et al.  Carbon dioxide induces increases in guard cell cytosolic free calcium , 1996 .

[66]  A. Hetherington,et al.  Changes in Stomatal Behavior and Guard Cell Cytosolic Free Calcium in Response to Oxidative Stress , 1996, Plant physiology.

[67]  M. Tazawa,et al.  MEMBRANE CONTROL IN THE CHARACEAE , 1987 .

[68]  M. Blatt,et al.  Phosphatase antagonist okadaic acid inhibits steady-state K+ currents in guard cells of Vicia faba , 1994 .

[69]  G. Farquhar,et al.  Gain of the feedback loop involving carbon dioxide and stomata: theory and measurement. , 1978, Plant physiology.

[70]  A. Hetherington,et al.  Visualizing Changes in Cytosolic-Free Ca2+ during the Response of Stomatal Guard Cells to Abscisic Acid. , 1992, The Plant cell.

[71]  J. Taylor,et al.  Stimulus-Induced Oscillations in Guard Cell Cytosolic Free Calcium. , 1995, The Plant cell.

[72]  J. Schroeder,et al.  Anion-Channel Blockers Inhibit S-Type Anion Channels and Abscisic Acid Responses in Guard Cells , 1995, Plant physiology.

[73]  S. Assmann,et al.  Signal transduction in guard cells. , 1993, Annual review of cell biology.

[74]  A. Webb,et al.  Calcium Ions as Intracellular Second Messengers in Higher Plants. , 1996 .

[75]  R. Hedrich,et al.  Ca2+ and nucleotide dependent regulation of voltage dependent anion channels in the plasma membrane of guard cells. , 1990 .

[76]  J. Richert,et al.  A reverse transcriptase-polymerase chain reaction assay for gene expression studies at the single cell level , 1996 .

[77]  E. Macrobbie.  ABA‐induced ion efflux in stomatal guard cells: multiple actions of ABA inside and outside the cell , 1995 .

[78]  I. R. Cowan,et al.  Guard cell pressure/aperture characteristics measured with the pressure probe , 1995 .

[79]  D. Sanders,et al.  Calcineurin, a Type 2B Protein Phosphatase, Modulates the Ca2+-Permeable Slow Vacuolar Ion Channel of Stomatal Guard Cells. , 1995, The Plant cell.

[80]  F. Krens,et al.  Stomatal Guard Cells Are Totipotent , 1996, Plant physiology.

[81]  M. Roelfsema,et al.  Effect of abscisic acid on stomatal opening in isolated epidermal strips of abi mutants of Arabidopsis thaliana , 1995 .

[82]  E. Grill,et al.  A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. , 1994, Science.

[83]  S. Assmann,et al.  Diacylglycerols induce both ion pumping in patch-clamped guard-cell protoplasts and opening of intact stomata. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[84]  G. Farquhar,et al.  Effect of abscisic Acid on the gain of the feedback loop involving carbon dioxide and stomata. , 1978, Plant physiology.

[85]  J. Ward,et al.  Calcium-Activated K+ Channels and Calcium-Induced Calcium Release by Slow Vacuolar Ion Channels in Guard Cell Vacuoles Implicated in the Control of Stomatal Closure. , 1994, The Plant cell.

[86]  R. Hedrich,et al.  Malate‐sensitive anion channels enable guard cells to sense changes in the ambient CO2 concentration , 1994 .

[87]  A. Campbell,et al.  Effects of mechanical signaling on plant cell cytosolic calcium. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[88]  E. Macrobbie.  Calcium and ABA-Induced Stomatal Closure , 1992 .

[89]  C. Fewtrell.  Ca2+ oscillations in non-excitable cells. , 1993, Annual review of physiology.

[90]  J. Schroeder,et al.  Strong regulation of slow anion channels and abscisic acid signaling in guard cells by phosphorylation and dephosphorylation events. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[91]  W. J. Lucas,et al.  In situ isolation of mRNA from individual plant cells: creation of cell-specific cDNA libraries. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[92]  P. V. Cutsem,et al.  Pectic Signal Transduction in Carrot Cells: Membrane, Cytosolic and Nuclear Responses Induced by Oligogalacturonides , 1994 .

[93]  S. Assmann,et al.  Abscisic Acid-Induced Phosphoinositide Turnover in Guard Cell Protoplasts of Vicia faba , 1996, Plant physiology.

[94]  M. Blatt,et al.  K+ channels of stomatal guard cells. Characteristics of the inward rectifier and its control by pH , 1992, The Journal of general physiology.

[95]  S. Assmann,et al.  Laser Microsurgery of Higher Plant Cell Walls Permits Patch-Clamp Access , 1996, Plant physiology.