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Calcium Signals in the Control of Stomatal Movements

  • Alex A. R. WebbEmail author
  • Fiona C. Robertson
Chapter
Part of the Signaling and Communication in Plants book series (SIGCOMM)

Abstract

The stomatal guard cell regulates gas exchange between the plant and the environment. The movements of the stomata are regulated by a myriad of signals. The signalling pathways regulating stomatal movements have been intensely investigated due to their importance in plant responses to environmental stresses and because transpiration from the stomatal pore is the major route for water flux from the soil to the atmosphere, having consequence for climate models. The ubiquitous second messenger, calcium, is an important regulator of stomatal movements. The role of calcium as a second messenger in abscisic acid-induced stomatal closure is described. The importance of repetitive oscillations in the concentration of cytosolic free Ca2+ is discussed. The use of network reconstruction tools and systems approaches to understanding the relationship between calcium signalling and the recently discovered kinase/phosphatase-based ABA signalling cascade is considered.

Keywords

Guard Cell Stomatal Closure Phosphatidic Acid Stomatal Movement Plasma Membrane Potential 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Allen GJ, Kwak JM, Chu SP, Llopis J, Tsien RY, Harper JF, Schroeder JI (1999) Cameleon calcium indicator reports cytoplasmic calcium dynamics in Arabidopsis guard cells. Plant J 19:735–747PubMedCrossRefGoogle Scholar
  2. Allen GJ, Chu SP, Schumacher K, Shimazaki CT, Vafeados D, Kemper A, Hawke SD, Tallman G, Tsien RY, Harper JF, Chory J, Schroeder JI (2000) Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science 289:2338–2342PubMedCrossRefGoogle Scholar
  3. Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffman T, Tang YY, Grill E, Schroeder JI (2001) A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411:1053–1057PubMedCrossRefGoogle Scholar
  4. Armstrong F, Leung J, Grabov A, Brearley J, Giraudat J, Blatt MR (1995) Sensitivity to abscisic acid of guard-cell K+ channels is suppressed by abi1-1, a mutant Arabidopsis gene encoding a putative protein phosphatase. Proc Natl Acad Sci USA 92:9520–9524PubMedCrossRefGoogle Scholar
  5. Barbier-Brygoo H, Vinauger M, Colcombet J, Ephritikhine G, Frachisse J-M, Maurel C (2000) Anion channels in higher plants: functional characterization, molecular structure and physiological role. Biochim Biophys Acta 1465:199–218PubMedCrossRefGoogle Scholar
  6. Dodd A, Parkinson K, Webb AAR (2004) Independent circadian regulation of assimilation and stomatal conductance in the ztl-1 mutant of Arabidopsis. New Phytol 162:63–70CrossRefGoogle Scholar
  7. Dodd AN, Gardner MJ, Hotta CT, Hubbard KE, Dalchau N, Love J, Assie JM, Robertson FC, Kyed Jakobsen M, Gonçalves J, Sanders D, Webb AAR (2007) A cADPR-based feedback loop modulates the Arabidopsis circadian clock. Science 318:1789–1792PubMedCrossRefGoogle Scholar
  8. Fujii H, Zhu J-K (2009) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc Natl Acad Sci USA 106:8380–8385PubMedCrossRefGoogle Scholar
  9. Fujii H, Chinnusamy V, Rodrigues A, Rubio S, Antoni R, Park S-Y, Cutler SR, Sheen J, Rodriguez PL, Zhu J-K (2009) In vitro reconstitution of an abscisic acid signaling pathway. Nature 462:660–666PubMedCentralPubMedCrossRefGoogle Scholar
  10. Galione A, Lee HC, Busa WB (1991) Ca2+-induced Ca2+ release in sea urchin egg homogenates: modulation by cyclic ADP-ribose. Science 253:1143–1146PubMedCrossRefGoogle Scholar
  11. Garcia-Mata C, Gay R, Sokolovski S, Hills A, Lamattina L, Blatt MR (2003) Nitric oxide regulates K+ and Cl channels in guard cells through a subset of abscisic acid-evoked signaling pathways. Proc Natl Acad Sci USA 100:11116–11121PubMedCrossRefGoogle Scholar
  12. Gardner MJ, Baker AJ, Assie J-M, Poethig RS, Haseloff JP, Webb AAR (2009) GAL4 GFP enhancer trap lines for analysis of stomatal guard cell development and gene expression. J Exp Bot 60:213–226PubMedCrossRefGoogle Scholar
  13. Geiger D, Scherzer S, Mumm P, Stange A, Marten I, Bauer H, Ache P, Matschi S, Liese A, Al-Rasheid KAS, Romeis T, Hedrich R (2009) Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase–phosphatase pair. Proc Natl Acad Sci USA 106:21425–21430PubMedCrossRefGoogle Scholar
  14. Gilroy S, Read ND, Trewavas AJ (1990) Elevation of cytoplasmic calcium by caged calcium or caged inositol trisphosphate initiates stomatal closure. Nature 346:769–771PubMedCrossRefGoogle Scholar
  15. Gobert A, Isayenkov S, Voelker C, Czempinski K, Maathuis FJM (2007) The two-pore channel TPK1 gene encodes the vacuolar K+ conductance and plays a role in K+ homeostasis. Proc Natl Acad Sci USA 104:10726–10731PubMedCrossRefGoogle Scholar
  16. Gonugunta VK, Srivastava N, Puli MR, Raghavendra AS (2008) Nitric oxide production occurs after cytosolic alkalinization during stomatal closure induced by abscisic acid. Plant Cell Environ 31:1717–1724PubMedCrossRefGoogle Scholar
  17. Gosti F, Beudoin N, Serizet C, Webb AAR, Vartanian N, Giraudat J (1999) The ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell 11:1897–1910PubMedCentralPubMedGoogle Scholar
  18. Grabov A, Blatt MR (1997) Parallel control of the inward-rectifier K+ channel by cytosolic free Ca2+ and pH in Vicia guard cells. Planta 201:84–95CrossRefGoogle Scholar
  19. Guo FQ, Okamoto M, Crawford NM (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302:100–103PubMedCrossRefGoogle Scholar
  20. Hamilton DWA, Hills A, Kohler B, Blatt MR (2000) Ca2+ channels at the plasma membrane of stomatal guard cells are activated by hyperpolarization and abscisic acid. Proc Natl Acad Sci USA 97:4967–4972PubMedCrossRefGoogle Scholar
  21. Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908PubMedCrossRefGoogle Scholar
  22. Hosy E, Vavasseur A, Mouline K, Dreyer I, Gaymard F, Poree F, Boucherez J, Lebaudy A, Bouchez D, Very AA, Simonneau T, Thibaud JB, Sentenac H (2003) The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration. Proc Natl Acad Sci USA 100:5549–5554PubMedCrossRefGoogle Scholar
  23. Kinoshita T, Nishimura M, Shimazaki K (1995) Cytosolic concentration of Ca2+ regulates the plasma membrane H+-ATPase in guard cells of Fava bean. Plant Cell 7:1333–1342PubMedCentralPubMedGoogle Scholar
  24. Leckie CP, McAinsh MR, Allen GJ, Sanders D, Hetherington AM (1998) Abscisic acid-induced stomatal closure mediated by cyclic ADP-ribose. Proc Natl Acad Sci USA 95:15837–15842PubMedCrossRefGoogle Scholar
  25. Lee YS, Choi YB, Suh S, Lee J, Assmann SM, Joe CO, Kelleher JF, Crain RC (1996) Abscisic acid-induced phosphoinositide turnover in guard cell protoplasts of Vicia faba. Plant Physiol 110:987–996PubMedCentralPubMedGoogle Scholar
  26. Lee SC, Lan W, Buchanan BB, Luan S (2009) A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc Natl Acad Sci USA 106:21419–21424PubMedCrossRefGoogle Scholar
  27. Lemtiri-Chlieh F, MacRobbie EAC, Webb AAR, Manison NF, Brownlee C, Skepper J, Chen J, Prestwich GD, Brearley CA (2003) Inositol hexakisphosphate mobilizes an endomembrane store of calcium in guard cells. Proc Natl Acad Sci USA 100:10091–10095PubMedCrossRefGoogle Scholar
  28. Leonhardt N, Kwak JM, Robert N, Waner D, Leonhardt G, Schroeder JI (2004) Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell 16:596–615PubMedCentralPubMedCrossRefGoogle Scholar
  29. Li S, Assmann SM, Albert R (2006) Predicting essential components of signal transduction networks: a dynamic model of guard cell abscisic acid signaling. PLoS Biol 4:e312PubMedCentralPubMedCrossRefGoogle Scholar
  30. Liu X, Yue Y, Li B, Nie Y, Li W, Wu W-H, Ma L (2007) A G protein-coupled receptor is a plasma membrane receptor for the plant hormone abscisic acid. Science 315:1712–1716PubMedCrossRefGoogle Scholar
  31. Love J, Dodd AN, Webb AAR (2004) Circadian and diurnal calcium oscillations encode photoperiodic information in Arabidopsis. Plant Cell 16:956–966PubMedCentralPubMedCrossRefGoogle Scholar
  32. Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068PubMedGoogle Scholar
  33. MacRobbie EAC (1992) Calcium and ABA-induced stomatal closure. Phil Transact R Soc Lond B 338:5–18CrossRefGoogle Scholar
  34. McAinsh MR, Brownlee C, Hetherington AM (1990) Abscisic acid-induced elevation of guard-cell cytosolic Ca2+ precedes stomatal closure. Nature 343:186–188CrossRefGoogle Scholar
  35. McAinsh MR, Webb AAR, Taylor JE, Hetherington AM (1995) Stimulus-induced oscillations in guard cell cytosolic free calcium. Plant Cell 7:1207–1219PubMedCentralPubMedGoogle Scholar
  36. Melcher K, Ng LM, Zhou XE, Soon FF, Xu Y, Suino-Powell KM, Park SY, Weiner JJ, Fujii H, Chinnusamy V, Kovach A, Li J, Wang YH, Li JY, Peterson FC, Jensen DR, Yong EL, Volkman BF, Cutler SR, Zhu JK, Xu HE (2009) A gate-latch-lock mechanism for hormone signalling by abscisic acid receptors. Nature 462:602–608PubMedCentralPubMedCrossRefGoogle Scholar
  37. Miyazono K, Miyakawa T, Sawano Y, Kubota K, Kang HJ, Asano A, Miyauchi Y, Takahashi M, Zhi YH, Fujita Y, Yoshida T, Kodaira KS, Yamaguchi-Shinozaki K, Tanokura M (2009) Structural basis of abscisic acid signaling. Nature 462:609–614PubMedCrossRefGoogle Scholar
  38. Mori IC, Murata Y, Yang YZ, Munemasa S, Wang YF, Andreoli S, Tiriac H, Alonso JM, Harper JF, Ecker JR, Kwak JM, Schroeder JI (2006) CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+-permeable channels and stomatal closure. PLoS Biol 4:e327PubMedCentralPubMedCrossRefGoogle Scholar
  39. Navazio L, Mariani P, Sanders D (2001) Mobilization of Ca2+ by cyclic ADP-ribose from the endoplasmic reticulum of cauliflower florets. Plant Physiol 125:2129–2138PubMedCentralPubMedCrossRefGoogle Scholar
  40. Negi J, Matsuda O, Nagasawa T, Oba Y, Takahashi H, Kawai-Yamada M, Uchimiya H, Hashimoto M, Iba K (2008) CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452:483–485PubMedCrossRefGoogle Scholar
  41. Ng CKY, Carr K, McAinsh MR, Powell B, Hetherington AM (2001) Drought-induced guard cell signal transduction involves sphingosine-1-phosphate. Nature 410:596–599PubMedCrossRefGoogle Scholar
  42. Nishimura N, Hitomi K, Arvai AS, Rambo RP, Hitomi C, Cutler SR, Schroeder JI, Getzoff ED (2009) Structural mechanism of abscisic acid binding and signaling by dimeric PYR1. Science 326:1373–1379PubMedCentralPubMedCrossRefGoogle Scholar
  43. Okamoto M, Tanaka Y, Abrams SR, Kamiya Y, Seki M, Nambara E (2009) High humidity induces abscisic acid 8′-hydroxylase in stomata and vasculature to regulate local and systemic abscisic acid responses in Arabidopsis. Plant Physiol 149:825–834PubMedCentralPubMedCrossRefGoogle Scholar
  44. Pandey S, Nelson DC, Assmann SM (2009) Two novel GPCR-Type G proteins are abscisic acid receptors in Arabidopsis. Cell 136:136–148PubMedCrossRefGoogle Scholar
  45. Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TFF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu JK, Schroeder JI, Volkman BF, Cutler SR (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071PubMedCentralPubMedGoogle Scholar
  46. Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734PubMedCrossRefGoogle Scholar
  47. Peiter E, Maathuis FJM, Mills LN, Knight H, Pelloux J, Hetherington AM, Sanders D (2005) The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement. Nature 434:404–408PubMedCrossRefGoogle Scholar
  48. Risk JM, Day CL, Macknight RC (2009) Reevaluation of abscisic acid-binding assays shows that G-protein-coupled receptor2 does not bind abscisic acid. Plant Physiol 150:6–11PubMedCentralPubMedCrossRefGoogle Scholar
  49. Robertson FC, Skeffington A, Gardner MJ, Webb AAR (2009) Interactions between circadian and hormonal signalling in plants. Plant Mol Biol 69:419–427PubMedCrossRefGoogle Scholar
  50. Sánchez JP, Duque P, Chua NH (2004) ABA activates ADPR cyclase and cADPR induces a subset of ABA-responsive genes in Arabidopsis. Plant J 38:381–395PubMedCrossRefGoogle Scholar
  51. Santiago J, Dupeux F, Round A, Antoni R, Park SY, Jamin M, Cutler SR, Rodriguez PL, Marquez JA (2009) The abscisic acid receptor PYR1 in complex with abscisic acid. Nature 462:665–668PubMedCrossRefGoogle Scholar
  52. Sato A, Sato Y, Fukao Y, Fujiwara M, Umezawa T, Shinozaki K, Hibi T, Taniguchi M, Miyake H, Goto DB, Uozumi N (2009) Threonine at position 306 of the KAT1 potassium channel is essential for channel activity and is a target site for ABA-activated SnRK2/OST1/SnRK2.6 protein kinase. Biochem J 424:439–448PubMedCrossRefGoogle Scholar
  53. Schroeder JI, Hagiwara S (1989) Cytosolic calcium regulates ion channels in the plasma membrane of Vicia faba guard cells. Nature 338:427–430CrossRefGoogle Scholar
  54. Shen YY, Wang XF, Wu FQ, Du SY, Cao Z, Shang Y, Wang XL, Peng CC, Yu XC, Zhu SY, Fan RC, Xu YH, Zhang DP (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443:823–826PubMedCrossRefGoogle Scholar
  55. Siegel RS, Xue S, Murata Y, Yang Y, Nishimura N, Wang A, Schroeder JI (2009) Calcium elevation-dependent and attenuated resting calcium-dependent abscisic acid induction of stomatal closure and abscisic acid-induced enhancement of calcium sensitivities of S-type anion and inward-rectifying K+ channels in Arabidopsis guard cells. Plant J 59:207–220PubMedCentralPubMedCrossRefGoogle Scholar
  56. Sirichandra C, Gu D, Hu HC, Davanture M, Lee S, Djaoui M, Valot B, Zivy M, Leung J, Merlot S, Kwak JM (2009) Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett 583:2982–2986PubMedCrossRefGoogle Scholar
  57. Somers D, Webb AAR, Pearson M, Kay SA (1998) The short period mutant, toc1-1 alters circadian clock regulation of multiple outputs throughout development in Arabidopsis thaliana. Development 125:485–494PubMedGoogle Scholar
  58. Staxén I, Pical C, Montgomery LT, Gray JE, Hetherington AM, McAinsh MR (1999) Abscisic acid induces oscillations in guard-cell cytosolic free calcium that involve phosphoinositide-specific phospholipase C. Proc Natl Acad Sci USA 96:1779–1784PubMedCrossRefGoogle Scholar
  59. Talbott L, Zeiger E (1998) The role of sucrose in guard cell osmoregulation. J Exp Bot 49:329–337CrossRefGoogle Scholar
  60. Vahisalu T, Kollist H, Wang YF, Nishimura N, Chan WY, Valerio G, Lamminmaki A, Brosche M, Moldau H, Desikan R, Schroeder JI, Kangasjarvi J (2008) SLAC1 is required for plant guard cell S-type anion channel function in stomatal signaling. Nature 452:487–489PubMedCentralPubMedCrossRefGoogle Scholar
  61. Very AA, Sentenac H (2003) Molecular mechanisms and regulation of K+ transport in higher plants. Ann Rev Plant Biol 54:575–603CrossRefGoogle Scholar
  62. Ward JM, Schroeder JI (1994) 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. Plant Cell 6:669–683PubMedCentralPubMedGoogle Scholar
  63. Webb AAR (1998) Stomatal rhythms. In: Lumsden P, Millar A (eds) Biological rhythms and photoperiodism in plants. Bios Scientific, Oxford, pp 69–80Google Scholar
  64. Webb AAR (2003) The physiology of circadian rhythms in plants. New Phytol 160:281–303CrossRefGoogle Scholar
  65. Webb AAR, McAinsh MR, Taylor JE, Hetherington AM (1996) Calcium as a second messenger in plant cells. Adv Bot Res 22:45–96CrossRefGoogle Scholar
  66. Webb AAR, Larman M, Montgomery LT, Taylor JE, Hetherington AM (2001) The role for calcium during ABA-induced gene expression and stomatal movements. Plant J 26:351–362PubMedCrossRefGoogle Scholar
  67. Wu FQ, Xin Q, Cao Z, Liu ZQ, Du SY, Mei C, Zhao CX, Wang XF, Shang Y, Jiang T, Zhang XF, Yan L, Zhao R, Cui ZN, Liu R, Sun HL, Yang XL, Su Z, Zhang DP (2009) The magnesium-chelatase H subunit binds abscisic acid and functions in abscisic acid signaling: new evidence in Arabidopsis. Plant Physiol 150:1940–1954PubMedCentralPubMedCrossRefGoogle Scholar
  68. Yamasaki-Mann M, Demuro A, Parker I (2009) cADPR stimulates SERCA activity in Xenopus oocytes. Cell Calcium 45:293–299PubMedCentralPubMedCrossRefGoogle Scholar
  69. Yin P, Fan H, Hao Q, Yuan XQ, Wu D, Pang YX, Yan CY, Li WQ, Wang JW, Yan N (2009) Structural insights into the mechanism of abscisic acid signaling by PYL proteins. Nat Struct Mol Biol 16:1230–1236PubMedCrossRefGoogle Scholar
  70. Zhang W, Qin C, Zhao J, Wang X (2004) Phospholipase Dα1-derived phosphatidic acid interacts with ABI1 phosphatase 2C and regulates abscisic acid signalling. Proc Natl Acad Sci USA 101:9508–9513PubMedCrossRefGoogle Scholar
  71. Zhao Z, Zhang W, Stanley BA, Assmann SM (2008) Functional proteomics of Arabidopsis thaliana guard cells uncovers new stomatal signaling pathways. Plant Cell 20:3210–3226PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  1. 1.Department of Plant SciencesUniversity of CambridgeCambridgeUK

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