Skip to main content

ABA Regulation of Stomatal Movement

  • Chapter
  • First Online:
Abscisic Acid: Metabolism, Transport and Signaling

Abstract

Plants loss water and intake CO2 mainly through stomata pores, which are surrounded by pairs of guard cells. Drought stress induces the production of ABA, and ABA functions as a main endogenous hormone to close stomata to prevent water loss. In the past decades, researchers have made exciting research progresses in ABA signaling transduction in guard cells, including the identification and isolation of a number of important components of ABA signaling network from upstream ABA receptors to downstream ion channels, and an uninterrupted and relatively complete ABA signaling pathway for ABA-induced stomatal closure has emerged. In this ABA signaling cascade, guard cells first sense ABA by the binding of ABA to ABA receptors to trigger the protein interaction between ABA receptors with PP2Cs, then protein kinases inhibited by PP2Cs can be released and further activate downstream S-type anion channel SLAC1, and the efflux of cations and anions through ion channels drives the stomatal closure. At the same time, a number of known components, small molecular messengers and newly identified components involving in ABA-induced stomatal closure have not been integrated into the ABA signaling network yet, and many scientific questions remain to be answered. This chapter will review the main progresses in the ABA regulation of stomatal movement, and some remaining questions will be discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ali R, Ma W, Lemtiri-Chlieh F, Tsaltas D, Leng Q, von Bodman S, Berkowitz GA. Death don’t have no mercy and neither does calcium: Arabidopsis cyclic nucleotide gated channel 2 and innate immunity. Plant Cell. 2007;19:1081–95.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Allen GJ, Sanders D. Control of ionic currents in guard cell vacuoles by cytosolic and luminal calcium. Plant J. 1996;10:1055–69.

    PubMed  CAS  Google Scholar 

  • Allen GJ, Kuchitsu K, Chu SP, Murata Y, Schroeder JI. Arabidopsis abi1-1 and abi2-1 phosphatase mutations reduce abscisic acid-induced cytoplasmic calcium rises in guard cells. Plant Cell. 1999;11:1785–98.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Allen TW, Kuyucak S, Chung SH. Molecular dynamics estimates of ion diffusion in model hydrophobic and KcsA potassium channels. Biophys Chem. 2000;86:1–14.

    PubMed  CAS  Google Scholar 

  • Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffmann T, Tang YY, Grill E, Schroeder JI. A defined range of guard cell calcium oscillation parameters encodes stomatal movement. Nature. 2001;411:1053–7.

    PubMed  CAS  Google Scholar 

  • Belin C, de Franco PO, Bourbousse C, Chaignepain S, Schmitter JM, Vavasseur A, Giraudat J, Barbier-Brygoo H, Thomine S. Identification of features regulating OST1 kinase activity and OST1 function in guard cells. Plant Physiol. 2006;141:1316–27.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Blackman PG, Davies WJ. Root to shoot communication in maize plants of the effects of soil drying. J Exp Bot. 1985;36:39–48.

    Google Scholar 

  • Brandt B, Brodsky DE, Xue S, Negi J, Iba K, Kangasjarvi J, Ghassemian M, Stephan AB, Hu H, Schroeder JI. Reconstitution of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatase action. Proc Natl Acad Sci USA. 2012;109:10593–8.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Briggs WR, Christie JM. Phototropins 1 and 2: versatile plant blue-light receptors. Trends Plant Sci. 2002;7:204–10.

    PubMed  CAS  Google Scholar 

  • Casson S, Gray JE. Influence of environmental factors on stomatal development. New Phytol. 2008;178:9–23.

    PubMed  CAS  Google Scholar 

  • Cheong YH, Pandey GK, Grant JJ, Batistic O, Li L, Kim BG, Lee SC, Kudla J, Luan S. Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J. 2007;52:223–39.

    PubMed  CAS  Google Scholar 

  • Cho D, Kim SA, Murata Y, Lee S, Jae S-K, Nam HG, Kwak JM. De-regulated expression of the plant glutamate receptor homolog AtGLR3.1 impairs long-term Ca2+-programmed stomatal closure. Plant J. 2009;58:437–49.

    PubMed  CAS  Google Scholar 

  • Daszkowska-Golec A, Chorazy E, Maluszynski M, Szarejko I. Towards the identification of new genes involved in ABA-dependent abiotic stresses using Arabidopsis suppressor mutants of abh1 hypersensitivity to ABA during seed germination. Int J Mol Sci. 2013;14:13403–32.

    PubMed  PubMed Central  Google Scholar 

  • De Angeli A, Monachello D, Ephritikhine G, Frachisse JM, Thomine S, Gambale F, Barbier-Brygoo H. The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature. 2006;442:939–42.

    PubMed  Google Scholar 

  • De Angeli A, Zhang J, Meyer S, Martinoia E. AtALMT9 is a malate-activated vacuolar chloride channel required for stomatal opening in Arabidopsis. Nature Commun. 2013;4:1804.

    Google Scholar 

  • Dong J, Bergmann DC. Stomatal patterning and development. Curr Top Dev Biol. 2010;91:267–97.

    PubMed  CAS  Google Scholar 

  • Du SY, Zhang XF, Lu Z, Xin Q, Wu Z, Jiang T, Lu Y, Wang XF, Zhang DP. Roles of the different components of magnesium chelatase in abscisic acid signal transduction. Plant Mol Biol. 2012;80:519–37.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Dubovskaya LV, Bakakina YS, Kolesneva EV, Sodel DL, McAinsh MR, Hetherington AM, Volotovski ID. cGMP-dependent ABA-induced stomatal closure in the ABA-insensitive Arabidopsis mutant abi1-1. New Phytol. 2011;191:57–69.

    PubMed  CAS  Google Scholar 

  • Dupeux F, Antoni R, Betz K, Santiago J, Gonzalez-Guzman M, Rodriguez L, Rubio S, Park SY, Cutler SR, Rodriguez PL, Marquez JA. Modulation of abscisic acid signaling in vivo by an engineered receptor-insensitive protein phosphatase type 2C allele. Plant Physiol. 2011;156:106–16.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Fan LM, Zhang W, Chen JG, Taylor JP, Jones AM, Assmann SM. Abscisic acid regulation of guard-cell K+ and anion channels in Gbeta- and RGS-deficient Arabidopsis lines. Proc Natl Acad Sci USA. 2008;105:8476–81.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Finkelstein RR, Somerville CR. Three classes of abscisic acid (ABA)-insensitive mutations of Arabidopsis define genes that control overlapping subsets of ABA responses. Plant Physiol. 1990;94:1172–9.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Finkelstein RR, Lynch TJ. The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell. 2000;12:599–609.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Franz S, Ehlert B, Liese A, Kurth J, Cazale AC, Romeis T. Calcium-dependent protein kinase CPK21 functions in abiotic stress response in Arabidopsis thaliana. Mol Plant. 2011;4:83–96.

    PubMed  CAS  Google Scholar 

  • Fujii H, Verslues PE, Zhu JK. Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. Plant Cell. 2007;19:485–94.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Fujii H, Verslues PE, Zhu J-K. Arabidopsis decuple mutant reveals the importance of SnRK2 kinases in osmotic stress responses in vivo. Proc Natl Acad Sci USA. 2011;108:1717–22.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Gaedeke N, Klein M, Kolukisaoglu U, Forestier C, Muller A, Ansorge M, Becker D, Mamnun Y, Kuchler K, Schulz B, Mueller-Roeber B, Martinoia E. The Arabidopsis thaliana ABC transporter AtMRP5 controls root development and stomata movement. EMBO J. 2001;20:1875–87.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Gao Y, Zeng Q, Guo J, Cheng J, Ellis BE, Chen JG. Genetic characterization reveals no role for the reported ABA receptor, GCR2, in ABA control of seed germination and early seedling development in Arabidopsis. Plant J. 2007;52:1001–13.

    PubMed  CAS  Google Scholar 

  • Gao QF, Fei CF, Dong JY, Gu LL, Wang YF. Arabidopsis CNGC18 is a Ca2+-permeable channel. Mol Plant. 2014;7:739–43.

    PubMed  CAS  Google Scholar 

  • Gayatri G, Agurla S, Raghavendra AS. Nitric oxide in guard cells as an important secondary messenger during stomatal closure. Front Plant Sci. 2013;4:425.

    PubMed  PubMed Central  Google Scholar 

  • Geelen D, Lurin C, Bouchez D, Frachisse JM, Lelievre F, Courtial B, Barbier-Brygoo H, Maurel C. Disruption of putative anion channel gene AtCLC-a in Arabidopsis suggests a role in the regulation of nitrate content. Plant J. 2000;21:259–67.

    PubMed  CAS  Google Scholar 

  • Geiger D, Scherzer S, Mumm P, Stange A, Marten I, Bauer H, Ache P, Matschi S, Liese A, Al-Rasheid KA, Romeis T, Hedrich R. Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc Natl Acad Sci USA. 2009;106:21425–30.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Geiger D, Maierhofer T, Al-Rasheid KA, Scherzer S, Mumm P, Liese A, Ache P, Wellmann C, Marten I, Grill E, Romeis T, Hedrich R. Stomatal closure by fast abscisic acid signaling is mediated by the guard cell anion channel SLAH3 and the receptor RCAR1. Sci Signal. 2011;4(173):ra32.

    PubMed  Google Scholar 

  • Giraudat J, Hauge BM, Valon C, Smalle J, Parcy F, Goodman HM. Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell. 1992;4:1251–61.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Gobert A, Isayenkov S, Voelker C, Czempinski K, Maathuis FJ. The two-pore channel TPK1 gene encodes the vacuolar K+ conductance and plays a role in K+ homeostasis. Proc Natl Acad Sci USA. 2007;104:10726–31.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Gray JE, Holroyd GH, van der Lee FM, Bahrami AR, Sijmons PC, Woodward FI, Schuch W, Hetherington AM. The HIC signalling pathway links CO2 perception to stomatal development. Nature. 2000;408:713–6.

    PubMed  CAS  Google Scholar 

  • Hamilton DW, Hills A, Kohler B, Blatt MR. Ca2+ channels at the plasma membrane of stomatal guard cells are activated by hyperpolarization and abscisic acid. Proc Natl Acad Sci USA. 2000;97:4967–72.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Han S, Tang R, Anderson LK, Woerner TE, Pei ZM. A cell surface receptor mediates extracellular Ca2+ sensing in guard cells. Nature. 2003;425:196–200.

    PubMed  CAS  Google Scholar 

  • Harada H, Kuromori T, Hirayama T, Shinozaki K, Leigh RA. Quantitative trait loci analysis of nitrate storage in Arabidopsis leading to an investigation of the contribution of the anion channel gene, AtCLC-c, to variation in nitrate levels. J Exp Bot. 2004;55:2005–14.

    PubMed  CAS  Google Scholar 

  • Hartung W, Sauter A, Hose E. Abscisic acid in the xylem: where does it come from, where does it go to? J Exp Bot. 2002;53:27–32.

    PubMed  CAS  Google Scholar 

  • Hashimoto M, Negi J, Young J, Israelsson M, Schroeder JI, Iba K. Arabidopsis HT1 kinase controls stomatal movement in response to CO2. Nature Cell Biol. 2006;8:391–7.

    PubMed  CAS  Google Scholar 

  • Himmelbach A, Iten M, Grill E. Signalling of abscisic acid to regulate plant growth. Philos Trans R Soc Lond B Biol Sci. 1998;353:1439–44.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Hoshino D, Hayashi A, Temmei Y, Kanzawa N, Tsuchiya T. Biochemical and immunohistochemical characterization of Mimosa annexin. Planta. 2004;219:867–75.

    PubMed  CAS  Google Scholar 

  • 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. The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movement and plant transpiration. Proc Natl Acad Sci USA. 2003;100:5549–54.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Hu H, Boisson-Dernier A, Israelsson-Nordstrom M, Bohmer M, Xue S, Ries A, Godoski J, Kuhn JM, Schroeder JI (2010) Carbonic anhydrases are upstream regulators of CO2-controlled stomatal movement in guard cells. Nature Cell Biol 12(81–88) 87-93; sup pp 81-18.

    Google Scholar 

  • Hua D, Wang C, He J, Liao H, Duan Y, Zhu Z, Guo Y, Chen Z, Gong Z. A plasma membrane receptor kinase, GHR1, mediates abscisic acid- and hydrogen peroxide-regulated stomatal movement in Arabidopsis. Plant Cell. 2012;24:2546–61.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Hugouvieux V, Kwak JM, Schroeder JI. An mRNA cap binding protein, ABH1, modulates early abscisic acid signal transduction in Arabidopsis. Cell. 2001;106:477–87.

    PubMed  CAS  Google Scholar 

  • Hugouvieux V, Murata Y, Young JJ, Kwak JM, Mackesy DZ, Schroeder JI. Localization, ion channel regulation, and genetic interactions during abscisic acid signaling of the nuclear mRNA cap-binding protein, ABH1. Plant Physiol. 2002;130:1276–87.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Jiang F, Hartung W. Long-distance signalling of abscisic acid (ABA): the factors regulating the intensity of the ABA signal. J Exp Bot. 2008;59:37–43.

    PubMed  CAS  Google Scholar 

  • Jossier M, Kroniewicz L, Dalmas F, Le Thiec D, Ephritikhine G, Thomine S, Barbier-Brygoo H, Vavasseur A, Filleur S, Leonhardt N. The Arabidopsis vacuolar anion transporter, AtCLCc, is involved in the regulation of stomatal movement and contributes to salt tolerance. Plant J. 2010;64:563–76.

    PubMed  CAS  Google Scholar 

  • Joudoi T, Shichiri Y, Kamizono N, Akaike T, Sawa T, Yoshitake J, Yamada N, Iwai S. Nitrated cyclic GMP modulates guard cell signaling in Arabidopsis. Plant Cell. 2013;25:558–71.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Kasahara M, Swartz TE, Olney MA, Onodera A, Mochizuki N, Fukuzawa H, Asamizu E, Tabata S, Kanegae H, Takano M, Christie JM, Nagatani A, Briggs WR. Photochemical properties of the flavin mononucleotide-binding domains of the phototropins from Arabidopsis, rice, and Chlamydomonas reinhardtii. Plant Physiol. 2002;129:762–73.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Klein M, Perfus-Barbeoch L, Frelet A, Gaedeke N, Reinhardt D, Mueller-Roeber B, Martinoia E, Forestier C. The plant multidrug resistance ABC transporter AtMRP5 is involved in guard cell hormonal signalling and water use. Plant J. 2003;33:119–29.

    PubMed  CAS  Google Scholar 

  • Kohler B, Blatt MR. Protein phosphorylation activates the guard cell Ca2+ channel and is a prerequisite for gating by abscisic acid. Plant J. 2002;32:185–94.

    PubMed  Google Scholar 

  • Konopka-Postupolska D, Clark G, Goch G, Debski J, Floras K, Cantero A, Fijolek B, Roux S, Hennig J. The role of annexin 1 in drought stress in Arabidopsis. Plant Physiol. 2009;150:1394–410.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Koornneef M, Reuling G, Karssen CM. The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiol Plant. 1984;61:377–83.

    CAS  Google Scholar 

  • Kovermann P, Meyer S, Hortensteiner S, Picco C, Scholz-Starke J, Ravera S, Lee Y, Martinoia E. The Arabidopsis vacuolar malate channel is a member of the ALMT family. Plant J. 2007;52:1169–80.

    PubMed  CAS  Google Scholar 

  • Kuhn JM, Boisson-Dernier A, Dizon MB, Maktabi MH, Schroeder JI. The protein phosphatase AtPP2CA negatively regulates abscisic acid signal transduction in Arabidopsis, and effects of abh1 on AtPP2CA mRNA. Plant Physiol. 2006;140:127–39.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Kwak JM, Murata Y, Baizabal-Aguirre VM, Merrill J, Wang M, Kemper A, Hawke SD, Tallman G, Schroeder JI. Dominant negative guard cell K+ channel mutants reduce inward-rectifying K+ currents and light-induced stomatal opening in Arabidopsis. Plant Physiol. 2001;127:473–85.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 2003;22:2623–33.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Laanemets K, Wang YF, Lindgren O, Wu J, Nishimura N, Lee S, Caddell D, Merilo E, Brosche M, Kilk K, Soomets U, Kangasjarvi J, Schroeder JI, Kollist H. Mutations in the SLAC1 anion channel slow stomatal opening and severely reduce K+ uptake channel activity via enhanced cytosolic [Ca2+] and increased Ca2+ sensitivity of K+ uptake channels. New Phytol. 2013;197:88–98.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Latorre R, Olcese R, Basso C, Gonzalez C, Munoz F, Cosmelli D, Alvarez O. Molecular coupling between voltage sensor and pore opening in the Arabidopsis inward rectifier K+ channel KAT1. J Gen Physiol. 2003;122:459–69.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Lebaudy A, Hosy E, Simonneau T, Sentenac H, Thibaud J-B, Dreyer I. Heteromeric K+ channels in plants. Plant J. 2008;54:1076–82.

    PubMed  CAS  Google Scholar 

  • Lee Y, Choi YB, Suh S, Lee J, Assmann SM, Joe CO, Kelleher JF, Crain RC. Abscisic acid-induced phosphoinositide turnover in guard cell protoplasts of Vicia faba. Plant Physiol. 1996;110:987–96.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Lee KH, Piao HL, Kim HY, Choi SM, Jiang F, Hartung W, Hwang I, Kwak JM, Lee IJ, Hwang I. Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell. 2006;126:1109–20.

    PubMed  CAS  Google Scholar 

  • Lee SC, Lan W, Buchanan BB, Luan S. A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc Natl Acad Sci USA. 2009;106:21419–24.

    Google Scholar 

  • Lemtiri-Chlieh F, Berkowitz GA. Cyclic adenosine monophosphate regulates calcium channels in the plasma membrane of Arabidopsis leaf guard and mesophyll cells. J Biol Chem. 2004;279:35306–12.

    PubMed  CAS  Google Scholar 

  • Lemtiri-Chlieh F, MacRobbie EA, Webb AA, Manison NF, Brownlee C, Skepper JN, Chen J, Prestwich GD, Brearley CA. Inositol hexakisphosphate mobilizes an endomembrane store of calcium in guard cells. Proc Natl Acad Sci USA. 2003;100:10091–5.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Leng Q, Mercier RW, Hua BG, Fromm H, Berkowitz GA. Electrophysiological analysis of cloned cyclic nucleotide-gated ion channels. Plant Physiol. 2002;128:400–10.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Leonhardt N, Kwak JM, Robert N, Waner D, Leonhardt G, Schroeder JI. Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell. 2004;16:596–615.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Leung J, Merlot S, Giraudat J. The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell. 1997;9:759–71.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Leung J, Bouvier-Durand M, Morris PC, Guerrier D, Chefdor F, Giraudat J. Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science. 1994;264:1448–52.

    PubMed  CAS  Google Scholar 

  • Liu X, Yue Y, Li B, Nie Y, Li W, Wu WH, Ma L. A G protein-coupled receptor is a plasma membrane receptor for the plant hormone abscisic acid. Science. 2007;315:1712–6.

    PubMed  CAS  Google Scholar 

  • Ma W. Roles of Ca2+ and cyclic nucleotide gated channel in plant innate immunity. Plant Sci. 2011;181:342–6.

    PubMed  CAS  Google Scholar 

  • Ma SY, Wu WH. AtCPK23 functions in Arabidopsis responses to drought and salt stresses. Plant Mol Biol. 2007;65:511–8.

    PubMed  CAS  Google Scholar 

  • Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science. 2009;324:1064–8.

    PubMed  CAS  Google Scholar 

  • MacRobbie EA. Signal transduction and ion channels in guard cells. Philos Trans R Soc London. 1998;353:1475–88.

    CAS  Google Scholar 

  • Merilo E, Jõesaar I, Brosché M, Kollist H. To open or to close: species-specific stomatal responses to simultaneously applied opposing environmental factors. New Phytol. 2014;202:499–508.

    Google Scholar 

  • Merlot S, Leonhardt N, Fenzi F, Valon C, Costa M, Piette L, Vavasseur A, Genty B, Boivin K, Muller A, Giraudat J, Leung J. Constitutive activation of a plasma membrane H+-ATPase prevents abscisic acid-mediated stomatal closure. EMBO J. 2007;26:3216–26.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Meyer S, Mumm P, Imes D, Endler A, Weder B, Al-Rasheid KA, Geiger D, Marten I, Martinoia E, Hedrich R. AtALMT12 represents an R-type anion channel required for stomatal movement in Arabidopsis guard cells. Plant J. 2010;63:1054–62.

    PubMed  CAS  Google Scholar 

  • Miao Y, Lv D, Wang P, Wang XC, Chen J, Miao C, Song CP. An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses. Plant Cell. 2006;18:2749–66.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Mori IC, Murata Y, Yang Y, Munemasa S, Wang YF, Andreoli S, Tiriac H, Alonso JM, Harper JF, Ecker JR, Kwak JM, Schroeder JI. CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+-permeable channels and stomatal closure. PLoS Biol. 2006;4:e327.

    PubMed  PubMed Central  Google Scholar 

  • Mortimer JC, Laohavisit A, Macpherson N, Webb A, Brownlee C, Battey NH, Davies JM. Annexins: multifunctional components of growth and adaptation. J Exp Bot. 2008;59:533–44.

    PubMed  CAS  Google Scholar 

  • Murata Y, Pei ZM, Mori IC, Schroeder J. Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell. 2001;13:2513–23.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Mustilli AC, Merlot S, Vavasseur A, Fenzi F, Giraudat J. Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell. 2002;14:3089–99.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Nadeau JA. Stomatal development: new signals and fate determinants. Curr Opin Plant Biol. 2009;12: 29–35.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Negi J, Matsuda O, Nagasawa T, Oba Y, Takahashi H, Kawai-Yamada M, Uchimiya H, Hashimoto M, Iba K. CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature. 2008;452:483–6.

    PubMed  CAS  Google Scholar 

  • Nishimura N, Hitomi K, Arvai AS, Rambo RP, Hitomi C, Cutler SR, Schroeder JI, Getzoff ED. Structural mechanism of abscisic acid binding and signaling by dimeric PYR1. Science. 2009;326:1373–9.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Nishimura N, Sarkeshik A, Nito K, Park SY, Wang A, Carvalho PC, Lee S, Caddell DF, Cutler SR, Chory J, Yates JR, Schroeder JI. PYR/PYL/RCAR family members are major in-vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. Plant J. 2010;61:290–9.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Pandey S, Nelson DC, Assmann SM. Two novel GPCR-type G proteins are abscisic acid receptors in Arabidopsis. Cell. 2009;136:136–48.

    PubMed  CAS  Google Scholar 

  • Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu JK, Schroeder JI, Volkman BF, Cutler SR. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science. 2009;324:1068–71.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Pei ZM, Ward JM, Schroeder JI. Magnesium sensitizes slow vacuolar channels to physiological cytosolic calcium and inhibits fast vacuolar channels in fava bean guard cell vacuoles. Plant Physiol. 1999;121:977–86.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Pei ZM, Kuchitsu K, Ward JM, Schwarz M, Schroeder JI. Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants. Plant Cell. 1997;9:409–23.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI. Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature. 2000;406:731–4.

    PubMed  CAS  Google Scholar 

  • Peiter E, Maathuis FJ, Mills LN, Knight H, Pelloux J, Hetherington AM, Sanders D. The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement. Nature. 2005;434:404–8.

    PubMed  CAS  Google Scholar 

  • Peuke AD, Jeschke WD, Hartung W. Flows of elements, ions and abscisic acid in Ricinus communis and site of nitrate reduction under potassium limitation. J Exp Bot. 2002;53:241–50.

    PubMed  CAS  Google Scholar 

  • Pottosin II, Martínez-Estévez M. Regulation of the fast vacuolar channel by cytosolic and vacuolar potassium. Biophy J. 2003;84:977–86.

    CAS  Google Scholar 

  • Quarrie SA, Jones HG. Effects of abscisic acid and water stress on development and morphology of wheat. J Exp Bot. 1977;28:192–203.

    CAS  Google Scholar 

  • Rae AM, Ferris R, Tallis MJ, Taylor G. Elucidating genomic regions determining enhanced leaf growth and delayed senescence in elevated CO2. Plant Cell Environ. 2006;29:1730–41.

    PubMed  CAS  Google Scholar 

  • Saez A, Robert N, Maktabi MH, Schroeder JI, Serrano R, Rodriguez PL. Enhancement of abscisic acid sensitivity and reduction of water consumption in Arabidopsis by combined inactivation of the protein phosphatases type 2C ABI1 and HAB1. Plant Physiol. 2006;141:1389–99.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Saez A, Apostolova N, Gonzalez-Guzman M, Gonzalez-Garcia MP, Nicolas C, Lorenzo O, Rodriguez PL. Gain-of-function and loss-of-function phenotypes of the protein phosphatase 2C HAB1 reveal its role as a negative regulator of abscisic acid signalling. Plant J. 2004;37:354–69.

    PubMed  CAS  Google Scholar 

  • Salisbury EJ. On the causes and ecological significance of stomatal frequency, with special reference to the woodland flora. Phil Trans R Soc Lond B. 1928;216:1–65.

    Google Scholar 

  • Santiago J, Dupeux F, Betz K, Antoni R, Gonzalez-Guzman M, Rodriguez L, Marquez JA, Rodriguez PL. Structural insights into PYR/PYL/RCAR ABA receptors and PP2Cs. Plant Sci. 2012;182:3–11.

    PubMed  CAS  Google Scholar 

  • Sasaki T, Mori IC, Furuichi T, Munemasa S, Toyooka K, Matsuoka K, Murata Y, Yamamoto Y. Closing plant stomata requires a homolog of an aluminum-activated malate transporter. Plant Cell Physiol. 2010;51:354–65.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Schroeder JI, Hagiwara S. Cytosolic calcium regulates ion channels in the plasma membrane of Vicia faba guard cells. Nature. 1989;338:427–30.

    Google Scholar 

  • Schroeder JI, Keller BU. Two types of anion channel currents in guard cells with distinct voltage regulation. Proc Natl Acad Sci USA. 1992;89:5025–9.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Schroeder JI, Nambara E. A quick release mechanism for abscisic acid. Cell. 2006;126:1023–5.

    PubMed  CAS  Google Scholar 

  • 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. The Mg-chelatase H subunit is an abscisic acid receptor. Nature. 2006;443:823–6.

    PubMed  CAS  Google Scholar 

  • Shimazaki K-I, Doi M, Assmann SM, Kinoshita T. Light regulation of stomatal movement. Ann Rev Plant Biol. 2007;58:219–47.

    CAS  Google Scholar 

  • Shkolnik-Inbar D, Adler G, Bar-Zvi D. ABI4 downregulates expression of the sodium transporter HKT1; 1 in Arabidopsis roots and affects salt tolerance. Plant J. 2013;73:993–1005.

    PubMed  CAS  Google Scholar 

  • Siegel RS, Xue S, Murata Y, Yang Y, Nishimura N, Wang A, Schroeder JI. 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. 2009;59:207–20.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Song Y, Miao Y, Song CP. Behind the scenes: the roles of reactive oxygen species in guard cells. New Phytol. 2014;201:1121–40.

    PubMed  CAS  Google Scholar 

  • Soon FF, Ng LM, Zhou XE, West GM, Kovach A, Tan MH, Suino-Powell KM, He Y, Xu Y, Chalmers MJ, Brunzelle JS, Zhang H, Yang H, Jiang H, Li J, Yong EL, Cutler S, Zhu JK, Griffin PR, Melcher K, Xu HE. Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases. Science. 2012;335:85–8.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Suh SJ, Wang YF, Frelet A, Leonhardt N, Klein M, Forestier C, Mueller-Roeber B, Cho MH, Martinoia E, Schroeder JI. The ATP binding cassette transporter AtMRP5 modulates anion and calcium channel activities in Arabidopsis guard cells. J Biol Chem. 2007;282:1916–24.

    PubMed  CAS  Google Scholar 

  • Sutter JU, Sieben C, Hartel A, Eisenach C, Thiel G, Blatt MR. Abscisic acid triggers the endocytosis of the Arabidopsis KAT1 K+ channel and its recycling to the plasma membrane. Curr Biol. 2007;17:1396–402.

    PubMed  CAS  Google Scholar 

  • Szyroki A, Ivashikina N, Dietrich P, Roelfsema MR, Ache P, Reintanz B, Deeken R, Godde M, Felle H, Steinmeyer R, Palme K, Hedrich R. KAT1 is not essential for stomatal opening. Proc Natl Acad Sci USA. 2001;98:2917–21.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Tang RH, Han S, Zheng H, Cook CW, Choi CS, Woerner TE, Jackson RB, Pei ZM. Coupling diurnal cytosolic Ca2+ oscillations to the CAS-IP3 pathway in Arabidopsis. Science. 2007;315:1423–6.

    PubMed  CAS  Google Scholar 

  • Tsuzuki T, Takahashi K, Inoue S-I, Okigaki Y, Tomiyama M, Hossain M, Shimazaki K-I, Murata Y, Kinoshita T. Mg-chelatase H subunit affects ABA signaling in stomatal guard cells, but is not an ABA receptor in Arabidopsis thaliana. J Plant Res. 2011;124:527–38.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Tsuzuki T, Takahashi K, Tomiyama M, Inoue S, Kinoshita T. Overexpression of the Mg-chelatase H subunit in guard cells confers drought tolerance via promotion of stomatal closure in Arabidopsis thaliana. Front Plant Sci. 2013;4:440.

    PubMed  PubMed Central  Google Scholar 

  • Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K, Ishihama Y, Hirayama T, Shinozaki K. Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc Natl Acad Sci U S A. 2009;106:17588–93.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Vahisalu T, Kollist H, Wang YF, Nishimura N, Chan WY, Valerio G, Lamminmaki A, Brosche M, Moldau H, Desikan R, Schroeder JI, Kangasjarvi J. SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature. 2008;452:487–91.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Vlad F, Rubio S, Rodrigues A, Sirichandra C, Belin C, Robert N, Leung J, Rodriguez PL, Lauriere C, Merlot S. Protein phosphatases 2C regulate the activation of the Snf1-related kinase OST1 by abscisic acid in Arabidopsis. Plant Cell. 2009;21:3170–84.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wang XQ, Ullah H, Jones AM, Assmann SM. G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. Science. 2001;292:2070–2.

    PubMed  CAS  Google Scholar 

  • Wang YF, Munemasa S, Nishimura N, Ren HM, Robert N, Han M, Puzorjova I, Kollist H, Lee S, Mori I, Schroeder JI. Identification of cyclic GMP-activated nonselective Ca2+-permeable cation channels and associated CNGC5 and CNGC6 genes in Arabidopsis guard cells. Plant Physiol. 2013;163:578–90.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Ward JM, Maser P, Schroeder JI. Plant ion channels: gene families, physiology, and functional genomics analyses. Ann Rev Physiol. 2009;71:59–82.

    CAS  Google Scholar 

  • Weiner JJ, Peterson FC, Volkman BF, Cutler SR. Structural and functional insights into core ABA signaling. Curr Opin Plant Biol. 2010;13:495–502.

    PubMed  PubMed Central  CAS  Google Scholar 

  • 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. The magnesium-chelatase H subunit binds abscisic acid and functions in abscisic acid signaling: new evidence in Arabidopsis. Plant Physiol. 2009;150:1940–54.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Xie X, Wang Y, Williamson L, Holroyd GH, Tagliavia C, Murchie E, Theobald J, Knight MR, Davies WJ, Leyser HM, Hetherington AM. The identification of genes involved in the stomatal response to reduced atmospheric relative humidity. Curr Biol. 2006;16:882–7.

    PubMed  CAS  Google Scholar 

  • Yoshida R, Umezawa T, Mizoguchi T, Takahashi S, Takahashi F, Shinozaki K. The regulatory domain of SRK2E/OST1/SnRK2.6 interacts with ABI1 and integrates abscisic acid (ABA) and osmotic stress signals controlling stomatal closure in Arabidopsis. J Biol Chem. 2006;281:5310–8.

    PubMed  CAS  Google Scholar 

  • Yoshida R, Hobo T, Ichimura K, Mizoguchi T, Takahashi F, Aronso J, Ecker JR, Shinozaki K. ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol. 2002;43:1473–83.

    PubMed  CAS  Google Scholar 

  • Young JJ, Mehta S, Israelsson M, Godoski J, Grill E, Schroeder JI. CO2 signaling in guard cells: calcium sensitivity response modulation, a Ca2+-independent phase, and CO2 insensitivity of the gca2 mutant. Proc Natl Acad Sci USA. 2006;103:7506–11.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song CP. Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol. 2001;126:1438–48.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang XF, Jiang T, Wu Z, Du SY, Yu YT, Jiang SC, Lu K, Feng XJ, Wang XF, Zhang DP. Cochaperonin CPN20 negatively regulates abscisic acid signaling in Arabidopsis. Plant Mol Biol. 2013;83(3):205–18.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC, Shang Y, Du SY, Wang XF, Wu FQ, Xu YH, Zhang XY, Zhang DP. Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell. 2007;19:3019–36.

    PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by Hundred Talents Program of Chinese Academy of Sciences (2010OHTP06) and the National Basic Research Program of China (973 program; grant No. 2012CB114300). The author apologizes to colleagues whose publications were not cited and discussed in this chapter because of space limitation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yong-Fei Wang .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Wang, YF. (2014). ABA Regulation of Stomatal Movement. In: Zhang, DP. (eds) Abscisic Acid: Metabolism, Transport and Signaling. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9424-4_15

Download citation

Publish with us

Policies and ethics