Abstract
Stomata are the major route of gas exchange between the atmosphere and the leaf interior. The size of the stomatal pore is controlled by the movements of the stomatal guard cells. The guard cells close the stomatal pore to conserve water during stress. In more favourable conditions, the stomatal movements optimise CO2 uptake whilst minimising water loss. The movements of stomata are controlled by an extensive network of signalling pathways responding to diverse stimuli. One of the regulators of stomata is the circadian clock. We discuss the physiological mechanisms by which the clock might regulate stomatal movements and the benefits that circadian regulation of stomatal behaviour could confer to the plant.
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Abbreviations
- ABA:
-
Abscisic acid
- ABAR:
-
ABA receptor
- ABH1 :
-
ABA HYPERSENSITIVE 1
- ABI1:
-
ABSCISIC ACID INSENSITIVE 1
- AtMRP5 :
-
ARABIDOPSIS MULTIDRUG RESISTANCE-RELATED PROTEIN 1
- AtRbohD :
-
ARABIDOPSIS RESPIRATORY BURST OXIDASE HOMOLOGUE 5
- AKT2/3 :
-
ARABIDOPSIS K + TRANSPORTER 2/3
- [Ca2+]cyt :
-
Concentration of cytosolic free calcium
- CAB2 :
-
CHLOROPHYLL A/B BINDING PROTEIN 2
- cADPR:
-
Cyclic adenosine diphosphate ribose
- CAM:
-
Crassulacean acid metabolism
- CBF:
-
C-REPEAT BINDING FACTOR
- CCA1:
-
CIRCADIAN CLOCK ASSOCIATED 1
- CCR2 :
-
COLD, CIRCADIAN, RHYTHM 2
- Ci:
-
Intercellular CO2 concentration
- CK:
-
Cytokinin
- CK2:
-
CAESIN KINASE 2
- CO:
-
CONSTANS
- CPK:
-
Ca2+-dependent protein kinase
- DD:
-
Continuous darkness
- EE:
-
Evening Element
- ELF3 :
-
EARLY FLOWERING 3
- ELF4 :
-
EARLY FLOWERING 4
- FT:
-
FLOWERING LOCUS T
- FV:
-
Fast vacuolar channel
- GI :
-
GIGANTEA
- GORK :
-
GUARD CELL-EXPRESSED OUTWARD-RECTIFYING K + CHANNEL
- IAA:
-
Indole-3-acetic acid
- Ins(1,4,5)P3 :
-
Inositol (1,4,5) trisphosphate
- InsP6 :
-
Inositol hexakisphosphate
- IRGA:
-
Infrared gas analysis
- LHY:
-
LATE ELONGATED HYPOCOTYL
- LKP2:
-
LIGHT, OXYGEN, VOLTAGE/KELCH PROTEIN 2
- LL:
-
Continuous light
- LUC :
-
LUCIFERASE
- LUX :
-
LUX ARRHYTHMIO
- NADPH:
-
Nicotinamide adenine dinucleotide phosphate
- NO:
-
Nitric oxide
- OST1:
-
OPEN STOMATA 1
- PEPC:
-
Phosphoenolpyruvate carboxylase
- PHYB :
-
PHYTOCHROME B
- PRR :
-
PSEUDO RESPONSE REGULATOR
- PP2C:
-
Protein phosphatase 2C
- PtdIns(3)P:
-
Phosphatidylinositol 3-phosphate
- PtdIns(4)P:
-
Phosphatidylinositol 4-phosphate
- PYL:
-
PYRABACTIN RESISTANCE-LIKE
- ROS:
-
Reactive oxygen species
- SLAC1:
-
SLOW ANION CHANNEL 1
- SnRK:
-
SNF-1-RELATED KINASE
- SV:
-
Slow vacuolar channel
- TOC1 :
-
TIMING OF CAB EXPRESSIONÂ 1
- TPC1 :
-
TWO PORE CHANNEL 1
- TPK1 :
-
TWO PORE K + CHANNEL 1
- VK:
-
Vacuolar K+ channel
- ZTL :
-
ZEITLUPE
References
Alabadà D, Oyama T, Yanovsky MJ, Harmon FG, Más P, Kay SA (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293:880–883
Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffmann T, Tang YY, Grill E, Schroeder JI (2001) A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411:1053–1057
Allen GJ, Sanders D (1996) Control of ionic currents in guard cell vacuoles by cytosolic and luminal calcium. Plant J 10:1055–1069
Ando E, Ohnisi Y, Wang Y, Matsushita T, Watanbe A, Hayashi Y, Fujii M, Ma JF, Inoue S, Kinoshita T (2013) Twin Sister of FT, Gigantea and Constans Have a Positive but Indirect Effect on Blue-Light Induced Stomatal Opening in Arabidopsis. Plant Physiol 162:1529–1538
Assmann SM, Wang XQ (2001) From milliseconds to millions of years: guard cells and environmental responses. Curr Opin Plant Biol 4:421–428
Bläsing OE, Gibon Y, Günther M, Höhne M, Morcuende R, Osuna D, Thimm O, Usadel B, Scheible W-R, Stitt Mark (2005) Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17:3257–3281
Blatt MR, Armstrong F (1993) K+ channels of stomatal guard cells: abscisic-acid-evoked control of the outward rectifier mediated by ctyoplasmic pH. Planta 191:330–341
Brandt B, Brodsky DE, Xue S, Negi J, Iba K, Kangasjärvi J, Ghassemian M, Stephan AB, Hu H, Schroeder JI (2012) 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 109:10593–10598
Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113–122
Chen ZH, Hills A, Bätz U, Amtmann A, Lew VL, Blatt MR (2012) Systems dynamic modeling of the stomatal guard cell predicts emergent behaviors in transport, signaling, and volume control. Plant Physiol 159:1235–1251
Correia MJ, Pereira JS, Chaves MM, Rodrigues ML, Pacheco CA (1995) ABA xylem concentrations determine maximum daily leaf conductance of field grown Vitis vinefera L. plants. Plant Cell Env 18:511–521
Dalchau N, Hubbard KE, Hotta CT, Robertson FC, Briggs HM, Stan G-B, Gonçalves JM, Webb AAR (2010) Correct biological timing in Arabidopsis requires multiple light signalling pathways. Proc Nat Acad Sci (USA). 107:13171–13176
Dios VR, Goulden ML, Ogle K, Richardson AD, Hollinger DY, Davidson EA, Alday JG, Barron-Gafford GA, Carrara A, Kowalski AS, Oechel WC, Reverter BR, Scott RL, Varner RK, DÃaz-Sierra R, Moreno JM (2012) Endogenous circadian regulation of carbon dioxide exchange in terrestrial ecosystems. Glob Chang Biol 18:1956–1970
Dodd AN, Parkinson K, Webb AAR (2004) Independent circadian regulation of assimilation and stomatal conductance in the ztl-1 mutant of Arabidopsis. New Phyt 162:63–70
Dodd AN, Salathia N, Hall A, Kevei E, Toth R, Nagy F, Hibberd JM, Millar AJ, Webb AAR (2005) Plant circadian clocks increase photosynthesis, growth, survival and competitive advantage. Science 309:630–633
Dodd AN, Kyed Jakobsen M, Baker AJ, Telzerow A, Hou S-W, Laplaze L, Barrot L, Poethig RS, Haseloff JM, Webb AAR (2006) Time of day modulation of Ca2 + signals in Arabidopsis. Plant J 48:962–973
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 318:1789–1792
Dodd AN, Gardner MJ, Baek S-J, Dalchau N, Webb AAR (2014) The circadian clock has transient plasticity of period and is required for timing of nocturnal processes in Arabidopsis. New Phytol 201:168–179
Dong MA, Farré EM, Thomashow MF (2011) Circadian clock-associated 1 and late elongated hypocotyl regulate expression of the C-repeat binding factor (CBF) pathway in Arabidopsis. Proc Natl Acad Sci 108:7241–7246
Edwards KD, Anderson PE, Hall A, Salathia NS, Locke JC, Lynn JR, Straume M, Smith JQ, Millar AJ (2006) FLOWERING LOCUS C mediates natural variation in the high-temperature response of the Arabidopsis circadian clock. Plant Cell 18:639–650
Edwards CE, Ewers BE, Williams DG, Xie Q, Lou P, Xu X, McClung CR, Weinig C (2011) The genetic architecture of ecophysiological and circadian traits in Brassica rapa. Genetics 189:375–390
Edwards CE, Ewers BE, McClung CR, Lou P, Weinig C (2012) Quantitative variation in water-use efficiency across water regimes and its relationship with circadian, vegetative, reproductive, and leaf gas-exchange traits. Mol Plant 5:653–668
Endo M, Shimizu H, Nohales MA, Araki T, Kay SA (2014) Tissue-specific clocks in Arabidopsis show asymmetric coupling. Nature 7527:419–422
Eriksson ME, Hanno S, Southern MM, Hall A, Millar AJ (2003) Response regulator homologues have complementary, light-dependent functions in the Arabidopsis circadian clock. Planta 218:159–162
Eskling M, Arvidsson P-O, Akerlund H-E (1997) The xanthophyll cycle, its regulation and components. Physiol Plant 100:806–816
Fogelmark K, Troein C (2014) Rethinking transcriptional activation in the Arabidopsis circadian clock. PLoS Comput Biol 10(7):e1003705
Fowler SG, Cook D, Thomashow MF (2005) Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol 137:961–968
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 462:660–666
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 signalling pathways. Proc Natl Acad Sci USA 100:11116–11121
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 60:213–226
Gehring CA, Irving HR, Parish RW (1990) Effects of auxin and abscisic acid on cytosolic calcium and pH in plant cells. Proc Natl Acad Sci USA 87:9645–9649
Geiger D, Scherzer S, Mumm P, Stange A, Marten I, Bauer H, Ache P, Hedrich R (2009) Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc Natl Acad Sci USA 106:21425–21430
Gendron JM, Pruneda-Paz JL, Doherty CJ, Gross AM, Kang SE, Kay SA (2012) Arabidopsis circadian clock protein, TOC1, is a DNA-binding transcription factor. Proc Natl Acad Sci 109:3167–3172
Gilroy S, Read ND, Trewavas AJ (1990) Elevation of cytoplasmic calcium by caged calcium or caged inositol triphosphate initiates stomatal closure. Nature 346:769–771
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 104:10726–10731
Gorton HL, Williams WE, Binns ME, Gemmell CN, Leheny EA, Shepherd AC (1989) Circadian stomatal rhythms in epidermal peels from Vicia faba. Plant Physiol 90:1329–1334
Gorton HL, Williams WE, Asmann SM (1993) Circadian rhythms in stomatal responsiveness to red and blue light. Plant Physiol 103:399–406
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 11:1883–1896
Gould PD, Locke JC, Larue C, Southern MM, Davis SJ, Hanano S, Moyle R, Milich R, Putterill J, Millar AJ, Hall A (2006) The molecular basis of tempertaure compensation in the Arabidopsis circadian clock. Plant Cell 18:1177–1187
Grabov A, Blatt MR (1997) Parallel control of the inward rectifier K+ channel by cytosolic free Ca2+ and pH in Vicia guard cells. Planta 201:84–95
Graf A, Schlereth A, Stitt M, Smith AM (2010) Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proc Natl Acad Sci 107:9458–9463
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 97:4967–4972
Harmer SL, Hogenesch JB, Straume Chang HS, Han B, Zhu T, Wang X, Kreps JA, Kay SA (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290:2110–2113
Haydon MJ, Mielczarek O, Robertson FC, Hubbard KE, Webb AAR (2013) Photosynthetic entrainment of the Arabidopsis circadian clock. Nature 502:689–692
Helfer A, Nusinow DA, Chow BY, Gehrke AR, Bulyk ML, Kay SA (2011) LUX ARRHYTHMO encodes a night time repressor of circadian gene expression in the Arabidopsis core clock. Curr Biol 21:126–133
Hennessey TL, Field CB (1991) Circadian rhythms in photosynthesis: oscillations in carbon assimilation and stomatal conductance under constant conditions. Plant Physiol 96:831–836
Herrero E, Kolmos E, Bujdoso N, Yuan Y, Wang M, Berns M, Coupland G, Saini R, Jaskolski M, Webb AAR, Gonçalves JM, Davis SJ (2012) EARLY FLOWERING4 recruitment of EARLY FLOWERING3 in the nucleus sustains the Arabidopsis circadian clock. Plant Cell 24:428–443
Hetherington AM, Grey JE, Leckie C, McAinsh MR, Ng C, Pical C, Priestley AJ, Staxén I, Webb AAR (1998) The control of specificity in guard cell signal transduction. Phil Trans Roy Soc Lond B 353:1489–1494
Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908
Hills A, Chen ZH, Amtmann A, Blatt MR, Lew VL (2012) OnGuard, a computational platform for quantitative kinetic modeling of guard cell physiology. Plant Physiol 159:1026–1042
Holmes MG, Klein WH (1986) Photocontrol of dark circadian rhythms in stomata of Phaseolus vulgaris L. Plant Physiol 82:28–33
Hosy E, Vavassuer A, Mouline K, Dreyer I, Gaymard I, 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 Adac Sci USA 100:5549–5554
Hsu PY, Devisetty UK, Harmer SL (2013) Accurate timekeeping is controlled by a cycling activator in Arabidopsis. Elife. 2
Hugouvieux V, Kwak JM, Schroeder JI (2001) An mRNA cap binding protien, ABH1, modulates early abscisic acid signal transduction in Arabidopsis. Cell 106:477–487
Hsu PY, Harmer SL (2014) Wheels within wheels: the plant circadian system. Trends Plant Sci 19:240–249
Hubbard KE, Nishimura N, Hitomi K, Getzoff ED, Schroeder JI (2010) Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. Genes Dev 24:1695–1708
Johnson CH, Knight MR, Kondo T, Masson P, Sedbrook J, Haley A, Trewavas A (1995) Circadian oscillations of cytosolic and chloroplastic free calcium in plants. Science 269:1863–1865
Jung JY, Kim YW, Kwak JM, Hwang JU, Young J, Schroeder JI, Hwang I, Lee Y (2002) Phosphatidylinositol 3- and 4-phosphate are required for normal stomatal movements. Plant Cell 14:2399–2412
Kiegle E, Moore CA, Haseloff J, Tester MA, Knight MR (2000) Cell-type-specific calcium responses to drought, salt and cold in the Arabidopsis root. Plant J 23:267–278
Kinoshita T, Mishimura M, Shimazaki K (1995) Cytosolic concentration of Ca2+ regulates the plasma membrane H+-ATPase in guard cells of Fava bean. Plant Cell 7:1333–1342
Kinoshita T, Ono N, Hayashi Y, Morimoto S, Nakamura S, Soda M, Kato Y, Ohnishi M, Nakano T, Inoue S, Shimizaki, K (2011) FLOWERING LOCUS T Regulates Stomatal Opening. Curr Biol 21:1232–1238
Klusener B, Young JJ, Murata Y, Allen GJ, Mori IC, Hugouvieux V, Schroeder JI (2002) Convergence of calcium signalling pathways of pathogenic elicitors and abscisic acid in Arabidopsis guard cells. Plant Physiol 130:2152–2163
Kollist H, Nuhkat M, Roelfsema MRG (2014) Closing gaps: linking elements that control stomatal movement. New Phytol 203:44–62
Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56:337–346
Krochko JE, Abrams GD, Loewen MK, Abrams SR, Cutler AJ (1998) (+)-Abscisic Acid 8’-hydroxylase is a cytochrome P450 monooxygenase. Plant Physiol 118:849–860
Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, Asami T, Hirai N, Koshiba T, Kamiya Y, Nambara E (2004) The Arabidopsis cytochrome P450 CYP707A encodes ABA 8’hydroxylases: key enzymes in ABA catabolism. EMBO J 23:1647–1656
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 95:15837–15842
Legnaioli T, Cuevas J, Mas P (2009) TOC1 functions as a molecular switch connecting the circadian clock with plant responses to drought. EMBO J 28:3745–3757
Lemichez E, Wu Y, Sanchez JP, Mettouchi A, Mathur J, Chua NH (2001) Inactivation of AtRac1 by abscisic acid is essential for stomatal closure. Genes Dev 15:1808–1816
Lemtiri-Chlieh F, MacRobbie EA, Webb AAR, Manison NF, Brownlee C, Skepper JN, Chen J, Prestwich GD, Brearly CA (2003) Inositol hexakisphosphate mobilizes an endomembrane store of calcium in guard cells. Proc Natl Acad Sci USA 97:8687–8692
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:e312
Locke JC, Southern MM, Kozma-Bognar L, Hibberd V, Brown PE, Turner MS, Millar AJ (2005a) Extension of a genetic network model by iterative experimentation and mathematical analysis. Mol Syst Biol 1(2005):0013
Locke JCW, Millar AJ, Turner MS (2005b) Modelling genetic networks with noisy and varied experimental data: the circadian clock in Arabidopsis thaliana. J Theor Biol 234:383–393
Love J, Dodd AN, Webb AAR (2004) Circadian and diurnal calcium oscillations encode photoperiodic information in Arabidopsis. Plant Cell 17:3257–3281
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 324:1064–1068
Martà MC, Stancombe MA, Webb AAR (2013) Cell- and stimulus-type-specific cytosolic-free Ca2+ signals in Arabidopsis thaliana. Plant Physiol 163:625–634
Matsushika A, Makino S, Kojima M, Mizuno T (2000) Circadian waves of expression of the APRR1/TOC1 family of pseudo-response regulators in Arabidopsis thaliana: insight into the plant circadian clock. Plant Cell Physiol 41:1002–1012
McAinsh MR, Brownlee C, Hetherington AM (1990) Abscisic acid-induced elevation of guard cell cytosolic Ca2+ precedes stpmatal closure. Nature 343:186–188
McAinsh MR, Webb A, Taylor JE, Hetherington AM (1995) Stimulus-induced oscillations in guard cell cytosolic free calcium. Plant Cell 7:1207–1219
Merlot S, Gosti F, Guerrier D, Vavasseur A, Giraudat J (2001) The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. Plant J 25:295–303
Michael TP, Mockler TC, Breton G, McEntee C, Byer A, Trout JD, Hazen SP, Shen R, Priest HD, Sullivan CM, Givan SA, Yanovsky M, Hong F, Kay SA, Chory J (2008) Network discovery pipeline elucidates conserved time-of-day-specific cis-regulatory modules. PLoS Genet 4:e14
Millar AJ (2004) Input signals to the plant circadian clock. J Exp Bot 55:277–283
Millar AJ, Kay SA (1996) Integration of circadian and phototransduction pathways in the network controlling CAB gene expression in Arabidopsis. Proc Natl Acad Sci USA 93:15491–15496
Mizoguchi T, Wright L, Fujiwara S, Cremer F, Lee K, Onouchi H, Mouradov A, Fowler S, Kamada H, Putterill J, Coupland G (2005) Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant Cell 17:2255–2270
Mori IC, Murata Y, Yang Y, Munemasa S, Wang Y-F et al (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(10):e327
Negi J, Matsuda O, Nagasawa T, Oba Y, Takahashi H, Kawai-Yamada M, Hirofumi U, Mimi H, Iba K (2008) CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452:483–486
Ng CK, Carr K, McAinsh MR, Powell B, Hetherington AM (2001) Drought-induced guard cell signal transduction involves sphingosine-1-phosphate. Nature 410:569–599
Noordally ZB, Ishii K, Atkins KA, Wetherill SJ, Kusakina J, Walton EJ, Kato M, Azuma M, Tanaka K, Hanaoka M, Dodd AN (2013) Circadian control of chloroplast transcription by a nuclear-encoded timing signal. Science 339:1316–1319
Ouyang Y, Andersson CR, Kondo T, Golden SS, Johnson CH (1998) Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci USA 95:8660–8664
Pallas JE Jr, Samish YB, Willmer CM (1974) Endogenous rhythmic activity of photosynthesis, transpiration, dark respiration and carbon dioxide compensation point of peanut leaves. Plant Physiol 53:907–911
Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow T-fF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu J-K, Schroeder JI, Volkman BF, Cutler SR (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071
Peiter E, Maathuis FJ, Mills LN, Knight H, Pelloux J, Hetherington AM, Sanders D (2005) The vacuolar Ca2+ activated channel TPC1 regulates germination and stomatal movement. Nature 434:404–408
Pittendrigh CS, Bruce VG (1959) Daily rhythms as coupled oscillator systems and their relation to thermoperiodism and photoperiodism. In: Withrow RB et al. (eds) Photoperiodism and related phenomena in plants and animals. Washington, A.A.A.S pp 465–505
Pokhilko A, Hodge SK, Stratford K, Knox K, Edwards KD, Thomson AW, Mizuno T, Millar AJ (2010) Data assimilation constrains new connections and components in a complex, eukaryotic circadian clock model. Mol Syst Biol 6:416
Pokhilko A, Fernández AP, Edwards KD, Southern MM, Halliday KJ, Millar AJ (2012) The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops. Mol Syst Biol 8(1)
Pokhilko A, Mas P, Millar A (2013) Modelling the widespread effects of TOC1 signalling on the plant circadian clock and its outputs. BMC Syst Biol 7:23
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 150:6–11
Roelfsema MRG, Hedrich R (2005) In the light of stomatal opening: new insights into ‘the Watergate’. New Phytol 167:665–691
Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signalling. Plant Cell 14:S401–S417
Sato A, Sato Y, Fukao Y, Fujiwara M, Umezawa T, Shinozaki K, Hibi T, 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 424:439–448
Schaffer R, Landgraf J, Accerbi M, Simon V, Larson M, Wisman E (2001) Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. Plant Cell 13:113–123
Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carré IA, Coupland G (1998) LATE ELONGATED HYPOCOTYL, an Arabidopsis gene encoding a MYB transcription factor, regulates circadian rhythmicity and photoperiodic responses. Cell 93:1219–1229
Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Ann Rev Plant Physiol Plant Mol Biol 52:627–658
Sharpe PJH, Wu H, Spence RD (1987) Stomatal mechanics. In: Zeiger E, Farquhar GD, Cowan IR (eds) Stomatal function. Stanford University Press, Standford, pp 91–114
Shope JC, EdWald DB, Mott KA (2003) Changes in surface area of intact guard cells are correlated with membrane internalization. Plant Physiol 133:1314–1321
Snaith PJ, Mansfield TA (1985) Responses of stomata to IAA and fusicoccin at the opposite phases of an entrained rhythm. J Exp Bot 36:937–944
Snaith PJ, Mansfield TA (1986) The circadian rhythm of stomatal opening—evidence for the involvement of potassium and chloride fluxes. J Exp Bot 37:188–199
Sirichandra C, Gu D, Hu HC, Davanture M, Lee S, Djaoui M, Valot B, Kwak JM (2009) Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett 583:2982–2986
Somers DE, 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 125:485–494
Somers DE, Schultz TF, Milnamow M, Kay SA (2000) ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis. Cell 101:319–329
Stadler R, Buttner M, Ache P, Hedrich R, Ivashikina N, Melzer M, Shearson SM, Smith SM, Sauer N (2003) Diurnal and light-regulated expression of AtSTP1 in guard cells of Arabidopsis. Plant Physiol 133:528–537
Stålfelt MG (1963) Diurnal dark reactions in the stomatal movements. Physiol Plant 16:756–766
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 96:1779–1784
Strayer C, Oyama T, Schultz TF, Raman R, Somers DE, Mas P, Panda S, Kreps JA, Kay SA (2000) Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 289:768–771
Suhita D, Raghavendra AS, Kwak JM, Vavasseur A (2004) Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate- and abscisic acid-induced stomatal closure. Plant Physiol 134:1536–1545
Tallman G (2004) Are diurnal patterns of stomatal movement the result of alternating metabolism of endogenous guard cell ABA and accumulation of ABA delivered to the apoplast around guard cells by transpiration? J Exp Bot 55:1963–1976
Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2006) Cytokinin and auxin inhibit abscisic acid-induced stomatal closse by enhancing ehtylene production in Arabidopsis. J Exp Bot 57:2259–2266
Tang RH, Han S, Zheng H, Cook CW, Choi CS, Woerner TE, Jackson RB, Pei ZM (2007) Coupling diurnal cytosolic Ca2 + oscillations to the CAS-IP3 pathway in Arabidopsis. Science 315:1423–1426
Vahisalu T, Kollist H, Wang YF, Nishimura N, Chan WY, Valerio G, Lamminmaki A, Brosche M, Moldau H, Desikan R, Schroeder JI, Kangasjärvi J (2008) SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature 452:487–491
Wang XQ, Ullah H, Jones AM, Assmann SM (2001) G protein regulation of ion channels and abscisic acid signalling in Arabidopsis guard cells. Science 292:2070–2072
Wang ZY, Tobin EM (1998) Constituitive expression of the CIRCADIAN CLOCK ASSOCIATED (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93:1207–1217
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 6:669–683
Webb AAR, Larman MG, Montgomery LT, Taylor JE, Hetherington AM (2001) The role of calcium in ABA-induced gene expression and stomatal movements. Plant J 26:351–362
Webb AAR (2003) The physiology of circadian rhythms in plants. New Phytol 160:281–303
Webb AAR (1998) Stomatal rhythms. In: Lumsden PJ, Millar AJ (eds) Biological rhythms and photoperiodism in plants. Bios Scientific Publishers pp 69–80
Xiong L, Zhu J-K (2003) Regulation of Abscisic acid biosynthesis. Plant Physiol 133:29–36
Yakir E, Hassidim M, Melamed-Book N, Hilman D, Kron I, Green RM (2011) Cell autonomous and cell-type specific circadian rhythms in Arabidopsis. Plant J 68:520–531
Yoshida R, Umezawa T, Mizoguchi T, Takahashi S, Takahashi F, Shinozaki K (2006) 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 281:5310–5318
Young MW, Kay SA (2001) Time zones: a comparative genetics of circadian clocks. Nat Rev Genet 2:702–715
Young JJ, Mehta S, Israelsson M, Godoski J, Grill E, Schroeder JI (2006) 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 103:7506–7511
Zhang SQ, Outlaw WH Jr (2001) Abscisic acid introduced into the transpiration stream accumulates in the guard-cell apoplast and causes stomatal closure. Plant Cell Env 24:1045–1054
Zhang C, Xie Q, Anderson RG, Ng G, Seitz NC, Peterson T, McClung CR, McDowell JM, Kong D, Kwak JM, Lu H (2013) Crosstalk between the circadian clock and innate immunity in Arabidopsis. PLoS Pathog 9:e1003370
Zou JJ, Wei FJ, Wang C, Wu JJ, Ratnasekera D, Liu WX, Wu WH (2010) Arabidopsis calcium-dependent protein kinase CPK10 functions in abscisic acid-and Ca2+-mediated stomatal regulation in response to drought stress. Plant Physiol 154:1232–1243
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Hubbard, K.E., Webb, A.A.R. (2015). Circadian Rhythms in Stomata: Physiological and Molecular Aspects. In: Mancuso, S., Shabala, S. (eds) Rhythms in Plants. Springer, Cham. https://doi.org/10.1007/978-3-319-20517-5_9
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