1 Frontiers in Plant Science 2013 Vol: 4():. DOI: 10.3389/fpls.2013.00138

Open or Close the Gate – Stomata Action Under the Control of Phytohormones in Drought Stress Conditions

Two highly specialized cells, the guard cells that surround the stomatal pore, are able to integrate environmental and endogenous signals in order to control the stomatal aperture and thereby the gas exchange. The uptake of CO2 is associated with a loss of water by leaves. Control of the size of the stomatal aperture optimizes the efficiency of water use through dynamic changes in the turgor of the guard cells. The opening and closing of stomata is regulated by the integration of environmental signals and endogenous hormonal stimuli. The various different factors to which the guard cells respond translates into the complexity of the network of signaling pathways that control stomatal movements. The perception of an abiotic stress triggers the activation of signal transduction cascades that interact with or are activated by phytohormones. Among these, abscisic acid (ABA), is the best-known stress hormone that closes the stomata, although other phytohormones, such as jasmonic acid, brassinosteroids, cytokinins, or ethylene are also involved in the stomatal response to stresses. As a part of the drought response, ABA may interact with jasmonic acid and nitric oxide in order to stimulate stomatal closure. In addition, the regulation of gene expression in response to ABA involves genes that are related to ethylene, cytokinins, and auxin signaling. In this paper, recent findings on phytohormone crosstalk, changes in signaling pathways including the expression of specific genes and their impact on modulating stress response through the closing or opening of stomata, together with the highlights of gaps that need to be elucidated in the signaling network of stomatal regulation, are reviewed.

Mentions
Figures
Figure 1: Regulation of ion channels, pumps, and transporters localized in the plasma membrane of the guard cells during stomatal opening and closure. During stomatal opening (A) H+-ATPase pumps H+ from the guard cells and hyperpolarizes the membrane, which leads to the activation of K+ inward rectifying channels (KAT1, KAT2, AKT1). Anionic species such as malate2− from the breakdown of starch and transported NO3- and Cl− ions contribute to the intracellular solute buildup that can mediate the import of sugars or can be used for the synthesis of sugars. Ions supplied into the guard cells together with water transported via aquaporins generate the turgor that is needed to keep stomata opened. During stomatal closure (B), H+-ATPase is inhibited and S-type and R-type anion channels are activated. As the plasma membrane is depolarized, S-type and R-type channels facilitate the efflux of malate2−, Cl−, and NO3-. At the same time, K+ outwardly rectifying channels such as GORK are activated through the depolarization of the membrane, which leads to the efflux of K+. The decreased level of malate2− is also caused by the gluconeogenic conversion of malate into starch. The elevation of the Ca2+ concentration as a result of the release of Ca2+- via channels situated in both the plasma membrane and in the tonoplast is another event that accompanies stomatal closure. Figure 2: Abscisic acid biosynthesis, catabolism, deconjugation, transport, and signaling. ABA biosynthesis (A) is mainly induced by upregulating NCED3, ZEP, and AAO genes. At the same time as the biosynthesis of ABA is induced, the catabolism (B) that is performed by CYP707A1-4 is inhibited. The balance between active and inactive ABA in the cell is achieved not only by the regulation of biosynthesis and catabolism but also by ABA conjugation and deconjugation. The most widespread conjugate is the ABA glucosyl ester (ABA-GE), which is catalyzed by ABA glucosyltransferase (C). ABA delivery to the guard cells via ABCG transporters such as AGCG22 (D) promotes a cascade of reactions. The core of early ABA signaling involves ABA receptors – PYR/PYL/RCAR proteins, PP2Cs, and SnRKs (E). After binding ABA to the receptor, the negative regulatory action of PP2Cs is inhibited and SnRKs are able to phosphorylate and activate downstream targets in order to transduce the ABA signal. Figure 3: The role of ABA in the diurnal regulation of stomatal movements. In the dark phase of the day (A), ABA biosynthesis is favored and at the same time the catabolism of ABA is inhibited. As a result of these processes, elevated levels of ABA are present in the guard cells. ABA activates the efflux of Ca2+ from internal stores, the activation of S-type and R-type anion channels leading to the efflux of Cl−, malate2−, and NO3-, the activation of GORK channel, which leads to the efflux of K+ and consequently to the closing of stomatal pores. The decreased level of malate2− is also caused by the gluconeogenic conversion of malate into starch. In the dawn (B), the first light promotes ABA catabolism processes and the level of ABA biosynthesis decreases, which leads to a decreased concentration of active ABA in the guard cells. Low endogenous ABA levels no longer inhibit H+-ATPase (H+-pump), which is then able to extrude H+ from the guard cells. At the same time, the accumulation of water and ions, such as K+, Cl−, malate2− occurs in order to generate the turgor that is needed to keep stomata open. Figure 4: ABA regulation of stomatal closure during drought stress. An increased level of endogenous ABA in response to drought activates a signal transduction pathway that involves a sequence of events such as the elevation of the cytosolic Ca2+ level, which consequently activates the anion channels (S-type and R-type), which leads to membrane depolarization. The latter activate GORK, which is responsible for extruding K+ from the guard cells. Simultaneous with the efflux of K+, an efflux of water is observed. Together, these events lead to a decrease in the turgor of the guard cells and to stomatal closure under drought conditions. The sequence of events, which is explained in detail in the main text and presented in green in the figure, is the core of the reactions that are induced or inhibited by different proteins that are activated by ABA. Blue arrows indicate activation, while red blunt ended lines indicate inhibition. Figure 5: Me-JA regulated stomatal closure during drought stress. MeJA, before it can be bound by a receptor in the plant cell, is converted into a biologically active form (+)-7-iso-Jasmonoyl-L-isoleucine (JA-Ile). JA-Ile is then bound by the receptor SCFCOI complex that contains the coronatine insensitive1 (COI1) F-box protein. This interaction leads to the JAZ degradation which is negative regulator of MYC2. Inactive JAZ is not able to repress MYC2 function which in turn activates JA-responsive genes. MeJA induces the formation of ROS and NO, which activate the efflux of Ca2+ from internal stores and the influx from the apoplast by channels in plasma membrane. CPK6 acts downstream of NO and ROS signaling and therefore may be the target of an NO-stimulated influx of Ca2+ into the cytoplasm. As a feedback loop, MeJA-induced influx of Ca2+ into the cytoplasm activates CPK6, which in turn is able to activate the S-type anion channel – SLAC1, which then leads to the MeJA-stimulated stomatal closure. Figure 6: Hormonal crosstalk in the regulation of stomatal closure and opening during water stress. The regulation of stomatal opening and closure is not only regulated by ABA, whose role is dominant, but also by other phytohormones. Jasmonates (JA) and brassinosteroids (BR) induce stomatal closure and inhibit stomatal opening under drought conditions, whereas the role of other hormones is ambiguous. Cytokinins (CK) and auxins (AUX) in low physiological concentrations promote stomatal opening while in high concentrations, they are able to inhibit this process. The role of ethylene (ET) is the most curious. It can stimulate the closing and opening of the stomata. The details are described in the text.
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References
  1. F. B. Abeles; P. W. Morgan; M. E. Saltveit Ethylene in Plant Biology , (1992) .
    • . . . However, most of them described experiments with detached leaves, which may not reflect the response of intact plants under drought conditions (Morgan et al., 1990; Abeles et al., 1992) . . .
    • . . . Another crucial problem is that most reports describe experiments with detached leaves, which may not reflect the response of intact plants under drought conditions (Morgan et al., 1990; Abeles et al., 1992; Dodd, 2012) . . .
  2. T. Berleth; T. Sachs Plant morphogenesis: long-distance coordination and local patterning Curr. Opin. Plant Biol. 4, 57-62 (2001) .
    • . . . Auxins and cytokinins are major phytohormones that are involved in processes related to plant growth and development such as cell division, growth and organogenesis, vascular differentiation, lateral root initiation as well as gravi- and phototropism (Berleth and Sachs, 2001) . . .
  3. M. R. Blatt; F. Armstrong K+ channels of stomatal guard cells: abscisic-acid evoked control of the outward rectifier mediated by cytoplasmic pH Planta 191, 330-341 (1993) .
    • . . . It was shown that the activity of KAT1 is inhibited by an elevation of ABA and cytosolic Ca2+ (Schroeder and Hagiwara, 1989; Blatt and Armstrong, 1993; Grabov and Blatt, 1999) via phosphorylation by SnRK, which in turn results in a decreased influx of K+ into the guard cells (Hubbard et al., 2010) . . .
  4. M. R. Blatt; G. Thiel K+ channels of stomatal guard cells: bimodal control of the K+ inward-rectifier evoked by auxin Plant J. 5, 55-68 (1994) .
    • . . . Low auxin concentrations activate inward K+ channels leading to stomatal opening, whereas high auxin level promotes outward K+ channels, while simultaneously inhibiting inward K+ channels, which results in stomatal closure (Lohse and Hedrich, 1992; Blatt and Thiel, 1994). . . .
  5. A. B. Bleecker; H. Kende Ethylene: a gaseous signal molecule in plants Annu. Rev. Cell Dev. Biol. 16, 1-18 (2000) .
    • . . . Ethylene is a gaseous phytohormone that is involved in the regulation of numerous plant processes such as seed germination, root-hair growth, leaf and flower senescence and abscission, fruit ripening, nodulation, and plant responses to stresses (Bleecker and Kende, 2000) . . .
  6. G. L. Boyer; J. Zeevaart Isolation and quantitation of β-d-glucopyranosyl abscisate from leaves of Xanthium and spinach Plant Physiol. 70, 227-231 (1982) .
    • . . . The most widespread conjugate is ABA glucosyl ester (ABA-GE), which is catalyzed by ABA glucosyltransferase (Boyer and Zeevaart, 1982) . . .
  7. J. Bright; R. Desikan; J. T. Hancock; I. S. Weir; S. J. Neill ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis Plant J. 45, 113-122 (2006) .
    • . . . Conversely, NO neither stimulates H2O2 synthesis nor does it require H2O2 for its action (Bright et al., 2006). . . .
  8. R. C. Cañamero; H. Boccalandro; J. Casal; L. Serna Use of confocal laser as light source reveals stomata-autonomous function PLoS ONE 1, e36 (2006) .
    • . . . Recently, a popular technique in stomatal observations is confocal microscopy (Cañamero et al., 2006) . . .
  9. W. H. Cheng; A. Endo; L. Zhou; J. Penney; H. C. Chen; A. Arroyo A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions Plant Cell 14, 2723-2743 (2002) .
    • . . . The first step is catalyzed by a short-chain alcohol dehydrogenase/reductase (SDR) that is encoded by the AtABA2 (ABA deficient 2) gene (Rook et al., 2001; Cheng et al., 2002; Gonzalez-Guzman et . . .
    • . . . Cheng et al. (2002) reported that the AtNCED3, AtZEP (Zeaxanthin epoxidase), and AtAAO3 (ABA-aldehyde oxidase) genes could be induced in Arabidopsis by ABA and studies in rice showed that OsNCED3 expression was induced by dehydration (Ye et al., 2011) . . .
  10. A. Chini; S. Fonseca; G. Fernández; B. Adie; J. M. Chico; O. Lorenzo The JAZ family of repressors is the missing link in jasmonate signalling Nature 448, 666-671 (2007) .
    • . . . This interaction leads to the degradation of the repressor protein, JAZ (Jasmonate ZIM-domain), by the 26S proteasome and as a result, to the activation of distinct JA response genes by MYC2 (MYC domain transcription factor 2) (Chini et al., 2007; Thines et . . .
  11. S. D. Clouse; J. M. Sasse BRASSINOSTEROIDS: essential regulators of plant growth and development Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 427-451 (1998) .
    • . . . Brassinosteroids (BR) are polyhydroxylated steroidal phytohormones that are involved in seed germination, stem elongation, vascular differentiation, and fruit ripening (Clouse and Sasse, 1998; Steber and McCourt, 2001; Symons et al., 2006) . . .
  12. E. Cominelli; M. Galbiati; A. Vavasseur; L. Conti; T. Sala; M. Vuylsteke A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance Curr. Biol. 15, 1196-1200 (2005) .
  13. R. Desikan; K. Last; R. Harrett-Williams; C. Tagliavia; K. Harter; R. Hooley Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis Plant J. 47, 907-916 (2006) .
    • . . . Desikan et al. (2006) proved that ethylene-mediated stomatal closure is dependent on the H2O2 that is generated by NADPH oxidase . . .
  14. K. J. Dietz; A. Sauter; K. Wichert; D. Messdaghi; W. Hartung Extracellular β-glucosidase activity in barley involved in the hydrolysis of ABA glucose conjugate in leaves J. Exp. Bot. 51, 937-944 (2000) .
    • . . . Abscisic acid is synthesized in the plastids and cytosol, mainly in the vascular parenchyma cells but also in the guard cells, through the cleavage of a C40 carotenoid precursor, followed by a two-step conversion of the intermediate xanthoxin into ABA via ABA-aldehyde (Taylor et al., 2000; Finkelstein and Rock, 2002; Schwartz et al., 2003; Endo et al., 2008; Melhorn et al., 2008) . . .
  15. Z. Ding; S. Li; X. An; X. Liu; H. Qin; D. Wang Transgenic expression of MYB15 confers enhanced sensitivity to abscisic acid and improved drought tolerance in Arabidopsis thaliana J. Genet. Genomics 36, 17-29 (2009) .
  16. I. A. Dodd Abscisic acid and stomatal closure: a hydraulic conductance conundrum? New Phytol. 197, 6-8 (2012) .
    • . . . Another crucial problem is that most reports describe experiments with detached leaves, which may not reflect the response of intact plants under drought conditions (Morgan et al., 1990; Abeles et al., 1992; Dodd, 2012) . . .
  17. A. Endo; Y. Sawada; H. Takahashi; M. Okamoto; K. Ikegami; H. Koiwai Drought induction of Arabidopsis 9-cis-epoxycarotenoid dioxygenase occurs in vascular parenchyma cells Plant Physiol. 147, 1984-1993 (2008) .
    • . . . Abscisic acid is synthesized in the plastids and cytosol, mainly in the vascular parenchyma cells but also in the guard cells, through the cleavage of a C40 carotenoid precursor, followed by a two-step conversion of the intermediate xanthoxin into ABA via ABA-aldehyde (Taylor et al., 2000; Finkelstein and Rock, 2002; Schwartz et al., 2003; Endo et al., 2008; Melhorn et . . .
    • . . . These data indicate that drought-induced ABA biosynthesis occurs primarily in the vascular parenchyma cells and that vascular-derived ABA might trigger stomatal closure via the transport to the guard cells (Endo et al., 2008) . . .
  18. P. Fernández-Calvo; A. Chini; G. Fernández-Barbero; J. M. Chico; S. Gimenez-Ibanez; J. Geerinck The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses Plant Cell 23, 701-715 (2011) .
    • . . . This interaction leads to the degradation of the repressor protein, JAZ (Jasmonate ZIM-domain), by the 26S proteasome and as a result, to the activation of distinct JA response genes by MYC2 (MYC domain transcription factor 2) (Chini et al., 2007; Thines et al., 2007; Fernández-Calvo et al., 2011) . . .
  19. R. R. Finkelstein; C. D. Rock; C. R. Somerville; E. M. Meyerowitz “Abscisic acid biosynthesis and response,” The Arabidopsis Book , 1-52 (2002) .
    • . . . Abscisic acid is synthesized in the plastids and cytosol, mainly in the vascular parenchyma cells but also in the guard cells, through the cleavage of a C40 carotenoid precursor, followed by a two-step conversion of the intermediate xanthoxin into ABA via ABA-aldehyde (Taylor et al., 2000; Finkelstein and Rock, 2002; Schwartz et al., 2003; Endo et al., 2008; Melhorn et al., 2008) . . .
  20. J. T. Finn; M. E. Grunwald; K. W. Yau Cyclic nucleotide-gated ion channels: an extended family with diverse functions Annu. Rev. Physiol. 58, 395-426 (1996) .
    • . . . Ca2+ channels are encoded by genes from three gene-families: TPC1 (two-pore channel 1) (Peiter et al., 2005), CNGC (cyclic nucleotide gated channel) (Finn et al., 1996), and GLR (glutamate receptor) (Lacombe et al., 2001) . . .
  21. S. Fonseca; J. M. Chico; R. Solano The jasmonate pathway: the ligand, the receptor and the core signalling module Curr. Opin. Plant Biol. 12, 539-547 (2009) .
    • . . . JA-Ile is then bound by the receptor SCFCOI complex that contains the coronatine insensitive1 (COI1) F-box protein (Fonseca et al., 2009; Sheard et al., 2010) . . .
  22. P. J. Franks; G. D. Farquhar The mechanical diversity of stomata and its significance in gas-exchange control Plant Physiol. 143, 78-87 (2007) .
    • . . . Franks and Farquhar (2007) addressed the problem of data integration in stomatal research . . .
  23. S. Franz; B. Ehlert; A. Liese; J. Kurth; A.-C. Cazale; T. Romeis Calcium-dependent protein kinase CPK21 functions in abiotic stress response in Arabidopsis thaliana Mol. Plant. 4, 83-96 (2010) .
  24. A. T. Fuglsang; Y. Guo; T. A. Cuin; Q. Qiu; C. Song; K. A. Kristiansen Arabidopsis protein kinase PKS5 inhibits the plasma membrane H+ -ATPase by preventing interaction with 14-3-3 protein Plant Cell 19, 1617-1634 (2007) .
    • . . . The dominant Arabidopsis mutant ost2 (opened stomata 2) in AHA1 (H+-ATPase 1 HA1) gene exhibited the constitutive activation of AHA1 H+-ATPase, which in turn resulted in an inability to close stomata in response to ABA (Merlot et al., 2007) . . .
  25. H. Fujii; J. K. Zhu Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction and stress Proc. Natl. Acad. Sci. U.S.A. 106, 8380-8385 (2009) .
    • . . . The inactivation of PP2Cs allows downstream targets to be phosphorylated and activated – Sucrose Non-fermenting 1-Related subfamily 2 protein Kinases (SnRK2) (Fujii and Zhu, 2009; Fujita et al., 2009; Umezawa et al., 2009; Kim et al., 2010) . . .
    • . . . The inactivation of PP2Cs such as ABI1 and ABI2 by the complex ABA-receptor facilitates the phosphorylation and activation of a downstream target of phosphatases – SnRK2, such as SnRK2.2/D, SnRK2.3/E, and SnRK2.6/OST1/E, which are the key players in the regulation of ABA signaling and abiotic stress response (Fujii and Zhu, 2009; Fujita et al., 2009; Umezawa et al., 2009) . . .
  26. Y. Fujita; K. Nakashima; T. Yoshida; T. Katagiri; S. Kidokoro; N. Kanamori Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis Plant Cell Physiol. 50, 2123-2132 (2009) .
    • . . . After ABA is received from ABC transporters by the guard cells, the PYR/PYL/RCAR (pyrabactin-resistance 1/pyrabactin-resistance like/regulatory component of ABA receptor) perceives ABA intracellularly and forms complexes that inhibit clade A of PP2Cs (protein phosphatase 2C), the negative regulators of ABA signaling, such as ABI1 (ABA insensitive 1), ABI2 (ABA insensitive 2), HAB1 (hypersensitive to ABA1) (Ma et al., 2009; Park et . . .
    • . . . The inactivation of PP2Cs such as ABI1 and ABI2 by the complex ABA-receptor facilitates the phosphorylation and activation of a downstream target of phosphatases – SnRK2, such as SnRK2.2/D, SnRK2.3/E, and SnRK2.6/OST1/E, which are the key players in the regulation of ABA signaling and abiotic stress response (Fujii and Zhu, 2009; Fujita et al., 2009; Umezawa et . . .
  27. C. A. Gehring; H. R. Irving; R. McConchie; R. W. Parish Jasmonates induce intracellular alkalinization and closure of Paphiopedilum the guard cells Ann. Bot. 80, 485-489 (1997) .
    • . . . The positive role of JA in the regulation of stomatal closure was observed in many studies (Gehring et al., 1997; Suhita et al., 2003, 2004; Munemasa et al., 2007) . . .
  28. D. Geiger; S. Scherzer; P. Mumm; I. Marten; P. Ache; S. Matschi Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities Proc. Natl. Acad. Sci. U.S.A. 107, 8023-8028 (2010) .
    • . . . SLAC1 phosphorylation, in turn, results in the activation of anion and the efflux of K+ (Geiger et al., 2010) . . .
    • . . . Geiger et al. (2010) showed a direct interaction between CPK6 and the SLAC1 – S-type anion channel . . .
  29. M. Gonzalez-Guzman; N. Apostolova; J. M. Belles; J. M. Barrero; P. Piqueras; M. R. Ponce The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde Plant Cell 14, 1833-1846 (2002) .
    • . . . The first step is catalyzed by a short-chain alcohol dehydrogenase/reductase (SDR) that is encoded by the AtABA2 (ABA deficient 2) gene (Rook et al., 2001; Cheng et al., 2002; Gonzalez-Guzman et . . .
  30. A. Grabov; M. R. Blatt A steep dependence of inward rectifying potassium channels on cytosolic free calcium concentration increase evoked by hyperpolarization in the guard cells Plant Physiol. 119, 277-288 (1999) .
    • . . . It was shown that the activity of KAT1 is inhibited by an elevation of ABA and cytosolic Ca2+ (Schroeder and Hagiwara, 1989; Blatt and Armstrong, 1993; Grabov and Blatt, 1999) via phosphorylation by SnRK, which in turn results in a decreased influx of K+ into the guard cells (Hubbard et al., 2010) . . .
  31. F.-Q. Guo; J. Young; N. M. Crawford The nitrate transporter AtNRT1.1 (CHL1) functions in stomatal opening and contributes to drought susceptibility in Arabidopsis Plant Cell 15, 107-117 (2003) .
  32. D. W. A. Hamilton; A. Hills; B. Köhler; M. R. Blatt Ca2+ channels at the plasma membrane of stomatal guard cells are activated by hyperpolarization and abscisic acid Proc. Natl. Acad. Sci. U.S.A. 97, 4967-4972 (2000) .
    • . . . Abscisic acid activates the Ca2+-permeable channels in the PM of the guard cells and triggers an influx of Ca2+ into the cytoplasm of the guard cells through the release of the second messenger, inositol-1,4,5-triphosphate (IP3), which in turn activates the Ca2+ channels that are located in the vacuole and endoplasmic reticulum (Schroeder and Hagiwara, 1990; Hamilton et al., 2000; Krinke et al., 2007; Kwak et al., 2008) . . .
  33. L. L. Haubrick; G. Torsethaugen; S. M. Assmann Effect of brassinolide, alone and in concert with abscisic acid, on control of stomatal aperture and potassium currents of Vicia faba guard cell protoplasts Physiol. Plant 128, 134-143 (2006) .
    • . . . Brassinosteroids (BR) are polyhydroxylated steroidal phytohormones that are involved in seed germination, stem elongation, vascular differentiation, and fruit ripening (Clouse and Sasse, 1998; Steber and McCourt, 2001; Symons et al., 2006) . . .
  34. M. A. Hossain; S. Munemasa; M. Uraji; Y. Nakamura; I. C. Mori; Y. Murata Involvement of endogenous abscisic acid in methyl jasmonate-induced stomatal closure in Arabidopsis Plant Physiol. 156, 430-438 (2011) .
    • . . . In order to clarify this hypothesis, Hossain et al. (2011) examined the effect of 0.1 μM of ABA on MeJA-induced stomatal closure in aba 2-2 (ABA deficient 2-2) mutants related to ABA biosynthesis . . .
  35. E. Hosy; A. Vavasseur; K. Mouline; I. Dreyer; F. Gaymard; F. Poree The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration Proc. Natl. Acad. Sci. U.S.A. 100, 5549-5554 (2003) .
  36. H. Hu; A. Boisson-Dernier; M. Israelsson-Nordström; M. Böhmer; S. Xue; A. Ries Carbonic anhydrases are upstream regulators in the guard cells of CO2-controlled stomatal movements Nat. Cell Biol. 12, 87-93 (2010) .
    • . . . The guard cells probably do not sense CO2 molecules but instead HCO3- is synthesized from CO2 (Hu et al., 2010), which activates S-type channels and leads to the efflux of Cl−, malate2−, and NO3- (Xue et al., 2011) (Figure 3A). . . .
  37. D. Huang; W. Wu; S. R. Abrams; A. J. Cutler The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors J. Exp. Bot. 59, 2991-3007 (2008) .
    • . . . This rapid reaction is regulated by a complex network of signaling pathways, in which the major and the best-known player, abscisic acid (ABA), acts in concert with jasmonates (JA), ethylene, auxins, and cytokinins (Nemhauser et al., 2006; Huang et al., 2008) . . .
    • . . . Jasmonates are lipid-derived phytohormones that are involved in the regulation of vegetative and reproductive growth and the defense response against abiotic stress (Katsir et al., 2008) . . .
  38. K. E. Hubbard; N. Nishimura; K. Hitomi; E. D. Getzoff; J. I. Schroeder Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions Genes Dev. 24, 1695-1708 (2010) .
    • . . . It was shown that the activity of KAT1 is inhibited by an elevation of ABA and cytosolic Ca2+ (Schroeder and Hagiwara, 1989; Blatt and Armstrong, 1993; Grabov and Blatt, 1999) via phosphorylation by SnRK, which in turn results in a decreased influx of K+ into the guard cells (Hubbard et al., 2010) . . .
  39. V. Hugouvieux; Y. Murata; J. J. Young; J. M. Kwak; D. Z. Mackesy; J. I. Schroeder Localization, ion channel regulation and genetic interactions during abscisic acid signaling of the nuclear mRNA cap-binding protein, ABH1 Plant Physiol. 130, 1276-1287 (2002) .
  40. G. D. Humble; K. Raschke Stomatal opening quantitatively related to potassium transport: evidence from electron probe analysis Plant Physiol. 48, 447-453 (1971) .
    • . . . K+ uptake is mainly responsible for the rapid increase of the turgor and the opening of stomata during the dawn (Humble and Raschke, 1971; Talbott and Zeiger, 1996) . . .
  41. L. Jeanguenin; A. Lebaudy; J. Xicluna; C. Alcon; E. Hosy; G. Duby Heteromerization of Arabidopsis Kv channel a-subunits Plant Signal. Behav. 3, 622-625 (2008) .
    • . . . Membrane depolarization creates a driving force for the efflux of K+ via K+ outwardly rectifying channels such as GORK (guard cell outwardly rectifying K+ channel) (Jeanguenin et al., 2008) . . .
    • . . . The slac1 mutant displayed a strongly impaired response to a range of stomatal closing stimuli such as ABA and Ca2+ (Negi et al., 2008; Vahisalu et . . .
  42. C. Jung; J. S. Seo; S. W. Han; Y. J. Koo; C. H. Kim; S. I. Song Overexpression of AtMYB44 enhances stomatal closure to confer abiotic stress tolerance in transgenic Arabidopsis Plant Physiol. 146, 623-635 (2007) .
  43. S. Kagale; U. K. Divi; J. E. Krochko; W. A. Keller; P. Krishna Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses Planta 225, 353-364 (2007) .
    • . . . It has been shown that epibrassinolide (eBL) promotes stomatal closure and inhibits stomatal opening in epidermal peels of Vicia faba through the negative regulation of the inwardly rectifying K+ channels that are responsible for the uptake of K+ during stomatal opening (Haubrick et al., 2006; Figure 6). eBL is able to activate the transcription of drought-inducible genes in Arabidopsis, such as RD29A (response to drought 29A), ERD10 (early response to drought 10), and RD22 (rehydration responsive 22) (Kagale et al., 2007) . . .
  44. L. Katsir; H. S. Chung; A. J. Koo; G. A. Howe Jasmonate signaling: a conserved mechanism of hormone sensing Curr. Opin. Plant Biol. 11, 428-435 (2008) .
    • . . . Jasmonates are lipid-derived phytohormones that are involved in the regulation of vegetative and reproductive growth and the defense response against abiotic stress (Katsir et al., 2008) . . .
  45. M. J. Kim; R. Shin; D. P. Schachtman A nuclear factor regulates abscisic acid responses in Arabidopsis Plant Physiol. 151, 1433-1445 (2009) .
  46. T.-H. Kim; M. Bohmer; H. Hu; N. Nishimura; J. I. Schroeder Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling Annu. Rev. Plant Biol. 61, 561-591 (2010) .
    • . . . Opening and closing is achieved by the swelling and shrinking of the guard cells, which is driven by ion exchange; cytoskeleton reorganization and metabolite production; the modulation of gene expression and the posttranslational modification of proteins (reviewed in Kim et al., 2010) . . .
    • . . . After ABA is received from ABC transporters by the guard cells, the PYR/PYL/RCAR (pyrabactin-resistance 1/pyrabactin-resistance like/regulatory component of ABA receptor) perceives ABA intracellularly and forms complexes that inhibit clade A of PP2Cs (protein phosphatase 2C), the negative regulators of ABA signaling, such as ABI1 (ABA insensitive 1), ABI2 (ABA insensitive 2), HAB1 (hypersensitive to ABA1) (Ma et al., 2009; Park et al., 2009; Santiago et al., 2009; Nishimura et al., 2010) . . .
  47. B. Kohler; A. Hills; M. R. Blatt Control of guard cell ion channels by hydrogen peroxide and abscisic acid indicates their action through alternate signaling pathways Plant Physiol. 131, 385-388 (2003) .
    • . . . Exogenous H2O2 activates permeable Ca2+ channels in the PM of Arabidopsis guard cells and inhibits inward K+ channels (Zhang et al., 2001; Kohler et al., 2003; Kwak et . . .
    • . . . In addition, H2O2 inhibits K+ channel activity, induces cytosolic alkalization in the guard cells and promotes NO signaling in response to ABA (Zhang et al., 2001; Kohler et al., 2003; Wang and Song, 2008) . . .
  48. O. Krinke; Z. Novotna; O. Valentova; J. Martinec Inositol trisphosphate receptor in higher plants: is it real? J. Exp. Bot. 58, 361-376 (2007) .
    • . . . Abscisic acid activates the Ca2+-permeable channels in the PM of the guard cells and triggers an influx of Ca2+ into the cytoplasm of the guard cells through the release of the second messenger, inositol-1,4,5-triphosphate (IP3), which in turn activates the Ca2+ channels that are located in the vacuole and endoplasmic reticulum (Schroeder and Hagiwara, 1990; Hamilton et al., 2000; Krinke et al., 2007; Kwak et al., 2008) . . .
  49. T. Kuromori; T. Miyaji; H. Yabuuchi; H. Shimizu; E. Sugimoto; A. Kamiya ABC transporter AtABCG25 is involved in abscisic acid transport and responses Proc. Natl. Acad. Sci. U.S.A. 107, 2361-2366 (2010) .
    • . . . ABCG25 is expressed primarily in vascular tissues where ABA is synthesized (Kuromori et al., 2010) . . .
  50. T. Kuromori; E. Sugimoto; K. Shinozaki Arabidopsis mutants of AtABCG22, an ABC transporter gene, increase water transpiration and drought susceptibility Plant J. 67, 885-894 (2011) .
    • . . . Kuromori et al. (2011) identified the ABA importer – ABCG22 (Arabidopsis thaliana ATP-binding cassette G22) . . .
    • . . . This is probably caused by an intensive ABA accumulation through the biosynthesis of ABA in the guard cells and the simultaneous import of endogenous ABA from the apoplast to the guard cells using ABA transporters such as ABCG22 (Kuromori et al., 2011), while at the same time, ABA catabolism processes are disfavored . . .
  51. T. Kushiro; M. Okamoto; K. Nakabayashi; K. Yamagishi; S. Kitamura; T. Asami The Arabidopsis cytochrome P450 CYP707A encodes ABA 8’-hydroxylases: key enzymes in ABA catabolism EMBO J. 23, 1647-1656 (2004) .
    • . . . Then, the ABA-aldehyde oxidase (AAO) with the molybdenum cofactor (MoCo) catalyzes the last step in the biosynthesis pathway – the conversion of ABA-aldehyde into ABA (Seo et al., 2004) (Figure 2A) . . .
  52. J. M. Kwak; P. Mäser; J. I. Schroeder The clickable guard cell, version II: interactive model of guard cell signal transduction mechanisms and pathways Arabidopsis Book 6, e0114 (2008) .
    • . . . Abscisic acid activates the Ca2+-permeable channels in the PM of the guard cells and triggers an influx of Ca2+ into the cytoplasm of the guard cells through the release of the second messenger, inositol-1,4,5-triphosphate (IP3), which in turn activates the Ca2+ channels that are located in the vacuole and endoplasmic reticulum (Schroeder and Hagiwara, 1990; Hamilton et al., 2000; Krinke et al., 2007; Kwak et al., 2008) . . .
  53. J. M. Kwak; J. H. Moon; Y. Murata; K. Kuchitsu; N. Leonhardt; A. DeLong Disruption of a guard cell-expressed protein phosphatase 2A regulatory subunit, RCN1, confers abscisic acid insensitivity in Arabidopsis Plant Cell 14, 2849-2861 (2002) .
    • . . . Disruption of the regulatory subunit RCN1 (roots curl in NPA) of the gene encoding PP2A (protein phosphatase 2A) led to a reduction of the ABA activation of anion channels and a decreased sensitivity of stomata to ABA (Kwak et al., 2002, Figure 4). . . .
  54. J. M. Kwak; I. C. Mori; Z. M. Pei; N. Leonhardt; M. A. Torres; J. L. Dangl NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis EMBO J. 22, 2623-2633 (2003) .
  55. B. Lacombe; D. Becker; R. Hedrich; R. DeSalle; M. Hollmann; J. M. Kwak The identity of plant glutamate receptors Science 292, 1486-1487 (2001) .
    • . . . Ca2+ channels are encoded by genes from three gene-families: TPC1 (two-pore channel 1) (Peiter et al., 2005), CNGC (cyclic nucleotide gated channel) (Finn et al., 1996), and GLR (glutamate receptor) (Lacombe et al., 2001) . . .
  56. O. S. Lau; D. C. Bergmann Stomatal development: a plant’s perspective on cell polarity, cell fate transitions and intercellular communication Development 139, 3683-3692 (2012) .
    • . . . For this reason, neighbor cells are part of a stomatal complex (Nadeau and Sack, 2002; Nadeau, 2009; Lau and Bergmann, 2012; Pillitteri and Torii, 2012; Vatén and . . .
  57. T. Lawson; W. James; J. Weyers A surrogate measure of stomatal aperture J. Exp. Bot. 49, 1397-1403 (1998) .
    • . . . In contrast, scanning microscopy (SEM) offers high resolution images of stomata but requires expensive equipment and is not suitable for collecting large numbers of probes (Lawson et al., 1998) . . .
  58. K. H. Lee; H. L. Piao; H. Y. Kim; S. M. Choi; F. Jian; W. Hartung Activation of glucosidase via stress-induced polymerization rapidly increased active pools of abscisic acid Cell 126, 1109-1120 (2006) .
    • . . . Lee et al. (2006) identified the AtBG1 (beta-1,3-glucanase 1) protein that is responsible for the release of ABA from ABA-GE . . .
  59. N. Leonhardt; A. Vavasseur; C. Forestier ATP binding cassette modulators control abscisic acid-regulated slow anion channels in the guard cells Plant Cell 11, 1141-1152 (1999) .
    • . . . In different species, S-type anion channels are activated in the guard cells by ABA, cytosolic Ca2+, and phosphorylation events (Schmidt et al., 1995; Pei et al., 1997; Leonhardt et al., 1999; Raschke et al., 2003; Roelfsema et al., 2004; Mori et al., 2006) . . .
  60. J. Leung; J. Giraudat Abscisic acid signal transduction Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 199-222 (1998) .
    • . . . The physiological mechanism of ethylene inhibition of the ABA-mediated stomatal closure may be related to the function of ethylene as a factor that ensures a minimum carbon dioxide supply for photosynthesis by keeping stomata half-opened under the stress conditions (Leung and Giraudat, 1998; Tanaka et al., 2005). . . .
  61. L. K. Levitt; D. B. Stein; B. Rubinstein Promotion of stomatal opening by indoleacetic acid and ethrel in epidermal strips of Vicia faba L Plant Physiol. 85, 318-321 (1987) .
    • . . . Ethylene has been linked to the promotion of both stomatal closure (Pallas and Kays, 1982) and stomatal opening (Madhavan et al., 1983; Levitt et al., 1987; Merritt et al., 2001; Figure 6) . . .
  62. W. X. Li; Y. Oono; J. Zhu; X. J. He; J. M. Wu; K. Iida The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance Plant Cell 20, 2238-2251 (2008) .
  63. Y. K. Liang; C. Dubos; I. C. Dodd; G. H. Holroyd; A. M. Hetherington; M. M. Campbell AtMYB61, an R2R3-MYB transcription factor controlling stomatal aperture in Arabidopsis thaliana Curr. Biol. 15, 1201-1206 (2005) .
  64. Y.-C. Liu; Y.-R. Wu; X.-H. Huang; J. Sun; Q. Xie AtPUB19, a U-Box E3 ubiquitin ligase, negatively regulates abscisic acid and drought responses in Arabidopsis thaliana Mol. Plant. 6, 938-946 (2011) .
  65. G. Lohse; R. Hedrich Characterization of the plasma-membrane H+-ATPase from Vicia faba guard cells Planta 188, 206-214 (1992) .
    • . . . Auxins typically play a positive role in stomatal opening but high concentrations of auxin can inhibit stomatal opening (Lohse and Hedrich, 1992; Figure 6) . . .
  66. Y. Ma; I. Szostkiewicz; A. Korte; D. Moes; Y. Yang; A. Christmann Regulators of PP2C phosphatase activity functions as abscisic acid sensors Science 324, 1064-1068 (2009) .
    • . . . After ABA is received from ABC transporters by the guard cells, the PYR/PYL/RCAR (pyrabactin-resistance 1/pyrabactin-resistance like/regulatory component of ABA receptor) perceives ABA intracellularly and forms complexes that inhibit clade A of PP2Cs (protein phosphatase 2C), the negative regulators of ABA signaling, such as ABI1 (ABA insensitive 1), ABI2 (ABA insensitive 2), HAB1 (hypersensitive to ABA1) (Ma et al., 2009; Park et . . .
    • . . . Recently, the core signalosome of ABA signaling including ABA receptors, phosphatases (PP2Cs), and kinases (SnRK2s) was established (Ma et al., 2009; Park et . . .
  67. E. A. C. MacRobbie Control of volume and turgor in stomatal guard cells J. Membr. Biol. 210, 131-142 (2006) .
    • . . . Another event that accompanies stomatal closure is an elevation of the cytoplasmic Ca2+ concentration as a result of Ca2+-release via channels situated in both the PM and in the tonoplast (MacRobbie, 2006) . . .
  68. S. Madhavan; A. Chrmoinski; B. N. Smith Effect of ethylene on stomatal opening in tomato and carnation leaves Plant Cell Physiol. 24, 569-572 (1983) .
    • . . . Ethylene has been linked to the promotion of both stomatal closure (Pallas and Kays, 1982) and stomatal opening (Madhavan et al., 1983; Levitt et al., 1987; Merritt et al., 2001; Figure 6) . . .
  69. E. Marin; L. Nussaume; A. Quesada; M. Gonneau; B. Sotta; P. Hugueney Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and corresponding to the ABA locus of Arabidopsis thaliana EMBO J. 15, 2331-2342 (1996) .
    • . . . The next step is the epoxidation of zeaxanthin and antheraxanthin into violaxanthin, which is then catalyzed by zeaxanthin epoxidase (ZEP) (Marin et al., 1996) . . .
  70. V. Melhorn; K. Matsumi; H. Koiwai; K. Ikegami; M. Okamoto; E. Nambara Transient expression of AtNCED3 and AAO3 genes in the guard cells causes stomatal closure in Vicia faba J. Plant Res. 121, 125-131 (2008) .
    • . . . Abscisic acid is synthesized in the plastids and cytosol, mainly in the vascular parenchyma cells but also in the guard cells, through the cleavage of a C40 carotenoid precursor, followed by a two-step conversion of the intermediate xanthoxin into ABA via ABA-aldehyde (Taylor et al., 2000; Finkelstein and Rock, 2002; Schwartz et al., 2003; Endo et al., 2008; Melhorn et . . .
  71. S. Merlot; N. Leonhardt; F. Fenzi; C. Valon; M. Costa; L. Piette Constitutive activation of a plasma membrane H+-ATPase prevents abscisic acid-mediated stomatal closure EMBO J. 26, 3216-3226 (2007) .
  72. F. Merritt; A. Kemper; G. Tallman Inhibitors of ethylene synthesis inhibit auxin-induced stomatal opening in epidermis detached from leaves of Vicia faba L Plant Cell Physiol. 42, 223-230 (2001) .
    • . . . Ethylene has been linked to the promotion of both stomatal closure (Pallas and Kays, 1982) and stomatal opening (Madhavan et al., 1983; Levitt et al., 1987; Merritt et al., 2001; Figure 6) . . .
  73. S. Meyer; P. Mumm; D. Imes; A. Endler; B. Weder; K. A. S. Al-Rasheid AtALMT12 represents an R-type anion channel required for stomatal movement in Arabidopsis guard cells Plant J. 63, 1054-1062 (2010) .
  74. P. W. Morgan; C. J. He; J. A. De Greef; M. P. De Proft Does water deficit stress promote ethylene synthesis by intact plants? Plant Physiol. 94, 1616-1624 (1990) .
    • . . . However, most of them described experiments with detached leaves, which may not reflect the response of intact plants under drought conditions (Morgan et al., 1990; Abeles et al., 1992) . . .
    • . . . Another crucial problem is that most reports describe experiments with detached leaves, which may not reflect the response of intact plants under drought conditions (Morgan et al., 1990; Abeles et al., 1992; Dodd, 2012) . . .
  75. I. C. Mori; Y. Murata; Y. Yang; S. Munemasa; Y. F. Wang; S. Andreoli CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion and Ca2+-permeable channels and stomatal closure PLoS Biol. 4, e327 (2006) .
  76. S. Munemasa; M. A. Hossain; Y. Nakamura; I. C. Mori; Y. Murata The Arabidopsis calcium dependent protein kinase, CPK6, functions as a positive regulator of methyl jasmonate signaling in the guard cells Plant Physiol. 155, 553-561 (2011) .
  77. S. Munemasa; K. Oda; M. Watanabe-Sugimoto; Y. Nakamura; Y. Shimoishi; Y. Murata The coronatine-insensitive 1 mutation reveals the hormonal signaling interaction between abscisic acid and methyl jasmonate in Arabidopsis guard cells. Specific impairment of ion channel activation and second messenger production Plant Physiol. 143, 1398-1407 (2007) .
  78. A. C. Mustilli; S. Merlot; A. Vavasseur; F. Fenzi; J. Giraudat Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production Plant Cell 14, 3089-3099 (2002) .
    • . . . Mutants in OST1 showed a wilty phenotype in water deficit conditions because of the impairment of stomatal closure and ROS production (Mustilli et al., 2002; Yoshida et al., 2006; Figure 4). . . .
  79. J. A. Nadeau Stomatal development: new signals and fate determinants Curr. Opin. Plant Biol. 12, 29-35 (2009) .
    • . . . For this reason, neighbor cells are part of a stomatal complex (Nadeau and Sack, 2002; Nadeau, 2009; Lau and Bergmann, 2012; Pillitteri and Torii, 2012; Vatén and Bergmann, 2012) . . .
  80. J. A. Nadeau; F. D. Sack Stomatal development in Arabidopsis Arabidopsis Book 1, e0066 (2002) .
    • . . . For this reason, neighbor cells are part of a stomatal complex (Nadeau and Sack, 2002; Nadeau, 2009; Lau and Bergmann, 2012; Pillitteri and Torii, 2012; Vatén and Bergmann, 2012) . . .
  81. J. Negi; O. Matsuda; T. Nagasawa; Y. Oba; H. Takahashi; M. Kawai-Yamada CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells Nature 452, 483-486 (2008) .
    • . . . The slac1 mutant displayed a strongly impaired response to a range of stomatal closing stimuli such as ABA and Ca2+ (Negi et al., 2008; Vahisalu et . . .
  82. S. Neill; R. Barros; J. Bright; R. Desikan; J. Hancock; J. Harrison Nitric oxide, stomatal closure and abiotic stress J. Exp. Bot. 59, 165-176 (2008) .
    • . . . Another crucial factor for stomatal closure is NO, which is generated in response to ABA (Neill et al., 2002, 2008) . . .
  83. S. J. Neill; R. Desikan; A. Clarke; J. T. Hancock Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells Plant Physiol. 128, 13-16 (2002) .
    • . . . Another crucial factor for stomatal closure is NO, which is generated in response to ABA (Neill et al., 2002, 2008) . . .
  84. J. L. Nemhauser; F. Hong; J. Chory Different plant hormones regulate similar processes through largely non-overlapping transcriptional responses Cell 126, 467-475 (2006) .
    • . . . This rapid reaction is regulated by a complex network of signaling pathways, in which the major and the best-known player, abscisic acid (ABA), acts in concert with jasmonates (JA), ethylene, auxins, and cytokinins (Nemhauser et al., 2006; Huang et al., 2008) . . .
  85. N. Nishimura; A. Sarkeshik; K. Nito; S. Y. Park; A. Wang; P. C. Carvalho PYR/PYL/RACR family members are major in vivo ABI1 protein phosphatase 2C interacting proteins in Arabidopsis Plant J. 61, 290-299 (2010) .
    • . . . After ABA is received from ABC transporters by the guard cells, the PYR/PYL/RCAR (pyrabactin-resistance 1/pyrabactin-resistance like/regulatory component of ABA receptor) perceives ABA intracellularly and forms complexes that inhibit clade A of PP2Cs (protein phosphatase 2C), the negative regulators of ABA signaling, such as ABI1 (ABA insensitive 1), ABI2 (ABA insensitive 2), HAB1 (hypersensitive to ABA1) (Ma et al., 2009; Park et al., 2009; Santiago et al., 2009; Nishimura et al., 2010) . . .
    • . . . Recently, the core signalosome of ABA signaling including ABA receptors, phosphatases (PP2Cs), and kinases (SnRK2s) was established (Ma et al., 2009; Park et al., 2009; Santiago et al., 2009; Nishimura et al., 2010) . . .
  86. H. M. North; A. De Almeida; J. P. Boutin; A. Frey; A. To; L. Botran The Arabidopsis ABA-deficient mutant aba4 demonstrates that the major route for stress-induced ABA accumulation is via neoxanthin isomers Plant J. 50, 810-824 (2007) .
    • . . . After a series of violaxanthin modifications that are controlled by the enzyme ABA4, violaxanthin is converted into 9-cis-epoxycarotenoid (North et al., 2007) . . .
  87. W. H. Outlaw Integration of cellular and physiological functions of the guard cells CRC Crit. Rev. Plant Sci. 22, 503-529 (2003) .
    • . . . It has been shown that ABA concentrations can increase up to 30-fold in response to drought stress (Outlaw, 2003) . . .
  88. J. E. Pallas; S. J. Kays Inhibition of photosynthesis by ethylene-a stomatal effect Plant Physiol. 70, 598-601 (1982) .
    • . . . Ethylene has been linked to the promotion of both stomatal closure (Pallas and Kays, 1982) and stomatal opening (Madhavan et al., 1983; Levitt et al., 1987; Merritt et al., 2001; Figure 6) . . .
  89. F. Parcy; J. Giraudat Interactions between the ABI1 and the ectopically expressed ABI3 genes in controlling abscisic acid responses in Arabidopsis vegetative tissues Plant J. 11, 693-702 (1997) .
  90. S. Y. Park; P. Fung; N. Nishimura; D. R. Jensen; H. Fujii; Y. Zhao Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins Science 324, 1068-1071 (2009) .
    • . . . After ABA is received from ABC transporters by the guard cells, the PYR/PYL/RCAR (pyrabactin-resistance 1/pyrabactin-resistance like/regulatory component of ABA receptor) perceives ABA intracellularly and forms complexes that inhibit clade A of PP2Cs (protein phosphatase 2C), the negative regulators of ABA signaling, such as ABI1 (ABA insensitive 1), ABI2 (ABA insensitive 2), HAB1 (hypersensitive to ABA1) (Ma et al., 2009; Park et . . .
    • . . . Recently, the core signalosome of ABA signaling including ABA receptors, phosphatases (PP2Cs), and kinases (SnRK2s) was established (Ma et al., 2009; Park et . . .
  91. Z. M. Pei; M. Ghassemian; C. M. Kwak; P. McCourt; J. I. Schroeder Role of farnesyltransferase in ABA regulation of guard cell anion channels and plant water loss Science 282, 287-290 (1998) .
  92. Z. M. Pei; K. Kuchitsu; J. M. Ward; M. Schwarz; J. I. Schroeder Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants Plant Cell 9, 409-423 (1997) .
  93. Z. M. Pei; Y. Murata; G. Benning; S. Thomine; B. Klusener; G. J. Allen Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in the guard cells Nature 406, 731-734 (2000) .
    • . . . The guard cells generate reactive oxygen species (ROS) such as hydrogen peroxide (H2O2) and nitric oxide (NO) in response to ABA (Pei et al., 2000; Zhang et al., 2001) . . .
  94. E. Peiter; F. J. M. Maathuis; L. N. Mills; H. Knight; J. Pelloux; A. M. Hetherington The vacuolar Ca2+- activated channel TPC1 regulates germination and stomatal movement Nature 434, 404-408 (2005) .
    • . . . Ca2+ channels are encoded by genes from three gene-families: TPC1 (two-pore channel 1) (Peiter et al., 2005), CNGC (cyclic nucleotide gated channel) (Finn et al., 1996), and GLR (glutamate receptor) (Lacombe et al., 2001) . . .
  95. L. J. Pillitteri; K. U. Torii Mechanisms of stomatal development Annu. Rev. Plant Biol. 63, 591-614 (2012) .
    • . . . For this reason, neighbor cells are part of a stomatal complex (Nadeau and Sack, 2002; Nadeau, 2009; Lau and Bergmann, 2012; Pillitteri and Torii, 2012; Vatén and Bergmann, 2012) . . .
  96. G. Pilot; B. Lacombe; F. Gaymard; I. Cherel; J. Boucherez; J. B. Thibaud Guard cell inward K+ channel activity in Arabidopsis involves expression of the twin channel subunits KAT1 and KAT2 J. Biol. Chem. 276, 3215-3221 (2001) .
    • . . . The efflux of H+ hyperpolarizes the PM and leads to K+ uptake via activation of inward K+ rectifying channels, such as KAT1 (potassium channel in Arabidopsis thaliana 1), KAT2 (potassium channel in Arabidopsis thaliana 2), and AKT1 (Arabidopsis thaliana K+ transporter 1) (Schachtman et al., 1992; Pilot et al., 2001; Szyroki et . . .
  97. J. Pospísilova Participation of phytohormones in the stomatal regulation of gas exchange during water stress Biol. Plant. 46, 491-506 (2003) .
    • . . . Drought stress inhibits the synthesis of cytokinins in roots and its transport to shoots, which in turn results in stomatal closure (Pospísilova, 2003; Pustovoitova et al., 2003) . . .
  98. T. N. Pustovoitova; I. S. Drozdova; N. E. Zhdanova; V. N. Zholkevich Leaf growth, photosynthetic rate and phytohormone contents in Cucumis sativus plants under progressive soil drought Russ. J. Plant Physiol. 50, 441-443 (2003) .
    • . . . Drought stress inhibits the synthesis of cytokinins in roots and its transport to shoots, which in turn results in stomatal closure (Pospísilova, 2003; Pustovoitova et al., 2003) . . .
  99. X. Qin; J. Zeevaart The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean Proc. Natl. Acad. Sci. U.S.A. 96, 15354-15361 (1999) .
    • . . . A significant increase in NCED transcript levels can be detected within 15–30 min after leaf detachment or dehydration treatment (Qin and Zeevaart, 1999; Thompson et al., 2000), which indicates that the activation of NCED genes can be fairly quick . . .
  100. K. Raschke; M. Shabahang; R. Wolf The slow and the quick anion conductance in whole guard cells: their voltage-dependent alternation, and the modulation of their activities by abscisic acid and CO2 Planta 217, 639-650 (2003) .
    • . . . In different species, S-type anion channels are activated in the guard cells by ABA, cytosolic Ca2+, and phosphorylation events (Schmidt et al., 1995; Pei et al., 1997; Leonhardt et al., 1999; Raschke et al., 2003; Roelfsema et al., 2004; Mori et al., 2006) . . .
  101. M. R. Roelfsema; R. Hedrich In the light of stomatal opening: new insights into ‘the Watergate’ New Phytol. 167, 665-691 (2005) .
    • . . . Anion channels such as rapid channels (R-type) and slow channels (S-type) facilitate the efflux of malate2−, Cl−, and NO3- (Roelfsema et al., 2004; Roelfsema and Hedrich, 2005) . . .
  102. M. R. Roelfsema; V. Levchenko; R. Hedrich ABA depolarizes the guard cells in intact plants, through a transient activation of R- and S-type anion channels Plant J. 37, 578-588 (2004) .
    • . . . Anion channels such as rapid channels (R-type) and slow channels (S-type) facilitate the efflux of malate2−, Cl−, and NO3- (Roelfsema et al., 2004; Roelfsema and Hedrich, 2005) . . .
    • . . . In different species, S-type anion channels are activated in the guard cells by ABA, cytosolic Ca2+, and phosphorylation events (Schmidt et al., 1995; Pei et al., 1997; Leonhardt et al., 1999; Raschke et al., 2003; Roelfsema et al., 2004; Mori et al., 2006) . . .
  103. F. Rook; F. Corke; R. Card; G. Munz; C. Smith; M. W. Bevan Impaired sucrose-induction mutants reveal the modulation of sugar-induced starch biosynthetic gene expression by abscisic acid signaling Plant J. 26, 421-433 (2001) .
    • . . . The first step is catalyzed by a short-chain alcohol dehydrogenase/reductase (SDR) that is encoded by the AtABA2 (ABA deficient 2) gene (Rook et al., 2001; Cheng et al., 2002; Gonzalez-Guzman et al., 2002) and that generates ABA-aldehyde . . .
  104. J. Santiago; F. Dupeux; A. Round; R. Antoni; S.-Y. Park; M. Jamin The abscisic acid receptor PYR1 in complex with abscisic acid Nature 462, 665-668 (2009) .
    • . . . After ABA is received from ABC transporters by the guard cells, the PYR/PYL/RCAR (pyrabactin-resistance 1/pyrabactin-resistance like/regulatory component of ABA receptor) perceives ABA intracellularly and forms complexes that inhibit clade A of PP2Cs (protein phosphatase 2C), the negative regulators of ABA signaling, such as ABI1 (ABA insensitive 1), ABI2 (ABA insensitive 2), HAB1 (hypersensitive to ABA1) (Ma et al., 2009; Park et . . .
    • . . . Recently, the core signalosome of ABA signaling including ABA receptors, phosphatases (PP2Cs), and kinases (SnRK2s) was established (Ma et al., 2009; Park et . . .
  105. D. P. Schachtman; J. I. Schroeder; W. J. Lucas; J. A. Anderson; R. F. Gaber Expression of an inward-rectifying potassium channel by the Arabidopsis KAT1 cDNA Science 258, 1654-1658 (1992) .
    • . . . The efflux of H+ hyperpolarizes the PM and leads to K+ uptake via activation of inward K+ rectifying channels, such as KAT1 (potassium channel in Arabidopsis thaliana 1), KAT2 (potassium channel in Arabidopsis thaliana 2), and AKT1 (Arabidopsis thaliana K+ transporter 1) (Schachtman et al., 1992; Pilot et al., 2001; Szyroki et al., 2001) . . .
  106. C. Schmidt; I. Schelle; Y. J. Liao; J. I. Schroeder Strong regulation of slow anion channels and abscisic acid signaling in the guard cells by phosphorylation and dephosphorylation events Proc. Natl. Acad. Sci. U.S.A. 92, 9535-9539 (1995) .
    • . . . In different species, S-type anion channels are activated in the guard cells by ABA, cytosolic Ca2+, and phosphorylation events (Schmidt et al., 1995; Pei et al., 1997; Leonhardt et al., 1999; Raschke et al., 2003; Roelfsema et al., 2004; Mori et al., 2006) . . .
  107. J. I. Schroeder; S. Hagiwara Cytosolic calcium regulates ion channels in the plasma membrane of Vicia faba guard cells Nature 338, 427-430 (1989) .
    • . . . It was shown that the activity of KAT1 is inhibited by an elevation of ABA and cytosolic Ca2+ (Schroeder and Hagiwara, 1989; Blatt and Armstrong, 1993; Grabov and Blatt, 1999) via phosphorylation by SnRK, which in turn results in a decreased influx of K+ into the guard cells (Hubbard et al., 2010) . . .
  108. J. I. Schroeder; S. Hagiwara Repetitive increases in cytosolic Ca2+ of the guard cells by abscisic acid activation of non-selective Ca2+ permeable channels Proc. Natl. Acad. Sci. U.S.A. 87, 9305-9309 (1990) .
    • . . . Abscisic acid activates the Ca2+-permeable channels in the PM of the guard cells and triggers an influx of Ca2+ into the cytoplasm of the guard cells through the release of the second messenger, inositol-1,4,5-triphosphate (IP3), which in turn activates the Ca2+ channels that are located in the vacuole and endoplasmic reticulum (Schroeder and Hagiwara, 1990; Hamilton et al., 2000; Krinke et al., 2007; Kwak et al., 2008) . . .
  109. J. I. Schroeder; J. M. Kwak; G. J. Allen Guard cell abscisic acid signalling and engineering drought hardiness in plants Nature 410, 327-330 (2001a) .
  110. J. I. Schroeder; G. J. Allen; V. Hugouvieux; J. M. Kwak; D. Waner Guard cell signal transduction Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 627-658 (2001b) .
    • . . . Stomatal closure is the earliest plant response to water deficit (Schroeder et al., 2001b) . . .
  111. S. H. Schwartz; X. Qin; J. Zeevaart Elucidation of the indirect pathway of abscisic acid biosynthesis by mutants, genes and enzymes Plant Physiol. 131, 1591-1601 (2003) .
    • . . . Abscisic acid is synthesized in the plastids and cytosol, mainly in the vascular parenchyma cells but also in the guard cells, through the cleavage of a C40 carotenoid precursor, followed by a two-step conversion of the intermediate xanthoxin into ABA via ABA-aldehyde (Taylor et al., 2000; Finkelstein and Rock, 2002; Schwartz et al., 2003; Endo et al., 2008; Melhorn et al., 2008) . . .
  112. S. H. Schwartz; B. C. Tan; D. A. Gage; J. A. D. Zeevaart; D. R. McCarty Specific oxidative cleavage of carotenoids by VP14 of maize Science 276, 1872-1874 (1997) .
    • . . . Oxidative cleavage of the major epoxycarotenoid 9-cis-neoxanthin by the 9-cis-epoxycarotenoid dioxygenase (NCED) yields a C15 intermediate – xanthoxin (Schwartz et al., 1997) . . .
  113. C. Seiler; V. T. Harshavardhan; K. Rajesh; P. S. Reddy; M. Strickert; H. Rolletschek ABA biosynthesis and degradation contributing to ABA homeostasis during barley seed development under control and terminal drought-stress conditions J. Exp. Bot. 62, 2615-2632 (2011) .
    • . . . Drought, like the dark part of a diurnal cycle, also promotes the deconjugation of the ABA-glucose ester (ABA-GE), which is stored in the vacuoles of leaf cells and also circulates in the plant (Xu et al., 2002; Seiler et al., 2011) . . .
  114. D. H. Seo; M. Y. Ryu; F. Jammes; J. H. Hwang; M. Turek; B. G. Kang Roles of four Arabidopsis U-Box E3 ubiquitin ligases in negative regulation of abscisic acid-mediated drought stress responses Plant Physiol. 160, 556-568 (2012) .
  115. M. Seo; H. Aoki; H. Koiwai; Y. Kamiya; E. Nambara; T. Koshiba Comparative studies on the Arabidopsis aldehyde oxidase (AAO) gene family revealed a major role of AAO3 in ABA biosynthesis in seeds Plant Cell Physiol. 45, 1694-1703 (2004) .
    • . . . Then, the ABA-aldehyde oxidase (AAO) with the molybdenum cofactor (MoCo) catalyzes the last step in the biosynthesis pathway – the conversion of ABA-aldehyde into ABA (Seo et al., 2004) (Figure 2A) . . .
  116. R. E. Sharp Interaction with ethylene: changing views on the role of abscisic acid in root and shoot growth responses to water stress Plant Cell Environ. 25, 211-222 (2002) .
    • . . . Generally, elevated ABA concentrations limit the production of ethylene; and therefore a dramatic increase of ABA concentration during water stress probably causes a reduction in the production of ethylene (Sharp, 2002) . . .
  117. L. B. Sheard; X. Tan; H. Mao; J. Withers; G. Ben-Nissan; T. R. Hinds Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor Nature 468, 400-405 (2010) .
    • . . . JA-Ile is then bound by the receptor SCFCOI complex that contains the coronatine insensitive1 (COI1) F-box protein (Fonseca et al., 2009; Sheard et al., 2010) . . .
  118. C. Sirichandra; D. Gu; H. C. Hu; M. Davanture; S. Lee; M. Djaoui Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase FEBS Lett. 583, 2982-2986 (2009) .
    • . . . The protein, OST1 (open stomata1), displays dominant kinase activity during drought stress response and is able to activate NADPH oxidase (Sirichandra et al., 2009) . . .
  119. C. P. Song; M. Agarwal; M. Ohta; Y. Guo; U. Halfter; P. Wang Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses Plant Cell 17, 2384-2396 (2005) .
  120. C. M. Steber; P. McCourt A role for brassinosteroids in germination in Arabidopsis Plant Physiol. 125, 763-769 (2001) .
    • . . . Brassinosteroids (BR) are polyhydroxylated steroidal phytohormones that are involved in seed germination, stem elongation, vascular differentiation, and fruit ripening (Clouse and Sasse, 1998; Steber and McCourt, 2001; Symons et al., 2006) . . .
  121. M. Stoll; B. Loveys; P. Dry Hormonal changes induced by partial rootzone drying of irrigated grapevine J. Exp. Bot. 51, 1627-1634 (2000) .
    • . . . Generally, exogenous cytokinins and auxins can inhibit ABA-induced stomatal closure in diverse species (Stoll et al., 2000; Tanaka et al., 2006). . . .
  122. S. J. Suh; Y. F. Wang; A. Frelet; N. Leonhardt; M. Klein; C. Forestier The ATP binding cassette transporter AtMRP5 modulates anion and calcium channel activities in Arabidopsis guard cells J. Biol. Chem. 282, 1916-1924 (2007) .
  123. D. Suhita; V. A. Kolla; A. Vavasseur; A. S. Raghavendra Different signaling pathways involved during the suppression of stomatal opening by methyl jasmonate or abscisic acid Plant Sci. 164, 481-488 (2003) .
    • . . . The positive role of JA in the regulation of stomatal closure was observed in many studies (Gehring et al., 1997; Suhita et al., 2003, 2004; Munemasa et al., 2007) . . .
  124. D. Suhita; A. S. Raghavendra; J. M. Kwak; A. Vavasseur Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate- and abscisic acid-induced stomatal closure Plant Physiol. 134, 1536-1545 (2004) .
    • . . . The positive role of JA in the regulation of stomatal closure was observed in many studies (Gehring et al., 1997; Suhita et al., 2003, 2004; Munemasa et al., 2007) . . .
    • . . . Suhita et al. (2004) showed that a disruption of both genes encoding NADPH oxidase, AtrbohD and AtrbohF, results in the impairment of MeJA-induced stomatal closure and ROS production . . .
  125. G. M. Symons; C. Davies; Y. Shavrukov; I. B. Dry; J. B. Reid; M. R. Thomas Grapes on steroids. Brassinosteroids are involved in grape berry ripening Plant Physiol. 140, 150-158 (2006) .
    • . . . Brassinosteroids (BR) are polyhydroxylated steroidal phytohormones that are involved in seed germination, stem elongation, vascular differentiation, and fruit ripening (Clouse and Sasse, 1998; Steber and McCourt, 2001; Symons et al., 2006) . . .
  126. A. Szyroki; N. Ivashikina; P. Dietrich; M. R. Roelfsema; P. Ache; B. Reintanz KAT1 is not essential for stomatal opening Proc. Natl. Acad. Sci. U.S.A. 98, 2917-2921 (2001) .
  127. L. D. Talbott; E. Zeiger Central roles for potassium and sucrose in guard-cell osmo-regulation Plant Physiol. 111, 1051-1057 (1996) .
    • . . . K+ uptake is mainly responsible for the rapid increase of the turgor and the opening of stomata during the dawn (Humble and Raschke, 1971; Talbott and Zeiger, 1996) . . .
  128. L. D. Talbott; E. Zeiger The role of sucrose in guard cell osmo-regulation J. Exp. Bot. 49, 329-337 (1998) .
    • . . . The accumulation of sugars such as glucose, fructose and sucrose has been reported during the light phase of the day (Talbott and Zeiger, 1998) . . .
  129. G. Tallman 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 (2004) .
    • . . . It has been proposed that this link is based on both the molecular connections between ABA and circadian-clock pathways and on ABA biosynthesis and response to light (reviewed in Tallman, 2004) . . .
    • . . . In the evening, ABA biosynthesis outweighs the ABA catabolism in the guard cells, which leads to stomatal closure (for review, see Tallman, 2004). . . .
  130. Y. Tanaka; T. Sano; M. Tamaoki; N. Nakajima; N. Kondo; S. Hasezawa Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis Plant Physiol. 138, 2337-2343 (2005) .
    • . . . Tanaka et al. (2005) showed that Arabidopsis plants exposed to gaseous ethylene first did not close their stomata after the application of ABA . . .
    • . . . In a drought stressed eto1 (ethylene overproducer 1) mutant, stomata closed more slowly and were less sensitive to ABA than in the drought-treated wild type (Tanaka et al., 2005) . . .
    • . . . The physiological mechanism of ethylene inhibition of the ABA-mediated stomatal closure may be related to the function of ethylene as a factor that ensures a minimum carbon dioxide supply for photosynthesis by keeping stomata half-opened under the stress conditions (Leung and Giraudat, 1998; Tanaka et al., 2005). . . .
  131. Y. Tanaka; T. Sano; M. Tamaoki; N. Nakajima; N. Kondo; S. Hasezawa Cytokinin and auxin inhibit abscisic acid-induced stomatal closure by enhancing ethylene production in Arabidopsis J. Exp. Bot. 57, 2259-2266 (2006) .
    • . . . Generally, exogenous cytokinins and auxins can inhibit ABA-induced stomatal closure in diverse species (Stoll et al., 2000; Tanaka et al., 2006). . . .
  132. I. B. Taylor; A. Burbidage; A. J. Thompson Control of abscisic acid synthesis J. Exp. Bot. 51, 1563-1574 (2000) .
    • . . . Abscisic acid is synthesized in the plastids and cytosol, mainly in the vascular parenchyma cells but also in the guard cells, through the cleavage of a C40 carotenoid precursor, followed by a two-step conversion of the intermediate xanthoxin into ABA via ABA-aldehyde (Taylor et al., 2000; Finkelstein and Rock, 2002; Schwartz et al., 2003; Endo et al., 2008; Melhorn et al., 2008) . . .
  133. B. Thines; L. Katsir; M. Melotto; Y. Niu; A. Mandaokar; G. Liu JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling Nature 448, 661-665 (2007) .
    • . . . This interaction leads to the degradation of the repressor protein, JAZ (Jasmonate ZIM-domain), by the 26S proteasome and as a result, to the activation of distinct JA response genes by MYC2 (MYC domain transcription factor 2) (Chini et al., 2007; Thines et . . .
  134. A. J. Thompson; A. C. Jackson; R. A. Parker; D. R. Morpeth; A. Burbidge; I. B. Taylor Abscisic acid biosynthesis in tomato: regulation of zeaxanthin epoxidase and 9-cis-epoxycarotenoid dioxygenase mRNAs by light/dark cycles, water stress and abscisic acid Plant Mol. Biol. 42, 833-845 (2000) .
    • . . . A significant increase in NCED transcript levels can be detected within 15–30 min after leaf detachment or dehydration treatment (Qin and Zeevaart, 1999; Thompson et al., 2000), which indicates that the activation of NCED genes can be fairly quick . . .
  135. K. Ueno; T. Kinoshita; S. Inoue; T. Emi; K. Shimazaki Biochemical characterization of plasma membrane H+-ATPase activation in guard cell protoplasts of Arabidopsis thaliana in response to blue light Plant Cell Physiol. 46, 955-963 (2005) .
    • . . . In plants, H+-ATPases belong to the multi-gene family of the P-type ATPases, with 11 genes in Arabidopsis, which are all expressed in the guard cells (Ueno et al., 2005) . . .
  136. T. Umezawa; N. Sugiyama; M. Mizoguchi; S. Hayashi; F. Myouga; K. Yamaguchi-Shinozaki Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis Proc. Natl. Acad. Sci. U.S.A. 106, 17588-17593 (2009) .
    • . . . After ABA is received from ABC transporters by the guard cells, the PYR/PYL/RCAR (pyrabactin-resistance 1/pyrabactin-resistance like/regulatory component of ABA receptor) perceives ABA intracellularly and forms complexes that inhibit clade A of PP2Cs (protein phosphatase 2C), the negative regulators of ABA signaling, such as ABI1 (ABA insensitive 1), ABI2 (ABA insensitive 2), HAB1 (hypersensitive to ABA1) (Ma et al., 2009; Park et . . .
    • . . . The inactivation of PP2Cs such as ABI1 and ABI2 by the complex ABA-receptor facilitates the phosphorylation and activation of a downstream target of phosphatases – SnRK2, such as SnRK2.2/D, SnRK2.3/E, and SnRK2.6/OST1/E, which are the key players in the regulation of ABA signaling and abiotic stress response (Fujii and Zhu, 2009; Fujita et al., 2009; Umezawa et . . .
  137. T. Vahisalu; H. Kollist; Y. F. Wang; N. Nishimura; W. Y. Chan; G. Valerio SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling Nature 452, 487-491 (2008) .
  138. A. Vatén; D. C. Bergmann Mechanisms of stomatal development: an evolutionary view Evodevo 3, 11 (2012) .
    • . . . For this reason, neighbor cells are part of a stomatal complex (Nadeau and Sack, 2002; Nadeau, 2009; Lau and Bergmann, 2012; Pillitteri and Torii, 2012; Vatén and . . .
  139. P. Wang; C. P. Song Guard-cell signalling for hydrogen peroxide and abscisic acid New Phytol. 178, 703-718 (2008) .
    • . . . In addition, H2O2 inhibits K+ channel activity, induces cytosolic alkalization in the guard cells and promotes NO signaling in response to ABA (Zhang et al., 2001; Kohler et al., 2003; Wang and Song, 2008) . . .
  140. X. Q. Wang; H. Ullah; A. M. Jones; S. M. Assmann G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells Science 292, 2070-2072 (2001) .
  141. J. M. Ward; J. I. Schroeder 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 (1994) .
    • . . . SV channels were shown to be calcium permeable and it was suggested that they facilitate a brief transient efflux of cations, including Ca2+, from vacuoles (Ward and Schroeder, 1994). . . .
  142. C. Wasternack Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development Ann. Bot. 100, 681-697 (2007) .
    • . . . JA biosynthesis is induced by stress conditions (Wasternack, 2007) and many genes related to JA signaling are regulated by drought stress (Huang et al., 2008) . . .
  143. C. Willmer; M. Fricker Stomata , (1996) .
    • . . . The decreased level of malate2− in guard cells is also linked with the gluconeogenic conversion of malate2− into starch (Willmer and Fricker, 1996) . . .
  144. Z. J. Xu; M. Nakajima; Y. Suzuki; I. Yamaguchi Cloning and characterization of the abscisic acid-specific glucosyltransferase gene from adzuki bean seedlings Plant Physiol. 129, 1285-1295 (2002) .
    • . . . Drought, like the dark part of a diurnal cycle, also promotes the deconjugation of the ABA-glucose ester (ABA-GE), which is stored in the vacuoles of leaf cells and also circulates in the plant (Xu et al., 2002; Seiler et al., 2011) . . .
  145. S. Xue; H. Hu; A. Ries; E. Merilo; H. Kollist; J. I. Schroeder Central functions of bicarbonate in S-type anion channel activation and OST1 protein kinase in CO2 signal transduction in guard cell EMBO J. 30, 1645-1658 (2011) .
    • . . . This is probably caused by an intensive ABA accumulation through the biosynthesis of ABA in the guard cells and the simultaneous import of endogenous ABA from the apoplast to the guard cells using ABA transporters such as ABCG22 (Kuromori et al., 2011), while at the same time, ABA catabolism processes are disfavored . . .
  146. N. Ye; G. Zhu; Y. Liu; Y. Li; J. Zhang ABA controls H2O2 accumulation through the induction of OsCATB in rice leaves under water stress Plant Cell Physiol. 52, 689-698 (2011) .
    • . . . Cheng et al. (2002) reported that the AtNCED3, AtZEP (Zeaxanthin epoxidase), and AtAAO3 (ABA-aldehyde oxidase) genes could be induced in Arabidopsis by ABA and studies in rice showed that OsNCED3 expression was induced by dehydration (Ye et al., 2011) . . .
  147. R. Yoshida; T. Umezawa; T. Mizoguchi; S. Takahashi; F. Takahashi; K. Shinozaki 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 (2006) .
    • . . . Mutants in OST1 showed a wilty phenotype in water deficit conditions because of the impairment of stomatal closure and ROS production (Mustilli et al., 2002; Yoshida et al., 2006; Figure 4). . . .
  148. X. Zhang; L. Zhang; F. Dong; J. Gao; D. W. Galbraith; C. P. Song Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba Plant Physiol. 126, 1438-1448 (2001) .
    • . . . The guard cells generate reactive oxygen species (ROS) such as hydrogen peroxide (H2O2) and nitric oxide (NO) in response to ABA (Pei et al., 2000; Zhang et al., 2001) . . .
    • . . . In addition, H2O2 inhibits K+ channel activity, induces cytosolic alkalization in the guard cells and promotes NO signaling in response to ABA (Zhang et al., 2001; Kohler et al., 2003; Wang and Song, 2008) . . .
  149. J. J. Zou; F.-J. Wei; C. Wang; J. J. Wu; D. Ratnasekera; W.-X. Li Arabidopsis calcium-dependent protein kinase CPK10 functions in abscisic acid- and Ca2+-mediated stomatal regulation in response to drought Plant Physiol. 154, 1232-1243 (2010) .
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