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Hormone interactions in stomatal function

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Abstract

Research in recent years on the biology of guard cells has shown that these specialized cells integrate both extra- and intra-cellular signals in the control of stomatal apertures. Among the phytohormones, abscisic acid (ABA) is one of the key players regulating stomatal function. In addition, auxin, cytokinin, ethylene, brassinosteroids, jasmonates, and salicylic acid also contribute to stomatal aperture regulation. The interaction of multiple hormones can serve to determine the size of stomatal apertures in a condition-specific manner. Here, we discuss the roles of different phytohormones and the effects of their interactions on guard cell physiology and function.

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Abbreviations

ABA:

Abscisic acid

ACC:

1-Aminocyclopropane-1-carboxylic acid

BRs:

Brassinosteroids

GA:

Gibberellins

JA:

Jasmonate

1-NAA:

1-Napthaleneacetic acid

SA:

Salicylic acid

References

  • Aharoni N, Blumenfeld A, Richmond AE (1977) Hormonal activity in detached lettuce leaves as affected by leaf water content. Plant Physiol 59:1169–1173

    PubMed  CAS  Google Scholar 

  • Allen GJ, Chu SP, Schumacher K, Shimazaki CT, Vafeados D, Kemper A, Hawke SD, Tallman G, Tsien RY, Harper JF, Chory J, Schroeder JI (2000) Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science 289:2338–2342. doi:10.1126/science.289.5488.2338

    PubMed  CAS  Google Scholar 

  • Assmann SM (2003) OPEN STOMATA1 opens the door to ABA signaling in Arabidopsis guard cells. Trends Plant Sci 8:151–153. doi:10.1016/S1360-1385(03)00052-9

    PubMed  CAS  Google Scholar 

  • Bandurska H, Stroiński A, Kubiś J (2003) The effect of jasmonic acid on the accumulation of ABA, proline and spermidine and its influence on membrane injury under water deficit in two barley genotypes. Acta Physiol Plant 25:279–285. doi:10.1007/s11738-003-0009-0

    CAS  Google Scholar 

  • Benedetti CE, Xie D, Turner JG (1995) Coi1-dependent expression of an Arabidopsis vegetative storage protein in flowers and siliques and in response to coronatine or methyl jasmonate. Plant Physiol 109:567–572. doi:10.1104/pp.109.2.567

    PubMed  CAS  Google Scholar 

  • Blackman PG, Davies WJ (1983) The effect of cytokinins and ABA on stomatal behaviour of maize and Commelina. J Exp Bot 34:1619–1626. doi:10.1093/jxb/34.12.1619

    CAS  Google Scholar 

  • Blatt MR, Armstrong F (1993) K+ channels of stomatal guard cells: abscisic acid-evoked control of the outward rectifier mediated by cytoplasmic pH. Planta 191:330–341. doi:10.1007/BF00195690

    CAS  Google Scholar 

  • Blatt MR, Thiel G (1994) K+ channels of stomatal guard cells: bimodal control of the K+ inward-rectifier evoked by auxin. Plant J 5:55–68. doi:10.1046/j.1365-313X.1994.5010055.x

    PubMed  CAS  Google Scholar 

  • Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–18. doi:10.1146/annurev.cellbio.16.1.1

    PubMed  CAS  Google Scholar 

  • 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. doi:10.1111/j.1365-313X.2005.02615.x

    PubMed  CAS  Google Scholar 

  • Catterou M, Dubois F, Schaller H, Aubanelle L, Vilcot B, Sangwan- Norreel BS, Sangwan RS (2001) Brassinosteroids, microtubules and cell elongation in Arabidopsis thaliana. I. Molecular, cellular and physiological characterization of the Arabidopsis bul1 mutant, defective in the Δ7-sterol-C5-desaturation step leading to brassinosteroid biosynthesis. Planta 212:659–672. doi:10.1007/s004250000466

    PubMed  CAS  Google Scholar 

  • Christian M, Hannah WB, Lüthen H, Jones AM (2008) Identification of auxins by a chemical genomics approach. J Exp Bot 59:2757–2767. doi:10.1093/jxb/ern133

    PubMed  CAS  Google Scholar 

  • Clouse SD, Sasse JM (1998) BRASSINOSTEROIDS: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427–451. doi:10.1146/annurev.arplant.49.1.427

    PubMed  CAS  Google Scholar 

  • Cominelli E, Galbiati M, Vavasseur A, Conti L, Sala T, Vuylsteke M, Leonhardt N, Dellaporta SL, Tonelli C (2005) A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Curr Biol 15:1196–1200. doi:10.1016/j.cub.2005.05.048

    PubMed  CAS  Google Scholar 

  • Coursol S, Fan LM, Le Stunff H, Spiegel S, Gilroy S, Assmann SM (2003) Sphingolipid signalling in Arabidopsis guard cells involves heterotrimeric G proteins. Nature 423:651–654. doi:10.1038/nature01643

    PubMed  CAS  Google Scholar 

  • Coursol S, Le Stunff H, Lynch DV, Gilroy S, Assmann SM, Spiegel S (2005) Arabidopsis sphingosine kinase and the effects of phytosphingosine-1-phosphate on stomatal aperture. Plant Physiol 137:724–737. doi:10.1104/pp.104.055806

    PubMed  CAS  Google Scholar 

  • Cramer MD, Nagel OW, Lips SH, Lambers H (1995) Reduction, assimilation and transport of N in normal and gibberellin deficient tomato plants. Physiol Plant 95:347–354. doi:10.1111/j.1399-3054.1995.tb00848.x

    CAS  Google Scholar 

  • Creelman RA, Mullet JE (1995) Jasmonic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress. Proc Natl Acad Sci USA 92:4114–4119. doi:10.1073/pnas.92.10.4114

    PubMed  CAS  Google Scholar 

  • Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol Plant Mol Biol 48:355–381. doi:10.1146/annurev.arplant.48.1.355

    PubMed  CAS  Google Scholar 

  • Das VSR, Rao IM, Raghavendra AS (1976) Reversal of abscisic acid induced stomatal closure by benzyl adenine. New Phytol 76:449–452. doi:10.1111/j.1469-8137.1976.tb01480.x

    CAS  Google Scholar 

  • Dat JF, Capelli N, Folzer H, Bourgeade P, Badot PM (2004) Sensing and signalling during plant flooding. Plant Physiol Biochem 42:273–282. doi:10.1016/j.plaphy.2004.02.003

    PubMed  CAS  Google Scholar 

  • Davies WJ, Zhang J (1991) Root signals and the regulation of growth and development of plants in drying soil. Annu Rev Plant Physiol 42:55–76. doi:10.1146/annurev.pp.42.060191.000415

    CAS  Google Scholar 

  • Delaney TP, Uknes S, Vernooij B, Friedrich L, Weymann K, Negrotto D, Gaffney T, Gut-Rella M, Kessmann H, Ward E, Ryals J (1994) A central role of salicylic acid in plant disease resistance. Science 266:1247–1250. doi:10.1126/science.266.5188.1247

    PubMed  CAS  Google Scholar 

  • Dello Ioio R, Linhares FS, Sabatini S (2008) Emerging role of cytokinin as a regulator of cellular differentiation. Curr Opin Plant Biol 11:23–27. doi:10.1016/j.pbi.2007.10.006

    PubMed  CAS  Google Scholar 

  • Dempsey DA, Shah J, Klessig DF (1999) Salicylic acid and disease resistance in plants. Crit Rev Plant Sci 18:547–575

    CAS  Google Scholar 

  • Desikan R, Griffiths R, Hancock J, Neill S (2002) A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc Natl Acad Sci USA 99:16314–16318. doi:10.1073/pnas.252461999

    PubMed  CAS  Google Scholar 

  • Desikan R, Last K, Harrett-Williams R, Tagliavia C, Harter K, Hooley R, Hancock JT, Neill SJ (2006) Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. Plant J 47:907–916. doi:10.1111/j.1365-313X.2006.02842.x

    PubMed  CAS  Google Scholar 

  • Dodd IC (2003) Hormonal interactions and stomatal responses. J Plant Growth Regul 22:32–46. doi:10.1007/s00344-003-0023-x

    CAS  Google Scholar 

  • Dong FC, Wang PT, Song CP (2001) The role of hydrogen peroxide in salicylic acid-induced stomatal closure in Vicia faba guard cells. Acta Phytophysiol Sinica 27:296–302

    CAS  Google Scholar 

  • Ephritikhine G, Fellner M, Vannini C, Lapous D, Barbier-Brygoo H (1999) The sax1 dwarf mutant of Arabidopsis thaliana shows altered sensitivity of growth responses to abscisic acid, auxin, gibberellins and ethylene and is partially rescued by exogenous brassinosteroid. Plant J 18:303–314. doi:10.1046/j.1365-313X.1999.00454.x

    PubMed  CAS  Google Scholar 

  • Evans NH (2003) Modulation of guard cell plasma membrane potassium currents by methyl jasmonate. Plant Physiol 131:8–11. doi:10.1104/pp.014266

    PubMed  CAS  Google Scholar 

  • Fan LM, Zhao Z, Assmann SM (2004) Guard cells: a dynamic signaling model. Curr Opin Plant Biol 7:537–546. doi:10.1016/j.pbi.2004.07.009

    PubMed  CAS  Google Scholar 

  • Feys B, Benedetti CE, Penfold CN, Turner JG (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6:751–759

    PubMed  CAS  Google Scholar 

  • Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14(Suppl):S15–S45

    PubMed  CAS  Google Scholar 

  • Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H, Ryals J (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754–756. doi:10.1126/science.261.5122.754

    PubMed  CAS  Google Scholar 

  • Garcia-Mata C, Gay R, Sokolovski S, Hills A, Lamattina L, Blatt MR (2003) Nitric oxide regulates K+ and Cl− channels in guard cells through a subset of abscisic acid-evoked signaling pathways. Proc Natl Acad Sci USA 100:11116–11121. doi:10.1073/pnas.1434381100

    PubMed  CAS  Google Scholar 

  • Gehring CA, Irving HR, McConchie R, Parish RW (1997) Jasmonates induce intracellular alkalinization and closure of Paphiopedilum guard cells. Ann Bot (Lond) 80:485–489. doi:10.1006/anbo.1997.0471

    CAS  Google Scholar 

  • Gehring CA, McConchie RM, Venis MA, Parish RW (1998) Auxin-binding-protein antibodies and peptides influence stomatal opening and alter cytoplasmic pH. Planta 205:581–586. doi:10.1007/s004250050359

    PubMed  CAS  Google Scholar 

  • Göring H, Koshuchowa S, Deckert C (1990) Influence of gibberellic acid on stomatal movement. Biochem Physiol Pflanz 186:367–374

    Google Scholar 

  • Gosti F, Beaudoin N, Serizet C, Webb AA, Vartanian N, Giraudat J (1999) ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell 11:1897–1910

    PubMed  CAS  Google Scholar 

  • Gowing DJ, Davies WJ, Jones HG (1990) A positive root-sourced signal as an indicator of soil drying in apple, Malus domestica Borkh. J Exp Bot 41:1535–1540. doi:10.1093/jxb/41.12.1535

    Google Scholar 

  • Guo H, Ecker JR (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7:40–49. doi:10.1016/j.pbi.2003.11.011

    PubMed  CAS  Google Scholar 

  • Guranowski A, Miersch O, Staswick PE, Suza W, Wasternack C (2007) Substrate specificity and products of side-reactions catalyzed by jasmonate:amino acid synthetase (JAR1). FEBS Lett 581:815–820. doi:10.1016/j.febslet.2007.01.049

    PubMed  CAS  Google Scholar 

  • Haubrick LL, Assmann SM (2006) Brassinosteroids and plant function: some clues, more puzzles. Plant Cell Environ 29:446–457. doi:10.1111/j.1365-3040.2005.01481.x

    PubMed  CAS  Google Scholar 

  • Haubrick LL, Torsethaugen G, Assmann SM (2006) 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. doi:10.1111/j.1399-3054.2006.00708.x

    CAS  Google Scholar 

  • Havlova M, Dobrev PI, Motyka V, Storchova H, Libus J, Dobra J, Malbeck J, Gaudinova A, Vankova R (2008) The role of cytokinins in responses to water deficit in tobacco plants over-expressing trans-zeatin O-glucosyltransferase gene under 35S or SAG12 promoters. Plant Cell Environ 31:341–353. doi:10.1111/j.1365-3040.2007.01766.x

    PubMed  CAS  Google Scholar 

  • Heping C, Shankun C (1995) Brassinosteroid-induced rice lamina joint inclination and its relation to indole-3-acetic acid and ethylene. Plant Growth Regul 16:189–196. doi:10.1007/BF00029540

    Google Scholar 

  • Herde O, Pena-Cortes H, Willmitzer L, Eisahn J (1997) Stomatal responses to jasmonic acid, linolenic acid and abscisic acid in wiid-type and ABA-deficient tomato plants. Plant Cell Environ 20:136–141. doi:10.1046/j.1365-3040.1997.d01-11.x

    CAS  Google Scholar 

  • Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908. doi:10.1038/nature01843

    PubMed  CAS  Google Scholar 

  • Hewitt FR, Hough T, O’Neill P, Sasse JM, Williams EG, Rowan KS (1985) Effect of brassinolide and other growth regulators on the germination and growth of pollen tubes of Prunus avium using a multiple hanging drop assay. Aust J Plant Physiol 12:201–211

    Article  CAS  Google Scholar 

  • Hirayama T, Shinozaki K (2007) Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA. Trends Plant Sci 12:343–351. doi:10.1016/j.tplants.2007.06.013

    PubMed  CAS  Google Scholar 

  • Huang D, Wu W, Abrams SR, Cutler AJ (2008) The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors. J Exp Bot 59:2991–3007. doi:10.1093/jxb/ern155

    PubMed  CAS  Google Scholar 

  • Hubick KT, Taylor JS, Reid DM (1986) The effect of drought on levels of abscisic acid, cytokinins, gibberellins and ethylene in aeroponically-grown sunflower plants. Plant Growth Regul 4:139–151. doi:10.1007/BF00025195

    CAS  Google Scholar 

  • Hwang JU, Lee Y (2001) Abscisic acid-induced actin reorganization in guard cells of dayflower is mediated by cytosolic calcium levels and by protein kinase and protein phosphatase activities. Plant Physiol 125:2120–2128. doi:10.1104/pp.125.4.2120

    PubMed  CAS  Google Scholar 

  • Irving HR, Gehring CA, Parish RW (1992) Changes in cytosolic pH and calcium of guard cells precede stomatal movements. Proc Natl Acad Sci USA 89:1790–1794. doi:10.1073/pnas.89.5.1790

    PubMed  CAS  Google Scholar 

  • Israelsson M, Siegel RS, Young J, Hashimoto M, Iba K, Schroeder JI (2006) Guard cell ABA and CO2 signaling network updates and Ca2+ sensor priming hypothesis. Curr Opin Plant Biol 9:654–663. doi:10.1016/j.pbi.2006.09.006

    PubMed  CAS  Google Scholar 

  • Jackson MB (2002) Long-distance signalling from roots to shoots assessed: the flooding story. J Exp Bot 53:175–181. doi:10.1093/jexbot/53.367.175

    PubMed  CAS  Google Scholar 

  • Jager CE, Symons GM, Ross JJ, Reid JB (2008) Do brassinosteroids mediate the water stress response? Physiol Plant 133:417–425. doi:10.1111/j.1399-3054.2008.01057.x

    PubMed  CAS  Google Scholar 

  • Jewer PC, Incoll LD (1980) Promotion of stomatal opening in the grass Anthephora pubescens nees by a range of natural and synthetic cytokinis. Planta 150:218–221. doi:10.1007/BF00390829

    CAS  Google Scholar 

  • Kagale S, Divi UK, Krochko JE, Keller WA, Krishna P (2007) Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta 225:353–364. doi:10.1007/s00425-006-0361-6

    PubMed  CAS  Google Scholar 

  • Katsir L, Chung HS, Koo AJ, Howe GA (2008a) Jasmonate signaling: a conserved mechanism of hormone sensing. Curr Opin Plant Biol 11:428–435. doi:10.1016/j.pbi.2008.05.004

    PubMed  CAS  Google Scholar 

  • Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA (2008b) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci USA 105:7100–7105. doi:10.1073/pnas.0802332105

    PubMed  CAS  Google Scholar 

  • Kazama H, Dan H, Imaseki H, Wasteneys GO (2004) Transient exposure to ethylene stimulates cell division and alters the fate and polarity of hypocotyl epidermal cells. Plant Physiol 134:1614–1623. doi:10.1104/pp.103.031088

    PubMed  CAS  Google Scholar 

  • Kepinski S (2007) The anatomy of auxin perception. Bioessays 29:953–956. doi:10.1002/bies.20657

    PubMed  CAS  Google Scholar 

  • Koornneef M, Hanhart CJ, Hilhorst HW, Karssen CM (1989) In vivo inhibition of seed development and reserve protein accumulation in recombinants of abscisic acid biosynthesis and responsiveness mutants in Arabidopsis thaliana. Plant Physiol 90:463–469

    PubMed  CAS  Google Scholar 

  • Kramell R, Atzorn R, Schneider G, Miersch O, Brückner C, Schmidt J, Sembdner G, Parthier B (1995) Occurrence and identification of jasmonic acid and its amino acid conjugates induced by osmotic stress in barley leaf tissue. J Plant Growth Regul 14:29–36. doi:10.1007/BF00212643

    CAS  Google Scholar 

  • Krishna P (2003) Brassinosteroid-mediated stress responses. J Plant Growth Regul 22:289–297. doi:10.1007/s00344-003-0058-z

    PubMed  CAS  Google Scholar 

  • Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633. doi:10.1093/emboj/cdg277

    PubMed  CAS  Google Scholar 

  • Lee J-S (1998) The mechanism of stomatal closing by salicylic acid in Commelina communis L. J Plant Biol 41:97–102

    Google Scholar 

  • 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. doi:10.1101/gad.900401

    PubMed  CAS  Google Scholar 

  • Leonhardt N, Kwak JM, Robert N, Waner D, Leonhardt G, Schroeder JI (2004) Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell 16:596–615. doi:10.1105/tpc.019000

    PubMed  CAS  Google Scholar 

  • Leung J, Bouvier-Durand M, Morris PC, Guerrier D, Chefdor F, Giraudat J (1994) Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264:1448–1452. doi:10.1126/science.7910981

    PubMed  CAS  Google Scholar 

  • Leung J, Merlot S, Giraudat J (1997) The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9:759–771

    PubMed  CAS  Google Scholar 

  • Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Physiol Plant Mol Biol 49:199–222. doi:10.1146/annurev.arplant.49.1.199

    PubMed  CAS  Google Scholar 

  • Levitt LK, Stein DB, Rubinstein B (1987) Promotion of stomatal opening by indoleacetic acid and ethrel in epidermal strips of Vicia faba L. Plant Physiol 85:318–321

    PubMed  CAS  Google Scholar 

  • Li J, Wang XQ, Watson MB, Assmann SM (2000) Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase. Science 287:300–303. doi:10.1126/science.287.5451.300

    PubMed  CAS  Google Scholar 

  • 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. doi:10.1371/journal.pbio.0040312

    PubMed  Google Scholar 

  • Liang YK, Dubos C, Dodd IC, Holroyd GH, Hetherington AM, Campbell MM (2005) AtMYB61, an R2R3-MYB transcription factor controlling stomatal aperture in Arabidopsis thaliana. Curr Biol 15:1201–1206. doi:10.1016/j.cub.2005.06.041

    PubMed  CAS  Google Scholar 

  • Lohse G, Hedrich R (1992) Characterization of the plasma-membrane H+-ATPase from Vicia faba guard cells. Planta 188:206–214. doi:10.1007/BF00216815

    CAS  Google Scholar 

  • Lü D, Zhang X, Jiang J, An GY, Zhang L, Song C-P (2005) NO may function in the downstream of H2O2 in ABA-induced stomatal closure in Vicia faba L. J Plant Physiol Mol Biol 31:62–70 (in Chinese)

    Google Scholar 

  • MacRobbie EA, Kurup S (2007) Signalling mechanisms in the regulation of vacuolar ion release in guard cells. New Phytol 175:630–640. doi:10.1111/j.1469-8137.2007.02131.x

    PubMed  CAS  Google Scholar 

  • MacRobbie EAC (1997) Signalling in guard cells and regulation of ion channel activity. J Exp Bot 48:515–528

    CAS  Google Scholar 

  • Madhavan S, Chrmoinski A, Smith BN (1983) Effect of ethylene on stomatal opening in tomato and carnation leaves. Plant Cell Physiol 24:569–572

    CAS  Google Scholar 

  • Manthe B, Schulz M, Schnable H (1992) Effects of salicylic acid on growth and stomatal movements on Vicia faba L.: evidence for salicylic acid metabolism. J Chem Ecol 18:1525–1539. doi:10.1007/BF00993226

    CAS  Google Scholar 

  • Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980. doi:10.1016/j.cell.2006.06.054

    PubMed  CAS  Google Scholar 

  • Melotto M, Underwood W, He SY (2008) Role of stomata in plant innate immunity and foliar bacterial diseases. Annu Rev Phytopathol 46:101–122. doi:10.1146/annurev.phyto.121107.104959

    PubMed  CAS  Google Scholar 

  • 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. doi:10.1046/j.1365-313x.2001.00965.x

    PubMed  CAS  Google Scholar 

  • Merritt F, Kemper A, Tallman G (2001) Inhibitors of ethylene synthesis inhibit auxin-induced stomatal opening in epidermis detached from leaves of Vicia faba L. Plant Cell Physiol 42:223–230. doi:10.1093/pcp/pce030

    PubMed  CAS  Google Scholar 

  • Miedema H, Assmann SM (1996) A membrane-delimited effect of internal pH on the K+ outward rectifier of Vicia faba guard cells. J Membr Biol 154:227–237. doi:10.1007/s002329900147

    PubMed  CAS  Google Scholar 

  • Morgan PW, He CJ, De Greef JA, De Proft MP (1990) Does water deficit stress promote ethylene synthesis by intact plants? Plant Physiol 94:1616–1624

    PubMed  CAS  Google Scholar 

  • Mori IC, Pinontoan R, Kawano T, Muto S (2001) Involvement of superoxide generation in salicylic acid-induced stomatal closure in Vicia faba. Plant Cell Physiol 42:1383–1388. doi:10.1093/pcp/pce176

    PubMed  CAS  Google Scholar 

  • Munemasa S, Oda K, Watanabe-Sugimoto M, Nakamura Y, Shimoishi Y, Murata Y (2007) 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. doi:10.1104/pp.106.091298

    PubMed  CAS  Google Scholar 

  • Murata Y, Pei ZM, Mori IC, Schroeder J (2001) Abscisic acid activation of plasma membrane Ca(2+) channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell 13:2513–2523

    PubMed  CAS  Google Scholar 

  • Mustilli AC, Merlot S, Vavasseur A, Fenzi F, Giraudat J (2002) 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. doi:10.1105/tpc.007906

    PubMed  CAS  Google Scholar 

  • Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185. doi:10.1146/annurev.arplant.56.032604.144046

    PubMed  CAS  Google Scholar 

  • Narayana I, Lalonde S, Saini HS (1991) Water-stress-induced ethylene production in wheat: a fact or artifact? Plant Physiol 96:406–410

    PubMed  CAS  Google Scholar 

  • Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson I (2008) Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot 59:165–176. doi:10.1093/jxb/erm293

    PubMed  CAS  Google Scholar 

  • Neill SJ, Desikan R, Clarke A, Hancock JT (2002) Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol 128:13–16. doi:10.1104/pp.128.1.13

    PubMed  CAS  Google Scholar 

  • Németh M, Janda T, Horváth E, Páldi E, Szalai G (2002) Exogenous salicylic acid increases polyamine content but may decrease drought tolerance in maize. Plant Sci 162:569–574. doi:10.1016/S0168-9452(01)00593-3

    Google Scholar 

  • Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126:467–475. doi:10.1016/j.cell.2006.05.050

    PubMed  CAS  Google Scholar 

  • Nilson SE, Assmann SM (2007) The control of transpiration. Insights from Arabidopsis. Plant Physiol 143:19–27. doi:10.1104/pp.106.093161

    PubMed  CAS  Google Scholar 

  • Outlaw WHJ (2003) Integration of cellular and physiological functions of guard cells. Crit Rev Plant Sci 22:503–529. doi:10.1080/713608316

    Google Scholar 

  • Pallas JE, Kays SJ (1982) Inhibition of photosynthesis by ethylene-a stomatal effect. Plant Physiol 70:598–601

    PubMed  CAS  Google Scholar 

  • Pandey S, Zhang W, Assmann SM (2007) Roles of ion channels and transporters in guard cell signal transduction. FEBS Lett 581:2325–2336. doi:10.1016/j.febslet.2007.04.008

    PubMed  CAS  Google Scholar 

  • Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734. doi:10.1038/35021067

    PubMed  CAS  Google Scholar 

  • Penninckx IA, Eggermont K, Terras FR, Thomma BP, De Samblanx GW, Buchala A, Metraux JP, Manners JM, Broekaert WF (1996) Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell 8:2309–2323

    PubMed  CAS  Google Scholar 

  • Pospíšilová J (2003) Participation of phytohormones in the stomatal regulation of gas exchange during water stress. Biol Plant 46:491–506. doi:10.1023/A:1024894923865

    Google Scholar 

  • Pustovoitova TN, Zhdanova NE, Zholkevich VN (2001) Epibrassinolide increases plant drought resistance. Dokl Biochem Biophys 376:36–38. doi:10.1023/A:1018852110393

    PubMed  CAS  Google Scholar 

  • Pustovoitova TN, Drozdova IS, Zhdanova NE, Zholkevich VN (2003) Leaf growth, photosynthetic rate, and phytohormone contents in Cucumis sativus plants under progressive soil drought. Russ J Plant Physiol 50:441–443. doi:10.1023/A:1024752219336

    CAS  Google Scholar 

  • Rajasekaran LR, Blake TJ (1999) New plant growth regulators protect photosynthesis and enhance growth under drought of jack pine seedlings. J Plant Growth Regul 18:175–181. doi:10.1007/PL00007067

    PubMed  CAS  Google Scholar 

  • Raskin I (1992) Salicylate, a new plant hormone. Plant Physiol 99:799–803

    PubMed  CAS  Google Scholar 

  • Saibo NJ, Vriezen WH, Beemster GT, Van Der Straeten D (2003) Growth and stomata development of Arabidopsis hypocotyls are controlled by gibberellins and modulated by ethylene and auxins. Plant J 33:989–1000. doi:10.1046/j.1365-313X.2003.01684.x

    PubMed  CAS  Google Scholar 

  • Sairam SK (1994) Effects of homobrassinolide application on plant metabolism and grain yield under irrigated and moisture-stress conditions of two wheat varieties. Plant Growth Regul 14:173–181. doi:10.1007/BF00025220

    CAS  Google Scholar 

  • Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57:431–449. doi:10.1146/annurev.arplant.57.032905.105231

    PubMed  CAS  Google Scholar 

  • Sakurai N, Akiyama M, Kuraishi S (1985) Role of abscisic acid and indoleacetic acid in the stunted growth of water-stressed, etiolated squash hypocotyls. Plant Cell Physiol 26:15–24

    CAS  Google Scholar 

  • Santakumari M, Fletcher RA (1987) Reversal of triazole-induced stomatal closure by gibberellic acid and cytokinins in Commelina benghalensis. Physiol Plant 71:95–99. doi:10.1111/j.1399-3054.1987.tb04623.x

    CAS  Google Scholar 

  • Schlagnhaufer C, Arteca RN (1985) Brassinosteroid induced epinasty in tomato plants. Plant Physiol 178:300–303

    Article  Google Scholar 

  • Schmelz EA, Engelberth J, Alborn HT, O’Donnell P, Sammons M, Toshima H, Tumlinson JHIII (2003) Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants. Proc Natl Acad Sci USA 100:10552–10557. doi:10.1073/pnas.1633615100

    PubMed  CAS  Google Scholar 

  • Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001a) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52:627–658. doi:10.1146/annurev.arplant.52.1.627

    PubMed  CAS  Google Scholar 

  • Schroeder JI, Kwak JM, Allen GJ (2001b) Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410:327–330. doi:10.1038/35066500

    PubMed  CAS  Google Scholar 

  • Schumacher K, Vafeados D, McCarthy M, Sze H, Wilkins T, Chory J (1999) The Arabidopsis det3 mutant reveals a central role for the vacuolar H(+)-ATPase in plant growth and development. Genes Dev 13:3259–3270. doi:10.1101/gad.13.24.3259

    PubMed  CAS  Google Scholar 

  • Serna L, Fenoll C (1996) Ethylene induces stomata differentiation in Arabidopsis. Int J Dev Biol 40:S123–S124

    Google Scholar 

  • She XP, Song XG (2006) Cytokinin- and auxin-induced stomatal opening is related to the change of nitric oxide levels in guard cells in broad bean. Physiol Plant 128:569–579. doi:10.1111/j.1399-3054.2006.00782.x

    CAS  Google Scholar 

  • Shen LM, Outlaw WH, Epstein LM (1995) Expression of an mRNA with sequence similarity to pea dehydrin (Psdhn1) in guard cells of Vicia faba in response to exogenous abscisic acid. Physiol Plant 95:99–105. doi:10.1111/j.1399-3054.1995.tb00814.x

    CAS  Google Scholar 

  • Shen Q, Ho TH (1995) Functional dissection of an abscisic acid (ABA)-inducible gene reveals two independent ABA-responsive complexes each containing a G-box and a novel cis-acting element. Plant Cell 7:295–307

    PubMed  CAS  Google Scholar 

  • Shimazaki K, Doi M, Assmann SM, Kinoshita T (2007) Light regulation of stomatal movement. Annu Rev Plant Biol 58:219–247. doi:10.1146/annurev.arplant.57.032905.105434

    PubMed  CAS  Google Scholar 

  • Snaith PJ, Mansfield TA (1982) Stomatal sensitivity to abscisic acid. Plant Cell Environ 5:309–311

    CAS  Google Scholar 

  • Sokolovski S, Hills A, Gay R, Garcia-Mata C, Lamattina L, Blatt MR (2005) Protein phosphorylation is a prerequisite for intracellular Ca2+ release and ion channel control by nitric oxide and abscisic acid in guard cells. Plant J 43:520–529. doi:10.1111/j.1365-313X.2005.02471.x

    PubMed  CAS  Google Scholar 

  • Song X, She X, He J, Huang C, Song T (2006) Cytokinin- and auxin-induced stomatal opening involves a decrease in levels of hydrogen peroxide in guard cells of Vicia faba. Funct Plant Biol 33:573–583. doi:10.1071/FP05232

    CAS  Google Scholar 

  • Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117–2127. doi:10.1105/tpc.104.023549

    PubMed  CAS  Google Scholar 

  • Staswick PE (2008) JAZing up jasmonate signaling. Trends Plant Sci 13:66–71. doi:10.1016/j.tplants.2007.11.011

    PubMed  CAS  Google Scholar 

  • Steber CM, McCourt P (2001) A role for brassinosteroids in germination in Arabidopsis. Plant Physiol 125:763–769. doi:10.1104/pp.125.2.763

    PubMed  CAS  Google Scholar 

  • Stoll M, Loveys B, Dry P (2000) Hormonal changes induced by partial rootzone drying of irrigated grapevine. J Exp Bot 51:1627–1634. doi:10.1093/jexbot/51.350.1627

    PubMed  CAS  Google Scholar 

  • Suhita D, Kolla VA, Vavasseur A, Raghavendra AS (2003) Different signaling pathways involved during the suppression of stomatal opening by methyl jasmonate or abscisic acid. Plant Sci 164:481–488. doi:10.1016/S0168-9452(02)00432-6

    CAS  Google Scholar 

  • 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. doi:10.1104/pp.103.032250

    PubMed  CAS  Google Scholar 

  • Sun TP, Gubler F (2004) Molecular mechanism of gibberellin signaling in plants. Annu Rev Plant Biol 55:197–223. doi:10.1146/annurev.arplant.55.031903.141753

    PubMed  CAS  Google Scholar 

  • Symons GM, Davies C, Shavrukov Y, Dry IB, Reid JB, Thomas MR (2006) Grapes on steroids. Brassinosteroids are involved in grape berry ripening. Plant Physiol 140:150–158. doi:10.1104/pp.105.070706

    PubMed  CAS  Google Scholar 

  • Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2005) Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol 138:2337–2343. doi:10.1104/pp.105.063503

    PubMed  CAS  Google Scholar 

  • Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2006) Cytokinin and auxin inhibit abscisic acid-induced stomatal closure by enhancing ethylene production in Arabidopsis. J Exp Bot 57:2259–2266. doi:10.1093/jxb/erj193

    PubMed  CAS  Google Scholar 

  • Thiel G, Blatt MR, Fricker MD, White IR, Millner P (1993) Modulation of K+ channels in Vicia stomatal guard cells by peptide homologs to the auxin-binding protein C terminus. Proc Natl Acad Sci USA 90:11493–11497. doi:10.1073/pnas.90.24.11493

    PubMed  CAS  Google Scholar 

  • Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448:661–665. doi:10.1038/nature05960

    PubMed  CAS  Google Scholar 

  • To JP, Kieber JJ (2008) Cytokinin signaling: two-components and more. Trends Plant Sci 13:85–92. doi:10.1016/j.tplants.2007.11.005

    PubMed  CAS  Google Scholar 

  • Underwood W, Melotto M, He SY (2007) Role of plant stomata in bacterial invasion. Cell Microbiol 9:1621–1629. doi:10.1111/j.1462-5822.2007.00938.x

    PubMed  CAS  Google Scholar 

  • Upreti KK, Murti GSR (2004) Effects of brassinosteroids on growth, nodulation, phytohormone content and nitrogenase activity in French bean under water stress. Biol Plant 48:407–411. doi:10.1023/B:BIOP.0000041094.13342.1b

    CAS  Google Scholar 

  • Vardhini BV, Rao SSR (2002) Acceleration of ripening of tomato pericarp discs by brassinosteroids. Phytochemistry 16:843–847. doi:10.1016/S0031-9422(02)00223-6

    Google Scholar 

  • Vavasseur A, Raghavendra AS (2005) Guard cell metabolism and CO2 sensing. New Phytol 165:665–682. doi:10.1111/j.1469-8137.2004.01276.x

    PubMed  CAS  Google Scholar 

  • Vert G, Nemhauser JL, Geldner N, Hong F, Chory J (2005) Molecular mechanisms of steroid hormone signaling in plants. Annu Rev Cell Dev Biol 21:177–201. doi:10.1146/annurev.cellbio.21.090704.151241

    PubMed  CAS  Google Scholar 

  • Voisin AS, Reidy B, Parent B, Rolland G, Redondo E, Gerentes D, Tardieu F, Muller B (2006) Are ABA, ethylene or their interaction involved in the response of leaf growth to soil water deficit? An analysis using naturally occurring variation or genetic transformation of ABA production in maize. Plant Cell Environ 29:1829–1840. doi:10.1111/j.1365-3040.2006.01560.x

    PubMed  CAS  Google Scholar 

  • Wang P, Song CP (2008) Guard-cell signalling for hydrogen peroxide and abscisic acid. New Phytol 178:703–718. doi:10.1111/j.1469-8137.2008.02431.x

    PubMed  CAS  Google Scholar 

  • Wang XQ, Ullah H, Jones AM, Assmann SM (2001) G protein regulation of ion channels and abscisic acid signaling in Arabidopsis guard cells. Science 292:2070–2072. doi:10.1126/science.1059046

    PubMed  CAS  Google Scholar 

  • Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565. doi:10.1038/35107108

    PubMed  CAS  Google Scholar 

  • Wilkinson S, Davies WJ (2002) ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ 25:195–210. doi:10.1046/j.0016-8025.2001.00824.x

    PubMed  CAS  Google Scholar 

  • Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280:1091–1094. doi:10.1126/science.280.5366.1091

    PubMed  CAS  Google Scholar 

  • Xu H-L, Shida A, Futatsuya F, Kumura A (1994a) Effects of epibrassinolide and abscisic acid on sorghum plants growing under soil water deficit. I. Effects on growth and survival. Jpn J Crop Sci 4:671–675

    Google Scholar 

  • Xu H-L, Shida A, Futatsuya F, Kumura A (1994b) Effects of epibrassinolide and abscisic acid on sorghum plants growing under soil water deficit. II. Physiological basis for drought resistance induced by exogenous epibrassinolide and abscisic acid. Jpn J Crop Sci 4:676–681

    Google Scholar 

  • Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251. doi:10.1146/annurev.arplant.59.032607.092804

    PubMed  CAS  Google Scholar 

  • Yasuda M, Ishikawa A, Jikumaru Y, Seki M, Umezawa T, Asami T, Maruyama-Nakashita A, Kudo T, Shinozaki K, Yoshida S, Nakashita H (2008) Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. Plant Cell 20:1678–1692. doi:10.1105/tpc.107.054296

    PubMed  CAS  Google Scholar 

  • Yi HC, Joo S, Nam KH, Lee JS, Kang BG, Kim WT (1999) Auxin and brassinosteroid differentially regulate the expression of three member of 1-aminocyclopropane-1-caboxylate synthase gene family in mungbean (Vigna radiate L.). Plant Mol Biol 41:443–454. doi:10.1023/A:1006372612574

    PubMed  CAS  Google Scholar 

  • 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. doi:10.1074/jbc.M509820200

    PubMed  CAS  Google Scholar 

  • Yu JQ, Huang LF, Hu WH, Zhou YH, Mao WH, Ye SF, Nogues S (2004) A role for brassinosteroids in the regulation of photosynthesis in Cucumis sativus. J Exp Bot 55:1135–1143. doi:10.1093/jxb/erh124

    PubMed  CAS  Google Scholar 

  • Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song CP (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448. doi:10.1104/pp.126.4.1438

    PubMed  CAS  Google Scholar 

  • Zhang Z, Ramirez J, Reboutier D, Brault M, Trouverie J, Pennarun AM, Amiar Z, Biligui B, Galagovsky L, Rona JP (2005) Brassinosteroids regulate plasma membrane anion channels in addition to proton pumps during expansion of Arabidopsis thaliana cells. Plant Cell Physiol 46:1494–1504. doi:10.1093/pcp/pci162

    PubMed  CAS  Google Scholar 

  • Zholkevich VN, Pustovoitova TN (1993) Growth and phytohormone content in Cucumis sativus L. leaves under water deficiency. Fiziol Rast (Moscow) Russ J Plant Physiol (Engl Transl) 40:676–680

    CAS  Google Scholar 

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Acknowledgments

We thank two anonymous reviewers and Dr. Tatsuo Kakimoto for helpful editorial comments. Research on guard cell signaling in the Assmann laboratory is supported by National Science Foundation (NSF) and the US Department of Agriculture (USDA).

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  1. Biology Department, Pennsylvania State University, 208 Mueller Laboratory, University Park, PA, 16802, USA

    Biswa R. Acharya & Sarah M. Assmann

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Correspondence to Sarah M. Assmann.

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Acharya, B.R., Assmann, S.M. Hormone interactions in stomatal function. Plant Mol Biol 69, 451–462 (2009). https://doi.org/10.1007/s11103-008-9427-0

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