Skip to main content

Integration of ROS and Hormone Signaling

  • Chapter
  • First Online:
Reactive Oxygen Species in Plant Signaling

Part of the book series: Signaling and Communication in Plants ((SIGCOMM))

Abstract

Plant hormones are major determinants of regulation of development and stress response of plants. Hormone signal networks are integrated in order to render an appropriate response to internal and external stimuli. Recently, emerging evidence suggests the role of reactive oxygen species (ROS) in hormone signal integration processes. In this chapter, we review the involvement of ROS in plant hormone responses and discuss the function of ROS in hormone signal integration in plant cells.

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

Access this chapter

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

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffmann T, Tang YY, Grill E, Schroeder JI (2001) A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411:1053–1057

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Allen GJ, Kwak JM, Chu SP, Llopis J, Tsien RY, Harper JF, Schroeder JI (1999) Cameleon calcium indicator reports cytoplasmic calcium dynamics in Arabidopsis guard cells. Plant J 19:735–747

    Article  PubMed  CAS  Google Scholar 

  • Babior BM (2004) NADPH oxidase. Curr Opin Immunol 16:42–47

    Article  PubMed  CAS  Google Scholar 

  • Beligni MV, Fath A, Bethke PC, Lamattina L, Jones RL (2002) Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant Physiol 129:1642–1650

    Article  PubMed  CAS  Google Scholar 

  • Bethke PC, Libourel IG, Aoyama N, Chung YY, Still DW, Jones RL (2007) The Arabidopsis aleurone layer responds to nitric oxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy. Plant Physiol 143:1173–1188

    Article  PubMed  CAS  Google Scholar 

  • Bi YM, Kenton P, Mur L, Darby R, Draper J (1995) Hydrogen peroxide does not function downstream of salicylic acid in the induction of pr protein expression. Plant J 8:235–245

    Article  PubMed  CAS  Google Scholar 

  • Bienert GP, Moller AL, Kristiansen KA, Schulz A, Moller IM, Schjoerring JK, Jahn TP (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 282:1183–1192

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Chen W, Singh KB (1999) The auxin, hydrogen peroxide and salicylic acid induced expression of the Arabidopsis GST6 promoter is mediated in part by an OCS element. Plant J 19:667–677

    Article  PubMed  CAS  Google Scholar 

  • Chen Z, Klessig DF (1991) Identification of a soluble salicylic acid-binding protein that may function in signal transduction in the plant disease-resistance response. Proc Natl Acad Sci USA 88:8179–8183

    Article  PubMed  CAS  Google Scholar 

  • Chen Z, Ricigliano JW, Klessig DF (1993a) Purification and characterization of a soluble salicylic acid-binding protein from tobacco. Proc Natl Acad Sci USA 90:9533–9537

    Article  CAS  Google Scholar 

  • Chen Z, Silva H, Klessig DF (1993b) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262:1883–1886

    Article  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

    Article  PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Demidchik V, Shabala SN, Coutts KB, Tester MA, Davies JM (2003) Free oxygen radicals regulate plasma membrane Ca2+- and K+-permeable channels in plant root cells. J Cell Sci 116:81–88

    Article  PubMed  CAS  Google Scholar 

  • Demidchik V, Shabala SN, Davies JM (2007) Spatial variation in H2O2 response of Arabidopsis thaliana root epidermal Ca2+ flux and plasma membrane Ca2+ channels. Plant J 49:377–386

    Article  PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445

    Article  PubMed  CAS  Google Scholar 

  • Durner J, Klessig DF (1995) Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defense responses. Proc Natl Acad Sci USA 92:11312–11316

    Article  PubMed  CAS  Google Scholar 

  • Ellson C, Davidson K, Anderson K, Stephens LR, Hawkins PT (2006) Ptdins3p binding to the px domain of p40phox is a physiological signal in NADPH oxidase activation. EMBO J 25:4468–4478

    Article  PubMed  CAS  Google Scholar 

  • Fath A, Bethke P, Beligni V, Jones R (2002) Active oxygen and cell death in cereal aleurone cells. J Exp Bot 53:1273–1282

    Article  PubMed  CAS  Google Scholar 

  • Fath A, Bethke PC, Jones RL (2001) Enzymes that scavenge reactive oxygen species are down-regulated prior to gibberellic acid-induced programmed cell death in barley aleurone. Plant Physiol 126:156–166

    Article  PubMed  CAS  Google Scholar 

  • Finkelstein R, Reeves W, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59:387–415

    Article  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

    Article  CAS  Google Scholar 

  • Gidrol X, Lin WS, Degousee N, Yip SF, Kush A (1994) Accumulation of reactive oxygen species and oxidation of cytokinin in germinating soybean seeds. Eur J Biochem 224:21–28

    Article  PubMed  CAS  Google Scholar 

  • Giraudat J (1995) Abscisic acid signaling. Curr Opin Cell Biol 7:232–238

    Article  PubMed  CAS  Google Scholar 

  • Henzler T, Steudle E (2000) Transport and metabolic degradation of hydrogen peroxide in Chara corallina: Model calculations and measurements with the pressure probe suggest transport of H2O2 across water channels. J Exp Bot 51:2053–2066

    Article  PubMed  CAS  Google Scholar 

  • Hu X, Jiang M, Zhang A, Lu J (2005) Abscisic acid-induced apoplastic H2O2 accumulation up-regulates the activities of chloroplastic and cytosolic antioxidant enzymes in maize leaves. Planta 223:57–68

    Article  PubMed  CAS  Google Scholar 

  • Hu X, Jiang M, Zhang J, Zhang A, Lin F, Tan M (2007) Calcium-calmodulin is required for abscisic acid-induced antioxidant defense and functions both upstream and downstream of H2O2 production in leaves of maize (Zea mays) plants. New Phytol 173:27–38

    Article  PubMed  CAS  Google Scholar 

  • Hu X, Zhang A, Zhang J, Jiang M (2006) Abscisic acid is a key inducer of hydrogen peroxide production in leaves of maize plants exposed to water stress. Plant Cell Physiol 47:1484–1495

    Article  PubMed  CAS  Google Scholar 

  • Joo JH, Bae YS, Lee JS (2001) Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol 126:1055–1060

    Article  PubMed  CAS  Google Scholar 

  • Joo JH, Yoo HJ, Hwang I, Lee JS, Nam KH, Bae YS (2005) Auxin-induced reactive oxygen species production requires the activation of phosphatidylinositol 3-kinase. FEBS Lett 579:1243–1248

    Article  PubMed  CAS  Google Scholar 

  • Jung JY, Kim YW, Kwak JM, Hwang JU, Young J, Schroeder JI, Hwang I, Lee Y (2002) Phosphatidylinositol 3- and 4-phosphate are required for normal stomatal movements. Plant Cell 14:2399–2412

    Article  PubMed  CAS  Google Scholar 

  • Kawano T (2003) Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Rep 21:829–837

    PubMed  CAS  Google Scholar 

  • Kawano T, Muto S (2000) Mechanism of peroxidase actions for salicylic acid-induced generation of active oxygen species and an increase in cytosolic calcium in tobacco cell suspension culture. J Exp Bot 51:685–693

    Article  PubMed  CAS  Google Scholar 

  • Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451

    Article  PubMed  CAS  Google Scholar 

  • Klüsener B, Young JJ, Murata Y, Allen GJ, Mori IC, Hugouvieux V, Schroeder JI (2002) Convergence of calcium signaling pathways of pathogenic elicitors and abscisic acid in Arabidopsis guard cells. Plant Physiol. 130:2152–2163

    Article  PubMed  Google Scholar 

  • Köhler B, Hills A, Blatt MR (2003) Control of guard cell ion channels by hydrogen peroxide and abscisic acid indicates their action through alternate signaling pathways. Plant Physiol 131:385–388

    Article  PubMed  Google Scholar 

  • Kopecny D, Pethe C, Sebela M, Houba-Herin N, Madzak C, Majira A, Laloue M (2005) High-level expression and characterization of Zea mays cytokinin oxidase/dehydrogenase in Yarrowia lipolytica. Biochimie 87:1011–1022

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Lam E, Kato N, Lawton M (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411:848–853

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Lee S, Choi H, Suh S, Doo IS, Oh KY, Choi EJ, Schroeder Taylor AT, Low PS, Lee Y (1999) Oligogalacturonic acid and chitosan reduce stomatal aperture by inducing the evolution of reactive oxygen species from guard cells of tomato and Commelina communis. Plant Physiol 121:147–152

    Article  PubMed  CAS  Google Scholar 

  • Liechti R, Farmer EE (2002) The jasmonate pathway. Science 296:1649–1650

    Article  PubMed  CAS  Google Scholar 

  • Liszkay A, van der Zalm E, Schopfer P (2004) Production of reactive oxygen intermediates O2•−, H2O2, and •OH by maize roots and their role in wall loosening and elongation growth. Plant Physiol 136:3114–3123; discussion 3001

    Article  PubMed  CAS  Google Scholar 

  • Loake G, Grant M (2007) Salicylic acid in plant defence – the players and protagonists. Curr Opin Plant Biol 10:466–472

    Article  PubMed  CAS  Google Scholar 

  • Manthe B, Schulz M, Schnabl H (1992) Effects of salycylic acid on growth and stomatal movements of Vicia faba l: Evidence for salicylic acid metabolization. J Chem Ecol 18:1525–1539

    Article  CAS  Google Scholar 

  • McAinsh MR, Clayton H, Mansfield TA, Hetherington AM (1996) Changes in stomatal behavior and guard cell cytosolic free calcium in response to oxidative stress. Plant Physiol 111:1031–1042

    PubMed  CAS  Google Scholar 

  • Memelink J, Lingthorst HJM, Schilperoort RA, Hoge HC (1990) Tobacco genes encoding acidic and basic isofroms of pathogenesis-related proteins display different expression patterns. Plant Mol Biol 14:119–126

    Article  PubMed  CAS  Google Scholar 

  • Mori IC, Schroeder JI (2004) Reactive oxygen species activation of plant Ca2+ channels. A signaling mechanism in polar growth, hormone transduction, stress signaling, and hypothetically mechanotransduction. Plant Physiol 135:702–708

    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

    CAS  Google Scholar 

  • Murata Y, Pei ZM, Mori IC, Schroeder J (2001) Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell 13:2513–2523

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Nakajima R, Yamazaki I (1979) The mechanism of indole-3-acetic acid oxidation by horseradish peroxidases. J Biol Chem 254:872–878

    PubMed  CAS  Google Scholar 

  • Neuenschwander U, Vernooij B, Friedrich L, Uknes S, Kessmann H, Ryals J (1995) Is H2O2 a second messenger of salicylic acid in systemic acquired resistance? Plant J 8:227–233

    Article  CAS  Google Scholar 

  • Omran RG (1977) The direct involvement of hydrogen peroxide in indoleacetic acid inactivation. Biochem Biophys Res Commun 78:970–976

    Article  PubMed  CAS  Google Scholar 

  • Overmyer K, Brosche M, Kangasjarvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8:335–342

    Article  PubMed  CAS  Google Scholar 

  • Overmyer K, Tuominen H, Kettunen R, Betz C, Langebartels C, Sandermann H Jr, Kangasjarvi J (2000) Ozone-sensitive arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. Plant Cell 12:1849–1862

    Article  PubMed  CAS  Google Scholar 

  • Park KY, Jung JY, Park J, Hwang JU, Kim YW, Hwang I, Lee Y (2003) A role for phosphatidylinositol 3-phosphate in abscisic acid-induced reactive oxygen species generation in guard cells. Plant Physiol 132:92–98

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Rao MV, Lee H, Creelman RA, Mullet JE, Davis KR (2000) Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell 12:1633–1646

    Article  PubMed  CAS  Google Scholar 

  • Rao MV, Lee HI, Davis KR (2002) Ozone-induced ethylene production is dependent on salicylic acid, and both salicylic acid and ethylene act in concert to regulate ozone-induced cell death. Plant J 32:447–456

    Article  PubMed  CAS  Google Scholar 

  • Rao MV, Paliyath G, Ormrod DP, Murr DP, Watkins CB (1997) Influence of salicylic acid on H2O2 production, oxidative stress, and H2O2-metabolizing enzymes. Salicylic acid-mediated oxidative damage requires H2O2. Plant Physiol 115:137–149

    Article  PubMed  CAS  Google Scholar 

  • Ryals J, Lawton KA, Delaney TP, Friedrich L, Kessmann H, Neuenschwander U, Uknes S, Vernooij B, Weymann K (1995) Signal transduction in systemic acquired resistance. Proc Natl Acad Sci USA 92:4202–4205

    Article  PubMed  CAS  Google Scholar 

  • Saito N, Munemasa S, Nakamura Y, Shimoishi Y, Mori IC, Murata Y (2008) Roles of rcn1, regulatory a subunit of protein phosphatase2A, in methyl jasmonate signaling and signal crosstalk between methyl jasmonate and abscisic acid. Plant Cell Physiol 49:1396–1401

    Article  PubMed  CAS  Google Scholar 

  • Savitsky PA, Gazaryan IG, Tishkov VI, Lagrimini LM, Ruzgas T, Gorton L (1999) Oxidation of indole-3-acetic acid by dioxygen catalysed by plant peroxidases: Specificity for the enzyme structure. Biochem J 340(Pt 3):579–583

    Article  PubMed  CAS  Google Scholar 

  • Schopfer P (2001) Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: Implications for the control of elongation growth. Plant J 28:679–688

    Article  PubMed  CAS  Google Scholar 

  • Schopfer P, Liszkay A, Bechtold M, Frahry G, Wagner A (2002) Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta 214:821–828

    Article  PubMed  CAS  Google Scholar 

  • Schroeder JI, Hagiwara S (1990) Repetitive increases in cytosolic Ca2+ of guard cells by abscisic acid activation of nonselective Ca2+ permeable channels. Proc Natl Acad Sci USA 87:9305–9309

    Article  PubMed  CAS  Google Scholar 

  • Schweikert C, Liszkay A, Schopfer P (2000) Scission of polysaccharides by peroxidase-generated hydroxyl radicals. Phytochemistry 53:565–570

    Article  PubMed  CAS  Google Scholar 

  • Smith AM, Morrison WL, Milham PJ (1982) Oxidation of indole-3-acetic acid by peroxidase: Involvement of reduced peroxidase and coumpound III with superoxide as a product. Biochemistry 21:4414–4419

    Article  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

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Sumimoto H (2008) Structure, regulation and evolution of nox-family nadph oxidases that produce reactive oxygen species. FEBS J 275:3249–3277

    Article  PubMed  CAS  Google Scholar 

  • Summermatter K, Sticher L, Metraux JP (1995) Systemic responses in Arabidopsis thaliana infected and challenged with Pseudomonas syringae pv syringae. Plant Physiol 108:1379–1385

    PubMed  CAS  Google Scholar 

  • Tamura S (1990). Historical aspects of gibberelins. Gibberellins N, Takahashi BO, Phinney J (eds) Macmillan, New York, pp 1–8

    Google Scholar 

  • Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14(Suppl):S153–S164

    PubMed  CAS  Google Scholar 

  • Zhang X, Dong FC, Gao JF, Song CP (2001) Hydrogen peroxide-induced changes in intracellular pH of guard cells precede stomatal closure. Cell Res 11:37–43

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Mori, I.C., Murata, Y., Uraji, M. (2009). Integration of ROS and Hormone Signaling. In: Rio, L., Puppo, A. (eds) Reactive Oxygen Species in Plant Signaling. Signaling and Communication in Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-00390-5_2

Download citation

Publish with us

Policies and ethics