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Reactive Oxygen Species in Ozone Toxicity

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Reactive Oxygen Species in Plant Signaling

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

Abstract

The entry of ozone (O3) to the leaf intercellular airspace is followed by its degradation to reactive oxygen species (ROS) and the induction of active ROS production by the plant itself. Using genetic and genomic tools, some of the components involved in plant O3 responses have begun to be delineated. Mutant screens and analyses in the model plant Arabidopsis thaliana have revealed a picture of the O3 response that is coming into focus in the form of recurring themes that constitute a core O3 response, which consists of a network of ROS and hormonal interactions controlling the magnitude of O3-induced cell death.

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Reference

  • Ahlfors R, Lång S, Overmyer K, Jaspers P, Brosché M, Tauriainen A, Kollist H, Tuominen H, Belles-Boix E, Piippo M, Inzé D, Palva ET, Kangasjärvi J (2004a) Arabidopsis radical-induced cell death 1 belongs to the WWE protein-protein interaction-domain protein family and modulates abscisic acid, ethylene, and methyl jasmonate responses. Plant Cell 16:1925–1937

    Article  CAS  Google Scholar 

  • Ahlfors R, Macioszek V, Rudd J, Brosché M, Schlichting R, Scheel D, Kangasjärvi J (2004b) Stress hormone-independent activation and nuclear translocation of mitogen-activated protein kinases (MAPKs) in Arabidopsis thaliana plants during ozone exposure. Plant J 40:512–522

    Article  CAS  Google Scholar 

  • Barth C, Conklin PL (2003) The lower cell density of leaf parenchyma in the Arabidopsis thaliana mutant lcd1-1 is associated with increased sensitivity to ozone and virulent Pseudomonas syringae. Plant J 35:206–218

    Article  PubMed  CAS  Google Scholar 

  • Bechtold U, Richard O, Zamboni A, Gapper C, Geisler M, Pogson B, Karpinski S, Mullineaux PM (2008) Impact of chloroplastic- and extracellular-sourced ROS on high light-responsive gene expression in Arabidopsis. J Exp Bot 59:121–133

    Article  PubMed  CAS  Google Scholar 

  • Belles-Boix E, Babiychuk E, Van Montagu M, Inzé D, Kushnir S (2000) CEO1, a new protein from Arabidopsis thaliana, protects yeast against oxidative damage. FEBS Lett 482:19–24

    Article  PubMed  CAS  Google Scholar 

  • Bienert GP, Moller ALB, 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 

  • Booker FL, Burkey KO, Overmyer K, Jones AM (2004) Differential responses of G-protein Arabidopsis thaliana mutants to ozone. New Phytol 162:633–641

    Article  CAS  Google Scholar 

  • Brosché M, Kangasjärvi S-L, Overmyer K, Wrzaczek M, Kangasjärvi J (2009) Stress signaling III: Reactive oxygen species. In: Pareek A, Sopory SK, Bohnert HJ, Govindjee (eds) Abiotic stress adaptation in plants: physiological, molecular and genomic foundation. Springer, Dordrecht, The Netherlands

    Google Scholar 

  • Clayton H, Knight MR, Knight H, McAinsh MR, Hetherington AM (1999) Dissection of the ozone-induced calcium signature. Plant J 17: 575–579

    Article  PubMed  CAS  Google Scholar 

  • Conklin PL, Norris SR, Wheeler GL, Williams EH, Smirnoff N, Last RL (1999) Genetic evidence for the role of GDP-mannose in plant ascorbic acid (vitamin C) synthesis. Proc Natl Acad Sci USA 96:4198–4203

    Article  PubMed  CAS  Google Scholar 

  • Conklin PL, Saracco SA, Norris SR, Last RA (2000) Identification of ascorbate acid-deficient Arabidopsis thaliana mutants. Genetics 154:847–856

    PubMed  CAS  Google Scholar 

  • Conklin PL, Williams EH, Last RL (1996) Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant. Proc Natl Acad Sci USA 93:9970–9974

    Article  PubMed  CAS  Google Scholar 

  • Eckardt NA, Pell EJ (1994) O3-induced degradation of rubisco protein and loss of rubisco messenger-RNA in relation to leaf age in Solanum-Tuberosum L. New Phytol 127:741–748

    Article  CAS  Google Scholar 

  • Ederli L, Morettini R, Borgogni A, Wasternack C, Miersch O, Reale L, Ferranti F, Tosti N, Pasqualini S (2006) Interaction between nitric oxide and ethylene in the induction of alternative oxidase in ozone-treated tobacco plants. Plant Physiol 142:595–608

    Article  PubMed  CAS  Google Scholar 

  • Evans NH, McAinsh MR, Hetherington AM, Knight MR (2005) ROS perception in Arabidopsis thaliana: the ozone-induced calcium response. Plant J 41:615–626

    Article  PubMed  CAS  Google Scholar 

  • Fiscus EL, Booker FL, Burkey KO (2005) Crop responses to ozone: uptake, modes of action, carbon assimilation and partitioning. Plant Cell Environ 28:997–1011

    Article  CAS  Google Scholar 

  • Fujibe T, Saji H, Arakawa K, Yabe N, Takeuchi Y, Yamamoto KT (2004) A methyl viologen-resistant mutant of Arabidopsis, which is allelic to ozone-sensitive rcd1, is tolerant to supplemental UV-B irradiation. Plant Physiol 134:275–285

    Article  PubMed  CAS  Google Scholar 

  • Fujibe T, Saji H, Watahiki MK, Yamamoto KT (2006) Overexpression of the radical-induced cell death1 (RCD1) gene of Arabidopsis causes weak rcd1 phenotype with compromised oxidative-stress responses. Biosci Biotech Biochem 70:1827–1831

    Article  CAS  Google Scholar 

  • Gomi K, Ogawa D, Katou S, Kamada H, Nakajima N, Saji H, Soyano T, Sasabe M, Machida Y, Mitsuhara I, Ohashi Y, Seo S (2005) A mitogen-activated protein kinase NtMPK4 activated by SIPKK is required for jasmonic acid signaling and involved in ozone tolerance via stomatal movement in tobacco. Plant Cell Physiol 46:1902–1914

    Article  PubMed  CAS  Google Scholar 

  • González-Bayón R, Kinsman EA, Quesada V, Vera A, Robles P, Ponce MR, Pyke KA, Micol JL (2006) Mutations in the RETICULATA gene dramatically alter internal architecture but have little effect on overall organ shape in Arabidopsis leaves. J Exp Bot 57:3019–3031

    Article  PubMed  Google Scholar 

  • Hamel LP, Miles GP, Samuel MA, Ellis BE, Seguin A, Beaudoin N (2005) Activation of stress-responsive mitogen-activated protein kinase pathways in hybrid poplar (Populus trichocarpa x Populus deltoides). Tree Physiol 25:277–288

    Article  PubMed  CAS  Google Scholar 

  • He YK, Tang RH, Hao Y, Stevens RD, Cook CW, Am SM, Jing LF, Yang ZG, Chen LG, Guo FQ, Fiorani F, Jackson RB, Crawford NM, Pei ZM (2004) Nitric oxide represses the Arabidopsis floral transition. Science 305:1968–1971

    Article  PubMed  CAS  Google Scholar 

  • Joo JH, Wang S, Chen JG, Jones AM, Fedoroff N (2004) Different signaling and cell death roles of heterotrimeric G protein α and β subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell 17:957–970

    Article  Google Scholar 

  • Kadono T, Yamaguchi Y, Furuichi T, Hirono M, Garrec J, Kawano T (2006) Ozone-induced cell death mediated with oxidative and calcium signaling pathways in tobacco Bel W3 and Bel B cell suspension cultures. Plant Signal Behav 1:321–322

    Article  Google Scholar 

  • Kangasjärvi J, Jaspers P, Kollist H (2005) Signalling and cell death in ozone-exposed plants. Plant Cell Environ 28:1021–1036

    Article  Google Scholar 

  • Kangasjärvi J, Talvinen J, Utriainen M, Karjalainen R (1994) Plant defence systems induced by ozone. Plant Cell Environ 17:783–794

    Article  Google Scholar 

  • Katiyar-Agarwal S, Zhu J, Kim K, Agarwal M, Fu X, Huang A, Zhu JK (2006) The plasma membrane Na+/H+ antiporter SOS1 interacts with RCD1 and functions in oxidative stress tolerance in Arabidopsis. Proc Natl Acad Sci USA 103:18816–18821

    Article  PubMed  CAS  Google Scholar 

  • Koch JR, Creelman RA, Eshita SM, Seskar M, Mullet JE, Davis KR (2000) Ozone sensitivity in hybrid poplar correlates with insensitivity to both salicylic acid and jasmonic acid. The role of programmed cell death in lesion formation. Plant Physiol 123:487–496

    Article  PubMed  CAS  Google Scholar 

  • Kollist T, Moldau H, Rasulov B, Oja V, Ramma H, Huve K, Jaspers P, Kangasjärvi J, Kollist H (2007) A novel device detects a rapid ozone-induced transient stomatal closure in intact Arabidopsis and its absence in abi2 mutant. Physiol Plant 129:796–803

    Article  CAS  Google Scholar 

  • Lee JS, Ellis BE (2007) Arabidopsis MAPK phosphatase 2 (MKP2) positively regulates oxidative stress tolerance and inactivates the MPK3 and MPK6 MAPKs. J Biol Chem 282:25020–25029

    Article  PubMed  CAS  Google Scholar 

  • Li PH, Mane SP, Sioson AA, Robinet CV, Heath LS, Bohnert HJ, Grene R (2006) Effects of chronic ozone exposure on gene expression in Arabidopsis thaliana ecotypes and in Thellungiella halophila. Plant Cell Environ 29:854–868

    Article  PubMed  CAS  Google Scholar 

  • Lorenzo O, Chico JM, Sánchez-Serrano JJ, Solano R (2004) Jasmonate-insensitive1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated responses in Arabidopsis. Plant Cell 16:1938–1950

    Article  PubMed  CAS  Google Scholar 

  • Moeder W, Barry CS, Tauriainen AA, Betz C, Tuomainen J, Utriainen M, Grierson D, Sandermann H, Langebartles C, Kangasjärvi J (2002) Ethylene synthesis regulated by bi-phasic induction of ACC synthase and ACC oxidase genes is required for H2O2 accumulation and cell death in ozone-exposed tomato. Plant Physiol 130:1918–1926

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Nickstadt A, Thomma BPHJ, Feussner I, Kangasjärvi J, Zeier J, Loeffler C, Scheel D, Berger S (2004) The jasmonate-insensitive mutant jin1 shows increased resistance to biotrophic as well as necrotrophic pathogens. Mol Plant Pathol 5:425–434

    Article  PubMed  CAS  Google Scholar 

  • Örvar BL, McPherson J, Ellis BE (1997) Pre-activating wounding response in tobacco prior to high-level ozone exposure prevents necrotic injury. Plant J 11:203–212

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Overmyer K, Brosché M, Pellinen R, Kuittinen T, Tuominen H, Ahlfors R, Keinanen M, Saarma M, Scheel D, Kangasjärvi J (2005) Ozone-induced programmed cell death in the Arabidopsis radical-induced cell death1 mutant. Plant Physiol 137:1092–1104

    Article  PubMed  CAS  Google Scholar 

  • Overmyer K, Kollist H, Tuominen H, Betz C, Langebartels C, Wingsle G, Kangasjärvi S-L, Brader G, Mullineaux P, Kangasjärvi J (2008) Complex phenotypic profiles leading to ozone sensitivity in Arabidopsis thaliana mutants. Plant Cell Environ 31:1237–1249

    Article  PubMed  CAS  Google Scholar 

  • Overmyer K, Tuominen H, Kettunen R, Betz C, Langebartels C, Sandermann H, Jr, Kangasjärvi J (2000) The 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 

  • Pasqualini S, Paolocci F, Borgogni A, Morettini R, Ederli L (2007) The overexpression of an alternative oxidase gene triggers ozone sensitivity in tobacco plants. Plant Cell Environ 30:1545–1556

    Article  PubMed  CAS  Google Scholar 

  • Pasqualini S, Piccioni C, Reale L, Ederli L, la Torre G, Ferranti F (2003) Ozone-induced cell death in tobacco cultivar Bel W3 plants. The role of programmed cell death in lesion formation. Plant Physiol 133:1122–1134

    Article  PubMed  CAS  Google Scholar 

  • Pell EJ, Schlagnhaufer CD, Arteca RN (1997) Ozone-induced oxidative stress: mechanisms of action and reaction. Physiol Plant 100:264–273

    Article  CAS  Google Scholar 

  • Pellinen R, Palva T, Kangasjärvi J (1999) Subcellular localization of ozone-induced hydrogen peroxide production in birch (Betula pendula) leaf cells. Plant J 20:349–356

    Article  PubMed  CAS  Google Scholar 

  • Pellinen RI, Korhonen MS, Tauriainen AA, Palva ET, Kangasjärvi J (2002) Hydrogen peroxide activates cell death and defense gene expression in birch. Plant Physiol 130:549–560

    Article  PubMed  CAS  Google Scholar 

  • Rao MV, Davis KR (1999) Ozone-induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acid. Plant J 17:603–614

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Samuel MA, Miles GP, Ellis BE (2000) Ozone treatment rapidly activates MAP kinase signalling in plants. Plant J 22:367–376

    Article  PubMed  CAS  Google Scholar 

  • Samuel MA, Walia A, Mansfield SD, Ellis BE (2005) Overexpression of SIPK in tobacco enhances ozone-induced ethylene formation and blocks ozone-induced SA accumulation. J Exp Bot 56:2195–2201

    Article  PubMed  CAS  Google Scholar 

  • Schraudner M, Langebartels C, Sandermann H, Jr (1997) Changes in the biochemical status of plants cells induced by the environmental pollutant ozone. Physiol Plant 100:274–280

    Article  CAS  Google Scholar 

  • Schraudner M, Moeder W, Wiese C, Van Camp W, Inzé D, Langebartels C, Sandermann H, Jr (1998) Ozone-induced oxidative burst in the ozone biomonitor plant, tobacco Bel W3. Plant J 16:235–245

    Article  CAS  Google Scholar 

  • Smirnoff N, Conklin PL, Loewus FA (2001) Biosynthesis of ascorbic acid in plants: a renaissance. Annu Rev Plant Physiol Plant Mol Biol 52:437–467

    Article  PubMed  CAS  Google Scholar 

  • Streatfield SJ, Weber A, Kinsman EA, Häusler RE, Li J, Post-Beittenmiller D, Kaiser WM, Pyke KA, Fluegge UI, Chory J (1999) The phosphoenolpyruvate/phosphate translocator is required for phenolic metabolism, palisade cell development, and plastid-dependent nuclear gene expression. Plant Cell 11:1609–1621

    Article  PubMed  CAS  Google Scholar 

  • Torsethaugen G, Pell EJ, Assmann SM (1999) Ozone inhibits guard cell K+ channels implicated in stomatal opening. Proc Natl Acad Sci USA 96:13577–13582

    Article  PubMed  CAS  Google Scholar 

  • Tuominen H, Overmyer K, Keinänen M, Kollist H, Kangasjärvi J (2004) Mutual antagonism of ethylene and jasmonic acid regulates ozone-induced spreading cell death in Arabidopsis. Plant J 39:59–69

    Article  PubMed  CAS  Google Scholar 

  • Vahala J, Ruonala R, Keinänen M, Tuominen H, Kangasjärvi J (2003) Ethylene insensitivity modulates ozone-induced cell death in birch. Plant Physiol 132:185–195

    Article  PubMed  CAS  Google Scholar 

  • Vahala J, Schlagnhaufer CD, Pell EJ (1998) Induction of an ACC synthase cDNA by ozone in light-grown Arabidopsis thaliana leaves. Physiol Plant 103:45–50

    Article  CAS  Google Scholar 

  • Vahisalu T, Kollist H, Wang Y-F, Nishimura N, Chan W-Y, Valerio G, Lamminmäki A, Brosché M, Moldau H, Desikan R, Schroeder JI, Kangasjärvi J (2008) SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature 452:487–493

    Article  PubMed  CAS  Google Scholar 

  • Wegener A, Gimbel W, Werner T, Hani J, Ernst D, Sandermann H (1997) Sequence analysis and ozone-induced accumulation of polyubiquitin mRNA in Pinus sylvestris. Can J For Res 27:945–948

    Article  CAS  Google Scholar 

  • Wohlgemuth H, Mittelstrass K, Kschieschan S, Bender J, Weigel HJ, Overmyer K, Kangäsjarvi J, Sandermann H, Langebartels C (2002) Activation of an oxidative burst is a general feature of sensitive plants exposed to the air pollutant ozone. Plant Cell Environ 25:717–726

    Article  CAS  Google Scholar 

  • Yoshida S, Tamaoki M, Shikano T, Nakajima N, Ogawa D, Ioki M, Aono M, Kubo A, Kamada H, Inoue Y, Saji H (2006) Cytosolic dehydroascorbate reductase is important for ozone tolerance in Arabidopsis thaliana. Plant Cell Physiol 47:304–308

    Article  PubMed  CAS  Google Scholar 

  • Zhang W, Gruszewski HA, Chevone BI, Nessler CL (2008) An Arabidopsis purple acid phosphatase with phytase activity increases foliar ascorbate. Plant Physiol 146:431–440

    Article  PubMed  CAS  Google Scholar 

  • Zybailov B, Rutschow H, Friso G, Rudella A, Emanuelsson O, Sun Q, van Wijk KJ (2008) Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS ONE 3:e1994; doi:10.1371/journal.pone.0001994

    Article  PubMed  Google Scholar 

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  1. Plant Biology, Department of Biological and Environmental Sciences, University of Helsinki, 00014, Helsinki, Finland

    Kirk Overmyer, Michael Wrzaczek & Jaakko Kangasjärvi

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  1. Kirk Overmyer
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  2. Michael Wrzaczek
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  3. Jaakko Kangasjärvi
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Correspondence to Jaakko Kangasjärvi .

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    Overmyer, K., Wrzaczek, M., Kangasjärvi, J. (2009). Reactive Oxygen Species in Ozone Toxicity. 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_12

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