Skip to main content
SpringerLink
Log in

Involvement of Phytohormones in Plant Responses to Ozone

  • Chapter
  • First Online:
Plant Hormones under Challenging Environmental Factors

Abstract

Among various contaminants, ozone (O3) is considered the most ubiquitous and phytotoxic atmospheric pollutant in industrialized and developing countries. It causes extensive risks for plant life, in terms of survival and productivity of wild and cultivated species. Plant response to O3 resembles the biotic defense reactions and includes two steps: the first is a biphasic oxidative burst with a massive, rapid, and transient increase in apoplastic reactive oxygen species (ROS) production; the second is the induction of the hypersensitive response (HR) and systemic acquired resistance (SAR). In particular, the acute O3 exposure (high concentrations for a few hours) results in the activation of programmed cell death (PCD) response that interacts with the synthesis of several hormones and other signaling molecules. The cross talk among all these molecules and their complex and interconnected signaling pathways are more important to determine (1) the initiation, propagation, and containment of O3-induced cell death, (2) the degree of the sensitivity of plants to this contaminant, and (3) the regulatory potential that plants have to promptly respond to oxidative stress. The present chapter reviews the role of phytohormones (such as ethylene, abscisic acid, gibberellins, auxins, and cytokinins) and other signaling molecules (such as salicylic and jasmonic acids, proline, and brassinosteroids), as well as their synergistic and antagonistic effects, in the complex signaling pathway involved in plant responses to O3 stress.

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

Access this chapter

Log in via an institution
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

  • Ahlfors R, Macioszek V, Rudd J, Brosché M, Schlichting R, Scheel D, Kangasjärvi J. Stress hormone-independent activation and nuclear translocation of mitogen-activated protein kinases in Arabidopsis thaliana during ozone exposure. Plant J. 2004;40:512–22.

    Article  CAS  PubMed  Google Scholar 

  • An Z, Jing W, Liu Y, Zhang W. Hydrogen peroxide generated by copper amine oxidase is involved in abscisic acid-induced stomatal closure in Vicia faba. J Exp Bot. 2008;59:815–25.

    Article  CAS  PubMed  Google Scholar 

  • Baier M, Kandlbinder A, Golldack D, Dietz KJ. Oxidative stress and ozone: perception, signalling and response. Plant Cell Environ. 2005;28:1012–20.

    Article  CAS  Google Scholar 

  • Bajguz A, Hayat S. Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol Biochem. 2009;47:1–8.

    Article  CAS  PubMed  Google Scholar 

  • Bartoli CG, Casalongué CA, Simontacchi M, Marquez-Garcia B, Foyer CH. Interactions between hormone and redox signalling pathways in the control of growth and cross tolerance to stress. Environ Exp Bot. 2013;94:73–88.

    Article  CAS  Google Scholar 

  • Bashandy T, Guilleminot J, Vernoux T, Caparros-Ruiz D, Ljung K, Meyer Y, Reichheld JP. Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling. Plant Cell. 2010;22:376–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beauchamp J, Wisthaler A, Hansel A, Kleist E, Miebach M, Niinemets U, Schurr U, Wildt J. Ozone induced emissions of biogenic VOC from tobacco: relationships between ozone uptake and emission of LOX products. Plant Cell Environ. 2005;28:1334–43.

    Article  CAS  Google Scholar 

  • Betz AG, Gerstner E, Olbrich M, Winkler B, Welzl G, Langebartels C, Heller W, Sandermann H, Ernst D. Effects of abiotic stress on gene transcription in European beech: ozone affects ethylene biosynthesis in saplings of Fagus sylvatica L. iForest. 2009;2:114–8.

    Google Scholar 

  • Black VJ, Stewart CA, Roberts JA, Black CR. Effects of ozone on the physiology, growth and reproduction of Brassica campestris L. New Phytol. 2007;176:150–63.

    Article  CAS  PubMed  Google Scholar 

  • Blomster T, Salojärvi J, Sipari N, Broschè M, Ahlfors R, Keinänen M, Overmeyer K, Kangasjärvi J. Apoplastic reactive oxygen species transiently decrease auxin signaling and cause stress-induced morphogenic response in Arabidopsis. Plant Physiol. 2011;157:1866–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Booker F, Muntifering R, McGrath M, Burkey K, Decoteau D, Fiscus E, Manning W, Krupa S, Chappelka A, Grantz D. The ozone component of global change: potential effects on agricultural and horticultural plant yield, product quality and interactions with invasive species. J Integr Plant Biol. 2009;51:337–51.

    Article  CAS  PubMed  Google Scholar 

  • Booker F, Burkey K, Morgan P, Fiscus E, Jones A. Minimal influence of G-protein null mutations on ozone-induced changes in gene expression, foliar injury, gas exchange and peroxidase activity in Arabidopsis thaliana L. Plant Cell Environ. 2012;35:668–81.

    Article  CAS  PubMed  Google Scholar 

  • Brock AK, Willmann R, Kolb D, Grefen L, Lajunen HM, Bethke G, Lee J, Nurnmerger T, Gust AA. The Arabidopsis mitogen-activated protein kinase phosphatase PP2C5 affects seed germination, stomatal aperture, and abscisic acid-inducible gene expression. Plant Physiol. 2010;153:1098–111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castagna A, Ranieri A. Detoxification and repair process of ozone injury: From O3 uptake to gene expression adjustment. Environ Pollut. 2009;157:1461–9.

    Article  CAS  PubMed  Google Scholar 

  • Castagna A, Ederli L, Pasqualini S, Mensuali-Sodi A, Baldan B, Donnini S, Ranieri A. The tomato ethylene receptor LE-ETR3 (NR) is not involved in mediating ozone sensitivity: casual relationships among ethylene emission, oxidative burst and tissue damage. New Phytol. 2007;174:342–56.

    Article  CAS  PubMed  Google Scholar 

  • Christians MJ, Gingerich DJ, Hansen M, Binder BM, Kieber JJ, Vierstra RD. The BTB ubiquitin ligases ETO1, EOL1 and EOL2 act collectively to regulate ethylene biosynthesis in Arabidopsis by controlling type-2 ACC synthase levels. Plant J. 2009;57:332–45.

    Article  CAS  PubMed  Google Scholar 

  • Intergovernmental Panel on Climate Change, IPCC. Fifth assessment report. 2013. http://www.ipcc.ch/report/ar5/index/.shtml

  • Dar TA, Uddin T, Khan MMA, Hakeem KR, Jaleel H. Jasmonates counter plant stress: a review. Environ Exp Bot. 2015;115:49–57.

    Article  CAS  Google Scholar 

  • Daszkowska-Golec A, Szarejko I. Open or close the gate – stomata action under the control of phytohormones in drought stress conditions. Front Plant Sci. 2013;4:138.

    Article  PubMed  PubMed Central  Google Scholar 

  • Devoto A, Turner JG. Jasmonate-regulated Arabidopsis stress signaling network. Physiol Plant. 2005;123:161–72.

    Article  CAS  Google Scholar 

  • Di Baccio D, Ederli L, Marabottini R, Badiani M, Francini A, Nali C, Antonelli M, Santangelo E, Sebastiani L, Pasqualini S. Similar foliar lesions but opposite hormonal patterns in a tomato mutant impaired in ethylene perception and its near isogenic wild type challenged with ozone. Environ Exp Bot. 2012;75:286–97.

    Article  CAS  Google Scholar 

  • Diara C, Castagna A, Baldan B, Mensuali Sodi A, Sahr T, Langebartels C, Sebastiani L, Ranieri A. Differences in the kinetics and scale of signaling molecule production modulate the ozone sensitivity of hybrid poplar clones: the roles of H2O2, ethylene and salicylic acid. New Phytol. 2005;168:351–64.

    Article  CAS  PubMed  Google Scholar 

  • Dobra J, Motyka V, Dobrev P, Malbeck J, Prasil I, Haisel D. Comparison of hormonal responses of heat, drought and combined stress in tobacco plants with elevated proline content. J Plant Physiol. 2010;167:1360–70.

    Article  CAS  PubMed  Google Scholar 

  • Döring AS, Pellegrini E, Campanella A, Trivellini A, Gennai C, Petersen M, Nali C, Lorenzini G. How sensitive is Melissa officinalis to realistic ozone concentrations? Plant Physiol Biochem. 2014;74:156–64.

    Article  PubMed  CAS  Google Scholar 

  • El-Khatib AA. The response of some common Egyptian plants to ozone and their use as biomonitors. Environ Pollut. 2003;124:419–28.

    Article  CAS  PubMed  Google Scholar 

  • Evans NH, McAinsh MR, Hetherington AM, Knight MR. ROS perception in Arabidopsis thaliana: the ozone-induced calcium response. Plant J. 2005;41:615–26.

    Article  CAS  PubMed  Google Scholar 

  • Farmer EE, Mueller MJ. ROS-mediated lipid peroxidation and RES-activated signaling. Annu Rev Plant Biol. 2013;64:429–50.

    Article  CAS  PubMed  Google Scholar 

  • Filippou P, Bouchagier P, Skotti E, Fotopoulos V. Proline and reactive oxygen/nitrogen species metabolism is involved in the tolerant response of the invasive plant species Ailanthus altissima to drought and salinity. Environ Exp Bot. 2014;97:1–10.

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G. Ascorbate and glutathione: the heart of the redox hub. Plant Physiol. 2011;155:2–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gallie DR, Geisler-Lee J, Chen JF, Jolley B. Tissue specific expression of the ethylene biosynthetic. Machinery regulates root growth in maize. Plant Mol Biol. 2009;69:195–211.

    Article  CAS  PubMed  Google Scholar 

  • Gan S, Amasino RM. Inhibition of leaf senescence by autoregulated production of cytokinin. Science. 1995;270:1986–8.

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem. 2010;48:909–30.

    Article  CAS  PubMed  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. 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. 2005;46:1902–14.

    Article  CAS  PubMed  Google Scholar 

  • Gosti F, Beaudoin N, Serizet C, Webb A, Vartanian N, Giraudat J. ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell. 1999;11:1879–909.

    Article  Google Scholar 

  • Gottardini E, Cristofori A, Cristofolini F, Nali C, Pellegrini E, Bussotti F, Ferretti M. Chlorophyll-related indicators are linked to visible ozone symptoms: evidence from a field study on native Viburnum lantana L. plants in northern Italy. Ecol Indic. 2014;39:65–74.

    Article  CAS  Google Scholar 

  • Ha S, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Tran L-SP. Cytokinins: metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci. 2012;17:172–9.

    Article  CAS  PubMed  Google Scholar 

  • Hamayun ML, Khan SA, Khan AL, Shin JH, Ahmad B, Shin DH, Lee IJ. Exogenous gibberellic acid reprograms soybean to higher growth and salt stress tolerance. J Agric Food Chem. 2010;23:7226–32.

    Article  CAS  Google Scholar 

  • Han L, Li GL, Yang KY, Mao G, Wang R, Liu Y, Zhang S. Mitogen-activated protein kinase 3 and 6 regulate Botrytis cinerea-induced ethylene production in Arabidopsis. Plant J. 2010;64:114–27.

    CAS  PubMed  Google Scholar 

  • Hasan SA, Hayat S, Ahmad A. Brassinosteroids protect photosynthetic machinery against the cadmium induced oxidative stress in two tomato cultivars. Chemosphere. 2011;84:1446–51.

    Article  CAS  PubMed  Google Scholar 

  • Heath RL. Modification of the biochemical pathways of plants induced by ozone: what are the varied routes to change? Environ Pollut. 2008;155:453–63.

    Article  CAS  PubMed  Google Scholar 

  • Horváth E, Szalai G, Janda T. Induction of abiotic stress tolerance by salicylic acid signaling. J Plant Growth Regul. 2007;26:290–300.

    Article  CAS  Google Scholar 

  • Hoshika Y, Watanabe M, Inada N, Koike T. Model-based analysis of avoidance of ozone stress by stomatal closure in Siebold’s beech (Fagus crenata). Ann Bot. 2013;112:1149–58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoshika Y, Watanabe M, Kitao M, Häberle KH, Grams TE, Koike T, Matissek R. Ozone induces stomatal narrowing in European and Siebold’s beeches: a comparison between two experiments of free-air ozone exposure. Environ Pollut. 2015;196:527–33.

    Article  CAS  PubMed  Google Scholar 

  • Iglesias MJ, Terrile MC, Bartoli CG, D’Ippólito S, Casalongué CA. Auxin signaling participates in the adaptative response against oxidative stress and salinity by interacting with redox metabolism in Arabidopsis. Plant Mol Biol. 2010;74:215–22.

    Article  CAS  PubMed  Google Scholar 

  • Iqbal N, Umar S, Khan NA, Khan MIR. A new perspective of phytohormones in salinity tolerance: regulation of proline metabolism. Environ Exp Bot. 2014;100:34–42.

    Article  CAS  Google Scholar 

  • Jabs T. Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem Pharmacol. 1999;57:231–45.

    Article  CAS  PubMed  Google Scholar 

  • Jayakannan M, Bose J, Babourina O, Rengel Z, Shabala S. Salicylic acid in plant salinity stress signaling and tolerance. Plant Growth Regul. 2015;76:25–40.

    Article  CAS  Google Scholar 

  • Jiang M, Zhang J. Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot. 2002;53:2401–10.

    Article  CAS  PubMed  Google Scholar 

  • Jibran R, Hunter DA, Dijkwel PP. Hormonal regulation of leaf senescence through integration of developmental and stress signals. Plant Mol Biol. 2013;82:547–61.

    Article  CAS  PubMed  Google Scholar 

  • Jones JDG, Dangl JL. The plant immune system. Nature. 2006;444:323–9.

    Article  CAS  PubMed  Google Scholar 

  • Joo JH, Wang S, Chen JG, Jones AM, Fedoroff NV. Different signaling and cell death roles of heterotrimeric G protein alpha and beta subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell. 2005;17:957–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kangasjärvi J, Jaspers P, Kollist H. Signaling and cell death in ozone-exposed plants. Plant Cell Environ. 2005;28:1021–36.

    Article  Google Scholar 

  • Kazan K. Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci. 2015;20:219–29.

    Article  CAS  PubMed  Google Scholar 

  • Khokon AR, Okuma E, Hossain MA, Munemasa S, Uraji M, Nakamura Y, Mori IC, Murata Y. Involvement of extracellular oxidative burst in salicylic acid-induced stomatal closure in Arabidopsis. Plant Cell Environ. 2011;34:434–43.

    Article  CAS  PubMed  Google Scholar 

  • Kim JI, Murphy AS, Baek D, Lee SW, Yun DJ, Bressan RA, Narasimhan ML. YUCCA6 over-expression demonstrates auxin function in delaying leaf senescence in Arabidopsis thaliana. J Exp Bot. 2011;62:3981–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kock JR, Creelman RA, Eshita SM, Seskar M, Mullet JE, Davis KR. 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. 2000;123:487–96.

    Article  Google Scholar 

  • Kovtun Y, Chiu WL, Tena G, Sheen J. Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci U S A. 2000;97:2940–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krupa SV. Joint effects of elevated levels of ultraviolet-B radiation, carbon dioxide and ozone in plants. Photochem Photobiol. 2003;78:535–42.

    Article  CAS  PubMed  Google Scholar 

  • Kudla J, Batistic O, Hashimoto K. Calcium signals: the lead currency of plant information processing. Plant Cell. 2010;22:541–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lamb C, Dixon RA. The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol. 1997;48:251–75.

    Article  CAS  PubMed  Google Scholar 

  • Leisner CP, Ainsworth E. Quantifying the effects of ozone on plant reproductive growth and development. Global Change Biol. 2012;18:606–16.

    Article  Google Scholar 

  • Leung J, Orfanidi S, Chefdor F, Meszaros T, Bolte S, Mizoguchi T, Shinozaki K, Giraudat J, Bogre L. Antagonistic interaction between MAP kinase and protein phosphatase 2C in stress recovery. Plant Sci. 2006;171:596–606.

    Article  CAS  Google Scholar 

  • Levitt J. Responses of plants to environmental stress. 2nd ed. New York: Academic; 1980. 697 pp.

    Google Scholar 

  • Li J, Yu K, Wei J, Ma Q, Wang B, Yu D. Gibberellin retards chlorophyll degradation during senescence of Paris polyphylla. Biol Plant. 2010;54:395–9.

    Article  CAS  Google Scholar 

  • Li G, Meng X, Wang R, Mao G, Han L, Liu Y, Zhang S. Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLoS Genet. 2012;8:1–14.

    Google Scholar 

  • Lin Z, Zhong S, Grierson D. Recent advances in ethylene research. J Exp Bot. 2009;60:3311–36.

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Wang Y, Xu J, Su T, Liu G, Ren D. Ethylene signalling is required for the acceleration of cell death induced by activation of AtMEK5 in Arabidopsis. Cell Res. 2008;18:422–32.

    Article  CAS  PubMed  Google Scholar 

  • Long SP, Naidu SL. Effects of oxidants at the biochemical, cell and physiological levels, with particular reference to ozone. In: Bell JNB, Treshow M, editors. Air pollution and plant life. 2nd ed. Chichester: Wiley; 2002. p. 69–88.

    Google Scholar 

  • Lorenzini G, Nali C, Pellegrini E. Summer heat waves, agriculture, forestry and related issues: an introduction (Editorial). Agrochimica. 2014a;LVIII(Special Issue):3–19.

    Google Scholar 

  • Lorenzini G, Pellegrini E, Campanella A, Nali C. It’s not just the heat and the drought: the role of ozone air pollution in the 2012 heat wave. Agrochimica. 2014b;LVIII(Special Issue):40–52.

    Google Scholar 

  • Ludwików A, Kierzek D, Gallois P, Zeef L, Sadowski J. Gene expression profiling of ozone-treated Arabidopsis abi1td insertional mutant: protein phosphatase 2C ABI1 modulates biosynthesis ratio of ABA and ethylene. Planta. 2009;230:1003–17.

    Article  PubMed  CAS  Google Scholar 

  • Ludwików A, Cieśla A, Kasprowicz-Maluśki, Mituła, Tajde M, Gałgański Ł, Piotr A Z, Kubiak, Małecka Arleta, PA, Szabat M, Górska A, Dąbrowski M, Ibragimow I, Sadowski J. Arabidopsis Protein Phosphatase 2C ABI1 interacts with Type I ACC Synthases and is involved in the regulation of ozone-induced ethylene biosynthesis. Mol Plant. 2015;7:960–76.

    Google Scholar 

  • Lyzenga WJ, Booth JK, Stone SL. The Arabidopsis RING-type E3 ligase XBAT32 mediates the proteasomal degradation of the ethylene biosynthetic enzyme, 1-aminocyclopropane-1-carboxylate synthase 7. Plant J. 2012;71:23–34.

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science. 2009;324:1064–8.

    CAS  PubMed  Google Scholar 

  • Manulis S, Haviv-Chesner A, Brandl MT, Lindow SE, Barash I. Differential involvement of indole-3-acetic acid biosynthetic pathways in pathogenicity and epiphytic fitness of Erwinia herbicola pv. gypsophilae. Mol Plant Microbe Interact. 1998;11:634–42.

    Article  CAS  PubMed  Google Scholar 

  • Meehl GA, Stocker TF, Collins WD, Friedlingstein P, Gaye AT, Gregory JM, Kitoh A, Knutti R, Murphy JM, Noda A, Raper SCB, Watterson IG, Weaver AJ, Zhao Z-C. Global climate projections. In: Climate change 2007: the physical basis. Contribution of working group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) 2007. Cambridge/New York: Cambridge University Press. p. 747–845

    Google Scholar 

  • Meng X, Xu J, He Y, Yang KY, Mordorski B, Liu Y, Zhang S. Phosphorylation of an ERF transcription factor by Arabidopsis MPK3/MPK6 regulates plant defense gene induction and fungal resistance. Plant Cell. 2013;25:1126–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Merewitz EB, Du H, Yu W, Liu Y, Gianfagna T, Huang B. Elevated cytokinin content in ipt transgenic creeping bentgrass promotes drought tolerance through regulating metabolite accumulation. J Exp Bot. 2012;63:1315–28.

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Blumwald E. The roles of ROS and ABA in systemic acquired acclimation. Plant Cell. 2015;27:64–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyazono K, Miyakawa T, Sawano Y, Kubota K, Kang HJ, Asano A, Miyauchi Y, Takahashi M, Zhi Y, Fujita Y, Yoshida T, Kodaira KS, Yamaguchi-Shinozaki K, Tanokura M. Structural basis of abscisic acid signaling. Nature. 2009;462:609–14.

    Article  CAS  PubMed  Google Scholar 

  • Moeder W, Barry CS, Tauriainen AA, Betz C, Tuomainen J, Utriainen M, Grierson D, Sandermann H, Langebartels C, Kangasjärvi J. Ethylene synthesis regulated by biphasic induction of 1-aminocyclopropane-1-carboxylic acid synthase and 1-aminocyclopropane-1-carboxylic acid oxidase genes is required for hydrogen peroxide accumulation and cell death in ozone-exposed tomato. Plant Physiol. 2002;130:1918–26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Møller IM, Jensen PE, Hansson A. Oxidative modifications to cellular components in plants. Annu Rev Plant Biol. 2007;58:459–81.

    Article  PubMed  CAS  Google Scholar 

  • Mudd JB. Biochemical basis for the toxicity of ozone. In: Yunus M, Iqbal M, editors. Plant response to air pollution. New York: Wiley; 1997. p. 267–84.

    Google Scholar 

  • Munemasa S, Muroyama D, Nagahashi H, Nakamura Y, Mori IC, Murata Y. Regulation of reactive oxygen species mediated abscisic acid signaling in guard cells and drought tolerance by glutathione. Front Plant Sci. 2013;4:472.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nakajima N, Matsuyama T, Tamaoki M, Saji H, Aono M, Kubo A, Kondo N. Effects of ozone exposure on the gene expression of ethylene biosynthetic enzymes in tomato leaves. Plant Physiol Biochem. 2001;39:993–8.

    Article  CAS  Google Scholar 

  • Nakashita H, Yasuda M, Nitta T, Asami T, Fujioka S, Arai Y, Sekimata K, Takausuto S, Yamaguchi I, Yoshida S. Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. Plant J. 2003;33:887–98.

    Article  CAS  PubMed  Google Scholar 

  • Negi J, Matsuda O, Nagasawa T, Oba Y, Takahashi H, Kawai-Yamada M, Iba K. CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature. 2008;452:483–6.

    Article  CAS  PubMed  Google Scholar 

  • Nickstadt A, Thomma BPHJ, Feussner I, Kangasjärvi J, Zeier J, Loeffler C, Scheel D, Berger S. The jasmonate-insensitive mutant jin1 shows increased resistance to biotrophic as well as necrotrophic pathogens. Mol Plant Pathol. 2004;5:425–34.

    Article  CAS  PubMed  Google Scholar 

  • Nishiyamaa R, WatanabeaY FY, Lea DT, Kojimaa M, Wernerc T, Vankovad R, Yamaguchi-Shinozaki K, Shinozaki K, Kakimotoe T, Sakakibaraa T, Schmülling T, Trana LP. Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell. 2011;6:2169–83.

    Article  CAS  Google Scholar 

  • Nunn AJ, Kozovits AR, Reiter IM, Heerdt C, Leuchner M, Lütz C, Liu X, Löw M, Winkler JB, Grams TEE, Häberle K-H, Werner H, Fabian P, Rennenberg H, Matyssek R. Comparison of ozone uptake and sensitivity between a phytotron study with young beech and a field experiment with adult beech (Fagus sylvatica). Environ Pollut. 2005;137:494–506.

    Article  CAS  PubMed  Google Scholar 

  • Ogawa D, Nakajima N, Sano T, Tamaoki M, Aono N, Kubo A, Kanna M, Ioki M, Kamada H, Saji H. Salicylic acid accumulation under O3 exposure is regulated by ethylene in tobacco plants. Plant Cell Physiol. 2005;46:1062–72.

    Article  CAS  PubMed  Google Scholar 

  • Ogawa D, Nakajima N, Tamaoki M, Aono M, Kubo A, Kamada H, Saji H. The isochorismate pathway is negatively regulated by salicylic acid signaling in O3-exposed Arabidopsis. Planta. 2007;226:1277–85.

    Article  CAS  PubMed  Google Scholar 

  • Okada K, Abe H, Arimura G. Jasmonates induce both defense responses and communication in monocotyledonous and dicotyledonous plants. Plant Cell Physiol. 2015;56:16–27.

    Article  PubMed  Google Scholar 

  • Örvar B-L, McPherson J, Ellis EB. Pre-activating wounding response in tobacco prior to high-level ozone exposure prevents necrotic injury. Plant J. 1997;11:203–12.

    Article  PubMed  Google Scholar 

  • Overmyer K, Tuomainen H, Kettunen R, Betz C, Langebartels C, Sandermann Jr H, Kangasjärvi J. The ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signalling pathways in regulating superoxide-dependent cell death. Plant Cell. 2000;12:1849–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Overmyer K, Brosché M, Pellinen R, Kuittinen T, Tuominen H, Ahlfors R, Keinänen M, Saarma M, Scheel D, Kangasjärvi J. Ozone-induced programmed cell death in the Arabidopsis radical-induced cell death1 mutant. Plant Physiol. 2005;137:1092–104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Overmyer K, Kollist H, Tuominen H. Complex phenotypic profiles leading to ozone sensitivity in Arabidopsis thaliana mutants. Plant Cell Environ. 2008;31:1237–49.

    Article  CAS  PubMed  Google Scholar 

  • Pandey S, Gupta K, Mukherjee A. Impact of cadmium and lead on Catharanthus roseus-A phytoremediation study. J Environ Biol. 2007;28:655–62.

    CAS  PubMed  Google Scholar 

  • Pasqualini S, Della Torre G, Ferranti F, Ederli L, Piccioni C, Reale L, Antonielli M. Salicylic acid modulates ozone-induced hypersensitive cell death in tobacco plants. Physiol Plant. 2002;115:204–12.

    Article  CAS  PubMed  Google Scholar 

  • Pauls KP, Thompson JE. Effects of cytokinins and antioxidants on the susceptibility of membranes to ozone damage. Plant Cell Physiol. 1982;23:821–32.

    CAS  Google Scholar 

  • Peleg Z, Blumwald E. Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol. 2011;14:290–5.

    Article  CAS  PubMed  Google Scholar 

  • Pellegrini E, Lorenzini G, Nali C. The 2003 European heat wave: which role for ozone? Some data from Tuscany, Central Italy. Water Air Soil Pollut. 2007;181:401–8.

    Article  CAS  Google Scholar 

  • Pellegrini E, Trivellini A, Campanella A, Francini A, Lorenzini G, Nali C, Vernieri P. Signaling molecules and cell death in Melissa officinalis plants exposed to ozone. Plant Cell Rep. 2013;32:1965–80.

    Article  CAS  PubMed  Google Scholar 

  • Perilli S, Moubayidin L, Sabatini S. The molecular basis of cytokinin function. Curr Opin Plant Biol. 2010;13:21–6.

    Article  CAS  PubMed  Google Scholar 

  • Pinto DM, Blande JD, Souza SR, Nerg A-M, Holopainen JK. Plant volatile organic compounds (VOCs) in ozone (O3) polluted atmosphere: the ecological effects. J Chem Ecol. 2010;36:22–34.

    Article  CAS  PubMed  Google Scholar 

  • Potters G, Pasternak TP, Guisez Y, Jansen MAK. Different stresses, similar morphogenic responses: integrating a plethora of pathways. Plant Cell Environ. 2009;32:158–69.

    Article  PubMed  Google Scholar 

  • Puckette M, Peal L, Steele J, Tang Y. Ozone responsive genes in Medicago truncatula: analysis by suppression subtraction hybridization. J Plant Physiol. 2009;166:1284–95.

    Article  CAS  PubMed  Google Scholar 

  • Qin F, Kodaira KS, Maruyama K, Mizoi J, Tran LSP, Fujita Y, Morimoto K, Shinozaki K, Yamaguchi-Shinozaki K. SPINDLY, a negative regulator of gibberellic acid signaling, is involved in the plant abiotic stress response. Plant Physiol. 2011;157:1900–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rao MV, Koch JR, Davis KR. Ozone: a tool for probing programmed cell death in plants. Plant Mol Biol. 2000;44:345–58.

    Article  CAS  PubMed  Google Scholar 

  • Rao MV, Lee H-I, Davis KR. 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. 2002;32:447–56.

    Article  CAS  PubMed  Google Scholar 

  • Rejeb KB, Abdelly C, Savouré A. How reactive oxygen species and proline face stress together. Plant Physiol Biochem. 2014;8:278–84.

    Article  CAS  Google Scholar 

  • Riefler M, Novak O, Strnad M, Schmülling T. Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell. 2006;18:40–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rivero RM, Gimeno J, Van Deynze A, Walia H, Blumwald E. Enhanced cytokinin synthesis in tobacco plants expressing P(SARK):IPT prevents the degradation of photosynthetic protein complexes during drought. Plant Cell Physiol. 2010;51:1929–41.

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues C, Vandenberghe LPD, de Oliveira J, Soccol CR. New perspectives of gibberellic acid production: a review. Crit Rev Biotechnol. 2011;32:263–73.

    Article  PubMed  CAS  Google Scholar 

  • Rohwer CL, Erwin JE. Horticultural applications of jasmonates: a review. J Hortic Sci Biotech. 2008;83:283–304.

    Article  CAS  Google Scholar 

  • Sandermann H. Ecotoxicology of ozone: bioactivation of extracellular ascorbate. Biochem Biophys Res Commun. 2008;366:271–4.

    Article  CAS  PubMed  Google Scholar 

  • Santino A, Taurino M, De Domenico S, Bonsegna S, Poltronieri P, Pastor V, Flors V. Jasmonate signaling in plant development and defense response to multiple (a)biotic stress. Plant Cell Rep. 2013;32:1085–98.

    Article  CAS  PubMed  Google Scholar 

  • Schlagnhaufer CD, Arteca RN, Pell EJ. Sequential expression of two 1-aminocyclopropane- 1-carboxylate synthase genes in response to biotic and abiotic stresses in potato (Solanum tuberosum L.) leaves. Plant Mol Biol. 1997;35:683–8.

    Article  CAS  PubMed  Google Scholar 

  • Schweighofer A, Kazanaviciute V, Scheikl E, Teige M, Doczi R, Hirt H, Schwanninger M, Kant M, Schuurink R, Mauch F. The PP2C-type phosphatase AP2C1, which negatively regulates MPK4 and MPK6, modulates innate immunity, jasmonic acid, and ethylene levels in Arabidopsis. Plant Cell. 2007;19:2213–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K. Gene networks involved in drought stress response and tolerance. J Exp Bot. 2007;58:221–7.

    Article  CAS  PubMed  Google Scholar 

  • Short EF, North KA, Roberts MR, Hetherington AM, Shirras AD, McAinsh MR. A stress-specific calcium signature regulating an ozone-responsive gene expression network in Arabidopsis. Plant J. 2012;71:948–61.

    Article  CAS  PubMed  Google Scholar 

  • Song Y, Miao Y, Song CP. Behind the scenes: the roles of reactive oxygen species in guard cells. New Phytol. 2014;201:1121–40.

    Article  CAS  PubMed  Google Scholar 

  • Stockwell WR, Kramm G, Scheel H-E, Mohnen VA, Seiler W. Ozone formation, destruction and exposure in Europe and the United States. In: Sandermann H, Wellburn AR, Heath RL, editors. Ecological Studies, Forest decline and ozone, vol. 127. Berlin/Heidelberg: Springer; 1997. p. 1–38.

    Google Scholar 

  • Szabados L, Savouré A. Proline: a multifunctional amino acid. Trends Plant Sci. 2010;15:89–97.

    Article  CAS  PubMed  Google Scholar 

  • Tamaoki M. The role of phytohormone signaling in ozone-induced cell death in plants. Plant Signal Behav. 2008;3:166–74.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tardieu F, Parent B, Simonneau T. Control of leaf growth by abscisic acid: hydraulic or non-hydraulic processes? Plant Cell Environ. 2010;33:636–47.

    Article  PubMed  Google Scholar 

  • The Royal Society. Ground-level ozone in the 21st century: future, trends, impact and policy implications: Royal Society Policy document 15–08. London. 2008. http://royalsociety.org/uploadedFiles/Royal_Society_Content/policy/publications/2008/7925.pdf

  • Tognetti VB, Mühlenbock P, Van Breusegem F. Stress homeostasis: the redox and auxin perspective. Plant Cell Environ. 2012;35:321–33.

    Article  CAS  PubMed  Google Scholar 

  • Tomlinson H, Rich S. Anti-senescent compounds reduce injury and steroid changes in ozonated leaves and their chloroplasts. Phytopathology. 1973;63:903–6.

    Article  CAS  Google Scholar 

  • Trivellini A, Ferrante A, Vernieri P, Serra G. Effects of abscisic acid on ethylene biosynthesis and perception in Hibiscus rosa-sinensis L. flower development. J Exp Bot. 2011;62:5437–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuchisaka A, Theologis A. Heterodimeric interactions among the 1-amino-cyclopropane-1-carboxylate synthase polypeptides encoded by the Arabidopsis gene family. PNAS. 2004;101:2275–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuchisaka A, Yu G, Jin H, Alonso JM, Ecker JR, Zhang X, Gao S, Theologis A. A combinatorial interplay among the 1-aminocyclopropane-1-carboxylate isoforms regulates ethylene biosynthesis in Arabidopsis thaliana. Genetics. 2009;183:979–1003.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuomainen J, Betz C, Kangasjärvi J, Ernst D, Yin ZH, Langebartels C, Sandermann Jr H. Ozone induction of ethylene emission in tomato plants: regulation by differential accumulation of transcripts for the biosynthetic enzymes. Plant J. 1997;12:1151–62.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Vahala J, Ruonala R, Keinänen M, Tuominen H, Kangasjärvi J. Ethylene insensitivity modulates ozone-induced cell death in birch. Plant Physiol. 2003;132:185–95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vahisalu T, Puzõrjova I, Brosché M, Valg E, Lepiku M, Moldau H, Pechter P, Wang YS, Lindgren O, Salojärvi LM, Kangasjärvi J, Kollist H. Ozone-triggered rapid stomatal response involves the production of reactive oxygen species, and is controlled by SLAC1 and OST1. Plant J. 2010;62:442–53.

    Article  CAS  PubMed  Google Scholar 

  • Vainonen JP, Kangasjärvi J. Plant signalling in acute ozone exposure. Plant Cell Environ. 2015;38:240–52.

    Article  CAS  PubMed  Google Scholar 

  • van Loon LC, Geraats BPJ, Linthorst HJM. Ethylene as a modulator of disease resistance in plants. Trends Plant Sci. 2006;11:184–91.

    Article  PubMed  CAS  Google Scholar 

  • Vandeputte O, Oden S, Mol A, Vereecke D, Goethals K, El Jaziri M, Prinsen E. Biosynthesis of auxin by the gram-positive phytopathogen Rhodococcus fascians is controlled by compounds specific to infected plant tissues. Appl Environ Microbiol. 2005;71:1169–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vaultier NV, Jolivet Y. Ozone sensing and early signaling in plants: an outline from the cloud. Environ Exp Bot. 2015;114:144–52.

    Article  CAS  Google Scholar 

  • Wang KL, Li H, Ecker JR. Ethylene biosynthesis and signaling networks. Plant Cell. 2002;14:131–51.

    Google Scholar 

  • Wang KL, Yoshida H, Lurin C, Ecker JR. Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature. 2004;428:945–50.

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Pajerowska-Mukhtar K, Culler AH, Dong X. Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr Biol. 2007a;17:1784–90.

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S. Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell. 2007b;19:63–73.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wildermuth MC, Dewdney J, Wu G, Ausubel FM. Isochorismate synthase is required to synthesize salicylic acid for plant defense. Nature. 2001;414:562–5.

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson S, Davies WJ. Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ. 2010;33:510–25.

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson S, Mills G, Illidge R, Davies WJ. How is ozone pollution reducing our food supply? J Exp Bot. 2011;1–10. doi:10.1093/jxb/err317.

    Google Scholar 

  • Wilkinson S, Mills G, Illidge R, Davies WJ. How is ozone pollution reducing our food supply? J Exp Bot. 2012;63:527–36.

    Article  CAS  PubMed  Google Scholar 

  • Winwood J, Pate AE, Price J, Hanke DE. Effects of long-term, free-air ozone fumigation on the cytokinin content of mature beech trees. Plant Biol. 2007;9:265–78.

    Article  CAS  PubMed  Google Scholar 

  • Woodward AW, Bartel B. Auxin: regulation, action, and interaction. Ann Bot. 2005;95:707–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wrzaczek M, Brosché M, Salojärvi J, Kangasjärvi S, Idänheimo N, Mersmann S, Robatzek S, Karpiński S, Karpińska B, Kangasjärvi J. Transcriptional regulation of the CRK/DUF26 group of Receptor-like protein kinases by ozone and plant hormones in Arabidopsis. Plant Biol. 2010;10:95–114.

    Google Scholar 

  • Xia X-J, Wang Y-J, Zhou Y-H, Tao Y, Mao WH, Shi K, Asami T, Chen ZX, Yu JQ. Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in Cucumber. Plant Physiol. 2009;15:801–14.

    Article  CAS  Google Scholar 

  • Xia X-J, Zhou Y-H, Shi K, Zhou J, Foyer CH, Yu JQ. Interplay between oxygen species and hormones in the control plant development and stress tolerance. J Exp Bot. 2015;66:2839–56.

    Article  CAS  PubMed  Google Scholar 

  • Yaeno T, Saito B, Katsuki T, Iba K. Ozone-induced expression of the Arabidopsis FAD7 gene requires salicylic acid, but not NPR1 and SID2. Plant Cell Physiol. 2006;47:355–62.

    Article  CAS  PubMed  Google Scholar 

  • Yasuda M, Ishikawa A, Jikumaru Y, Seki M, Umezawa T, Asami T, Maruyama-Nakashita A, Kudo T, Shinozaki K, Yoshida S, Nakashida H. Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. Plant Cell. 2008;20:1678–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoo S-D, Cho Y-H, Tena G, Xiong Y, Sheen J. Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature. 2008;451:789–95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida H, Wang KL, Chang CM, Mori K, Uchida E, Ecker JR. The ACC synthase TOE sequence is required for interaction with ETO1 family proteins and destabilization of target proteins. Plant Mol Biol. 2006;62:427–37.

    Article  CAS  PubMed  Google Scholar 

  • Zheng Y, Cheng D, Simmons M. Ozone pollution effects on gas exchange, growth and biomass yield of salinity-treated winter wheat cultivars. Sci Total Environ. 2014;499:18–26.

    Article  CAS  PubMed  Google Scholar 

  • Zhou C, Cai Z, Guo Y, Gan S. An Arabidopsis mitogen-activated protein kinase cascade, MKK9–MPK6, plays a role in leaf senescence. Plant Physiol. 2009;150:167–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Agriculture, Food and Environment, University of Pisa, via del Borghetto 80, 56124, Pisa, Italy

    Elisa Pellegrini, Lorenzo Cotrozzi, Paolo Vernieri & Cristina Nali

  2. Institute of Life Science, Scuola Superiore Sant’Anna, Pisa, 56124, Italy

    Alice Trivellini

Authors
  1. Elisa Pellegrini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alice Trivellini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lorenzo Cotrozzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paolo Vernieri
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cristina Nali
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cristina Nali .

Editor information

Editors and Affiliations

  1. Department of Horticulture, Zhejiang University, Hangzhou, China

    Golam Jalal Ahammed

  2. Department of Horticulture, Zhejiang University, Hangzhou, Zhejiang, China

    Jing-Quan Yu

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Pellegrini, E., Trivellini, A., Cotrozzi, L., Vernieri, P., Nali, C. (2016). Involvement of Phytohormones in Plant Responses to Ozone. In: Ahammed, G., Yu, JQ. (eds) Plant Hormones under Challenging Environmental Factors. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-7758-2_9

Download citation

Publish with us

Policies and ethics

Search

Navigation