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Tropospheric ozone as a fungal elicitor

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Abstract

Tropospheric ozone has been proven to trigger biochemical plant responses that are similar to the ones induced by an attack of fungal pathogens, i.e. it resembles fungal elicitors. This suggests that ozone can represent a valid tool for the study of stress responses and induction of resistance to pathogens. This review provides an overview of the implications of such a phenomenon for basic and applied research. After an introduction about the environmental implications of tropospheric ozone and plant responses to biotic stresses, the biochemistry of ozone stress is analysed, pointing out its similarities with plant responses to pathogens and its possible applications.

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Abbreviations

ACC:

1-aminocyclopropyl-1-carboxylic acid

AOX:

alternate oxidase

ATP:

adenosine triphosphate

GRAS:

generally considered as safe

HR:

hypersensitive response

NADH:

nicotinamide adenine dinucleotide

NADPH:

nicotinamide adenine dinucleotide phosphate

NO:

nitric oxide

NOS:

NO synthase

PR:

proteins, proteins related to pathogenesis

PS:

photosystem

ROS:

reactive oxygen species

SA:

salicylic acid

SAR:

systemically acquired resistance

SMV:

Soybean mosaic virus

US:

ultrasound

UV:

ultraviolet

References

  • Apel K and Hirt H 2004 Reactive oxygen species: metabolism, oxidative stress, and signal transduction; Annu. Rev. Plant Biol. 55 373–399

    CAS  PubMed  Google Scholar 

  • Baker C J and Orlandi E W 1995 Active oxygen in plant pathogenesis; Annu. Rev. Phytopathol. 33 299–321

    CAS  PubMed  Google Scholar 

  • Bilgin D D, Aldea M, O’Neill B F, Benitez M, Li M, Clough S J and DeLucia E H 2008 Elevated ozone alters soybean-virus interaction; Mol. Plant Mic. Interact. 21 1297–1308

    CAS  Google Scholar 

  • Bol J F, Linthorst H J M and Cornelissen B J C 1990 Plant pathogenesis-related proteins induced by virus infection; Annu. Rev. Phytopathol. 28 113–138

    CAS  Google Scholar 

  • Booker F and Miller J 1998 Phenylpropanoid metabolism and phenolic composition of soybean [Glycine max (L.) Merr.] leaves following exposure to ozone; J. Exp. Bot. 49 1191–1202

    CAS  Google Scholar 

  • Bowles D J 1990 Defense-related proteins in higher plants; Annu. Rev. Biochem. 59 873–907

    CAS  PubMed  Google Scholar 

  • Byvoet P, Balis J U, Shelley S A, Montgomery M R and Barber M J 1995 Detection of hydroxyl radicals upon interaction of ozone with aqueous media or extracellular surfactant: the role of trace iron; Arch. Biochem. Biophys. 319 464–469

    CAS  PubMed  Google Scholar 

  • Cabane M, Pireaux J C, Leger E, Weber E, Dizengremel P, Pollet B and Lapierre C 2004 Condensed lignins are synthesized in poplar leaves exposed to ozone; Plant Physiol. 134 586–594

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carter G A and Knapp A K 2001 Leaf optical properties in higher plants: linking spectral characteristics to stress and chlorophyll concentration; Am. J. Bot. 88 677–684

    CAS  PubMed  Google Scholar 

  • Castagna A, Diara C, Baldan B, Mensuali-Sodi A, Soldatini G F and Ranieri A 2005 Ozono: percezione del pericolo e reazioni precoci di difesa. Il caso del pioppo; Forest@ 1 98–106 (in Italian).

    Google Scholar 

  • Castillo F J and Heath R L 1990 Ca2+ transport in membrane vesicles from “pinto” bean leaves and its alteration after ozone exposure; Plant Physiol. 94 788–795

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chameides W L and Lodge J P 1992 Tropospheric ozone: formation and fate; in Surface level ozone exposures and their effects on vegetation (ed.) A S Lefohn (USA: Lewis Publishers) pp 1–30

    Google Scholar 

  • Chandra S, Heinstein P F and Low P S 1996 Activation of phospholipase A by plant defense elicitors; Plant Physiol. 110 979–986

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chiron H, Drouet A, Lieutier F, Payer H, Ernst D and Sandermann H Jr 2000 Gene induction of stilbene biosynthesis in Scots pine in response to ozone treatment, wounding, and fungal infection; Plant Physiol. 124 865–872

    CAS  PubMed  PubMed Central  Google Scholar 

  • Conklin P L and Last R L 1995 Differential accumulation of antioxidant mRNAs in Arabidopsis thaliana exposed to ozone; Plant Physiol. 109 203–212

    CAS  PubMed  PubMed Central  Google Scholar 

  • Conklin P L, Williams E H and Last R L 1996 Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant; Proc. Natl. Acad. Sci. USA 93 9970–9974

    CAS  PubMed  Google Scholar 

  • Cowan M M 1999 Plant products as antimicrobial agents; Clin. Microbiol. Rev. 12 564–582

    CAS  PubMed  PubMed Central  Google Scholar 

  • Crutzen P J 1973 A discussion of the chemistry of atmosphere and troposphere; Pure Appl. Geophys. 106–108 1385–1399

    Google Scholar 

  • Dangl J 1998 Innate immunity. Plants just say NO to pathogens; Nature (London) 394 525–526

    CAS  Google Scholar 

  • Dann M S and Pell E J 1989 Decline of activity and quantity of ribulose bisphosphate carboxylase/oxygenase and net photosynthesis in ozone-treated potato foliage; Plant Physiol. 91 427–432

    CAS  PubMed  PubMed Central  Google Scholar 

  • Darvill A G and Albersheim P 1984 Phytoalexins and their elicitors — a defense against microbial infection in plants; Annu. Rev. Plant Physiol. 35 243–275

    CAS  Google Scholar 

  • Datta S K and Muthukrishnan S (eds) 1999 Pathogenesis-related proteins in plants (Washington DC: CRC Press).

    Google Scholar 

  • Davis K R, Darvill A G and Albersheim P 1986 Several biotic and abiotic elicitors act synergistically in the induction of phytoalexin accumulation in soybean; Plant Mol. Biol. 6 23–32

    CAS  PubMed  Google Scholar 

  • De Moraes C M, Schultz J C, Mescher M C and Tumlinson J H 2004 Induced plant signaling and its implications for environmental sensing; J. Toxicol. Environ. Health A 67 819–834

    PubMed  Google Scholar 

  • Delledonne M, Xia Y, Dixon R A and Lamb C 1998 Nitric oxide functions as a signal in plant disease resistance; Nature (London) 394 585–588

    CAS  Google Scholar 

  • Dominy P J and Heath R L 1985 Inhibition of the K+-stimulated ATPase of the plasmalemma of pinto bean leaves by ozone; Plant Physiol. 77 43–45

    CAS  PubMed  PubMed Central  Google Scholar 

  • Durner J, Shah J and Klessig D F 1997 Salicylic acid and disease resistance in plants; Trends Plant Sci. 2 266–274

    Google Scholar 

  • Durner J, Wendehenne D and Klessig D F 1998 Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose; Proc. Natl. Acad. Sci. USA 95 10328–10333

    CAS  PubMed  Google Scholar 

  • Ebel J and Cosio E G 1994 Elicitors of plant defense responses; Int. Rev. Citol. 148 1–36

    CAS  Google Scholar 

  • Eckardt N A and Pell E J 1994 O3-induced degradation of Rubisco protein and loss of Rubisco mRNA in relation to leaf age in Solanum tuberosum L.; New Phytol. 127 741–748

    CAS  Google Scholar 

  • Eckey-Kaltenbach H, Ernst D, Heller W and Sandermann H Jr 1994 Biochemical plant responses to ozone. IV. Cross-induction of defensive pathways in parsley (Petroselinum crispum L.) plants; Plant Physiol. 104 67–74

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eckey-Kaltenbach H, Ernst D, Heller W, Sandermann H and Feucht W 1994 Cross-induction of defensive phenylpropanoid pathways in parsley plants by ozone; Acta Hortic. 381 192–198

    CAS  Google Scholar 

  • Eckey-Kaltenbach H, Kiefer E, Grosskopf E, Ernst D and Sandermann H Jr 1997 Differential transcript induction of parsley pathogenesis-related proteins and of a small heat shock protein by ozone and heat shock; Plant Mol. Biol. 33 343–350

    CAS  PubMed  Google Scholar 

  • Elstner E F, Osswald W and Youngman R J 1985 Basic mechanisms of pigment bleaching and loss of structural resistance in spruce (Picea abies) needles: advances in phytomedical diagnostics; Experientia 41 591–597

    CAS  Google Scholar 

  • Ernst D, Bodemann A, Schmelzer E, Langebartels C and Sandermann H Jr 1996 β-1,3-glucanase mRNA is locally, but not systemically induced in Nicotiana tabacum L. cv. Bel W3 after ozone fumigation; J. Plant Physiol. 148 215–221

    CAS  Google Scholar 

  • Ernst D, Schraudner M, Langebartels C and Sandermann H Jr 1992 Ozone-induced changes of mRNA levels of β-1,3-glucanase, chitinase and “pathogenesis-related” protein 1b in tobacco plants; Plant Mol. Biol. 20 673–682

    CAS  PubMed  Google Scholar 

  • Fiscus E L, Booker F L and Burkey K O 2005 Crop responses to ozone: uptake, modes of action, carbon assimilation and partitioning; Plant Cell Environ. 28 997–1011

    CAS  Google Scholar 

  • Flatø F, Hov Ø, Gerbig C and Oltmans S J 1996 Model studies of the meteorology and chemical composition of the troposphere over the North Atlantic during August 18–30, 1993: North Atlantic Regional Experiment (NARE); J Geophys. Res. 101 29317–29334

    Google Scholar 

  • Fuchs A, Davidse L C, de Waard M A and de Wit P J G M 1983 Contemplations and speculations on novel approaches in the control of fungal plant diseases; Pesticide Sci. 14 3272–3293

    Google Scholar 

  • Glick R E, Schlagnhaufer C D, Arteca R N and Pell E J 1995 Ozone-induced ethylene emission accelerates the loss of ribulose-1,5-bisphosphate carboxylase-oxygenase and nuclearencoded mRNAs in senescing potato leaves; Plant Physiol. 109 891–898

    CAS  PubMed  PubMed Central  Google Scholar 

  • Greenberg J T 1997 Programmed cell death in plant-pathogen interactions; Annu. Rev. Plant Physiol. Plant Mol. Biol. 48 525–545

    CAS  PubMed  Google Scholar 

  • Greenberg J T, Guo A, Klessig D F and Ausubel F M 1994 Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions; Cell 77 551–563

    CAS  PubMed  Google Scholar 

  • Grimes H D, Perkins K K and Boss W F 1983 Ozone degrades into hydroxyl radical under physiological conditions. A spin trapping study; Plant Physiol. 72 1016–1020

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grimmig B, Gonzalez-Perez M N, Leubner-Metzger G, Vögeli-Lange R, Meins F Jr, Hain R, Penuelas J, Heidenreich B, Langebartels C, Ernst D and Sandermann H Jr 2004 Ozoneinduced gene expression occurs via ethylene-dependent and -independent signalling. Plant Mol. Biol. 51 599–607

    Google Scholar 

  • Grossmann K 1996 A role for cyanide, derived from ethylene biosynthesis, in the development of stress symptoms; Physiol. Plant. 97 772–775

    CAS  Google Scholar 

  • Günthardt-Goerg M S, McQuattie C J, Scheidegger C, Rhiner C and Matyssek R 1997 Ozone-induced cytochemical and ultrastructural changes in leaf mesophyll cell walls; Can. J. Forest Res. 27 453–463

    Google Scholar 

  • Guidi L, Mori S, Degl’Innocenti E and Pecchia S 2007 Effects of ozone exposure or fungal pathogen on white lupin leaves as determined by imaging of chlorophyll a fluorescence; Plant Physiol. Biochem. 45 851–857

    CAS  PubMed  Google Scholar 

  • Guidi L, Nali C, Lorenzini G, Filippia F and Soldatini G F 2001 Effect of chronic ozone fumigation on the photosynthetic process of poplar clones showing different sensitivity; Environ. Pollut. 113 245–254

    CAS  PubMed  Google Scholar 

  • Guo H and Ecker J R 2004 The ethylene signaling pathway: new insights; Curr. Opin. Plant Biol. 7 40–49

    CAS  Google Scholar 

  • Hahn M G 1996 Microbial elicitors and their receptors in plants; Ann. Rev. Phytopathol. 34 387–412

    CAS  Google Scholar 

  • Hammerschmidt R 1999 Phytoalexins: what have we learned after 60 years?; Ann. Rev. Phytopathol. 37 285–306

    CAS  Google Scholar 

  • Heath R L 1987a Biochemical mechanisms of pollutant stress; in Assessment of crop loss from air pollutants (eds) W W Heck, O C Taylor and D T Tingey (London: Elsevier Science) pp 259–286

    Google Scholar 

  • Heath R L 1987b The biochemistry of ozone attack on the plasma membrane of plant cells; Recent Adv. Phytochem. 21 29–54

    CAS  Google Scholar 

  • Heath R L 1994 Possible mechanisms for the inhibition of photosynthesis by ozone; Photosynth. Res. 39 439–451

    CAS  PubMed  Google Scholar 

  • Heath R L 2000 Hypersensitive response-related death; Plant Mol. Biol. 44 321–334

    CAS  PubMed  Google Scholar 

  • Heath R L and Taylor G E 1997 Physiological processes and plant responses to ozone exposure; in Forest decline and ozone: a comparison of controlled chamber and field experiments (eds) H Sandermann, A R Wellburn and R L Heath (Berlin: Springer) pp 317–368

    Google Scholar 

  • Hewitt C N, Monson R K and Fall R 1990 Isoprene emissions from the grass Arundo donax L. are not linked to photorespiration; Plant Sci. 66 139–144

    CAS  Google Scholar 

  • Hough A M and Derwent R G 1990 Changes in the global concentration of tropospheric ozone due to human activities; Nature (London) 344 645–648

    CAS  Google Scholar 

  • Inclán R, Alonso R, Pujadas M, Teres J and Gimeno B S 1998 Ozone and drought stress: interactive effects on gas exchange in Aleppo pine (Pinus halepensis Mill); Chemosphere 36 685–690

    Google Scholar 

  • Ishida T 2005 Biotransformation of terpenoids by mammals, microorganisms, and plant-cultured cells; Chem. Biodiv. 2 569–590

    CAS  Google Scholar 

  • Izuta T 2006 Ozone threat to Japan’s forest. Tropospheric ozone, a growing threat. Acid Deposition and Oxidant Research Center. Available at: www.adorc.gr.jp/ozone/ozone1.pdf

  • Kärenlampi S O, Airaksinen K, Miettinen A T E, Kokko H I, Holopainen J K, Karenlampi L V and Karjalainen R O 1994 Pathogenesis-related proteins in ozone-exposed Norway spruce (Picea abies L. (Karst)); New Phytol. 126 81–89

    Google Scholar 

  • Kangasjärvi J, Talvinen J, Utriainen M and Karjalainen R 1994 Plant defense systems induced by ozone; Plant Cell Environ. 17 783–794

    Google Scholar 

  • Karaivazoglou N A, Papakosta D K, Sfaciotakis E M and Koutroubas S D 2004 Ethylene biosynthesis, ripening and senescence behavior of tobacco (Nicotiana tabacum L.) leaves; in New directions for a diverse planet: Proceedings of the 4th International Crop Science Congress, Brisbane, Australia, 26 Sep–1 Oct 2004

  • Keen N T and Taylor O C 1975 Ozone injury in soybeans. Isoflavonoid accumulation is related to necrosis; Plant Physiol. 55 731–733

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kivimänpää M, Selldénb G and Sutinen S 2005 Ozone-induced changes in the chloroplast structure of conifer needles, and their use in ozone diagnostics. Environ. Pollut. 137 466–475

    Google Scholar 

  • Kombrink E and Somssich I E 1995 Defense responses of plants to pathogens; Adv. Bot. Res. 21 1–34

    CAS  Google Scholar 

  • Kopper B J and Lindroth R L 2003 Responses of trembling aspen (Populus tremuloides) phytochemistry and aspen blotch leafminer (Phyllonorycter tremuloidiella) performance to elevated levels of atmospheric CO2 and O3; Agric. Forest Entomol. 5 17–26

    Google Scholar 

  • Koricheva J, Larsson S, Haukioja E and Keinanen M 1998 Regulation of woody plant secondary metabolism by resource availability: hypothesis testing by means of meta-analysis; Oikos 83 212–226

    CAS  Google Scholar 

  • Krapp A, Hofmann B, Schäfer C and Stitt M 1993 Regulation of the expression of rbcS and other photosynthetic genes by carbohydrates: a mechanism for the ’sink regulation’ of photosynthesis; Plant J. 3 817–828

    CAS  Google Scholar 

  • Kraus T E, McKersie B D and Fletcher R A 1995 Paclobutrazol-induced tolerance of wheat leaves to paraquat may involve incrased antioxidant enzyme activity; J. Plant Physiol. 145 570–576

    CAS  Google Scholar 

  • Kunz W, Schurter R and Maetzke T 1997 The chemistry of benzothiadiazole plant activators; Pest. Sci. 50 275–282

    CAS  Google Scholar 

  • Lamb C and Dixon R A 1997 The oxidative burst in plant disease resistance; Annu. Rev. Plant Physiol. Plant Mol. Biol. 48 251–275

    CAS  PubMed  Google Scholar 

  • Lange B M, Lapierre C and Sandermann H Jr 1995 Elicitor-induced spruce stress lignin. Structural similarity to early developmental lignins; Plant Physiol. 108 1277–1287

    CAS  PubMed  PubMed Central  Google Scholar 

  • Langebartels C, Heller W, Fuhrer G, Lippert M, Simons S and Sandermann H 1998 Memory effects in the action of ozone on conifers; Ecotoxicol. Environ. Saf. 41 62–72

    CAS  PubMed  Google Scholar 

  • Langebartels C, Wohlgemuth H, Kschieschan S, Grun S and Sandermann H Jr 2002 Oxidative burst and cell death in ozoneexposed plants; Plant Physiol. Biochem. 40 567–575

    CAS  Google Scholar 

  • Liao H, Chen W and Seinfeld J 2006 Role of climate change in predictions of future tropospheric ozone and aerosols; American Geophysical Union, Fall Meeting 2006, Abstract #A42B-06.

  • Lim P O, Woo H R and Nam H G 2003 Molecular genetics of leaf senescence in Arabidopsis; Trends Plant Sci. 8 272–278

    CAS  PubMed  Google Scholar 

  • Ljubešić N and Britvec M 2006 Tropospheric ozone-induced structural changes in leaf mesophyll cell walls in grapevine plants; Biologia 61 85–90

    Google Scholar 

  • Loreto F and Velikova V 2001 Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes; Plant Physiol. 127 1781–1787

    CAS  PubMed  PubMed Central  Google Scholar 

  • Luwe M W F, Takahama U and Heber U 1993 Role of ascorbate in detoxifying ozone in the apoplast of spinach (Spinacia oleracea L.) leaves; Plant Physiol. 101 969–976

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mauch-Mani B and Métraux J P 1998 Salicylic acid and systemic acquired resistance to pathogen attack; Ann. Bot. 82 535–540

    CAS  Google Scholar 

  • Métrauxs J P 2001 Systemic acquired resistance and salicylic acid: current state of knowledge; Eur. J. Plant Pathol. 107 13–18

    Google Scholar 

  • Mehdy M C, Sharma Y K, Sathasivan K and Bays N W 1996 The role of activated oxygen species in plant disease resistance; Physiol. Plant. 98 365–374

    CAS  Google Scholar 

  • Mehlhorn H, Tabner B J and Wellburn A R 1990 Electron spin resonance evidence for the formation of free radicals in plants exposed to ozone; Physiol. Plant. 79 377–383

    CAS  Google Scholar 

  • Mehlhorn H and Wellburn A R 1987 Stress ethylene formation determines plant sensitivity to ozone; Nature (London) 327 417–418

    CAS  Google Scholar 

  • Mert-Türk F 2002 Phytoalexins: defence or just a response to stress?; J. Cell Mol. Biol. 1 1–6

    Google Scholar 

  • Miller J D, Arteca R N and Pell E J 1999 Senescence-associated gene expression during ozone-induced leaf senescence in Arabidopsis; Plant Physiol. 120 1015–1023

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M and Van Breusegem F 2004 Reactive oxygen gene network in plants; Trends Plant Sci. 9 490–498

    CAS  PubMed  Google Scholar 

  • Møller I M 2001 Plant mitochondria and oxidative stress: electron transport, NADPH turnover and metabolism of reactive oxygen species; Annu. Rev. Plant Physiol. Plant Mol. Biol. 52 561–591

    PubMed  Google Scholar 

  • Moeder W, Barry C S, Tauriainen A A, Betz C, Tuomainen J, Utriainen M, Grierson D, Sandermann H, Langebartels C and Kangasjärvi J 2002 Ethylene synthesis regulated by bi-phasic 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. 130 1918–1926

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mano J, Ohno C, Domae Y and Asada K 2001 Chloroplastic ascorbate peroxidase is the primary target of methylviologen-induced photooxidative stress in spinach leaves: its relevance to monodehydroascorbate radical detected with in vivo ESR; Biochim. Biophys. Acta 1504 275–287

    CAS  PubMed  Google Scholar 

  • Montesano M, Brader G and Palva E T 2003 Pathogen derived elicitors: searching for receptors in plants; Mol. Plant Pathol. 4 73–79

    CAS  PubMed  Google Scholar 

  • Mur L A J, Naylor G, Warner S A J, Sugars J M, White R F and Draper J 1996 Salicylic acid potentiates defence gene expression in tissue exhibiting acquired resistance to pathogen attack; Plant J. 9 559–571

    CAS  Google Scholar 

  • Nadas A, Olmo M and Garcìa J M 2006 Growth of Botrytis cinerea and strawberry quality in ozone-enriched atmospheres; J. Food Sci. 68 1798–1802

    Google Scholar 

  • Neufeld H, Chappelka A, Somers G, Burkey K, Davison A and Finkelstein P 2006 Visible foliar injury caused by ozone alters the relationship between SPAD meter readings and chlorophyll concentrations in cutleaf coneflower; Photosynth. Res. 87 281–286

    CAS  PubMed  Google Scholar 

  • Noormets A, Podila G K and Karnosky D F 2000 Rapid response of antioxidant enzymes to O3-induced oxidative stress in Populus tremuloides clones varying in O3 tolerance; Forest Genet. 7 335–338

    Google Scholar 

  • Örvar B L, McPherson J and Ellis B E 1997 Pre-activating wounding response in tobacco prior to high-level ozone exposure prevents necrotic injury; Plant J. 11 203–212

    PubMed  Google Scholar 

  • Ogawa D, Nakajima N, Sano T, Tamaoki M, Aono M, Kubo A, Kanna M, Ioki M, Kamada H and Saji H 2005 Salicylic acid accumulation under O3 exposure is regulated by ethylene in tobacco plants; Plant Cell Physiol. 46 1062–1072

    CAS  PubMed  Google Scholar 

  • Oksanen E, Häikiö E, Sober J and Karnosky D F 2004 Ozone-induced H2O2 accumulation in field-grown aspen and birch is linked to foliar ultrastructure and peroxisomal activity; New Phytol. 161 791–799

    CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Overmyer K, Tuominen H, Kettunen R, Betz C, Langebartels C, Sandermann H Jr and Kangasjärvi 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pääkkönen E, Seppänen S, Holopainen T, Kokko H, Kärenlampi S, Kärenlampi L and Kangasjärvi J 1998 Induction of genes for the stress proteins PR-10 and PAL in relation to growth, visible injuries and stomatal conductance in birch (Betula pendula) clones exposed to ozone and/or drought; New Phytol. 138 295–305

    Google Scholar 

  • Płazek A, Hura K, Rapacz M and Zur I 2001 The influence of ozone fumigation on metabolic efficiency and plant resistance to fungal pathogens; J. Appl. Bot. 75 8–13

    Google Scholar 

  • Pandey S, Ranade S A, Nagar P K and Kumar N 2000 Role of polyamines and ethylene as modulators of plant senescence; J. Biosci. 25 291–299

    CAS  PubMed  Google Scholar 

  • Paolacci A R, D’ovidio R, Marabottini R, Nali C, Lorenzini G, Abenavoli M R and Badiani M 2001 Ozone induces a differential accumulation of phenyalanine ammonia-lyase, chalcone synthase and chalcone isomerase RNA transcripts in sensitive and resistant bean cultivars; Aust. J. Plant Physiol. 28 425–428

    CAS  Google Scholar 

  • Pasqualini S, Antonielli M, Ederli L, Piccioni C and Loreto F 2002a Ozone uptake and its effect on photosynthetic parameters of two tobacco cultivars with contrasting ozone sensitivity; Plant Physiol. Biochem. 40 599–603

    CAS  Google Scholar 

  • Pasqualini S, Della Torre G, Ferranti F, Ederli L, Piccioni C, Reale L and Antonielli M 2002b Salicylic acid modulates ozone-induced hypersensitive cell death in tobacco plants; Physiol. Plant. 115 204–212

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Pedras M S C, Okanga F I, Zaharia I L and Khan AQ 2000 Phytoalexins from crucifers: synthesis, biosynthesis, and biotransformation; Phytochemistry 53 161–176

    CAS  PubMed  Google Scholar 

  • Pell E J and Dann M S 1991 Multiple stress-induced foliar senescence and implications for whole-plant longevity; in Response of plants to multiple stresses (eds) H A Mooney, W E Winner and E J Pell (San Diego, CA: Academic Press) pp 189–204

    Google Scholar 

  • Pell E J, Eckardt N and Enyedi A J 1992 Timing of ozone stress and resulting status of ribulose bisphosphate carboxylase/oxygenase and associated net photosynthesis; New Phytol. 120 397–405

    CAS  Google Scholar 

  • Pell E J, Landry L G, Eckardt N A and Glick R E 1994 Air pollution and RubisCO: effects and implications; in Plant responses to the gaseous environment (eds) R G Alscher and A R Wellburn (London: Chapman and Hall) pp 239–254

    Google Scholar 

  • Pell E J, Schlagnhaufer C D and Arteca R N 1997 Ozone-induced oxidative stress: mechanisms of action and reaction; Physiol. Plant. 100 264–273

    CAS  Google Scholar 

  • Plessl M, Elstner E F, Rennenberg H, Habermeyer J and Heiser I 2007 Influence of elevated CO2 and ozone concentrations on late blight resistance and growth of potato plants; Environ. Exp. Bot. 60 447–457

    CAS  Google Scholar 

  • Pontier D, Balague C and Roby D 1998 The hypersensitive response. A programmed cell death associated with plant resistance; C. R. Acad. Sci. III 321 721–734

    CAS  PubMed  Google Scholar 

  • Pryor W A and Church D F 1991 Aldehydes, hydrogen peroxide, and organic radicals as mediators of ozone toxicity; Free Radic. Biol. Med. 11 41–46

    CAS  PubMed  Google Scholar 

  • Puckette M C, Weng H and Mahalingam R 2007 Physiological and biochemical responses to acute ozone-induced oxidative stress in Medicago truncatula; Plant Physiol. Biochem. 45 70–79

    CAS  PubMed  Google Scholar 

  • Ranieri A, D’Urso G, Nali C, Lorenzini G and Soldatini G F 1996 Ozone stimulates the apoplastic antioxidant systems in pumpkin leaves; Physiol. Plant. 97 381–387

    CAS  Google Scholar 

  • Ranieri A, Giuntini D, Ferraro F, Nali C, Baldan B, Lorenzinib G and Soldatini G F 2001 Chronic ozone fumigation induces alterations in thylakoid functionality and composition in two poplar clones; Plant Physiol. Biochem. 39 999–1008

    CAS  Google Scholar 

  • Rao M V, Lee H I and Davis K R 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

    CAS  PubMed  Google Scholar 

  • Reid M S 1989 The role of ethylene in flower senescence; Acta Hortic. 261 157–169

    Google Scholar 

  • Repka V, Fischerová I and Šilhárová K 2004 Methyl jasmonate is aov potent elicitor of multiple defense responses in grapevine leaves and cell-suspension cultures; Biol. Plant. 48 273–283

    CAS  Google Scholar 

  • Riehl Koch J, Scherzer A J, Eshita S M and Davis K R 1998 Ozone sensitivity in hybrid poplar is correlated with a lack of defensegene activation; Plant Physiol. 118 1243–1252

    CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson J M and Britz S J 2001 Ascorbate-dehydroascorbate level and redox status in leaflets of field-grown soybeans exposed to elevated ozone; Int. J. Plant Sci. 162 119–125

    CAS  Google Scholar 

  • Ryals J A, Neuenschwander U H, Willits M G, Molina A, Steiner H Y and Hunt M D 1996 Systemic acquired resistance; Plant Cell 8 1809–1819

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sandermann H 1996 Ozone and plant health; Annu. Rev. Phytopathol. 34 347–366

    CAS  PubMed  Google Scholar 

  • Sandermann H 2000 Ozone/biotic disease interactions: molecular biomarkers as a new experimental tool; Environ. Pollut. 108 327–332

    CAS  PubMed  Google Scholar 

  • Sandermann H 2004 Molecular ecotoxicology of plants; Trends Plant Sci. 9 406–413

    CAS  PubMed  Google Scholar 

  • Sandermann H, Ernst D, Heler W and Langebartels C 1998 Ozone: an abiotic elicitor of plant defence reactions; Trends Plant Sci. 3 47–50

    Google Scholar 

  • Sarig P, Zahvi T, Zutkhi Y, Yannai S, Lisker N and Ben-Arie R 1996 Ozone for control of post-harvest decay of table grapes caused by Rhizopus stolonifer; Physiol. Mol. Plant Pathol. 48 403–415

    CAS  Google Scholar 

  • Schlagnhaufer C D, Arteca R N and Pell E J 1998 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. 35 683–688

    Google Scholar 

  • Schmid J and Amrhein N 1995 Molecular organization of the shikimate pathway in higher plants; Phytochemistry 39 737–749

    CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Schubert R, Fischer R, Hain R, Schreier P H, Bahnweg G, Ernst D and Sandermann H Jr 1997 An ozone-responsive region of the grapevine resveratrol synthase promoter differs from the basal pathogen-responsive sequence; Plant Mol. Biol. 34 417–426

    CAS  PubMed  Google Scholar 

  • Setyadjit D, Joyce C, Irving D E and Simons D H 2004 Development and senescence of grevillea “sylvia” inflorescences, flowers and flower parts; Plant Growth Regul. 44 133–146

    CAS  Google Scholar 

  • Sharma Y K and Davis K R 1994 Ozone-induced expression of stress-related genes in Arabidopsis thaliana; Plant Physiol. 105 1089–1096

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma Y K, Léon J, Raskin I and Davis K R 1996 Ozone-induced responses in Arabidopsis thaliana: the role of salicylic acid in the accumulation of defense related transcripts and induced resistance; Proc. Natl. Acad. Sci. USA 93 5099–5104

    CAS  PubMed  Google Scholar 

  • Sinn J P, Schlagnhaufer C D, Arteca R N and Pell E J 2004 Ozone-induced ethylene and foliar injury responses are altered in 1-aminocyclopropane-1-carboxylate synthase antisense potato plants; New Phytol. 164 267–277

    CAS  Google Scholar 

  • Sohal R S and Weindruch S 1996 Oxidative stress, caloric restriction and ageing; Science 273 59–63

    CAS  PubMed  PubMed Central  Google Scholar 

  • Soldatini G F, Degl’Innocenti E, Guidi L and Genovesi S 2005 Photosynthetic process and activities of enzymes involved in the phenylpropanoid pathway in resistant and sensitive genotypes of Lycopersicon esculentum L. exposed to ozone; Plant Sci. 168 153–160

    Google Scholar 

  • Soylu S, Bennett M H and Mansfield J W 2002 Induction of phytoalexin accumulation in broad bean (Vicia faba L.) cotyledons following treatments with biotic and abiotic elicitors; Turk. J. Agric. For. 26 343–348

    Google Scholar 

  • Stockwell W R, Kirchner F, Kuhn M and Seefeld S 1997 A new mechanism for regional atmospheric chemistry modeling; J. Geophys. Res. 102(D22) 25847–25879

    CAS  Google Scholar 

  • Sudhakar N, Nagendra-Prasad D, Mohan N and Murugesan K 2006 Induction of systemic resistance in Lycopersicon esculentum cv. PKM1 (tomato) against Cucumber mosaic virus by using ozone; J. Virol. Methods 139 71–77

    PubMed  Google Scholar 

  • Takamura H and Gardner H W 1996 Oxygenation of (3Z)-alkenal to (2E)-4-hydroxy-2-alkenal in soybean seed (Glycine max L.); Biochim. Biophys. Acta 1303 83–91

    PubMed  Google Scholar 

  • Takashi Y, Bunnai S, Tsutomu K and Koh I 2006 Ozone-induced expression of the Arabidopsis FAD7 gene requires salicylic acid, but not NPR1 and SID2; Plant Cell Physiol. 47 355–362

    Google Scholar 

  • Taylor N L, Day D A and Millar A H 2002 Environmental stress causes oxidative damage to plant mitochondria leading to inhibition of glycine decarboxilase; J. Biol. Chem. 277 42663–42668

    CAS  PubMed  Google Scholar 

  • Thalmair M, Bauw G, Thiel S, Döhring T, Langebartels C and Sandermann H Jr 1996 Ozone and ultraviolet B effects on the defense-related proteins β-1,3-glucanase and chitinase in tobacco; J. Plant Physiol. 148 222–228

    CAS  Google Scholar 

  • Tingey D T, Standley C and Field R W 1976 Stress ethylene evolution: a measure of ozone effects on plants; Atmos. Environ. 10 969–974

    CAS  PubMed  Google Scholar 

  • Tuomainen J, Betz C, Kangasjärvvi J, Ernst D, Yin Z H, Langebartels C and Sandermann H Jr 1997 Ozone induction of ethylene emission in tomato plants: regulation by differential transcript accumulation for the biosynthetic enzymes; Plant J. 12 1151–1162

    CAS  Google Scholar 

  • US Food and Drug Administration 1997 Substances generally recognized as safe, proposed rule; Fed. Regist. 62 18937–18964

    Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Van Buuren M L, Guidi L, Fornalè S, Ghetti F, Franceschetti M, Soldatini G F and Bagni N 2002 Ozone-response mechanisms in tobacco: implications of polyamine metabolism; New Phytol. 156 389–398

    Google Scholar 

  • Van Hove L W A, Bossen M E, San Gabino B G and Sgreva C 2001 The ability of apoplastic ascorbate to protect poplar leaves against ambient ozone concentrations: a quantitative approach; Environ. Pollut. 114 371–382

    PubMed  Google Scholar 

  • Van Loon L C, Rep M and Pieterse C M J 2006 Significance of inducible defense-related proteins in infected plants; Ann. Rev. Phytopathol. 44 135–162

    Google Scholar 

  • Vernooij B, Friedrich L, Ahl Goy P, Staub T, Kessmann H and Ryals J 1995 2,6-Dichloroisonicotinic acid-induced resistance to pathogens without the accumulation of salicylic acid; Mol. Plant Microbe Interact. 8 228–234

    CAS  Google Scholar 

  • Watanabe N and Lam E 2006 The hypersensitive response in plant disease resistance; in Multigenic and induced systemic resistance in plants (eds) S Tuzun and E Bent (US: Springer) pp 83–111

    Google Scholar 

  • Wellburn F A M and Wellburn A R 1996 Variable patterns of antioxidant protection but similar ethene emission differences in several ozone-sensitive and ozone-tolerant plant selections; Plant Cell Environ. 19 754–760

    CAS  Google Scholar 

  • Willekens H, Van Camp W, Van Montagu M, Inze D, Langebartels C and Sandermann H Jr 1994 Ozone, sulphur dioxide, and ultraviolet B have similar effects on mRNA accumulation of antioxidant genes in Nicotiana plumbaginifolia (L.); Plant Physiol. 106 1007–1014

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wohlgemuth H, Mittelstrass K, Kschieschan S, Bender J, Weigel H J, Overmyer K, Kangasjärvi J, Langebartels C and Sandermann H Jr 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

    CAS  Google Scholar 

  • Woltering E J, de Jong A, Hoeberichts FA, Iakimova E and Kapchina V 2005 Plant programmed cell death, ethylene and flower senescenc;. Acta Hortic. (ISHS) 669 159–170

    CAS  Google Scholar 

  • Wu J and Lin L 2002 Elicitor-like effects of low-energy ultrasound on plant (Panax ginseng) cells: induction of plant defense responses and secondary metabolite production; Appl. Microbiol. Biotechnol. 59 51–57

    CAS  PubMed  Google Scholar 

  • Yalpani N, Enyedi A J, León J and Raskin I 1994 Ultraviolet light and ozone stimulate accumulation of salicylic acid, pathogenesis-related proteins and virus resistance in tobacco; Planta 193 372–376

    CAS  Google Scholar 

  • Yang T F, Gonzalez-Carranza Z H, Maunders M J and Roberts J A 2008 Ethylene and the regulation of senescence processes in transgenic Nicotiana sylvestris plants; Ann. Bot. 101 301–310

    CAS  PubMed  Google Scholar 

  • Yin Z H, Langebartels C and Sandermann H Jr 1994 Specific induction of ethylene biosynthesis in tobacco plants by the air pollutant, ozone; Proc. R. Soc. Edinburgh Sect. B 102 127–130

    Google Scholar 

  • Zinser C, Ernst D and Sandermann H Jr 1998 Induction of stilbene synthase and cinnamyl alcohol dehydrogenase mRNAs in Scots pine (Pinus sylvestris L.) seedlings; Planta 204 169–176

    CAS  Google Scholar 

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  1. Department of Crop Biology, Section of Plant Physiology, University of Pisa, Pisa, Italy

    Paolo Zuccarini

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Zuccarini, P. Tropospheric ozone as a fungal elicitor. J Biosci 34, 125–138 (2009). https://doi.org/10.1007/s12038-009-0014-6

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