Skip to main content
SpringerLink
Log in
SpringerLink
Log in

The Interplay Between Salicylic Acid and Reactive Oxygen Species During Cell Death in Plants

  • Chapter
Salicylic Acid: A Plant Hormone

Abstract

There is increasing interest in the interactive role between salicylic acid (SA), reactive oxygen species (ROS) and other plant signalling molecules in regulating cell death in plants. Initial evidence suggested that SA was a potent inhibitor of heme-containing enzymes such as catalase and ascorbate peroxidase, thus capable of stimulating ROS accumulation during various biotic and abiotic stress conditions. However, others suggested that the mode of action of SA may in fact be related to its ability to prime the defense response, by increasing the levels of various defense compounds. SA was also proposed as both a potent inducer of the NADPH-oxidase and an inhibitor of the alternative oxidase, thus capable of indirect regulation of the redox status of plant cells. This role in regulating the redox status has been linked to the programmed cell death (PCD) typically observed during the hypersensitive response (HR) but also during development (leaf laces, tracheary elements, root cap, germinationl) and some abiotic stress responses (salt and heavy metal stress, anoxia). Today, an interplay between SA, ROS and other signalling molecules is proposed in the regulation of PCD in plants. The present chapter reviews the evidence that has accumulated on the interactive nature of the relationship between ROS and SA and addresses this love-hate relationship in view of cell death in plants.

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 189.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
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

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Abramovitch, R., and Martin, G., 2004. Strategies used by bacterial pathogens to suppress plant defenses. Curr. Opin. Plant Biol.., 7: 1-9.

    Article  CAS  Google Scholar 

  • Alvarez, M., Pennell, R., Meijer, P., Ishikawa, A., Dixon, R., and Lamb, C., 1998. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell., 92: 773-784.

    Article  PubMed  CAS  Google Scholar 

  • Antoniw, J., and White, R., 1980. The effects of aspirin on polyarymic acid on soluble leaf proteins and resistance to virus infection in five cultivars of tobacco. Phytopath Z., 98: 331-341.

    CAS  Google Scholar 

  • Baier, M., Kandlbinder, A., Golldack, D., and Dietz, K.-J., 2005. Oxidative stress and ozone: perception, signalling and response. Plant Cell Env., 28: 1012-1020.

    Article  CAS  Google Scholar 

  • Balk, J., Leaver, C., and McCabe, P., 1999. Translocation of cytochrome c from the mitochondria to the cytosol occurs during heat-induced programmed cell death in cucumber plants. Febs Lett., 463: 141-154.

    Article  Google Scholar 

  • Beligni, M., and Lamattina, L., 1999. Nitric oxide counteracts cytoxic processes mediated by active oxygen species in plant tissues. Planta, 208: 337-344.

    Article  CAS  Google Scholar 

  • Bethke, P., and Jones, R., 2001. Cell death of barley aleurone proropasts is mediated by reactive oxygen species. Plant J., 25: 19-29.

    Article  PubMed  CAS  Google Scholar 

  • Bethke, P., Lonsdale, J., Fath, A., and Jones, R., 1999. Hormonally regulated programmed cell death in barley aleurone cells. Plant Cell, 11: 1033-1045.

    Article  CAS  PubMed  Google Scholar 

  • Bhatia, M., 2004. Apoptosis versus necrosis in acute pancreatitis. Am. J. Physiol., 286: G189-G196.

    Article  CAS  Google Scholar 

  • Bi, Y., Kenton, P., Mur, L., Darby, R., and Draper, J., 1995. Hydrogen peroxide does not function downstream of salicylic acid in the induction of PR protein expression. Plant J., 8: 235-245.

    Article  PubMed  CAS  Google Scholar 

  • Bidle, K., and Falhowski, P., 2004. Cell death in planktonic photosynthetic microorganisms. Nature Rev., 2: 643-655.

    Article  CAS  Google Scholar 

  • Böhm, I., and Schild, H., 2003. Apoptosis: The complex scenario for a silent cell death. Mol. Imag. Biol., 5: 2-14.

    Article  Google Scholar 

  • Bolwell, G., 1999. Role of active oxygen species and NO in plant defense responses. Curr. Opin. Plant Biol., 2: 287-294.

    Article  PubMed  CAS  Google Scholar 

  • Borsani, O., Valpuesta, V., and Botella, M., 2001. Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol., 126: 1024-1030.

    Article  PubMed  CAS  Google Scholar 

  • Brodersen, P., Gro Malinovsky, F., Hèmaty, K., Newman, M., and Mundy, J., 2005. The role of salicylic acid in the induction of cell death in Arabidopsis acd11. Plant Physiol., 138: 1037-1045.

    Article  PubMed  CAS  Google Scholar 

  • Brodersen, P., Petersen, M., Pike, H., Olszak, B., Skov, S., Odum, N., et al, 2002. Knockout of Arabidopsis ACCELERATED-CELL-DEATH11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense. Genes Dev., 16: 490-502.

    Article  PubMed  CAS  Google Scholar 

  • Casolo, V., Petrussa, E., Krajnakova, J., Macri, F., and Vianello, A., 2005. Involvement of the mitochondrial K(+)ATP channel in H2O2 or NO-induced programmed death of soybean suspension cell cultures. J. Exp. Bot., 56: 997-1006.

    Article  PubMed  CAS  Google Scholar 

  • Castagne, V., Barneoud, P., and Clarke, P., 1999. Protection of axotomized ganglion cells by salicylic acid. Brain Res., 40: 162-166.

    Article  Google Scholar 

  • Chammongpol, S., Willekens, H., Moeder, W., Langebartels, C., Sandermann, H., Van Montagu, M., Inzè, D., and Van Camp, W. 1998. Defense activation and enhanced pathogen tolerance induced in H2O2 in transgenic tobacco. Proc. Natl. Acad. Sci. USA, 95: 5818-5823.

    Article  Google Scholar 

  • Chen, H., Qualls, R., and GC, M., 2002. Adaptive responses of Lepidium latifolium to soil flooding: biomass allocation, adventitious roots, aerenchyma formation and ethylene production. Env. Exp. Bot., 48: 119-128.

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Chen, Z., Ricigliano, J., and Klessig, D., 1993a. Purification and characterisation of a soluble salicylic acid-binding protein from tobacco. Proc. Natl. Acad. Sci. USA., 90: 9533-9537.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Chong, J., Pierrel, M., Atanassova, R., Werck-Reichhart, D., Fritig, B., and Saindrenan, P., 2001. Free and conjugated benzoic acid in tobacco plants and cell cultures. Induced accumulation upon elicitation of defense responses and role of salicylic acid precursors. Plant Physiol., 125: 318-328.

    Article  PubMed  CAS  Google Scholar 

  • Clarke, A., Desikan, R., Hurst, R., Hancock, J., and Neill, S., 2000. NO way back: nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures. Plant J., 24: 667-677.

    Article  PubMed  CAS  Google Scholar 

  • Conrath, U., Chen, Z., Ricigliano, J., and Klessig, D., 1995. Two inducers of plant defense responses, 2,6-dichloroisionicotinic acid and salicylic acid, inhibit catalse activity in tobacco. Proc. Natl. Acad. Sci. USA., 92: 7143-7147.

    Article  PubMed  CAS  Google Scholar 

  • Curtin, J., Donovan, M., and Cotter, T., 2002. Regulation and measurement of oxidative stress in apoptosis J. Immu. Meth., 265: 49-72.

    Article  CAS  Google Scholar 

  • Dangl, J.. and Jones, J., 2001. Plant pathogens and integrated defense responses to infection. Nature, 411: 826-833.

    Article  PubMed  CAS  Google Scholar 

  • Dat, J., Capelli, N., Folzer, H., Bourgeade, P., and Badot, P., 2004. Sensing and signalling during plant flooding. PPB., 42: 273-282.

    PubMed  CAS  Google Scholar 

  • Dat, J., Foyer, C., and Scott, I., 1998b. Changes in salicylic acid and antioxidants during induced thermotolerance in mustard seedlings. Plant Physiol., 118: 1455-1461.

    Article  CAS  Google Scholar 

  • Dat, J., Inzè, D., and Van Breusegem, F., 2001. Catalase-deficient plants: tools for in Planta studies on the role of hydrogen peroxide. Redox Rep., 6: 37-42.

    Article  PubMed  CAS  Google Scholar 

  • Dat, J., Lopez-Delgado, H., Foyer, C., and Scott, I., 1998a. Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol., 116: 1351-1357.

    Article  CAS  Google Scholar 

  • Dat, J., Lopez-Delgado, H., Foyer, C., and Scott, I., 2000a. Effects of salicylic acid on oxidative stress and thermotolerance in tobacco. J. Plant Physiol., 156: 659-665.

    CAS  Google Scholar 

  • Dat, J., Pellinen, R., Beeckman, T., Van De Cotte, B., Langebartels, C., Kangasjarvi, J., Inzè, D., and Van Breusegem, F., 2003. Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco. Plant J., 33: 621-632.

    Article  PubMed  CAS  Google Scholar 

  • Dat, J., Vandenabeele, S., Vranova, E., Van Montagu, M., Inzè, D., and Van Breusegem, F., 2000b. Dual action of the active oxygen species during plant stress responses. CMLS., 57: 779-795.

    CAS  Google Scholar 

  • Delaney, T., 1997. Genetic dissection of acquired resistance to disease. Plant Physiol., 113: 5-12.

    Article  PubMed  CAS  Google Scholar 

  • Delaney, T., Uknes, S., Bernooij, B., Friedrich, L., Weymann, K., Negrotto, D., et al, 1994. A central role of salicylic acid in plant disease resistance. Science., 266: 1247-1250.

    Article  CAS  PubMed  Google Scholar 

  • Delledonne, M., 2005. NO news is good news for plants. Curr. Opin. Plant Biol., 8: 390-396.

    Article  PubMed  CAS  Google Scholar 

  • Delledonne, M., Xia, Y., Dixon, R. and Lamb, C., 1998. Nitric oxide functions as a signal in plant disease resistance. Nature., 394: 585-588.

    Article  PubMed  CAS  Google Scholar 

  • Delledonne, M., Zeier, J., Marocco, A. and Lamb, C., 2001. Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. PNAS., 98: 13454-13459.

    Article  PubMed  CAS  Google Scholar 

  • Dempsey, D., Shah, J. and Klessig, D., 1999. Salicylic acid and disease resistance in plants. Crit. Rev. Plant Sci., 18: 547-575.

    Article  CAS  Google Scholar 

  • Desikan, R., Clarke, A., Hancock, J. and Neill, S., 1999. H2O2 activates a MAP kinase-like enzyme in Arabisopsis thaliana suspension cultures. J. Exp. Bot.,50: 1863-1866.

    Article  CAS  Google Scholar 

  • Desikan, R., Mackerness, S., Hancock, J. and Neill, S., 2001. Regulation of the Arabidopsistranscriptome by oxidative stress. Plant Physiol., 127: 159-172.

    Article  PubMed  CAS  Google Scholar 

  • Dietrich, R., Delaney, T., Uknes, S., Ward, E., Ryals, J., and Dangl, J., 1994. Arabidopsis mutants simulating disease resistance response. Cell, 77: 565-577.

    Article  PubMed  CAS  Google Scholar 

  • Doherty, H., Selvendran, R., and Bowles, D., 1988. The wound response of tomato plants can be inhibited by aspirin and related hydroxy-benzoic acids. Physiol. Mol. Plant Path., 33: 377-384.

    Article  CAS  Google Scholar 

  • Doke, N., 1997. The oxidative burst: Roles in signal transduction and plant stress. In JG Scandalios (Ed.), Oxidative stress and the molecular biology of antioxidant defenses. Cold Spring Harbor Laboratory Press, Plainview: pp. 785-813.

    Google Scholar 

  • Dong, X., 2004. NPR1, all things considered. Curr. Opin. Plant Biol., 7: 547-552.

    Article  PubMed  CAS  Google Scholar 

  • Dordas, C., Hasinoff, B., Igamberdiev, A., Manac’h, N., Rivoal, J., and Hill, R., 2003. Expression of a stress-induced hemoglobin affects NO levels produced by alfalfa root cultures under hypoxic stress. Plant J.,35: 763-770.

    Article  PubMed  CAS  Google Scholar 

  • Dorey, S., Kopp, M., Geoffroy, P., Fritig, B., and Kauffmann, S., 1999. Hydrogen peroxide from the oxidative burst is neither necessary nor sufficient for hypersensitive cell death induction, phenylalanine ammonia lyase stimulation, salicylic acid accumulation, or scopoletin consumption in cultured tobacco cells treated with elicitin. Plant Physiol., 121: 163-171.

    Article  PubMed  CAS  Google Scholar 

  • Draper, J., 1997. Salicylate, superoxide synthesis and cell suicide in plant defense. TIPS., 2: 162-165.

    Google Scholar 

  • Drew, M., 1997. Oxygen deficiency and root metabolism: injury and acclimation under hyopxia and anoxia. Annu. Rev. Plant Phys. Plant Mol. Biol., 48: 223-250.

    Article  CAS  Google Scholar 

  • Drew, M., He, C., and Morgan, P., 2000. Programmed cell death and aerenchyma formation in roots. TIPS., 5: 123-127.

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Edwards, R., 1994. Conjugation and metabolism of salicylic acid in tobacco. J. Plant Physiol., 143: 608-614.

    Google Scholar 

  • Enyedi, A., Yalpani, N., Silverman, P., and Raskin, I., 1992. Localisation, conjugation, and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. Proc. Natl. Acad. Sci. USA., 89: 2480-2484.

    Article  PubMed  CAS  Google Scholar 

  • Evans, D., 2004. Tansley review: Aerenchyma formation. New Phytol., 161: 35-49.

    Article  Google Scholar 

  • Feys, B., and Parker, J., 2000. Interplay of signalling pathways in plant disease resistance. Tren. Gen., 16: 449-455.

    Article  CAS  Google Scholar 

  • Foyer, C., and Noctor, G., 2005. Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell, 17: 1866-1875.

    Article  PubMed  CAS  Google Scholar 

  • Frank, S. and Barr, C., 2003. Programmed cell death and hybrid incompability. J. Heredity, 94: 181-183.

    Article  CAS  Google Scholar 

  • Fukuda, H., 2000. Programmed cell death of tracheary elements as a paradigm in plants. Plant Mol. Biol., 44: 245-253.

    Article  PubMed  CAS  Google Scholar 

  • Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., et al, 1993. Requirement of salicylic acid for induction of systemic acquired resistance. Science, 261: 754-756.

    Article  CAS  PubMed  Google Scholar 

  • Glazener, J., Orlandi, E., and Baker, C., 1996. The active oxygen response of cell suspensions to incompatible bacteria is not sufficient to cause the hypersensitive cell death. Plant Physiol., 110: 759-763.

    PubMed  CAS  Google Scholar 

  • Grant, J., and Loak, G., 2000. Role of reactive oxygen intermediates and cognate redox signalling in disease resistance. Plant Physiol., 124: 21-29.

    Article  PubMed  CAS  Google Scholar 

  • Greenberg, J., 1996. Programmed cell death: A way of life for plants. Proc. Natl. Acad. Sci. USA., 93: 12094-12097.

    Article  PubMed  CAS  Google Scholar 

  • Groom, Q., Torres, M., Forham-Skelton, A., Hammond-Kosack, K., Robinson, N., and Jones, J., 1996. rbohA, a rice homologue of the mammalian gp91phox respiratory burst oxidase gene. Plant J., 10: 515-522.

    Article  PubMed  CAS  Google Scholar 

  • Groover, A., DeWitt, N., Heidel, A., and Jones, A., 1997. Programmed cell death of plant tracheary elements differentiating in vitro. Protoplasma, 196: 197-211.

    Article  Google Scholar 

  • Guan, L., and Scandalios, J., 1995. Developmentally related responses of maize catalase genes to salicylic acid. Proc. Natl. Acad. Sci. USA., 92: 5930-5934.

    Article  PubMed  CAS  Google Scholar 

  • Gunawaredena, A., Greewood, J., and Dengler, N., 2004. Programmed cell death remodels lace plant leaf shape during development. Plant Cell, 16: 60-73.

    Article  CAS  Google Scholar 

  • Gunawaredena, A., Pearce, D., Jackson, M., Hawes, C., and Evans, D., 2001a. Characterization of programmed cell death during aerenchyma formation by ethylene or hypoxia in roots of maize (Zea mays L.). Planta, 212: 205-214.

    Article  Google Scholar 

  • Gunawaredena, A., Pearce, D., Jackson, M., Hawes, C., and Evans, D., 2001b. Rapid changes in cell wall pectic polysaccharides are closely associated with early stages of arenchyma formation, a spatially localized form of programmed cell dath in roots of maize promoted by ethylene. Plant Cell Env.,24: 1369-1375.

    Article  Google Scholar 

  • Haddad, J., 2004. Redox and oxidant-mediated regulation of apoptosis signalling pathways: immuno-pharmaco-redox conception of oxidative siege versus cell death commitment. Int. Immunopharm., 4: 475-493.

    Article  CAS  Google Scholar 

  • Hancock, J., Desikan, R., Clarke, A., Hurst, R., and Neill, S., 2002. Cell signalling following plant/pathogen interactions involves the generation of reactive oxygen and reactive nitrogen species. PPB.,40: 611-617.

    CAS  Google Scholar 

  • Hancock, J., Desikan, R., and Neill, S., 2001. Role of active oxygen species in cell signalling pathways. Bioch Soc. Trans., 29: 345-350.

    Article  CAS  Google Scholar 

  • He, C., Drew, M., and Morgan, P., 1994. Induction of enzymes associated with lysigenous aerenchyma formation in roots of Zea maysduring hypoxia and nitrogen starvation. Plant Physiol., 105: 861-865.

    PubMed  CAS  Google Scholar 

  • He, C., Morgan, P., and Drew, M., 1996. Transduction of an ethylene signal is required for cell death and lysis in the root cortex of maize during aerenchyma formation induced by hypoxia. Plant Physiol., 112: 463-472.

    PubMed  CAS  Google Scholar 

  • He, Y., Liu, Y., Cao, W., Huai, M., Xu, B., and Huang, B., 2005. Effects of salicylic acid on heat tolerance associated with antioxidant metabolism in Kentucky Bluegrass. Crop Sci., 45: 988-995.

    Article  CAS  Google Scholar 

  • Heath, M., 2000. Hypersensitive response-related death. Plant Mol. Biol., 44: 321-334.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hildeman, D., 2004. Regulation of T-cell apoptosis by reactive oxygen species. Free Rad. Biol. Med. 36: 1496-1504.

    Article  PubMed  CAS  Google Scholar 

  • Hoeberichts, F., and Woltering, E., 2002. Multiple mediators of plant programmed cell death mechanisms and plant-specific regulators. BioEssays, 25: 47-57.

    Article  CAS  Google Scholar 

  • Houot, V., Etienne, P., Petitot, A., Barbier, S., Blein, J., and Suty, L., 2001. Hydrogen peroxide induces programmed cell death features in cultured tobacco BY-2 cells, in a dose-dependent manner. J. Exp. Bot., 52: 1721-1730.

    Article  PubMed  CAS  Google Scholar 

  • Huang, X., Stettmaier, K., Michel, C., Hutzler, P., Mueller, M., and Durner, J., 2004. Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana. Planta, 218: 939-946.

    Article  CAS  Google Scholar 

  • Jabs, T., 1999. Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem. Pharma.,57: 231-245.

    Article  CAS  Google Scholar 

  • Jabs, T., Dietrich, R., and Dangl, J., 1996. Initiation of runaway cell death in an Arabidopsismutant by extracellular superoxide. Science,273: 1853-1856.

    Article  PubMed  CAS  Google Scholar 

  • Janda, T., Szalai, G., Tari, I., and Paldi, E., 1999. Hydroponic treatment with salicylic acid decrease the effects of chilling injury in maize (Zea mays L.) plants. Planta,208: 175-180.

    Article  CAS  Google Scholar 

  • Jones, A., 2000,. Does the mitochondria integrate cellular stress and regulate programmed cell death? TIPS.,5: 225-230.

    CAS  Google Scholar 

  • Jones, J., and Dangl, J., 1996. Logjam at the Styx: programmed cell death in plants. TIPS., 1: 114-119.

    Google Scholar 

  • Kachroo, P., Shanklin, J., Shah, J., Whittle, E., and Klessig, D., 2001. A fatty acid desaturase modulates the activation of defense signaling pathways in plants. PNAS., 98: 9448-9453.

    Article  PubMed  CAS  Google Scholar 

  • Kadota, Y., Watanabe, T., Fujii, S., Higashi K, Sano, T., Nagata, T., et al, 2004. Crosstalk between elicitor-induced cell death and cell cycle regulation in tobacco BY-2 cells. Plant J., 40: 131-142.

    Article  PubMed  CAS  Google Scholar 

  • Kangasjarvi, J., Jaspers, P., and Kollist, H., 2005. Signalling and cell death in ozone-exposed plants. Plant Cell Env., 28: 1021-1036.

    Article  CAS  Google Scholar 

  • Karpinski, S., Gabrys, H., Mateo, A., Karpinska, B., and Mullineaux, P., 2003. Light perception in plant disease defence signalling. Curr. Opin. Plant Biol., 6: 390-396.

    Article  PubMed  CAS  Google Scholar 

  • Karpinski, S., Reynolds, H., Karpinska, B., Wingsle, G., Creissen, G., and Mullineaux, P., 1999. Systemic signalling and acclimation in response to excess excitation energy in Arabidopsis. Science, 284: 654-657.

    Article  PubMed  CAS  Google Scholar 

  • Kawai, K., Samarajeewa, P., Barrero, R., Nishiguchi, M., and Uchimiya, H., 1998. Cellular dissection of the degradation pattern of cortical cell death during aerenchyma formation of rice roots. Planta, 204: 277-287.

    Article  CAS  Google Scholar 

  • Kawasaki, T., Henmi, K., Ono, E., Hatakeyama, S., Iwano, M., Satoh, H., and Shimamoto, K., 1999. The small GTP-binding protein rac is a regulator of cell death in plants. Proc. Natl. Acad. Sci. USA., 96: 10922-10926.

    Article  PubMed  CAS  Google Scholar 

  • Keller, T., Damude, H., Werner, D., Doerner, P., Dixon, R., and Lamb, C., 1998. A plant homolog of the neutrophil NADPH-oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2 binding motifs. Plant Cell, 10: 255-266.

    Article  PubMed  CAS  Google Scholar 

  • Kende, H., 1993. Ethylene biosynthesis. Ann. Rev. Plant Phys. Plant Mol. Biol., 44: 283-307.

    Article  CAS  Google Scholar 

  • Klepper, L., 1991, NOx evolution by soybean leaves treated by salicylic acid and selected derivatives. Pest Biochem Physiol., 39: 43-48.

    Article  CAS  Google Scholar 

  • Kloek, A., Verbsky, M., Sharma, S., Schoelz, J., Vogel, J., Klessig, D., and Kunkel, B., 2001. Resistance to Pseudonomas synringaeconferred by an Arabidopsis thaliana coronatine-insensitive (coi1) mutation occurs through two distinct mechanisms. Plant J.,26: 509-522.

    Article  PubMed  CAS  Google Scholar 

  • Koch, J., Creelman, J., Eshita, S., Seskar, M., Mullet, J., and Davis, K., 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: 1-10.

    Article  Google Scholar 

  • Korsmeyer, S., Yin, X., Oltvai, Z., Veis-Novack, D., and Linette, G., 1995. Reactive oxygen species and the regulation of cell death by the Bcl-2 gene family. Biochem. Biophys. Acta, 1271: 63-66.

    PubMed  Google Scholar 

  • Kowaltowski, A., Castilho, R., and Vercesi, A., 2001. Mitochondrial permeability transition and oxidative stress. Febs Lett., 495: 12-15.

    Article  PubMed  CAS  Google Scholar 

  • Kunkel, B., and Brooks, D., 2002. Cross talk between signaling pathways in pathogen defense. Curr. Opin. Plant Biol.,5: 325-331.

    Article  PubMed  CAS  Google Scholar 

  • Kuriyama, H., and Fukuda, H., 2002. Developmental programmed cell death in plants. Curr. Opin. Plant Biol., 5: 568-573.

    Article  PubMed  CAS  Google Scholar 

  • Kwak, J., Mori, I., Pei, Z., Leonhardt, N., Torres, M., Dangl, J., et al, 2003. NADPH oxidase AtrbohDand AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. Embo J., 22: 2623-2633.

    Article  PubMed  CAS  Google Scholar 

  • Laloi, C., Apel, K., and Danon, A., 2004. Reactive oxygen signalling: the latest news. Curr. Opin. Plant Biol., 7: 232-328.

    Article  CAS  Google Scholar 

  • Lam, E., 2004. Controlled cell death, plant survival and development. Nature Rev.,5: 305-315.

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Langebartels, C., Wohlgemuth, H., Kschieschan, S., Grun, S., and Sandermann, H., 2002. Oxidative burst and cell death in ozone-exposed plants. PPB., 40: 567-575.

    CAS  Google Scholar 

  • Larkindale, J., Hall, J., Knight, M., and Vierling, E., 2005. Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol., 138: 882-897.

    Article  PubMed  CAS  Google Scholar 

  • Leon, J., Lawton, M., and Raskin, I., 1995. Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol., 108: 1673-1678.

    PubMed  CAS  Google Scholar 

  • Levine, A., Tenhaken, R., Dixon, R., and Lamb, C., 1994. H2O2 from the oxidative burst orchestrates the hypersensitive response. Cell, 79: 583-593.

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Delgado, H., Dat, J., Foyer, C., and Scott, I., 1998. Induction of thermotolerance in potato microplasnts by acetylsalicylic acid and H2O2. J. Exp. Bot., 49: 713-730.

    Article  CAS  Google Scholar 

  • Lorbiecke, R., and Sauter, M., 1999. Adventitious root growth and cell-cycle induction in deepwater rice. Plant Physiol., 119: 21-29.

    Article  CAS  PubMed  Google Scholar 

  • Mach, J., Castillo, A., Hoogstraten, R., and Greenberg, J., 2001. TheArabidopsis-accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proc. Natl. Acad. Sci. USA., 98: 771-776.

    Article  PubMed  CAS  Google Scholar 

  • Malamy, J., Carr, J., Klessig, D., and Raskin, I., 1990. Salicylic acid: a likely endogenous signal in the resistance for tobacco mosaic viral infection. Science, 250: 1002-1004.

    Article  CAS  PubMed  Google Scholar 

  • Malamy, J., and Klessig, D., 1992. Salicylic acid and plant disease resistance. Plant J.,2: 643-654.

    CAS  Google Scholar 

  • Masuda, Y., Yamada, T., and Marubashi, W., 2003. Time course analysis of apoptotic cell death during expression of hybrid lethality in hybrid tobacco cells (Nicotiana suaveolens x N. tabacum). Plant Cell Env., 44: 420-427.

    CAS  Google Scholar 

  • Mauch-Mani, B., and Slusarenko, A., 1996. Production of salicylic acid precursors is a major function of phenylalanine ammonia-lyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell, 8: 203-212.

    Article  PubMed  CAS  Google Scholar 

  • McCabe, and Leaver, C., 2000. Programmed cell death in cell cultures. Plant Mol. Biol., 44: 359-368.

    Article  PubMed  CAS  Google Scholar 

  • McCabe, P., Levine, A., Meijer, P., Tapon, N., and Pennell, R., 1997. A programmed cell death pathway activated in carrot cells cultured at low density. Plant J., 12: 267-280.

    Article  CAS  Google Scholar 

  • Mètraux, J., 2002. Recent breakthroughs in the study of salicylic acid biosynthesis. TIPS., 7: 1-3.

    Google Scholar 

  • Mètraux, J., Signer, H., Ryals, J., Ward, E., and Wyss-Benz, M., 1990. Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science, 250: 1004-1006.

    Article  PubMed  Google Scholar 

  • Mikolajczyk, M., Awotunde, O., Muszynska, G., Klessig, D., and Dobrowolska, G., 2000. Osmotic stress induces rapid activation of a salicylic acid-induced protein kinase and a homolog of protein kinase ASK1 in tobacco cells. Plant Cell, 12: 165-178.

    Article  PubMed  CAS  Google Scholar 

  • Mittler, R., 2002. Oxidative stress, antioxidants and stress tolerance.TIPS., 7: 405-410.

    CAS  Google Scholar 

  • Mittler, R., Herr, E., Orvar, B., Van Camp, W., Willekens, H., Inzè, D., and Ellis, B., 1999. Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyper-responsive to pathogen attack. Proc. Natl. Acad. Sci. USA., 96: 14165-14170.

    Article  PubMed  CAS  Google Scholar 

  • Mittler, R., Vanderauwera, S., Gollery, M., and Van Breusegem, F., 2004. Reactive oxygen gene network of plants. TIPS., 9: 490-498.

    CAS  Google Scholar 

  • Moeder, W., Barry, C., Tauriainen, A., Betz, C., Tuomainen, J., Utriainen, M., Grierson, D., Sandermann, H., Langebartels, C. and Kangasjarvi, 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 H2O2 accumulation and cell death in ozone-exposed tomato. Plant Physiol., 130: 1918-1926.

    Article  PubMed  CAS  Google Scholar 

  • Molina, A., Bueno, P., Marlin, M., Rodriguez-Rosales, M., Belver, A., Venema, K., and Danaire, J., 2002. Involvement of endogenous salicylic acid content lipoxygenase and antioxidant enzyme activities in response of tomato cell suspension cultures to NaCl. New Phytol., 156: 409-415.

    Article  CAS  Google Scholar 

  • Montillet, J., Chammongpol, S., Rusterucci, C., Dat, J., Van De Cotte, B., Agnel, J., Battesti, C., Inzè, D., Van Breusegem, F., and Triantaphylides, C., 2005. Fatty acid hydroperoxides and H2O2 in the execution of hypersensitive cell death in tobacco leaves. Plant Physiol., 138: 1516-1526.

    Article  PubMed  CAS  Google Scholar 

  • Moore, A., Albury, M., Crichton, P., and Affourtit, C., 2002. Function of the alternative oxidase: is it still a scavenger ? TIPS., 7: 478-481.

    CAS  Google Scholar 

  • Nawrath, C., and Mètraux, J., 1999. Salicylic acid induction-deficient mutants of Arabidopsisexpress PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell, 11: 1393-1404.

    Article  PubMed  CAS  Google Scholar 

  • Nibbe, M., Hilpert, B., Wasternack, C., Miersch, O., and Apel, K., 2002. Cell death and salicylate- and jasmonate-dependent stress responses inArabidopsis are controlled by single cet genes. Planta, 216: 120-128.

    Article  PubMed  CAS  Google Scholar 

  • Noctor, G., and Foyer, C., 1998. Ascorbate and glutathion: keeping active oxygen under control. Annu. Rev. Plant Phys. Plant Mol. Biol., 49: 249-279.

    Article  CAS  Google Scholar 

  • O’Brien, I., Baguley, B., Murray, B., Morris, B., and Ferguson, I., 1998. Early stages of the apoptotic pathway in plant cells are reversible. Plant J., 13: 803-814.

    Article  CAS  Google Scholar 

  • Ono, E., Wong, H., Kawasaki, T., Hasegawa, M., Kodama, O., and Shimamoto, K., 2001. Essential role of the small GTPase Rac in disease resistance of rice. Proc. Natl. Acad. Sci. USA., 98: 759-764.

    Article  PubMed  CAS  Google Scholar 

  • Orozco-Cardenas, M., Narvaez-Vasquez, J., and Ryan, C., 2001. Hydrogen peroxide acts as a secondary messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell, 13: 179-191.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Overmyer, K., Brochè, M., Pellinen, R., Kuittinen, T., Tuominen, H., Ahlfors, R., Keinänen, M., Saarma, M., Scheel, D. and Kangasjarvi, J. 2005. Ozone-induced programmed cell death in the Arabidopsis radical-induced cell death1mutant. Plant Physiol., 137: 1092-1104.

    Article  PubMed  CAS  Google Scholar 

  • Overmyer, K., Pellinen, R., Kuittinen, T., Betz, C., Langebartels, C., Sandermann, H., and Kangasjarvi, J., 2000. The ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signalling pathways in regulating superoxide-dependent cell death. Plant Cell, 12: 1849-1862.

    Article  PubMed  CAS  Google Scholar 

  • Pellinen, R., Korhonen, M., Tauriainen, A., Palva, E., and Kangasjarvi, J., 2002. Hydrogen peroxide activates cell death and defense gene expression in birch. Plant Physiol., 130: 549-560.

    Article  PubMed  CAS  Google Scholar 

  • Pellinen, R., Palva, J., and Kangasjarvi, 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 

  • Pennell, R., and Lamb, C., 1997. Programmed cell death in plants. Plant Cell,9: 1157-1168.

    Article  PubMed  CAS  Google Scholar 

  • Petersen, M., Brodersen, P., Naested, H., Andreasson, E., Lindhart, U., Johansen, B., Nielsen, H., Lacy, M., Austin, M., and Parker, J. 2000. Arabidopsis map kinase 4 negatively regulates systemic acquired resistance. Cell, 103: 1111-1120.

    Article  PubMed  CAS  Google Scholar 

  • Petit, P., Santos-Antonio, S., Zamzami, N., Mignotte, B., and Kroemer, G., 1996. Mitochondria and programmed cell death: back to the future. FEBS Lett., 396: 7-13.

    Article  PubMed  CAS  Google Scholar 

  • Rao, M., and Davis, K., 2000. The physiology of ozone induced cell death. Planta., 213: 682-690.

    Article  CAS  Google Scholar 

  • Rao, M., and Davis, R., 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, M., and Davis, R., 2001. The physiology of ozone-induced cell death. Planta, 213: 682-690.

    Article  PubMed  CAS  Google Scholar 

  • Rao, M., Koch, J., and Davis, K., 2000. Ozone: a tool for probing programmed cell death in plants. Plant Mol. Biol., 44: 345-358.

    Article  PubMed  CAS  Google Scholar 

  • Rao, M., Lee, H.-I., and Davis, K., 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, M., Paliyath, G., Ormrod, D., Murr, D., and Watkins, C., 1997. Influence of salicylic acid on H2O2 production, oxidative stress, and H2O2-metabolizing enzymes. Plant Physiol., 115: 137-149.

    Article  PubMed  CAS  Google Scholar 

  • Raskin, I., 1992. Role of salicylic acid in plants. Annu. Rev. Plant Phys. Plant Mol. Biol., 43: 439-463.

    Article  CAS  Google Scholar 

  • Rasmussen, J., Hammerschmidt, R., and Zook, M., 1991. Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudonomas syringae pv syringae. Plant Physiol., 97: 1342-1347.

    PubMed  CAS  Google Scholar 

  • Rate, D., Cuenca, J., Bowman, G., Guttman, D., and Greenberg, J., 1999. The gain-of-function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death, defenses, and cell growth. Plant Cell, 11: 1695-1708.

    Article  PubMed  CAS  Google Scholar 

  • Ribnicky, D., Shuvalev, V., and Raskin, I., 1998. Intermediates of salicylic acid biosynthesis in tobacco. Plant Physiol., 118: 565-572.

    Article  CAS  PubMed  Google Scholar 

  • Rizhsky, L., Hallak-Herr, E., Van Breusegem, F., Rachmilevitch, S., Barr, J., Rodermel, S., Inzè, D., and Mittler, R. 2002. Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stres than single antisense plants lacking ascorbate peroxidase or catalase. Plant J., 32: 329-342.

    Article  PubMed  CAS  Google Scholar 

  • Robson, C., and Vanlerberghe, G., 2002. Transgenic plant cells lacking mitochondrial alternative oxidase have increased susceptibility to mitochondrial-dependent and -independent pathways of programmed cell death. Plant Physiol., 129: 1908-1920.

    Article  PubMed  CAS  Google Scholar 

  • Rogers, E., and Ausubel, F., 1997. Arabidopsis enhanced disease susceptibility mutants exhibit enhanced susceptibility to several bacterial pathogens and alterations in PR-1 gene expression. Plant Cell, 9: 305-316.

    Article  PubMed  CAS  Google Scholar 

  • Rubenstein, B., 2000. Regulation of cell death in flower petals. Plant Mol. Biol., 44: 303-318.

    Article  Google Scholar 

  • Ryals, J., Neuenschwander, U., Willits, M., Molina, A., Steiner, H. and Hunt, M., 1996, Systemic acquired resistance. Plant Cell, 8: 1809-1819.

    Article  PubMed  CAS  Google Scholar 

  • Ryan, C. and Jadendorf, A., 1995. Self defense by plants. Proc. Natl. Acad. Sci. USA., 92: 4075.

    Article  PubMed  CAS  Google Scholar 

  • Samuilov, V., Oleskin, A., and Lagunova, E., 2000. Programmed cell death. Biochem. (Moscow)., 65: 873-887.

    CAS  Google Scholar 

  • Sanchez-Casas, P., and Klessig, D., 1994. A salicylic acid-binding activity and a salicylic acid-inihibitable catalase activity are present in a variety of plant species. Plant Physiol., 106: 1675-1679.

    PubMed  CAS  Google Scholar 

  • Sandermann, H., Ernst, D., Heller, W., and Langebartels, C., 1998. Ozone: an abiotic elicitor of plant defense reactions. TIPS., 3: 47-50.

    Google Scholar 

  • Scandalios, J., 1997. Molecular genetics of superoxide dismutases in plants. In JG Scandalios (Ed.) Oxidative Stress and the Molecular Biology of Antioxidant defenses. Cold Spring Harbor Laboratory Press, New York. pp. 353-406.

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Schussler, E., and Longstreth, D., 2000. Changes in cell structure during the formation of root aerenchyma in Sagittaria lancifolia. Am. J. Bot.,87: 12-19.

    Article  PubMed  Google Scholar 

  • Senaratna, T., Touchell, D., Bunn, E., and Dixon, K., 2000. Acetyl salicylic acid and salicylic acid induce multiple stress tolerance in bean and tomato plants. Plant Growth Regul.,30: 157-161.

    Article  CAS  Google Scholar 

  • Shah, J., 2003. The salicylic acid loop in plant defense. Curr. Opin. Plant Biol., 6: 365-371.

    Article  PubMed  CAS  Google Scholar 

  • Sharma, Y., and Davis, K., 1997. The effects of ozone on antioxidant responses in plants. Free Rad. Biol. Med., 23: 480-488.

    Article  PubMed  CAS  Google Scholar 

  • Sharma, Y., Leon, J., Raskin, I., and Davis, K., 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.

    Article  PubMed  CAS  Google Scholar 

  • Shirasu, K., Nakajima, H., Krishnamachari, R., Dixon, R., and Lamb, C., 1997. Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell,9: 261-270.

    Article  PubMed  CAS  Google Scholar 

  • Siegrist, J., Jeblick, W., and Kauss, H., 1994. Defense responses in infected and elicited cucumber (Cucumis sativus L.) hypocotyl segments exhibiting acquired resistance. Plant Physiol.,105: 1365-1374.

    PubMed  CAS  Google Scholar 

  • Silverman, P., Seskar, M., Kanter, D., Schweizer, P., Mètraux, J., and Raskin, I., 1995. Salicylic acid in rice. Biosynthesis, conjugation and possible role. Plant Physiol., 108: 633-639.

    PubMed  CAS  Google Scholar 

  • Simon-Plas, F., Elmayan, T., and Blein, J., 2002. The plasma membrane oxidase NtrbohD is responsible for AOS production in elicited tobacco cells. Plant J., 31: 137-147.

    Article  PubMed  CAS  Google Scholar 

  • Slaymaker, D., Navarre, D., Clark, D., del Pozo, O., Martin, G., and Klessig, D., 2002,. The tobacco salicylic acid-binding protein 3 (SABP3) is the chloroplast carbonic anhydrase, which exhibits antioxidant activity and plays a role in the hypersensitive defense response. Proc. Natl. Acad. Sci. USA., 99: 11640-11645.

    Article  PubMed  CAS  Google Scholar 

  • Smirnov, S., Shulaev, V., and Turner, N., 1997. Expression of pokeweed antiviral protein in transgenic plants induces virus resistance in grafted wild-type plants independently of salicylic acid accumulation and pathogenesis-related protein synthesis. Plant Physiol.,114: 1113-1121.

    PubMed  CAS  Google Scholar 

  • Solomon, Belenghi, B., Delledonne, M., Menachem, E., and Levine, A., 1999. The involvement of cysteine proteases and protease inihibitor genes in the regulation of programmed cell death in plants. Plant Cell,11: 431-443.

    Article  PubMed  CAS  Google Scholar 

  • Song, F., and Goodman, R., 2001. Activity of nitric oxide is dependent on, but is partially required for function of, salicylic acid in the signaling pathway in tobacco systemic acquired resistances. Mol. Plant-Micro. Inter., 14: 1458-1462.

    Article  CAS  Google Scholar 

  • Souter, M., and Lindsey, K., 2000. Polarity and signalling in plant embryogenesis. J. Exp. Bot., 51: 971-983.

    Article  PubMed  CAS  Google Scholar 

  • Spoel, S., Koornneef, A., Claessens, S., Korzelius, J., Van Pelt, J., Mueller, M., Bauchala, A., Mètraux, J., Brown, R., and Kazan, K.2003. NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell, 15: 760-770.

    Article  PubMed  CAS  Google Scholar 

  • Sticher, L., Mauch-Mani, B., and Mètraux, J., 1997. Systemic acquired resistance. Annu. Rev. Phytopatho.,35: 325-370.

    Google Scholar 

  • Summermatter, K., Sticher, L., and Mètraux, J., 1995. Systemic responses in Arabidopsis thalianainfected and challenged with Pseudonomas syringae pv synringae. Plant Physiol., 108: 1379-1385.

    PubMed  CAS  Google Scholar 

  • Swidzinski, J., Leaver, C., and Sweetlove, L., 2004. A proteomic analysis of plant programmed cell death. Phytochem., 65: 1829-1838.

    Article  CAS  Google Scholar 

  • Swidzinski, J., Sweetlove, L., and Leaver, C., 2002. A custom microarray analysis of gene expression during programmed cell death in Arabidopsis thaliana. Plant J.,30: 431-446.

    Article  PubMed  CAS  Google Scholar 

  • Takahashi, H., Chen, Z., Du, H., Liu, Y., and Klessig, D., 1997. Development of necrosis and activation of disease resistance in transgenic tobacco plants with severely reduced catalase levels. Plant J., 11: 993-1005.

    Article  PubMed  CAS  Google Scholar 

  • Tanaka, S., Hayakawa, K., Umetani, Y., and Tabata, M., 1990. Glucosyltion of isomeric hydroxybenzoic acids by cell suspension cultures of Mallotus japonicus. Phytochem., 29: 1555-1558.

    Article  CAS  Google Scholar 

  • Tenhaken, R., and Rubel, C., 1997. Salicylic acid is needed in hypersensitive cell death in soybean but does not act as a catalase inhibitor. Plant Physiol., 115: 291-298.

    PubMed  CAS  Google Scholar 

  • Thomas, H., Ougham, H., Wagstaff, C., and Stead, A., 2003. Defining senescence and death. J. Exp. Bot.,54: 1127-1132.

    Article  PubMed  CAS  Google Scholar 

  • Torres, M., and Dangl, J., 2005. Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr. Opin. Plant Biol., 8: 397-403.

    Article  PubMed  CAS  Google Scholar 

  • Torres, M., Dangl, J., and Jones, J., 2002. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for the accumulation of reactive oxygen intermeadiates in the plant defense response. Proc. Natl. Acad. Sci. USA., 99: 523-528.

    Article  CAS  Google Scholar 

  • Torres, M., Onouchi, H., Hamada, S., Machida, C., Hammond-Kosack, K., and Jones, J., 1998. Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox). Plant J., 14: 365-370.

    Article  PubMed  CAS  Google Scholar 

  • Tuomainen, J., Betz, C., Kangasjarvi, J., Ernst, D., Yin, Z., Langebartels, C., and Sandermann, H., 1997. Ozone induction of ethylene emission in tomato plants: Regulation by differential accumulation of transcripts for the biosynthetic enzymes. Plant J., 12: 1151-1162.

    Article  CAS  Google Scholar 

  • Uknes, S., Dincher, S., Friedrich, L., Negrotto, D., Williams, S., Thompson-Taylor, H., Potter, S., Ward, E., and Ryals, J., 1993, Regulation of pathogenesis-related protein-1a gene expression. Plant Cell, 5: 159-169.

    Article  PubMed  CAS  Google Scholar 

  • Van Camp, W., Van Montagu, M., and Inzè, D., 1998. H2O2 and NO: redox signals in disease resistance. TIPS., 3: 330-334.

    Google Scholar 

  • Vandenabeele, S., Van Ser Kelen, K., Dat, J., Gadjev, I., Boonefaes, T., Morsa, S., Rottiers, P., Slooten, L., Van Montagu, M., Zabeau, M., Inzè, D., and Van Breusegem, F., 2003. A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. Proc. Natl. Acad. Sci. USA., 100: 16113-16118.

    Article  PubMed  CAS  Google Scholar 

  • Vandenabeele, S., Vanderauwera, S., Vuylsteke, M., Rombauts, S., Langebartels, C., Seidlitz, H., Zabeau, M., Van Montagu, M., Inzè, D., and Van Breusegem, F., 2004. Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana. Plant J., 39: 45-58.

    Article  PubMed  CAS  Google Scholar 

  • Vanderauwera, S., Zimmermann, P., Rombauts, S., Vandenabeele, S., Langebartels, C., Gruissem, W., Inzè, D., and Van Breusegem, F., 2005. Genome-wide analysis of hydrogen peroxide regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiol., 139: 806-821.

    Article  PubMed  CAS  Google Scholar 

  • Vanlerberghe, G., Robson, C., and Yip, J., 2002. Induction of mitonchondrial alternative oxidase in response to a cell signal pathway down-regulating the cytochrome pathway prevents programmed cell death. Plant Physiol., 129: 1829-1842.

    Article  PubMed  CAS  Google Scholar 

  • Vartapatian, B., and Jackson, M., 1997. Plant adaptations to anaerobic stress. Ann. Bot., 79: 3-20.

    Article  Google Scholar 

  • Vidal, S., Eriksson, A., Montesano, M., Denecke, J., and Tapio Talva, E., 1997. Cell wall degrading enzymes from Erwinia carotovoracooperate in the salicylic acid-independent induction of a plant defence response. Mol. Plant-Micro. Inter., 11: 23-32.

    Article  Google Scholar 

  • Vranova, E., Inzè, D., and Van Breusegem, F., 2002. Signal transduction during oxidative stress. J. Exp. Bot., 53: 1227-1236.

    Article  PubMed  CAS  Google Scholar 

  • Wang, K., Li, H., and Ecker, J., 2002. Ethylene biosynthesis and signaling networks. Plant Cell, 14: S131-S151.

    PubMed  CAS  Google Scholar 

  • Ward, E., Uknes, S., Williams, S., Dincher, S., Wiederhold, D., Alexander, D., Ahl-Goy, P., Mètraux, J., and Ryals, J., 1991. Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell, 3: 1085-1094.

    Article  PubMed  CAS  Google Scholar 

  • White, R., 1979. Acetylsalicylic acid (aspirin) induces the resistance to tobacco mosaic virus in tobacco. Virology, 99: 410-412.

    Article  CAS  PubMed  Google Scholar 

  • Wildermuth, M., Dewdney, J., Wu, G., and Ausubel, F., 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defense. Nature, 414: 562-565.

    Article  PubMed  CAS  Google Scholar 

  • Willekens, H., Langebartels, C., Tirè, C., Van Montagu, M., Inzè, D., and Van Camp, W., 1994. Differential expression of catalase in Nicotiana plumginifolia L. Proc. Natl. Acad. Sci. USA.,91: 10450-10454.

    Article  PubMed  CAS  Google Scholar 

  • Yalpani, N., Enyedi, A., Leon, J., and Raskin, I., 1994. Ultraviolet light and ozone stimulate accumulation of salicylic acid and pathogenesis-related proteins and virus resistance in tobacco. Planta, 193: 373-376.

    Article  Google Scholar 

  • Yalpani, N., Schulz, M., Davis, M., and Balke, N., 1992. Partial purification and properties of an inducible uridine 5’-diphosphate-glucose: salicylic acid glucosyltransferase from oat roots. Plant Physiol.,100: 457-463.

    PubMed  CAS  Google Scholar 

  • Yalpani, N., Silverman, P., Wilson, T., Kleier, S., and Raskin, I., 1991. Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus infected tobacco. Plant Cell, 3: 809-818.

    Article  PubMed  CAS  Google Scholar 

  • Yang, Y., Qi, M., and Mei, C., 2004. Endogenous salicylic acid protects rice plants from oxidative damage caused by aging as well as biotic and abiotic stress. Plant J., 40: 909-919.

    Article  PubMed  CAS  Google Scholar 

  • Yoshioka, H., Numata, N., Nakajima, K., Katou, S., Kawakita, K., Rowland, O., et al, 2003. Nicotiana benthamiana gp91(phox) homologue NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophtora infestans. Plant Cell, 15: 706-718.

    Article  PubMed  CAS  Google Scholar 

  • Young, T., and Gallie, D., 2000. Programmed cell death during endosperm development. Plant Mol. Biol., 44: 283-301.

    Article  PubMed  CAS  Google Scholar 

  • Zhao, Y., Thilmony, R., Bender, C., Schaller, A., He, S., and Howe, G., 2003. Virulence systems to Pseudonomas synringae pv. tomato promote bacterial speak disease in tomato by targeting the jasmonate signalling pathway. Plant J., 36: 485-499.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratoire de Biologie Environnementale (EA 3154 MRT, UC INRA), Universitè de Franche- Comtè, UFR Sciences et Techniques, Place Leclerc, F-25030, Besancon Cedex, France

    J. F. Dat & N. Capelli

  2. Department of Plant Systems Biology, Ghent University, VIB, Technologie Park 927, B-9052, Gent, Belgium

    F. Van Breusegem

Authors
  1. J. F. Dat
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. Capelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. F. Van Breusegem
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Botany, Aligarh Muslim University, Aligarh, 202002, India

    S. Hayat

  2. Department of Botany, Aligarh Muslim University, Aligarh, 202002, India

    A. Ahmad

Rights and permissions

Reprints and permissions

Copyright information

© 2007 Springer

About this chapter

Cite this chapter

Dat, J.F., Capelli, N., Van Breusegem, F. (2007). The Interplay Between Salicylic Acid and Reactive Oxygen Species During Cell Death in Plants. In: Hayat, S., Ahmad, A. (eds) Salicylic Acid: A Plant Hormone. Springer, Dordrecht. https://doi.org/10.1007/1-4020-5184-0_9

Download citation

Publish with us

Policies and ethics

Search

Navigation