Advertisement

Role of Salicylic Acid in the Induction of Abiotic Stress Tolerance

  • T. Janda
  • E. Horváth
  • G. Szalai
  • E. PáLdi
Chapter

Abstract

Investigations on compounds capable of reducing the stress sensitivity of crops are of great importance from both the theoretical and the practical point of view. In terms of stress physiology, salicylic acid was first demonstrated to play a role in responses to biotic stress. However, it was gradually found to have more and more effects that could be of importance for other stress factors, and a great deal of evidence has accumulated in recent years suggesting that salicylic acid also plays a role in responses to abiotic stress effects (such as low and high temperature, UV-B irradiation, ozone, heavy metals, etc.). Most papers, on this subject, have reported on the protective effect of exogenous salicylic acid against abiotic stress. When applied in satisfactory concentrations salicylic acid may cause a temporary low level of oxidative stress in plants, which acts as a hardening process, improving the antioxidative capacity of the plants and helping to induce the synthesis of protective compounds such as polyamines. Numerous mutant or transgenic plants are now available in which the salicylic acid metabolism has been modified in some way. These allow us to obtain a more accurate picture of the endogenous effect and role of salicylic acid. Evidence now suggests the existence of a regulatory defence mechanism in which salicylic acid plays an important role, but which is not stress-specific, apparently functioning against many different stress factors. This chapter provides a review of the effects exerted by salicylic acid and related compounds in relation to abiotic stress tolerance.

Key words

Abiotic stresses oxidative stress salicylic acid signal transduction 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Agarwal, S., Sairam, R. K., Srivastava, G. C., Tyagi, A., and Meena, R. C., 2005. Role of ABA, salicylic acid, calcium and hydrogen peroxide on antioxidant enzymes induction in wheat seedlings. Plant Sci., 169: 559-570.Google Scholar
  2. Agrawal, G. K., Agrawal, S. K., Shibato, J., Iwahashi, H., and Rakwal, R., 2003. Novel rice MAP kinases OsMSRMK3 and OsWJUMK1 involved in encountering diverse environmental stresses and developmental regulation. Biochem Biophys. Res. Com., 300: 775-783.PubMedGoogle Scholar
  3. Ahlfors, R., Macioszek, V., Rudd, J., Brosche, M., Schlichting, R., Scheel, D., and Kangasjarvi, J., 2004. Stress hormone-independent activation and nuclear translocation of mitogen-activated protein kinases in Arabidopsis thaliana during ozone exposure. Plant J., 40: 512-522.PubMedGoogle Scholar
  4. Ananieva, E. A., Alexieva, V. S., and Popova, L. P., 2002. Treatment with salicylic acid decreases the effects of paraquat on photosynthesis. J. Plant Physiol., 159: 685-693.Google Scholar
  5. Anderson, M. D., Chen, Z., and Klessig, D. F., 1998. Possible involvement of lipid peroxidation in salicylic acid-mediated induction of PR-1 gene expression. Phytochem., 47: 555-566.Google Scholar
  6. Azevedo, H., Lino-Neto, T., and Tavares, R. M., 2004. Salicylic acid up-regulates the expression of chloroplastic Cu,Zn-superoxide dismutase in needles of maritime pine (Pinus pinaster Ait.). Ann. For. Sci., 61: 847-850.Google Scholar
  7. Baier, M., Kandlbinder, A., Golldack, D., and Dietz, K. J., 2005. Oxidative stress and ozone: perception, signalling and response. Plant Cell Environ., 28: 1012-1020.Google Scholar
  8. Bandurska, H., and Stroinski, A. 2005. The effect of salicylic acid on barley response to water deficit. Acta Physiol. Plant., 27: 379-386.Google Scholar
  9. Ball, L., Accotto, G. P., Bechtold, U., Creissen, G., Funck, D., Jimenez, A., Kular, B., Leyland, N., Mejia-Carranza, J., Reynolds, H., Karpinski, S., and Mullineaux, P. M., 2004. Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. Plant Cell, 16: 2448-2462.PubMedGoogle Scholar
  10. Bassett, C. L., 2001. The molecular biology of plant hormone reception. Hort. Rev., 26: 49–84.Google Scholar
  11. Bassett, C. L., Nickerson, M. L., Farrell, R. E., Artlip, T. S., El Ghaouth, A., Wilson, C.L., and Wisniewski, M. E., 2005. Characterization of an S-locus receptor protein kinase-like gene from peach. Tree Physiol., 25: 403-411.PubMedGoogle Scholar
  12. Bernard, F., Shaker-Bazarnov, H., and Kaviani, B., 2002. Effects of salicylic acid on cold preservation and cryopreservation of encapsulated embryonic axes of Persian lilac (Melia azedarach L.). Euphytica, 123: 85-88.Google Scholar
  13. Black, V. J., Black, C. R., Roberts, J. A., and Stewart, C. A., 2000. Impact of ozone on the reproductive development of plants. New Phytol., 147: 421-447.Google Scholar
  14. Borsani O., Valpuesta V., and Botella M. A. 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.PubMedGoogle Scholar
  15. Bowler, C., and Fluhr, R., 2000. The role of calcium and activated oxygens as signals for controlling cross-tolerance. Trends Plant Sci., 5: 241–246.PubMedGoogle Scholar
  16. Brune, A., Urbach, W., and Dietz, K.-J. 1995. Differential toxicity of heavy metals is partly related to a loss of preferential extraplasmic compartmentation: a comparison of Cd-, Mo-, Ni- and Zn-stress. New Phytol., 129: 404–409Google Scholar
  17. Chai, T. Y., Zhang, Y. X., 1999. Gene expression analysis of a proline-rich protein from bean under biotic and abiotic stress. Acta Bot. Sin., 41: 111-113.Google Scholar
  18. Chakraborty, U., and Tongden, C., 2005. Evaluation of heat acclimation and salicylic acid treatments as potent inducers of thermotolerance in Cicer arietinum L. Curr. Sci., 89: 384-389.Google Scholar
  19. Chen, Z., Silva, H., and Klessig, D. F. 1993a. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science, 262: 1883-1886.Google Scholar
  20. Chen, Z., Ricigliano, J. R., and Klessig, D. F. 1993b. Purification and characterization of a soluble salicylic acid binding protein from tobacco. Proc. Natl. Acad. Sci. USA, 90: 9533-9537.Google Scholar
  21. Chen, Z., Iyer, S., Caplan, A., Klessig, D. F., and Fan, B. 1997. Differential accumulation of salicylic acid and salicylic acid-sensitive catalase in different rice tissues. Plant Physiol., 114: 193-201.PubMedGoogle Scholar
  22. Chen, Y. C., Tseng, B. W., Huang, Y. L., Liu, Y. C., and Jeng, S. T., 2003. Expression of the ipomoelin gene from sweet potato is regulated by dephosphorylated proteins, calcium ion and ethylene. Plant Cell Environ., 26: 1373-1383.Google Scholar
  23. Chen, B. J., Wang, Y., Hu, Y. L., Wu, Q., and Lin, Z. P., 2005. Cloning and characterization of a drought-inducible MYB gene from Boea crassifolia. Plant Sci., 168: 493-500.Google Scholar
  24. Chico, J. M., Raíces, M., Tellez-Iñón, M. T., and Ulloa, R. M., 2002. A calcium-dependent protein kinase is systemically induced upon wounding in tomato plants. Plant Physiol., 128: 256–270.PubMedGoogle Scholar
  25. Chini, A., Grant, J. J., Seki, M., Shinozaki, K., and Loake, G. J., 2004. Drought tolerance established by enhanced expression of the CC-NBS-LRR gene, ADR1, requires salicylic acid, EDS1 and ABI1. Plant J., 38: 810-822.PubMedGoogle Scholar
  26. Chong, J., Pierrel, M.-A., 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 as salicylic acid precursors. Plant Physiol., 125: 318–328.PubMedGoogle Scholar
  27. Chung, I. M., Park, M. R., Rehman, S., and Yun, S. J., 2001. Tissue specific and inducible expression of resveratrol synthase gene in peanut plants. Mol. Cells, 12: 353-359.PubMedGoogle Scholar
  28. Chung, I. M., Park, M. R., Chun, J. C., and Yun, S. J., 2003. Resveratrol accumulation and resveratrol synthase gene expression in response to abiotic stresses and hormones in peanut plants. Plant Sci., 164: 103-109.Google Scholar
  29. Chung, E., Park, J. M., Oh, S. K., Joung, Y. H., Lee, S., and Choi, D., 2004. Molecular and biochemical characterization of the Capsicum annuum calcium-dependent protein kinase 3 (CaCDPK3) gene induced by abiotic and biotic stresses. Planta, 220: 286-295.PubMedGoogle Scholar
  30. Clarke, S. M., Mur, L. A. J., Wood, J. E., and Scott, I. M., 2004. Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquired thermotolerance in Arabidopsis thaliana. Plant J., 38: 432-447.PubMedGoogle Scholar
  31. Cleland, C. F., 1974. Isolation of flower-inducing and flower-inhibitory factors from aphid honeydew. Plant Physiol., 54: 899-903.PubMedGoogle Scholar
  32. Cleland, C. F. and Ajami, A., 1974. Identification of the flower-inducing factor isolated from aphid honeydew as being salicylic acid. Plant Physiol., 54: 904-906.PubMedGoogle Scholar
  33. Conklin, P. L., and Last, R. L., 1995. Differential accumulation of antioxidant mRNAs in Arabidopsis thaliana exposed to ozone. Plant Physiol., 109, 203–212.PubMedGoogle Scholar
  34. Conklin, P. L., and Barth C., 2004. Ascorbic acid, a familiar small molecule intertwined in the response of plants to ozone, pathogens and the onset of senescence. Plant Cell Environ., 27: 959-970.Google Scholar
  35. Conrath U., Chen Z., Ricigliano J.R., and Klessig D.F. 1995. Two inducers of plant defense responses, 2,6-dichloroisonicotinic acid and salicylic acid, inhibit catalase activity in tobacco. Proc. Natl. Acad. Sci. USA, 92: 7143-7147.PubMedGoogle Scholar
  36. Cronje, M. J., and Bornman, L., 1999. Salicylic acid influences Hsp70/Hsc70 expression in Lycopersicon esculentum: Dose- and time-dependent induction or potentiation. Biochem. Biophys. Res. Com., 265: 422-427.PubMedGoogle Scholar
  37. Dat, J. F., Lopez-Delgado, H., Foyer, C. H., and Scott, I. M., 1998a. Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol., 116: 1351-1357.Google Scholar
  38. Dat, J. F., Foyer, C. H., and Scott, I. M., 1998b. Changes in salicylic acid and antioxidants during induced thermotolerance in mustard seedlings. Plant Physiol., 118: 1455-1461.Google Scholar
  39. Dat, J. F., Lopez-Delgado, H., Foyer, C. H., and Scott, I. M., 2000. Effects of salicylic acid on oxidative stress and thermotolerance in tobacco. J. Plant Physiol., 156: 659-665.Google Scholar
  40. Davletova, S., Mészáros, T., Miskolczi P., Oberschall, A., Török, K., Magyar, Z., Dudits, D., and Deák, M., 2001. Auxin and heat shock activation of a novel member of the calmodulin-like domain protein kinase gene family in cultured alfalfa cells. J. Exp. Bot., 52: 215–221.PubMedGoogle Scholar
  41. Dean, J. V., Shah, R. P., and Mohammed, L. A., 2003. Formation and localization of salicylic acid glucose conjugates in soybean cell suspension cultures. Physiol. Plant., 118: 328-336.Google Scholar
  42. DeKock, P. C., Grabowsky, F. B., and Innes, A. M., 1974. The effect of salicylic acid on the growth of Lemna gibba. Ann. Bot., 38: 903-908.Google Scholar
  43. Djajanegara, I., Finnegan, P. M., Mathieu, C., McCabe, T., Whelan, J., and Day, D. A., 2002. Regulation of alternative oxidase gene expression in soybean. Plant Mol. Biol., 50: 735-742.PubMedGoogle Scholar
  44. Do, H. M., Lee, S. C., Jung, H. W., Sohn, K. H., and Hwang, B. K., 2004. Differential expression and in situ localization of a pepper defensin (CADEF1) gene in response to pathogen infection, abiotic elicitors and environmental stresses in Capsicum annuum. Plant Sci., 166: 1297-1305.Google Scholar
  45. Duan, H., and Schuler, M. A., 2005. Differential expression and evolution of the Arabidopsis CYP86A subfamily. Plant Physiol., 137: 1067-1081.PubMedGoogle Scholar
  46. Durner, J., and Klessig, D. F., 1996. Salicylic acid is a modulator of tobacco and mammalian catalases. J. Biol. Chem., 271: 28492-28501.PubMedGoogle Scholar
  47. El Tayeb, M. A., 2005. Response of barley grains to the interactive effect of salinity and salicylic acid. Plant Growth Regul., 45: 215-224.Google Scholar
  48. Enyedi, A. J., Yalpani, N., Silverman, P., and Raskin, I., 1992. Localization, conjugation, and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. Proc. Natl. Acad. Sci. USA, 89: 2480-2484.PubMedGoogle Scholar
  49. Enyedi, A. J., 1999. Induction of salicylic acid biosynthesis and systemic acquired resistance using the active oxygen species generator rose bengal. J. Plant Physiol., 154: 106-112.Google Scholar
  50. Ervin, E. H., Zhang, X. Z., and Fike, J. H., 2004. Ultraviolet-B radiation damage on Kentucky Bluegrass II: Hormone supplement effects. Hort Sci., 39: 1471-1474.Google Scholar
  51. Ervin, E. H., Zhang, X. Z., and Schmidt, R. E., 2005. Exogenous salicylic acid enhances post-transplant success of heated Kentucky bluegrass and tall fescue sod. Crop Sci., 45: 240-244.Google Scholar
  52. Evans, N. H., McAinsh, M. R., Hetherington, A. M., and Knight, M. R., 2005. ROS perception in Arabidopsis thaliana: the ozone-induced calcium response. Plant J., 41: 615-626.PubMedGoogle Scholar
  53. Farmer, E. E., and Ryan, C.A., 1992. Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducibe proteinase inhibitors. Plant Cell, 4: 129-134.PubMedGoogle Scholar
  54. Federico, M. L., Kaeppler, H. F., and Skadsen, R. W., 2005. The complex developmental expression of a novel stress-responsive barley Ltp gene is determined by a shortened promoter sequence. Plant Mol. Biol., 57: 35-51.PubMedGoogle Scholar
  55. Feys, B. J., and Parker, J. E., 2000. Interplay of signaling pathways in plant disease resistance. Trends Genet., 16: 449–455.PubMedGoogle Scholar
  56. Foley, S., Navaratnam, S., McGarvey, D. J., Land, E. J., Truscott, G., and Rice-Evans, C. A., 1999. Singlet oxygen quenching and the redox properties of hydroxycinnamic acids. Free Radical Bio. Med., 26: 1202-1208.Google Scholar
  57. Freeman, J. L., Persans, M. W., Nieman, K., Albrecht, C., Peer, W., Pickering, I. J., and Salt, D. E., 2004. Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell, 16: 2176–2191.PubMedGoogle Scholar
  58. Freeman, J. L., Garcia, D., Kim, D., Hopf, A., and Salt, D. E., 2005. Constitutively elevated salicylic acid signals glutathione-mediated nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Physiol., 137: 1082-1091.PubMedGoogle Scholar
  59. Fung, R. W. M., Wang, C. Y., Smith, D. L., Gross, K. C. and Tian, M. S., 2004. MeSA and MeJA increase steady-state transcript levels of alternative oxidase and resistance against chilling injury in sweet peppers (Capsicum annuum L.). Plant Sci., 166: 711-719.Google Scholar
  60. Gaffney, T., Friedrich, L., Vernooij, B., Negrotto, D., Nye, G., Uknes, S., Ward, E., Kessmann, H., and Ryals, J., 1993. Requirement of salicylic acid for the induction of systemic acquired resistance. Science, 261: 754-756.Google Scholar
  61. Ganesan, V., and Thomas, G., 2001. Salicylic acid response in rice: influence of salicylic acid on H2O2 accumulation and oxidative stress. Plant Sci., 160: 1095-1106.Google Scholar
  62. Garretón, V., Carpinelli, J., Jordana, X., and Holuigue, L., 2002. The as-1 promoter element is an oxidative stress-responsive element and salicylic acid activates it via oxidative species. Plant Physiol., 130: 1516-1526.PubMedGoogle Scholar
  63. Gechev, T., Gadjev, I., Van Breusegem, F., Inze, D., Dukiandjiev, S., Toneva, V., and Minkov, I., 2002. Hydrogen peroxide protects tobacco from oxidative stress by inducing a set of antioxidant enzymes. Cell. Mol. Life Sci., 59: 708-714.PubMedGoogle Scholar
  64. Ghasempour, H. R., Anderson, E. M., and Gaff, D.F., 2001. Effects of growth substances on the protoplasmic drought tolerance of leaf cells of the resurrection grass, Sporobolus stapfianus. Aust. J. Plant Physiol., 28: 1115-1120.Google Scholar
  65. Glass, A. D. M., 1973. Influence of phenolic acids on ion uptake. I. Inhibition of phosphate uptake. Plant Physiol., 51: 1037-1041.PubMedGoogle Scholar
  66. Glass, A. D. M., 1974a. Influence of phenolic acids on ion uptake. III. Inhibition of potassium absorption. J. Exp. Bot., 25: 1104-1113.Google Scholar
  67. Glass, A. D. M., 1974b. Influence of phenolic acids on ion uptake. IV. Depolarization of membrane potentials. Plant Physiol., 54: 855-858.Google Scholar
  68. Godoy, A. V., Lazzaro, A. S., Casalongue, C. A., and San Segundo, B., 2000. Expression of a Solanum tuberosum cyclophilin gene is regulated by fungal infection and abiotic stress conditions. Plant Sci., 152: 123-134.Google Scholar
  69. Grant, J. J., Chini, A., Basu, D., and Loake, G. J., 2003. Targeted activation tagging of the Arabidopsis NBS LRR gene, ADR1, conveys resistance against virulent pathoges. Mol. Plant Microbe Interact., 16: 669-681.PubMedGoogle Scholar
  70. Guan, L., and Scandalios, J. G., 1995. Developmentally related responses of maize catalase genes to salicylic acid. Proc. Natl. Acad. Sci. USA, 92: 5930-5934.PubMedGoogle Scholar
  71. Guerinot, M. L., and Salt, D. E., 2001. Fortified foods and phytoremediation: two sides of the same coin. Plant Physiol., 125: 164–167.PubMedGoogle Scholar
  72. Gupta, V., Willits, M. G., and Glazebrook, J., 2000. Arabidopsis thalianaEDS4 contributes to salicylic acid (SA)-dependent expression of defense responses: evidence for inhibition of jasmonic acid signaling by SA. Mol. Plant Microbe Interact., 13: 503–511.PubMedGoogle Scholar
  73. Hamada, A. M., 1998. Effects of exogenously added ascorbic acid, thiamin or aspirin on photosynthesis and some related activities of drought-stressed wheat plants. In: Photosynthesis: Mechanisms and effects, G., Garab ed., Kluwer Acad. Publ., Dordrecht, Vol. 4 pp. 2581-2584.Google Scholar
  74. Hamada, A. M., and Al-Hakimi, A. M. A., 2001. Salicylic acid versus salinity-drought-induced stress on wheat seedlings. Rostl. Vyr., 47: 444-450.Google Scholar
  75. Harmon, A. C., Gribskov, M., Gubrium, E., and Harper, J. F., 2001. The CDPK superfamily of protein kinase. New Phytol., 151: 175–183.Google Scholar
  76. He, C. Y., Zhang, J.S., and Chen, S.Y., 2002. A soybean gene encoding a proline-rich protein is regulated by salicylic acid, an endogenous circadian rhythm and by various stresses. Theor. Appl. Gen., 104: 1125-1131.Google Scholar
  77. He, Y. L., Liu, Y. L., Cao, W. X., Huai, M. F., Xu, B. G., and Huang, B. G., 2005. Effects of salicylic acid on heat tolerance associated with antioxidant metabolism in Kentucky bluegrass. Crop Sci., 45: 988-995.Google Scholar
  78. Hettiarachchi, G. H. C. M., Reddy, M. K., Sopory, S. K., and Chattopadhyay, S., 2005. Regulation of TOP2 by various abiotic stresses including cold and salinity in pea and transgenic tobacco plants. Plant Cell Physiol., 46: 1154-1160.PubMedGoogle Scholar
  79. Holk, A., Rietz, S., Zahn, M., Quader, H., and Scherer, G. F. E., 2002. Molecular Identification of Cytosolic, Patatin-Related Phospholipases A from Arabidopsis with Potential Functions in Plant Signal Transduction. Plant Physiol., 130: 90-101.PubMedGoogle Scholar
  80. Hollósy, F., 2002. Effects of ultraviolet radiation on plant cells. Micron, 33: 179-197.PubMedGoogle Scholar
  81. Horváth, E., Janda, T., Szalai G., and Páldi, E., 2002. In vitro salicylic acid inhibition of catalase activity in maize: differences between the isozymes and a possible role in the induction of chilling tolerance. Plant Sci., 163: 1129-1135.Google Scholar
  82. Hoyos, M. E., and Zhang, S.Q., 2000. Calcium-independent activation of salicylic acid-induced protein kinase and a 40-kilodalton protein kinase by hyperosmotic stress. Plant Physiol., 122: 1355-1363.PubMedGoogle Scholar
  83. Hung, W. C., Huang, D. D., Yeh, C. M., and Huang, H. J., 2005. Reactive oxygen species, calcium and serine/threonine phosphatase are required for copper-induced MAP kinase geneOsMAPK2, expression in rice. Plant Growth Regul., 45: 233-241.Google Scholar
  84. Inada, M., Ueda, A., Shi, W. M., and Takabe, T., 2005. A stress-inducible plasma membrane protein 3 (AcPMP3) in a monocotyledonous halophyte, Aneurolepidium chinense, regulates cellular Na+ and K+ accumulation under salt stress. Planta, 220: 395-402.PubMedGoogle Scholar
  85. Ito, Y., Saisho, D., Nakazono, M., Tsutsumi, N., and Hirai, A., 1997. Transcript levels of tandem-arranged alternative oxidase genes in rice are increased by low temperature. Gene, 203: 121-129.PubMedGoogle Scholar
  86. Iuchi, S., Yamaguchi-Shinozaki, K., Urao, T., and Shinozaki, K., 1996. Characterization of two cDNAs for novel drought-inducible genes in the highly drought-tolerant cowpea. J. Plant Res., 109: 415-424.Google Scholar
  87. Jagendorf, A. T., and Takabe, T., 2001. Inducers of glycinebetaine synthesis in barley. Plant Physiol., 127: 1827-1835.PubMedGoogle Scholar
  88. Jain, A., and Srivastava, H. S. 1981. Effect of salicylic acid on nitrate reductase activity in maize seedlings. Physiol. Plant., 51: 339-342.Google Scholar
  89. Janda, T., Szalai, G., Tari, I., and Páldi, E., 1997. Exogenous salicylic acid has an effect on chilling symptoms in maize (Zea mays L.) plants. P., Sowinski, B., Zagdanska, A., Aniol, P., Klaus eds., Crop development for cool and wet Europian climate, ECSP-EEC-EAEC, Brussels, Belgium 179-187.Google Scholar
  90. Janda, T., Szalai, G., Antunovics, Zs. Ducruet, J.-M., and P′ldi, E. 1998. Effects of salicylic acid and related compounds on photosynthetic parameters in young maize (Zea maysL.) plants. G., Garab ed., Photosynthesis: Mechanisms and effects, Kluwer Acad. Publ., Dordrecht, Kluwer Acad. Publ. pp. 3869-3872.Google Scholar
  91. Janda, T., Szalai, G., Tari, I., and Páldi, E., 1999. Hydroponic treatment with salicylic acid decreases the effect of chilling injury in maize (Zea mays L.) plants. Planta, 208: 175-180.Google Scholar
  92. Janda, T., Szalai, G., Antunovics, Zs., Horváth, E., and Páldi, E., 2000. Effect of benzoic acid and aspirin on chilling tolerance and photosynthesis in young maize plants. Maydica, 45: 29-33.Google Scholar
  93. Janda, T., Szalai, G., Rios-Gonzalez, K., Veisz, O., and Páldi, E., 2003. Comparative study of frost tolerance and antioxidant activity in cereals. Plant Sci., 164: 301-306.Google Scholar
  94. Jang, C. S., Lee, H. J., Chang, S. J., and Seo, Y. W., 2004. Expression and promoter analysis of the TaLTP1 gene induced by drought and salt stress in wheat (Triticum aestivum L.). Plant Sci., 167: 995-1001.Google Scholar
  95. Janowiak, F., and Dörffling, K., 1996. Chilling tolerance of 10 maize genotypes as related to chilling-induced changes in ACC and MACC contents. J. Agron. Crop Sci., 177: 175-184.Google Scholar
  96. Jonak, C., Ökrész, L., Bögre, L., and Hirt, H. 2002. Complexity, cross talk and integration of plant MAP kinase signalling. Curr. Opin. Plant Biol., 5: 415–424.PubMedGoogle Scholar
  97. Kader, J. C., 1996. Lipid transfer proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol., 47: 627–654.PubMedGoogle Scholar
  98. Kang, H. M., and Saltveit, M. E., 2002. Chilling tolerance of maize, cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. Physiol. Plant., 115: 571-576.PubMedGoogle Scholar
  99. Kang, G. Z., Wang, C. H., Sun, G. C., and Wang, Z. X., 2003a. Salicylic acid changes activities of H2O2-metabolizing enzymes and increases the chilling tolerance of banana seedlings. Environ. Exp. Bot., 50: 9-15.Google Scholar
  100. Kang, G. Z., Wang, Z. X., and Sun, G. C., 2003b. Participation of H2O2 in enhancement of cold chilling by salicylic acid in banana seedlings. Acta Bot. Sin., 45: 567-573.Google Scholar
  101. Kanofsky, J. R., and Sima, P., 1991. Singlet oxygen production from the reactions of ozone with biological molecules. J. Biol. Chem., 266: 9039-9042.PubMedGoogle Scholar
  102. Khan, W., Prithiviraj, B., and Smith, D. L., 2003. Photosynthetic responses of corn and soybean to foliar application of salicylates. J. Plant Physiol., 160: 485-492.PubMedGoogle Scholar
  103. Kiba, A., Nishihara, M., Tsukatani, N., Nakatsuka, T., Kato, Y., and Yamamura, S., 2004. A peroxiredoxin Q homolog from gentians is involved in both resistance against fungal disease and oxidative stress. Plant Cell Physiol., 46: 1007-1015.Google Scholar
  104. Kim, H., Mun, J. H., Byun, B. H., Hwang, H. J., Kwon, Y. M., and Kim, S. G., 2002. Molecular cloning and characterization of the gene encoding osmotin protein in Petunia hybrida. Plant Sci., 162: 745-752.Google Scholar
  105. Kim, A. S., Kim, Y. O., Ryu, H. J., Kwak, Y. S., Lee, J. Y., and Kang, H. S., 2003a. Isolation of stress-related genes of rubber particles and latex in fig tree (Ficus carica) and their expressions by abiotic stress or plant hormone treatments. Plant Cell Physiol., 44: 412-419.Google Scholar
  106. Kim JA, Agrawal GK, Rakwal R, Han KS, Kim KN, Yun CH, Heu S, Park SY, Lee YH, and Jwa NS., 2003b. Molecular cloning and mRNA expression analysis of a novel rice (Oryza sativa L.) MAPK kinase kinase, OsEDR1, an ortholog of Arabidopsis AtEDR1, reveal its role in defense/stress signalling pathways and development. Biochem. Biophys. Res. Comm., 300: 868-876.Google Scholar
  107. Kim, M., Yang, K. S., Kim, Y. K., Paek, K. H., and Pai, H. S., 2003c. Molecular characterization of NbPAF encoding the alpha 6 subunit of the 20S proteasome in Nicotiana benthamiana. Mol. Cells, 15: 127-132.Google Scholar
  108. Kim, S. T., Kim, S. G., Hwang, D. H., Kang, S. Y., Koo, S. C., Cho, M. J., and Kang, K. Y., 2004. Expression of a salt-induced protein (SALT) in suspension-cultured cells and leaves of rice following exposure to fungal elicitor and phytohormones. Plant Cell Rep., 23: 256-262.PubMedGoogle Scholar
  109. Klessig, D. F., Durner, J., Noad, R., Navarre, D. A., Wendehenne, D., Kumar, D., Zhou, J. M., Shah, J., Zhang, S., Kachroo, P., Trifa, Y., Pontier, D., Lam, E., and Silva, H., 2000. Nitric oxid and salicylic acid signalling in plant defense. Proc. Natl. Acad. Sci. USA, 97: 8849-8855.PubMedGoogle Scholar
  110. Kling, G. J., and Meyer, M. M., 1983. Effect of phenolyc compounds and indolacetic acid on adventitious root initiation in cuttings of Phaseolus aureus, Acer saccharinum, and Acer griseum. Hort. Sci., 18: 352-354.Google Scholar
  111. Knörzer, O. C., Lederer, B., Durner, J., and Böger, P., 1999. Antioxidative defense activation in soybean cells. Physiol. Plant., 107: 294-302.Google Scholar
  112. Kocsy, G., Owttrim, G., Brander, K., and Brunold, C., 1997. Effect of chilling on the diurnal rhythm of enzymes involved in protection against oxidative stress in a chilling tolerant and a chilling sensitive maize genotype. Physiol. Plant., 99: 249-254.Google Scholar
  113. Kocsy, G., Galiba, G., and Brunold, C., 2001. Role of glutathione in adaptation and signalling during chilling and cold acclimation in plants. Physiol. Plant., 113: 158-164.PubMedGoogle Scholar
  114. Kocsy, G., Kobrehel, K., Szalai, G., Duviau, M.P., Búzás, Z., and Galiba, G., 2004. Abiotic stress-induced changes in glutathione and thioredoxin h levels in maize. Environ. Exp. Bot., 52: 101-112.Google Scholar
  115. Korkmaz, A., Tiryaki, I., Nas, M. N., and Ozbay, N., 2004. Inclusion of plant growth regulators into priming solution improves low-temperature germination and emergence of watermelon seeds. Can. J. Plant Sci., 84: 1161-1165.Google Scholar
  116. Korkmaz, A., 2005. Inclusion of acetyl salicylic acid and methyl jasmonate into the priming solution improves low temperature germination and emergence of sweet pepper. Hort Sci., 40: 197-200.Google Scholar
  117. Krämer, U, Pickering, I. J., Prince, R. C., Raskin, I., and Salt, D. E., 2000. Subcellular localization and speciation of nickel in hyperaccumulator and nonaccumulator Thlaspi species. Plant Physiol., 122: 1343–1353.PubMedGoogle Scholar
  118. Lam, E., Benfey, P. N., Gilmartin, P. M., Fang, R.-X., and Chua, N.-H., 1989. Site-specific mutations alter in vitro factor binding and change promoter expression pattern in transgenic plants. Proc. Natl. Acad. Sci. USA, 86: 7890–7894.PubMedGoogle Scholar
  119. Lamarck, J. B., 1778. In: Flore Francaise 3. L’Emprimerie Royale, Paris, pp. 537-539.Google Scholar
  120. Lance, C., 1972. La respiration de l’Arum maculatum au cours du developpement de l’inflorescence. Ann. Sci. Nat. Bot. Biol. Veg. Ser. 12, 13: 477-495.Google Scholar
  121. Landberg, T., and Greger, M., 2002. Differences in oxidative stress in heavy metal resistant and sensitive clones of Salix viminalis. J. Plant Physiol., 159: 69-75.Google Scholar
  122. Larkindale, J., and Knight, M. R., 2002. Protection against heat stress-induced oxidative damage in arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol., 128: 682-695.PubMedGoogle Scholar
  123. Larkindale, J., and Huang, B., 2004. Thermotolerance and antioxidant systems in Agrostis stolonifera: Involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide, and ethylene. J. Plant Physiol., 161: 405-413.PubMedGoogle Scholar
  124. Larkindale, J., Hall, J. D., Knight, M. R., and Vierling, E., 2005. Heat stress phenotypes of arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol., 138: 882-897.PubMedGoogle Scholar
  125. Larque-Saavedra, A., 1978. The antitranspirant effect of acetylsalicylic acid on Phaseolus vulgaris L. Physiol. Plant., 43: 126-128.Google Scholar
  126. Larque-Saavedra, A., 1979. Stomatal closure in response to acetylsalicylic acid treatments. Z. Pflanzenphysiol., 93: 371-375.Google Scholar
  127. Leclercq, J., Ranty, B., Sanchez-Ballesta, M. T., Li, Z. G., Jones, B., Jauneau, A., Pech, J. C., Latche, A., Ranjeva, R., and Bouzayen, M., 2005. Molecular and biochemical characterization of LeCRK1, a ripening-associated tomato CDPK-related kinase. J. Exp. Bot., 56: 25-35.PubMedGoogle Scholar
  128. Lee, S. S., Kawakita, K., Tsuge, T., and Doke, N., 1992. Stimulation of phospholipase A2 in strawberry cells treated with AF-toxin 1 produced by Alternaria alternata strawberry phenotype. Physiol. Mol. Plant Pathol., 41: 283-294.Google Scholar
  129. Lee, H., León, J., and Raskin, I., 1995. Biosynthesis and metabolism of salicylic acid. Proc. Natl. Acad. Sci. USA , 92: 4076-4079.PubMedGoogle Scholar
  130. Lee, S. C., and Hwang, B. K., 2003. Identification of the pepper SAR8.2 gene as a molecular marker for pathogen infection, abiotic elicitors and environmental stresses in Capsicum annuum. Planta, 216: 387-396.PubMedGoogle Scholar
  131. León, J., Lawton, M. A., and Raskin, I., 1995. Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol., 108: 1673-1678.PubMedGoogle Scholar
  132. Li, Z. G, Zhao, L. X, Kai, G. Y., Yu, S. W., Cao, Y. F., Pang, Y. Z., Sun, X. F., and Tang, K. X., 2004. Cloning and expression analysis of a water stress-induced gene from Brassica oleracea. Plant Physiol. Biochem., 42: 789-794.PubMedGoogle Scholar
  133. Liu, G. S., Sheng, X. Y., Greenshields, D. L., Ogieglo, A., Kaminskyj, S., Selvaraj, G., and Wei, Y. D., 2005. Profiling of wheat class III peroxidase genes derived from powdery mildew-attacked epidermis reveals distinct sequence-associated expression patterns. Mol. Plant Microbe. Interact., 18: 730-741.PubMedGoogle Scholar
  134. Lopez-Delgado, H., Dat, J. F., Foyer, C. H., and Scott, I. M., 1998. Induction of thermotolerance in potato microplants by acetylsalicylic acid and H2O2. J. Exp. Bot., 49: 713-720.Google Scholar
  135. Luo, J. P., Jiang, S. T., and Pan, L. J., 2001. Enhanced somatic embryogenesis by salicylic acid of Astragalus adsurgens Pall.: relationship with H2O2 production and H2O2-metabolizing enzyme activities, Plant Sci., 161: 125-132.Google Scholar
  136. Luxova, M., Gasparikova, O., 1999. The effect of low temperature on root respiration in maize. Biologia, 54: 453-458.Google Scholar
  137. Malamy, J., Carr, J. P., Klessig, D. F., and Raskin, I., 1990. Salicylic acid: A likely endogenous signal in the resistance response of tobacco to viral infection. Science, 250: 1002-1004.Google Scholar
  138. Margispinheiro, M., Marivet, J., and Burkard, G., 1994. Bean class-IV chitinase gene - structure, developmental expression and induction by heat-stress. Plant Sci., 98: 163-173.Google Scholar
  139. Marivet, J., Margispinheiro, M., Frendo, P., and Burkard, G., 1994. Bean cyclophilin gene-expression during plant development and stress conditions. Plant Mol. Biol., 26: 1181-1189.PubMedGoogle Scholar
  140. Marivet, J., Frendo, P., and Burkard, G., 1995. DNA-sequence analysis of a cyclophilin gene from maize - developmental expression and regulation by salicylic-acid. Mol. Gen. Genet., 247: 222-228.PubMedGoogle Scholar
  141. Martin, M. L, and Busconi, L., 2001. A rice membrane-bound calcium-dependent protein kinase is activated in response to low temperature. Plant Physiol., 125: 1442–1449.PubMedGoogle Scholar
  142. Mauzerall, D. L., and Wang, X., 2001. Protecting agricultural crops from the effects of tropospheric ozone exposure: reconciling science and standard setting in the United states, Europe and Asia. Annu. Rev. Energy Environ., 26: 237-268.Google Scholar
  143. Maxwell, D. P., Nickels, R., and McIntosh, L., 2002. Evidence of mitochondrial involvement in the transduction of signals required for the induction of genes associated with pathogen attack and senescence. Plant J., 29: 269-279.PubMedGoogle Scholar
  144. McClintock, B., 1984, The significance of responses of the genome to challenge. Science, 226: 792–801.PubMedGoogle Scholar
  145. Meeuse, B. J. D., Raskin, I., 1988. Sexual reproduction in the Arum lily family with emphasis on thermogenicity. Sex. Plant Reprod., 1: 3-15.Google Scholar
  146. 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.Google Scholar
  147. Métraux, J.-P., Signer, H., Ryals, J., Ward, E., Wyss-Benz, M., Gaudin, J., Raschdorf, K., Schmid, E., Blum, W., and Inverardi, B., 1990. Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science, 250: 1004-1006.Google Scholar
  148. Metwally, A., Finkemeier, I., Georgi, M., and Dietz, K.-J. 2003. Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant. Physiol., 132: 272-281.PubMedGoogle Scholar
  149. Milla, M. A. R., Maurer, A., Huete, A. R., and Gustafson, J. P., 2003. Glutathione peroxidase genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signalling pathways. Plant J., 36: 602-615.Google Scholar
  150. Minibaeva, F. V., and Gordon, L. K., 2003. Superoxide production and the activity of extracellular peroxidase in plant tissues under stress conditions. Rus. J. Plant Physiol., 50: 411-416.Google Scholar
  151. Mishra, A., and Choudhuri, M. A., 1997. Ameliorating effects of salicylic acid on lead and mercury – induced inhibition of germination and early seedling growth of two rice cultivars. Seed Sci. Technol., 25: 263-270.Google Scholar
  152. Mittler, R., 2002. Oxidative stress, antioxidants and stess tolerance. Trends Plant Sci., 7: 405-410.PubMedGoogle Scholar
  153. Moons, A., 2003. Osgstu3 and osgtu4, encoding tau class glutathione S-transferases, are heavy metal- and hypoxic stress-induced and differentially salt stress-responsive in rice roots. FEBS Lett., 553: 427-432.PubMedGoogle Scholar
  154. Morris, P. C., 2001. MAP kinase signal transduction pathways in plants. New Phytol., 151: 67-89.Google Scholar
  155. Moynihan, M. R., Ordentlich, A., and Raskin, I., 1995. Chilling-induced heat evolution in plants. Plant Physiol., 108: 995-999.PubMedGoogle Scholar
  156. Munne-Bosch, S., and Penuelas, J., 2003. Photo- and antioxidative protection, and a role for salicylic acid during drought and recovery in field-grown Phillyrea angustifolia plants. Planta, 217: 758-766.PubMedGoogle Scholar
  157. Narusaka, Y., Narusaka, M., Seki, M., Fujita, M., Ishida, J., Nakashima, M., Enju, A., Sakurai, T., Satou, M., Kamiya, A., Park, P., Kobayashi, M., and Shinozaki, K., 2003. Expression profiles of Arabidopsis phospholipase A IIA gene in response to biotic and abiotic stresses. Plant Cell Physiol., 44: 1246-1252.PubMedGoogle Scholar
  158. Narusaka, Y., Narusaka, M., Seki, M., Umezawa, T., Ishida, J., Nakajima, M., Enju, A., and Shinozaki, K., 2004. Crosstalk in the responses to abiotic and biotic stresses in Arabidopsis: Analysis of gene expression in cytochrome P450 gene superfamily by cDNA microarray. Plant Mol. Biol., 55: 327-342.PubMedGoogle Scholar
  159. Németh, M., Janda, T., Horváth, E., Páldi, E., and Szalai, G., 2002. Exogenous salicylic acid increases polyamine content but may decrease drought tolerance in maize. Plant Sci., 162: 569-574.Google Scholar
  160. Niki, T., Mitsuhara, I., Seo, S., Ohtsubo, N., and Ohashi, Y., 1998. Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant Cell Physiol., 39: 500–507.Google Scholar
  161. Norman, C., Howell, K. A., Millar, A. H., Whelan, J. M., and Day, D. A., 2004. Salicylic acid is an uncoupler and inhibitor of mitochondrial electron transport, Plant Physiol., 134: 492-501.PubMedGoogle Scholar
  162. 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.PubMedGoogle Scholar
  163. Pál, M., Szalai, G., Horváth, E., Janda, T., and Páldi, E., 2002. Effect of salicylic acid during heavy metal stress. Acta Biol. Szegediensis, 46: 119-120.Google Scholar
  164. Pál, M., Horváth, E., Janda, T., Páldi, E., and Szalai, G., 2005. Cadmium stimulate accumulation of salicylic acid and its putative precursors in maize (Zea mays L.) plants. Physiol. Plant., 125: 356-364.Google Scholar
  165. Pancheva, T. V., and Popova, L. P., 1998. Effect of salicylic acid on the synthesis of ribulose-1,5-bisphosphate carboxylase/oxygenase in barley leaves. J. Plant Physiol., 152: 381-386.Google Scholar
  166. Pastori, G. M., and Foyer, C. H., 2002. Common components, networks and pathways of cross-tolerance to stress. The central role of ’redox’ and abscisic acid-mediated controls. Plant Physiol., 129: 460-468.PubMedGoogle Scholar
  167. 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.Google Scholar
  168. Qi, Y. H., Kawano, N., Yamauchi, Y., Ling, J. Q., Li, D. B., and Tanaka, K., 2005. Identification and cloning of a submergence-induced gene OsGGT (glycogenin glucosyltransferase) from rice (Oryza sativa L.) by suppression subtractive hybridization. Planta, 221: 437-445.PubMedGoogle Scholar
  169. Quiroz-Figueroa, F. Mendez-Zeel, M., Larque-Saavedra, A., and Loyola-Vargas, V. M., 2001. Picomolar concentrations of salicylates induce cellular growth and enhance somatic embryogenesis in Coffea arabica tissue culture. Plant Cell Rep., 20: 679-684.Google Scholar
  170. Rai, V. K., Sharma, S. S., and Sharma, S., 1986. Reversal of ABA-induced stomatal closure by phenolic compounds. J. Exp. Bot., 37: 129-134.Google Scholar
  171. Rajasekaran, L. R., Stiles, A., and Caldwell, C. D., 2002. Stand establishment in processing carrots- Effects of various temperature regimes on germination and the role of salicylates in promoting germination at low temperatures. Can. J. Plant Sci., 82: 443-450.Google Scholar
  172. Rakwal, R., Agraval, G. K., and Agraval, V. P., 2001. Jasmonate, salicylate, protein phophatase 2A inhibitors and kinetin up-regulate OsPR5 expression in cut-responsive rice (Oryza sativa). J. Plant Physiol., 158: 1357-1362.Google Scholar
  173. Rao, M. V., Paliyath, G., Ormrod, D. P., Murr, D. P., and Watkins, C. B., 1997. Influence of salicylic acid on H2O2 production, oxidative stress, and H2O2-metabolizing enzymes. Plant Physiol., 115: 137-149.PubMedGoogle Scholar
  174. Rao, M. V., and Davis, K. R., 1999. Ozone-induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acid. Plant J., 17: 603-614.PubMedGoogle Scholar
  175. Rao, M. V., Lee, H. I., Creelman, R. A., Mullet, J. E., and Davis, K. R., 2000. Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell, 12: 1633-1646.PubMedGoogle Scholar
  176. Rao, M. V. and Davis, K. R., 2001. The physiology of ozone-induced cell death. Planta, 213: 682-690.PubMedGoogle Scholar
  177. Rao, M. V., Lee, H., 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.PubMedGoogle Scholar
  178. Raskin, I., Ehmann, A., Melander, W. R., and Meeuse, B. J. D., 1987. Salicylic acid: a natural inducer of heat production in Arum lilies. Science, 237: 1601-1602.Google Scholar
  179. Raskin, I., Skubatz, H., Tang, W., and Meeuse, B. J. D., 1990. Salicylic acid levels in thermogenic and non-thermogenic plants. Ann. Bot., 66: 369-373.Google Scholar
  180. Raskin, I., 1992. Role of salicylic acid in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol., 43: 439-463.Google Scholar
  181. Raskin, I., 1995. Salicylic acid. Plant hormones. Physiology, Biochemistry and Molecular Biology 2nd Edition, P. J., Davies ed., Kluwer Acad. Publ. Dordrecht, The Netherlands. pp188-205.Google Scholar
  182. Rhoads, D. M., and McIntosh, L., 1992. Cytochrome and alternative pathway respiration in tobacco. Effects of salicylic acid. Plant Physiol., 103: 877-883.Google Scholar
  183. Ribas-Carbo, M., Aroca, R., Gonzalez-Meler, M. A., Irigoyen, J. J., and Sanchez-Diaz, M., 2000. The electron partitioning between the cytochrome and alternative respiratory pathways during chilling recovery in two cultivars of maize differing in chilling sensitivity. Plant Physiol., 122: 199-204.PubMedGoogle Scholar
  184. Rietz, S., Holk, A., and Scherer, G. F. E., 2004. Expression of the patatin-related phospholipase A gene AtPLA IIA in Arabidopsis thaliana is up-regulated by salicylic acid, wounding, ethylene, and iron and phosphate deficiency. Planta, 219: 743-753.PubMedGoogle Scholar
  185. Rüffer, M., Steipe, B., and Zenk, M. H., 1995. Evidence against specific binding of salicylic acid to plant catalase. FEBS Lett., 377: 175-180.PubMedGoogle Scholar
  186. Sahu, G. K., Kar, M., and Sabat, S. C., 2002. Electron transport activities of isolated thylakoids from wheat plants grown in salicylic acid. Plant Biol., 4: 321-328.Google Scholar
  187. Saijo, Y., Hata, S., Kyozuka, J., Shimamoto, K., and Izui, K., 2000. Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J., 23: 319–327.PubMedGoogle Scholar
  188. Saitanis, C. J., and Karandinos, M. G., 2002. Effects of ozone on tobacco (Nicotiana tabacum L.) varieties. J. Agron. Crop Sci., 188: 51-58.Google Scholar
  189. Salzman, R. A., Brady, J. A., Finlayson, S. A., Buchanan, C. D., Summer, E. J., Sun, F., Klein, P. E., Klein, R. R., Pratt, L. H., Cordonnier-Pratt, M. M., and Mullet, J. E., 2005. Transcriptional profiling of sorghum induced by methyl jasmonate, salicylic acid, and aminocyclopropane carboxylic acid reveals cooperative regulation and novel gene responses. Plant Physiol., 138: 352-368.PubMedGoogle Scholar
  190. Samuel, M. A., Walia, A., Mansfield, S. D., and Ellis, B. E., 2005. Overexpression of SIPK in tobacco enhances ozone-induced ethylene formation and blocks ozone-induced SA accumulation. J. Exp. Bot., 56: 2195-2201.PubMedGoogle Scholar
  191. Sánchez-Casas P., and Klessig D. F., 1994. A salicylic acid-binding activity and a salicylic acid-inhibitable catalase activity are present in a variety of plant species. Plant Physiol., 106: 1675-1679.PubMedGoogle Scholar
  192. Sandermann, H. Jr., 1996. Ozone and plant health. Annu. Rev. Phytopathol., 34: 347-366.PubMedGoogle Scholar
  193. Sandermann, H. Jr., Ernst, D., Heller, W., and Langebartels, C., 1998. Ozone: an abiotic elicitor of plant defence reactions. Trends Plant Sci., 3: 47–50.Google Scholar
  194. Scherer, G. F. E., and André, B. 1989. A rapid response to a plant hormone: auxin stimulates phospholipase A2 in vivo and in vitro. Biochem. Biophys. Res. Comm., 163: 111-117.PubMedGoogle Scholar
  195. Scott, I. M., Clarke, S. M., Wood, J. E., and Mur, L. A. J., 2004. Salicylate accumulation inhibits growth at chilling temperature in Arabidopsis. Plant Physiol., 135: 1040-1049.PubMedGoogle Scholar
  196. Senaratna, T., Touchell, D., Bunn, E., and Dixon, K., 2000. Acetyl salicylic acid (Aspirin) and salicylic acid induce multiple stress tolerance in bean and tomato plants. Plant Growth Regul., 30: 157-161.Google Scholar
  197. Senaratna, T., Merritt, D., Dixon, K., Bunn, E., Touchell, D., and Sivasithamparam, K., 2003. Benzoic acid may act as the functional group in salicylic acid and derivatives in the induction of multiple stress tolerance in plants. Plant Growth Regul., 39: 77-81.Google Scholar
  198. Seo, S., Ishizuka, K., and Ohashi, Y., 1995a. Induction of salicylic-acid beta-glucosidase in tobacco-leaves by exogenous salicylic-acid. Plant Cell Physiol., 36: 447-453.Google Scholar
  199. Seo, S., Okamoto, M., Seto, H., Ishizuka, K., Sano, H., and Ohashi, Y., 1995b. Tobacco MAP kinase: a possible mediator in wound signal transduction pathways. Science, 270: 1988-1992.Google Scholar
  200. Seppanen, M. M., Cardi, T., Hyokki, M. B., and Pehu, E., 2000. Characterization and expression of cold-induced glutathione S-transferase in freezing tolerant Solanum commersonii, sensitive S.-tuberosum and their interspecific somatic hybrids. Plant Sci., 153: 125-133.Google Scholar
  201. Singh, N. K., Bracker, C. A., Hasegawa, P. M., Handa, A. K., Buckel, S., Hermodson, M. A., Pfankoch, E., Regnier, F. E., and Bressan, R. A., 1987. Characterization of osmotin 1. A thaumatin-like protein associated with osmotic adaptation in plant cells. Plant Physiol., 85: 529-536.PubMedGoogle Scholar
  202. Singh, B., and Usha, K., 2003. Salicylic acid induced physiological and biochemical changes in wheat seedlings under water stress. Plant Growth Regul., 39: 137-141.Google Scholar
  203. Singh, B. N., Mishra, R. N., Agarwal, P. K., Goswami, M., Nair, S., Sopory, S. K., and Reddy, M. K., 2004. A pea chloroplast translation elongation factor that is regulated by abiotic factors. Biochem. Biophys. Res. Comm., 320: 523-530.PubMedGoogle Scholar
  204. Sinha, S. K., Srivastava, H. S., and Tripathi, R. D., 1994. Influence of some growth-regulators and divalent-cations on the inhibition of nitrate reductase activity by lead in maize leaves. Chemosphere, 29: 1775-1782.Google Scholar
  205. Sakhabutdinova, A. R., Fatkhutdinova, D. R., and Shakirova, F. M., 2004. Effect of salicylic acid on the activity of antioxidant enzymes in wheat under conditions of salination. Appl. Biochem. Microbiol., 40: 501-505.Google Scholar
  206. Shakirova, F. M., Sakhabutdinova, A. R., Bezrukova, M. V., Fatkhutdinova, R. A., and Fatkhutdinova, D. R., 2003. Changes in the hormonal status of wheat seedlings induced by salicylic acid and salinity. Plant Sci., 164: 317-322.Google Scholar
  207. Sharma, Y. K., León, 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.PubMedGoogle Scholar
  208. Shen, Y, Tang, M. J., Hu, Y. L., and Lin, Z. P., 2004. Isolation and characterization of a dehydrin-like gene from drought-tolerant Boea crassifolia. Plant Sci., 166: 1167-1175.Google Scholar
  209. Shinozaki, K., and Yamaguchi-Shinozaki, K., 1996. Molecular responses to drought and cold stress. Curr. Opin. Biotech., 7: 161–167.PubMedGoogle Scholar
  210. Shunwu, Y. W., Zhang, L. D., Zuo, K. J., Li, Z. G., and Tang, K. X., 2004. Isolation and characterization of a BURP domain-containing gene BnBDC1 from Brassica napus involved in abiotic and biotic stress. Physiol. Plant., 122: 210-218.Google Scholar
  211. Sticher, L., Mauch-Mani, B., and Métraux, J. P., 1997. Systemic acquired resistance. Annu. Rev. Phytopathol., 35: 235–270.PubMedGoogle Scholar
  212. Strobel, N. E., and Kuc, A., 1995. Chemical and biological inducers of systemic acquired resistance to pathogens protect cucumber and tobacco from damage caused by paraquat and cupric chloride. Phytopathol., 85: 1306-1310.Google Scholar
  213. Szalai, G., Tari, I., Janda, T., Pestenácz, A., and Páldi, E., 2000. Effects of cold acclimation and salicylic acid on changes in ACC and MACC contents in maize during chilling. Biol. Plant., 43: 637-640.Google Scholar
  214. Szepesi, Á., Csiszár, J., Bajkán, Sz., Gémes, K., Horváth F., Erdei, L., Deér, A., Simon, L. M., and Tari, I., 2005. Role of salicylic aicd pre-treatment on the acclimation of tomato plants to salt- and osmotic stress. Acta Biol. Szegediensis, 49: 123-125.Google Scholar
  215. Takizawa, M,, Goto, A., and Watanabe, Y., 2005. The tobacco ubiquitin-activating enzymes NtE1A and NtE1B are induced by tobacco mosaic virus, wounding and stress hormones. Mol. Cells, 19: 228-231.PubMedGoogle Scholar
  216. Tamaoki, M., Nakajima, N., Kubo, A., Aono, M., Matsuyama, T., and Saji, H., 2003. Transcriptome analysis of O3-exposed Arabidopsis reveals that multiple signal pathways act mutually antagonistically to induce gene expression. Plant Mol. Biol., 53: 443-456.PubMedGoogle Scholar
  217. Tang, D. Z., Christiansen, K. M., and Innes, R. W., 2005, Regulation of plant disease resistance, stress responses, cell death, and ethylene signaling in Arabidopsis by the EDR1 protein kinase. Plant Physiol., 138: 1018-1026.PubMedGoogle Scholar
  218. Tapia, G, Verdugo, I, Yanez, M., Ahumada, I., Theoduloz, C., Cordero, C., Poblete, F., Gonzalez, E., and Ruiz-Lara, S., 2005. Involvement of ethylene in stress-induced expression of the TLC1.1 retrotransposon from Lycopersicon chilense Dun. Plant Physiol., 138: 2075-2086.PubMedGoogle Scholar
  219. Tari, I., Csiszár, J., Szalai, G., Horváth, F., Pécsváradi, A., Kiss, G., Szepesi, Á., Szabó, M., and Erdei, L., 2002. Acclimation of tomato plants to salinity stress after a salicylic acid pre-treatment. Acta. Biol. Szegediensis, 46: 55-56.Google Scholar
  220. Tari, I., Simon, L. M., Deér, K. A., Csiszár, J., Bajkán, Sz., Kis, Gy., and Szepesi, Á., 2004. Influence of salicylic acid on salt stress acclimation of tomato plants: oxidative stress responses and osmotic adaptation. Acta Physiol. Plant., 26S: 237.Google Scholar
  221. Tasgin, E., Atici, O., and Nalbantoglu, B. 2003. Effects of salicylic acid and cold on freezing tolerance in winter wheat leaves. Plant Growth Regul., 41: 231-236.Google Scholar
  222. Urao, T., Yamaguchi-Shinozaki, K., Urao, S. and Shinozaki, K., 1993. An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell, 5: 1529–1539.PubMedGoogle Scholar
  223. Vacchina, V, Mari, S., Czernic, P., Marqués, L., Pianelli, K., Schaumlöffel, D., Lebrun, M., and Lobinski, R., 2003. Speciation of nickel in a hyperaccumulating plant by high-performance liquid chromatography-inductively coupled plasma mass spectroscopy and electrospray MS/MS assisted by cloning using yeast complementation. Anal. Chem., 75: 2740–2745.PubMedGoogle Scholar
  224. Van Camp, W., Van Montagu, M., and Inzé, D. 1998. H2O2 and NO: redox signals in disease resistance. Trends Plant Sci., 3: 330-334.Google Scholar
  225. Vandeventer, H. A., 1985. Cyanide-resistant respiration and cold resistance in seedlings of maize (Zea Mays L.). Ann. Bot., 56: 561-563.Google Scholar
  226. Van Wees, S. C. M., and Glazebrook, J., 2003. Loss of non-host resistance of Arabidopsis NahG to Pseudomonas syringae pv. Phaseolicola is due to degradation products of salicylic acid. Plant J., 33: 733-742.PubMedGoogle Scholar
  227. Vernooij, B., Friedrich, L., Morse, A., Reist, R., Kolditz-Jawhar, R., Ward, E., Uknes, S., Kessmann, H., and Ryals, J. 1994. Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell, 6: 959-965.PubMedGoogle Scholar
  228. Vierling, E., 1991. The roles of heat shock proteins in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol., 42: 579–620.Google Scholar
  229. Vranová, E., Atichartpongkul, S., Villarroel, R., Van Montagu, M., Inze, D., and Van Camp, W., 2002. Comprehensive analysis of gene expression in Nicotiana tabacum leaves acclimated to oxidative stress. Proc. Natl. Acad. Sci. USA, 99: 10870–10875.PubMedGoogle Scholar
  230. Wang, S. J. Lan, Y. C., Chen, S. F., Chen, Y. M., and Yeh, K. W., 2002. Wound-response regulation of the sweet potato sporamin gene promoter region. Plant Mol. Biol., 48: 223-231.PubMedGoogle Scholar
  231. Watahiki, M. K., Mori, H., and Yamamoto, K. T., 1995. Inhibitory effects of auxins and related substances on the activity of an Arabidopsis glutathione S-transferase isozyme expressed in Escherichia coli. Physiol. Plant., 94: 566-574.Google Scholar
  232. Wiese, J., Kranz, T., and Schubert, S., 2004. Induction of pathogen resistance in barley by abiotic stress. Plant Biol., 6: 529-536.PubMedGoogle Scholar
  233. Wildermuth, M. C. Dewdney, J., Wu, G., and Ausube, F. M., 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature, 414: 562–565PubMedGoogle Scholar
  234. Xue, G.-P., 2002. An AP2 domain transcription factor HvCBF1 activates expression of cold-responsive genes in barley through interaction with a (G/a)(C/t)CGAC motif. Biochim. Biophys. Acta, 1577: 63–72.PubMedGoogle Scholar
  235. Xue, G.-P., 2003. The DNA-binding activity of an AP2 transcriptional activator HvCBF2 involved in regulation of low-temperature responsive genes in barley is modulated by temperature. Plant J., 33: 373–383.PubMedGoogle Scholar
  236. Yalpani, N., Silverman, P., Wilson, T. M. A., Kleier, D. A., 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.PubMedGoogle Scholar
  237. Yalpani, N., Leon, J., Lawton, M. A., and Raskin, I., 1993. Pathway of salicylic acid biosynthesis in healthy and virus-inoculated tobacco. Plant Physiol., 103: 315–321.PubMedGoogle Scholar
  238. 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.Google Scholar
  239. Yang, G., and Komatsu, S., 2000. Involvement of calcium-dependent protein kinase in rice (Oryza sativa L.) lamina inclination caused by brassinolide. Plant Cell Physiol., 41: 1243–1250.PubMedGoogle Scholar
  240. Yang, T. B., and Poovaiah, B. W., 2002. A calmodulin-binding/CGCG box DNA-binding protein family involved in multiple signaling pathways in plants. J. Biol. Chem., 277: 45049-45058.PubMedGoogle Scholar
  241. Yang, Z. M., Wang, J., Wang, S. H., and Xu, L. L., 2003. Salicylic acid-induced aluminium tolerance by modulation of citrate efflux from roots of Cassia tora L. Planta, 217: 168-174.PubMedGoogle Scholar
  242. Yoon, G. M., Cho, H. S., Ha, H. J., Liu, J. R., and Lee, H. P., 1999. Characterization of NtCDPK1, a calcium-dependent protein kinase gene in Nicotiana tabacum, and the activity of its encoded protein. Plant Mol. Biol., 39: 991–1001.PubMedGoogle Scholar
  243. Yoon, H. S., Lee, H., Lee, I. A., Kim, K. Y., and Jo, J. K., 2004. Molecular cloning of the monodehydroascorbate reductase gene from Brassica campestris and analysis of its mRNA level in response to oxidative stress. Biochim. Biophys. Acta, 1658: 181-186.PubMedGoogle Scholar
  244. Yordanova, R. Y., Christov, K. N., and Popova, L. P., 2004. Antioxidative enzymes in barley plants subjected to soil flooding. Environ. Exp. Bot., 51: 93-101.Google Scholar
  245. Yu, X.-M., Griffith, M., and Wiseman, S. B., 2001. Ethylene induces antifreeze activity in winter rye leaves. Plant Physiol., 126: 1232-1240.PubMedGoogle Scholar
  246. Zamski, E., Guo, W. W., Yamamoto, Y. T., Pharr, D. M., and Williamson, J. D., 2001. Analysis of celery (Apium graveolens) mannitol dehydrogenase (Mtd) promoter regulation in Arabidopsis suggests roles for MTD in key environmental and metabolic responses. Plant Mol. Biol., 47: 621-631.PubMedGoogle Scholar
  247. Zhang, S., and Klessig, D. F., 1997. Salicylic Acid Activates a 48-kD MAP Kinase in Tobacco Plant Cell, 9: 809-824.PubMedGoogle Scholar
  248. Zhang, S. Q., and Klessig, D. F., 1998. The tobacco wounding-activated mitogen-activated protein kinase is encoded by SIPK. Proc. Natl. Acad. Sci. USA., 95: 7225-7230.PubMedGoogle Scholar
  249. Zhang, H. B., Zhang, D. B., Chen, J., Yang, Y. D., Huang, Z. J., Huang, D. F., Wang, X. C., and Huang, R. F., 2004. Tomato stress-responsive factor TSRF1 interacts with ethylene responsive element GCC box and regulates pathogen resistance to Ralstonia solanacearum. Plant Mol. Biol., 55: 825-834.PubMedGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • T. Janda
    • 1
  • E. Horváth
    • 1
  • G. Szalai
    • 1
  • E. PáLdi
    • 1
  1. 1.Agricultural Research Institute of the Hungarian Academy of SciencesMartonvásárHungary

Personalised recommendations