Salicylic acid as a defense-related plant hormone roles of oxidative and calcium signaling paths in salicylic acid biology

Salicylic Acid: A Plant Hormone

Volumn , Issue , 2007, Pages 277-321

  Kawano, Tomonori ^a   Furuichi, Takuya ^b  

^a UNIVERSITY OF KITAKYUSHU   (Japan)

^b NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Calcium; gene expression; plant defense; reactive oxygen species; salicylic acid; signal transduction

Indexed keywords

EID: 84920066935     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/1-4020-5184-0_10     Document Type: Chapter

References (181)

1. Alayash, A. I., 1999. Hemoglobin-based blood substitutes: oxygen carriers, pressor agents, or oxidants?. Nat. Biotechnol., 17: 545-549.
2. Alvarez, M. E., 2000. Salicylic acid in the machinery of hypersensitive cell death and disease resistance. Plant Mol. Biol., 44: 429-442.
3. 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.
4. Antoniw, J. F., and White, R. F., 1980. The effects of aspirin and polyacrylic acid on soluble leaf proteins and resistance to virus infection in five cultivars of tobacco. Phytopath. Z., 98: 331-341.
5. Apel, K., and Hirt, H., 2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol., 55: 373-399.
6. Arabidopsis Genome Initiative, 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408: 796-815.
7. Aubin, N., Curet, O., Deffois, A., and Carter, C., 1998. Aspirin and salicylate protect against MPTP-induced dopamine depletion in mice. J. Neurochem., 71: 1635-1642.
8. 2-producing xylem of Zinna elegans. J. Plant Res., 112: 383-390.
9. Bolwell, G. P., Bindschedler, L. V., Blee, K. A., Butt, V. S., Davies, D. R., Gardner, S. L., Gerrish, C., and Minibayeva, F., 2002. The apoplastic oxidative burst in response to biotic stress in plants: A three-component system. J. Exp. Bot., 53: 1367-1376.
10. Cao, H., Bowling, S. A., Gordon, A. S., and Dong, X., 1994. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell, 6: 1583-1592.
11. 2+-pectate binding site on an apoplastic peroxidase. Plant Cell, 13: 511-520.
12. 2+-independent excretion modes of salicylic acid in tobacco cell suspension culture. J. Exp. Bot. 52: 1219- 1226.
13. Chen, H-J., Hou, W.-C., Kuc, J., and Lin, Y.-H., 2002. Salicylic acid mediates alternative signal transduction pathways for pathogenesis-related acidic β-1, 3-glucanase (protein N) induction in tobacco cell suspension culture. J. Plant Physiol., 159: 331-337.
14. 2+-dependent excretion of salicylic acid in tobacco cell suspension culture. Botanic. Bul. Acad. Sinica, 40: 267-273.
15. Chen, Z., Ricigliano, J. R., and Klessig, D. F., 1993a. Purification and characterization of soluble salicylic acid binding protein from tobacco. Proc. Natl. Acad. Sci. USA., 90: 9533- 9537.
16. Chen, Z., Silva, H., and Klessig, D. F., 1993b. Active oxygen species in the induction of plant systemic acquired resistance induced by salicylic acid. Science, 262: 1883-1886.
17. Christiane, N., and Métraux, J.-P., 2002. Towards the elucidation of the pathway leading to salicylic acid biosynthesis. Biol. Plant-Microbe Interact., 3: 64-71.
18. Clarke, J. D., Volko, S.M., Ledford, H., Ausubel, F. M., and Dong, X., 2000. Roles of salicylic acid, jasmonic acid, and ethylene in cpr-induced resistance in Arabidopsis. Plant Cell, 12: 2175-2190.
19. Conrath, U., Chen, Z., Ricigliano, J. R., and Klessig, D. F., 1995. Two inducers of plant defense response, 2, 6-dichloroisonicotinic acid and salicylic acid, inhibit catalase activities in tobacco. Proc. Natl. Acad. Sci. USA., 92: 7143-7147.
20. Delaney, T. P., 2004. Salicylic acid, in: Plant hormones. Biosynthesis, signal transduction, action!, Davies, P. J. (Ed.) Kluwer Academic Publishers, Dordrecht, Boston, London, pp. 635-653.
21. Delaney, T. P., Friedrich, L., and Ryals, J. A., 1995. Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc. Natl. Acad. Sci. USA., 92: 6602-6606.
22. Després, C., Chubak, C., Rochon, A., Clerk, R., Bethune, T., Desvwaux, D., and Fobert, P. R., 2003. The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1. Plant Cell, 15: 2181-2191.
23. Devoto, A., Nieto-Rosto, M., Xie, D. X., Dllis, C., Harmston, R., Patrick, E., Davis, J., Sherratt, L., Coleman, M., and Turner, J. G., 2002. COI1 links jasmonate signaling and fertility to the SCF ubiquitin-ligase complex in Arabidopsis. Plant J., 32: 457-466.
24. Du, H. and Klessig, D. F., 1997. Identification of a soluble, high-affinity salicylic acidbinding protein in tobacco. Plant Physiol., 113: 1319-1327.
25. 2+/calmodulin-binding protein involved in transcriptional regulation: Interaction with fsh/Ring3 class transcription activators. Plant Mol. Biol., 54: 549-569.
26. Durner, J., and Klessig, D. F., 1995. Inhibition of ascorbate peroxidase by salicylic acid and 2, 6-dichloroisonicotinic acid, two inducers of plant defense responses. Proc. Natl. Acad. Sci. USA., 92: 11312-11316.
27. Durner, J., and Klessig, D. F., 1996. Salicylic acid is a modulator of tobacco and mammalian catalases, J. Biol. Chem., 272: 28492-28501.
28. Eckardt, N. E., 2003. A new twist on systemic acquired resistance: Redox control of the NPR1-TGA1 interaction by salicylic acid. Plant Cell, 15: 1947-1949.
29. Effmert, U., Saschenbrecker, S., Ross, J., Negre, F., Fraser, C. M., Noel, J. P., Dudareva, N., and Piechulla, B., 2005. Floral benzenoid carboxyl methyltransferases: from in vitro to in planta function. Phytochem., 66: 1211-1230.
30. Ellis, J., Dodds, P., and Pryor, T., 2000. Structure, function and evolution of plant disease resistance genes. Curr. Opin. Plant Biol., 3: 278-284.
31. +-linked transport of salicylic acid, an NSAID, in the human trophoplast cell line BeWo. Amer. J. Physiol., 282: C1064-C1075.
32. Enyedi, A. J., and Raskin, I., 1993. Induction of UDP-glucose:salicylic acid glucosyltransferase activity in tobacco mosaic virus-inoculated tobacco (Nicotiana tabacum) leaves. Plant Physiol., 101: 1375-1380.
33. 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.
34. Fan, W., and Dong, X., 2002. In vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid-mediated gene activation in Arabidopsis. Plant Cell, 14: 1377-1389.
35. Fell, H. H., Honstein, S., Steinmeyer, R., and Hedrich, R., 2000. Dynamics of ionic activities in the apoplast of the sub-stomatal cavity of intact Vicia faba leaves during stomatal closure evoked by ABA and darkness. Plant J., 24: 297-304.
36. Feys, B. J., Moisan, L. J., Newman, M.-A., and Parker, J. E., 2001. Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO J., 20: 5400-5411.
37. Fobert, P.R., and Després, C., 2005. Redox control of systemic acquired resistance. Curr. Opin. Plant Biol., 8: 378-382.
38. Forouhar, F., Yang, Y., Kumar, D., Chen, Y., Fridman, E., Park, S. W., Chiang, Y., Acton, T. B., Montelione, G. T., Pichersky, E., Klessig, D. F., and Tong, L., 2005. Structural and biochemical studies identify tobacco SABP2 as a methyl salicylate esterase and implicate it in plant innate immunity. Proc. Natl. Acad. Sci. USA., 102: 1773-1778.
39. Friedrich, L., Vernooij, B., Gaffney, T., Morse, A., and Ryals, J., 1995. Characterization of tobacco plants expressing a bacterial salicylate hydroxylase gene. Plant Mol Biol., 29: 959-968.
40. Fukami, H., Asakura, T., Hirano, H., Abe, K., Shimomura, K., and Yamakawa, T., 2002. Salicylic acid carboxyl methyltransferase induced in hairy root cultures of Atropa belladonna after treatment with exogeneously added salicylic acid. Plant Cell Physiol., 43: 1054-1058.
41. 2+ flux in Arabidopsis leaf cells. Plant Cell Physiol., 42: 900-905.
42. Garreton, 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.
43. Gozzo, F., 2003. Systemic acquired resistance in crop protection: from nature to a chemical approach. J. Agric. Food Chem., 51: 4487-4503.
44. Grootveld, M., and Halliwell, B., 1986. Aromatic hydroxylation as a potential measure of hydroxyl-radical formation in vivo. Identification of hydroxylated derivatives of salicylate in human body fluids. Biochem. J., 273: 499-504.
45. Gupta, R., and Luan, S., 2003. Redox control of protein tyrosine phosphatases and mitogenactivated protein kinases in plants. Plant Physiol., 132: 1149-1152.
46. Halliwell, B., Kaur, H., and Ingelman-Sundberg, M., 1991. Hydroxylation of salicylate as an assay for hydroxyl radicals: A cautionary note. Free Radical Biol. Med., 10: 439-441.
47. 2+ channel, OsTPC1, expressed in yeast cells lacking its homologous gene CCH1. Plant Cell Physiol., 45: 496-500.
48. 2+ and nucleotide dependent regulation of voltage dependent anion channels in the plasma membrane of guard cells. EMBO J., 9: 3889-3092.
49. Hennig, J., Malamy, J., Grynkiewicz, G., Indulski, J., and Klessig, D. F., 1993. Interconversion of the salicylic acid signal and its glucoside in plants. Plant J., 4: 593-600.
50. Heo, W. D., Lee, S. H., Kim, M. C., Chung, W. S., Chun, H. J., Lee, K. J., Park, C. Y., Park, H. C., Choi, J. H., and Cho, M. J., 1999. Involvement of specific calmodulin isoforms in salicylic acid-independent activation of plant disease resistance responses. Proc. Natl. Acad. Sci. USA., 96: 766-771.
51. 2+ signaling in plants. Annu. Rev. Plant Biol., 55: 401-427.
52. Hiraga, S., Sasaki, k., Ito, H., Ohashi, Y., and Matsui, H., 2001. A large family of class III plant peroxidases. Plant Cell Physiol., 42: 462-468.
53. Howes, B.D., Feis, A., Raimondi, L., Indiani, C., and Smulevich, G., 2001. The critical role of the proximal calcium ion in the structural properties of horseradish peroxidase. J. Biol. Chem., 276: 40704-40711.
54. Hunt, M. D, Neuenschwander, U. H., Delaney, T. P., Weymann, K. B., Friedrich, L. B., Lawton, K. A., Steiner, H. Y., and Ryals, J. A., 1996. Recent advances in systemic acquired resistance research - A review. Gene, 179: 89-95.
55. Ingelman-Sundberg, M., Kaur, H., Terelius, Y., Persson, J. O., and Halliwell, B., 1991. Hydroxylation of salicylate by microsomal fractions and cytochrome P-450. Lack of production of 2, 3-dihydroxybenzoate unless hydroxyl radical formation is permitted. Biochem. J., 276: 753-757.
56. Ishibashi, K., Suzuki, M., and Imai, M., 2000. Molecular cloning of a novel form (two-repeat) protein related to voltage-gated sodium and calcium channels. Biochem. Biophys. Res. Commun., 270: 370-376.
57. Johnson, C., Boden, E., and Arias, J., 2003. Salicylic acid and NPR1 induce the recruitment of trans-activation TGA factors to a defense gene promoter in Arabidopsis. Plant Cell, 15: 1846-1858.
58. 2+ transients and defense responses in tobacco BY-2 cells. Biochem. Biophys. Res. Commun., 317: 823-830.
59. Katou, S., Karita, E., Yamakawa, H., Seo, S., Mitsuhara, I., Kuchitsu, K., and Ohashi, Y., 2005. Catalytic activation of the plant MAPK phosphatase NtMKP1 by its physiological substrate salicylic acid-induced protein kinase but not by calmodulins, J. Biol. Chem., 280: 39569-39581.
60. Katou, S., Yamamoto, H., Yoshioka, H., Kawakita, K., and Doke, N., 2003. Functional analysis of potato mitogen-activated protein kinase kinase, StMEK1. J. Gen. Plant Pathol., 69: 161-168.
61. Kawano, T., 2003. Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Rep., 21: 829-837.
62. Kawano, T., Kawano, N., and Lapeyrie, F., 2002d. A fungal auxin antagonist, hypaphorine prevents the indole-3-acetic acid-dependent irreversible inactivation of horseradish peroxidase: inhibition of Compound III-mediated formation of P-670. Biochem. Biophys. Res. Commun., 294: 553-559.
63. Kawano, T., Furuichi, T., and Muto, S., 2004b. Controlled free salicylic acid levels and corresponding signaling mechanisms in plants. Plant Biotech., 21: 319-335.
64. 2+ channels. Biochem. Biophys. Res. Commun., 324: 40-45.
65. Kawano, T., Kadono, T., Furuichi, T., Muto, S., and Lapeyrie, F., 2003. Aluminum-induced distortion in calcium signaling involving oxidative bursts and channel regulations in tobacco BY-2 cells. Biochem. Biophys. Res. Commun., 308: 35-42.
66. Kawano, T., Kawano, N., Hosoya, H., and Lapeyrie, F., 2001. Fungal auxin antagonist hypaphorine competitively inhibits indole-3-acetic acid-dependent superoxide generation by horseradish peroxidase. Biochem. Biophys. Res. Commun., 288: 546-551.
67. Kawano, T., and Muto, S., 2000. Mechanism of peroxidase actions for salicylic acid-induced generation of active oxygen species and an increase in cytosolic calcium in tobacco suspension culture. J. Exp. Bot., 51: 685-693.
68. Kawano, T., Muto, S., Adachi, M., Hosoya, H., and Lapeyrie, F., 2002a. Spectroscopic evidence that salicylic acid converts a temporal inactive form of horseradish peroxidase (Compound III) to the irreversibly inactivated verdohemoprotein (P-670). Biosci. Biotech. Biochem., 66: 646-650.
69. Kawano, T., Muto, S., Adachi, M., Hosoya, H., and Lapeyrie, F., 2002b. Spectroscopic evidence in support of horseradish peroxidase Compound II-catalyzed oxidation of salicylic acid but not of phenylethylamine. Biosci. Biotech. Biochem., 66: 651-654.
70. Kawano, T., Pinontoan, R., Hosoya, H., and Muto, S., 2002c. Monoamine-dependent production of reactive oxygen species catalyzed by pseudoperoxidase activity of human hemoglobin. Biosci. Biotech. Biochem., 66: 1224-1232.
71. Kawano, T., Sahashi, N., Takahashi, K., Uozumi, N., and Muto, S., 1998. Salicylic acid induces extracellular generation of superoxide followed by an increase in cytosolic calcium ion in tobacco suspension culture: The earliest events in salicylic acid signal transduction. Plant Cell Physiol., 39: 721-730.
72. Kawano, T., Tanaka, S., Kadono, T., and Muto, S., 2004a. Salicylic acid glucoside acts as a slow inducer of oxidative burst in tobacco suspension culture. Z. Naturforsch., 59: 684-692.
73. Keller, H., Hohlfeld, H., Wray, V., Hahlbrock, K., Scheel, D., and Strack, D., 1996. Changes in the accumulation of soluble and cell wall-bound phenolics in elicitor-treated cell suspension culture and fungus-infected leaves of Solanum tuberosum. Phytochem., 42: 389-396.
74. 2+ binding motifs. Plant Cell, 10: 255-266.
75. Kessmann, H., and Ryals, J., 1993. Requirement of salicylic acid for the induction of systemic acquired resistance. Science, 261:754-756.
76. Klick, S., and Herrmann, K., 1988. Glucosides and glucose esters of hydroxybenzoic acids in plants, Phytochem., 27: 2127-2180.
77. Knight, M. R., Campbell, A. K., Smith, S. M., and Trewavas, A. J., 1991. Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytosolic calcium. Nature, 352: 524-526.
78. Kumar, D., and Klessig, D. F., 2003. High-affinity salicylic acid-binding protein 2 is required for plant innate immunity and has salicylic acid-stimulated lipase activity. Proc. Natl. Acad. Sci. USA., 100: 16101-16106.
79. Kunkel, B. N., and Brooks, D. M., 2002. Cross talk between signaling pathways in pathogen defense, Curr. Opin. Plant Biol., 5: 325-331.
80. 2+ influx and regulation of growth and development in rice. Plant Cell Physiol., 45: 693-702.
81. Kvaratskhelia, M., George, S. J., and Thorneley, R. N. F., 1997. Salicylic acid is a reducing substrate and not an effective inhibitor of ascorbate peroxidase. J. Biol. Chem., 272: 20998-21001.
82. Laberge, M., Huang, Q., Schweitzer-Stenner, R., and Fidy, J., 2003. The endogenous calcium ions of horseradish peroxidase C are required to maintain the functional nonplanarity of the heme. Biophys. J., 84: 2542-2552.
83. Lee, J.-S., 1998. The mechanism of stomatal closing by salicylic acid in Commelina communis L. J. Plant Biol., 41: 97-102.
84. Léon, J., Yalpani, N., Raskin, I., and Lawton, M. A., 1993. Induction of benzoic acid 2- hydroxylase in virus-inoculated tobacco. Plant Physiol., 103: 323-328.
85. Lieberherr, D., Wagner, U., Dubis, P.-H., Métraux, J.-P., and Mauch, F., 2003. The rapid induction of glutathione S-transferases AtGSTF2 and AtGSTF6 by Avirulent Pseudomonas syringae is the result of combined salicylic acid and ethylene signaling. Plant Cell Physiol., 44: 750-757.
86. Lin, C., Yu, Y., Kadono, T., Iwata, M., Umemura, K., Furuichi, T., Kuse, M., Isobe, M., Yamamoto, Y., Mastumoto, H., Yoshizuka, K., and Kawano, T., 2005. Action of aluminum, novel TPC1-type channel inhibitor, against salicylate-induced and cold shockinduced calcium influx in tobacco BY-2 cells. Biochem. Biophys. Res. Commun., 332: 823-830.
87. Longu, S., Medda, R., Padiglia, A., Pedersen, J. Z., and Floris, G., 2004. The reaction mechanism of plant peroxidases. Ital. J. Biochem., 53: 41-45.
88. 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.
89. Malamy, J., Hennig, J., and Klessig, D. F., 1992. Temperature-dependent induction of salicylic acid and its conjugates during the resistance response to tobacco mosaic virus infection. Plant Cell, 4: 359-366.
90. Manthe, B., Schulz, M., and Schnable, H., 1992. Effects of salicylic acid on growth and stomatal movement on Vicia faba L.: evidence for salicylic acid metabolism. J. Chem. Ecol., 18: 1525-1539.
91. Mauch, F., Mauch-Mani, B., Gaille, C., Kull, B., Haas, D., and Reimmann, C., 2001. Manipulation of salicylic acid content in Arabidopsis thaliana by the expression of an engineered bacterial salicylate synthase. Plant J., 25: 67-77.
92. Mauch-Mani, B., and Sulsarenko, A. J., 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.
93. 2+ ions in the reaction mechanism of Euphorbia characias peroxidase. Biochem., 42: 8909-8918.
94. Mercado-Blanco, J., van der Drift, K. M. G. M., Olson, P. E., Thomas-Oates, J., van Loon, L. C., and Bakker, P. A. H. M., 2001. Analysis of the pmsCEAB gene cluster involved in biosynthesis of salicylic acid and the siderophore pseudomonine in the biocontrol strain Pseudomonas fluorescens WCS374. J. Bacteriol., 183: 1909-1920.
95. Messner, B., and Schroder, P., 1999. Burst amplifying system in cell suspension cultures of spurs (Pices abies). Modulation of elicitor-induced release of hydrogen peroxidase (oxidative burst) by ionophores and salicylic acid. J. Appl. Bot., 73: 6-10.
96. Métraux, J.-P., 2002. Recent breakthrough in the study of salicylic acid biosynthesis. Tren. Plant Sci., 7: 332-334.
97. 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.
98. Midoh, N., and Iwata, M., 1996. Cloning and characterization of a probenazole-inducible gene for an intracellular pathogenesis-related protein in rice. Plant Cell Physiol., 37: 9-18.
99. Miyake, C., Sano, S., and Asada, K., 1996. A new assay of ascorbate peroxidase using the coupled system with monodehydroascorbate radical reductase. in: Plant Peroxidases: Biochemistry and Physiology, Obinger, C., Burner, U., Ebermann, R., Penel, C., Greppin., eds, Univ. Geneva, Vienna. pp. 386-389.
100. Mori, I. C., Pinontoan, R., Kawano, T., and Muto, S., 2001. Involvement of superoxide generation in salicylic acid-induced stomatal closure in Vicia faba. Plant Cell Physiol., 42: 1383-1388.
101. 2+ channels. A signaling mechanism in polar growth, hormone transduction, stress signaling, and hypothetically mechanotransduction. Plant Physiol., 135: 702-708.
102. Mou, Z., Fan, W. H., and Dong, X., 2003. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell, 113: 935-944.
103. 2+/calmodulin-binding peroxidase from Euphorbia latex: Nobel aspects of calciumhydrogen peroxidase cross-talk in the regulation of plant defenses. Biochem., 44: 14120- 14130.
104. 2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi-1 and abi-2 protein phosphatase 2C mutants. Plant Cell, 13: 2513-2523.
105. Muto, S., and Miyachi, S., 1977. Properties of a protein activator of NAD kinase from plants. Plant Physiol., 59: 55-60.
106. Mölders, W., Buchala, A., and Métraux, J.-P., 1996. Transport of salicylic acid in tobacco necrosis virus-infected cucumber plants. Plant Physiol., 112: 787-792.
107. Niederl, S., Kirsch, T., Riederer, M., and Schreiber, L., 1998. Co-permeability of 3H-labeled water and 14C-labeled organic acids across isolated plant cuticles. Plant Physiol., 116: 117-123.
108. 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.
109. Ohashi, Y., Murakami, T., Mitsuhara, I., and Seo, S., 2004. Rapid down and upward translocation of salicylic acid in tobacco plants. Plant Biotech., 21: 95-101.
110. Passardi, F., Cosio, C., Penel, C., and Dunand, C., 2005. Peroxidases have more functions than a Swiss army knife. Plant Cell Rep., 24: 255-265.
111. Pei, Z. M., Murata, Y., Benning, G., Thomine, S., Klusener, B., Allen, G. J., Grill, E., and Schroeder, J. I., 2000. Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells. Nature, 406: 731-734.
112. 2+-activated channel TPC1 regulates germination and stomatal movement. Nature, 434: 404-408.
113. Penel, C., 2000. The peroxidase system in higher plants, in: Integrated Plant Systems, Greppin, H., Penel, C., Broughton, W. J. and Strasser, R., eds, Univ. Geneva, Geneva, pp. 359-367.
114. Penel, C., Gasper, T., and Greppin, H., 1992. Plant peroxidases 1980-1990, Univ. Geneva, Geneva.
115. Pfeiffer, W., and Hoftberger, M., 2001. Oxidative burst in Chenopodium rubrum suspension cells: Induction by auxin and osmotic changes. Physiol. Plant., 111:144-150.
116. Pieterse, C. M. J., and van Loon, L. C., 2004. NPR1: the spider in the web of induced resistance signaling pathways. Cur. Opin. Plant Biol., 7:456-464.
117. Pott, M. B., Effmert, U., and Piechulla, B., 2003. Transcriptional and post-translational regulation of S-adenosyl-L-methionine: salicylic acid carboxyl methyltransferase (SAMT) during Stephanotis floribunda flower development. J. Plant Physiol., 160: 635-643.
118. Pott, M. B., Hippauf, F., Saschenbrecker, S., Chen, F., Ross, J., Kiefer, I., Slusarenko, A., Noel, J. P., Pichersky, E., Effmert, U., and Piechulla, B., 2004. Biochemical and structural characterization of benzenoid carboxyl methyltransferases involved in floral scent production in Stephanotis floribunda and Nicotiana suaveolens. Plant Physiol., 135: 1946- 1955.
119. Qin, X. F., Holuigue, L., Horvath, D. M., and Chua, N. H., 1994. Immediate early transcription activation by salicylic acid via the cauliflower mosaic virus as-1 element. Plant Cell, 6: 863-874.
120. Rainsford, D. K., 1984. Aspirin and Salicylates. Butterworth, London.
121. Ramakrishna, W., Emberton, J., SanMiguel, P., Ogden, M., Llaca, V., Messing, J., and Bennetzen, J. L., 2002. Comparative sequence analysis of the sorghum Rph region and the maize Rp1 resistance gene complex. Plant Physiol., 130: 1728-1738.
122. Raskin I., 1995. Salicylic acid. In: Plant Hormone, 2nd Ed., Davies, P. J. (Ed.), Kluwer Academic Press, Dordrecht. pp. 188-205.
123. Rasmussen, J. B., Hammerschmidt, R., and Zook, M. N., 1991. Sytemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv. Syringae. Plant Physiol., 97:1342-1347.
124. Raz, V., and Fluhr, R., 1992. Calcium requirement for ethylene-dependent responses. Plant Cell, 4: 1123-1130.
125. Ren, D., Yang, H., and Zhang, S., 2002. Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J. Biol. Chem., 277: 559-565.
126. Rhoads, D. M., and McIntosh, L., 1992. Salicylic acid regulation of respiration in higher plants: A lternative oxidase expression. Plant Cell, 4: 1131-1139.
127. Sagi, M., and Fluhr, R., 2001. Superoxide production by plant homologues of the gp91phox NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol., 126: 1281-1290.
128. Sagone, A. L., and Husney, R. M., 1987. Oxidation of salicylates by stimulated granulocytes: evidence that these drugs act as free radical scavengers in biological systems. J. Immunol., 138: 2127-2183.
129. Samuel, M. A., Hall, H., Krzymowska, M., Drzewiecka, K., Hennig, J., and Ellis, B.E., 2005b. SIPK signaling controls multiple components of harpin-induced cell death in tobacco. Plant J., 42: 406-416.
130. Samuel, M. A., Walia, A., and Mansfield, S. D., 2005a. Overexpression of SIPK in tobacco enhances ozone-induced ethylene formation and blocks ozone-induced SA accumulation. J. Exper. Bot., 56: 2195-2201.
131. Sanders, D., Brownlee, C., and Harper, J. F., 1999. Communicating with calcium. Plant Cell, 11: 691-706.
132. Sanders, D., Pelloux, J., Brownlee, C., and Harper, J. F., 2002. Calcium at the crossroads of signaling. Plant Cell, 14: 401-417.
133. 2+ in the induction of chitinase activity in carrot suspension culture. Physiol. Mol. Plant Pathol., 45: 101-109.
134. Seo, S., Ichizawa, K., and Ohashi, Y., 1995. Induction of salicylic acid-β-glucosidase in tobacco leaves by exogenous salicylic acid. Plant Cell Physiol., 36: 447-453.
135. Serino, L., Reimmann, C., Baur, H., Beyeler, M., Visca, P., and Haas, D., 1995. Structural genes for salicylate biosynthesis from chorismate in Pseudomonas aeruginosa. Mol. Gen. Genet., 249: 217-228.
136. Shah, J., 2003. The salicylic acid loop in plant defense. Curr. Opin. Plant Biol., 6: 365-371.
137. Shah, J., Kachroo, P., and Klessig, D. F., 1999. The Arabidopsis ssi1 mutation restores pathogenesis-related gene expression in npr1 plants and renders Defensin gene expression SA dependent. Plant Cell, 11: 191-206.
138. Shah, J., Tsui, F., and Klessig, D. F., 1997. Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SAinducible expression of the tms2 gene. Mol. Plant Microbe Interact., 10: 69-78.
139. 2+-pectate binding peroxidase from Arabidopsis leaves. Phytochem., 65: 307-312.
140. Shirano, Y., Kachroo, P., Shah, J., and Klessig, D. F., 2002. A gain-of-function mutation in an Arabidopsis toll interleukin 1 receptor-nucleotide binding site-leucine-rich repeat type R gene triggers defense responses and results in enhanced disease resistance. Plant Cell, 14: 3149-3162.
141. Shulaev, V., Leon, J., and Raskin, I., 1995. Is salicylic acid a translocated signal of systemic acquired resistance in tobacco? Plant Cell, 7: 1691-1701.
142. Shulaev, V., Silverman, P., and Raskin, I., 1997. Airborne signalling by methyl salicylate in plant pathogen resistance. Nature, 385: 718-721.
143. Singh, D. P., Moore, C. A., Gilliland, A., and Carr, J. P., 2004. Activation of multiple antiviral defense mechanisms by salicylic acid. Mol. Plant Pathol., 5: 57-63.
144. Slaymaker, D. H., Navarre, D. A., Clark, D., Del Pozo, O., Martin, G. B., and Klessig, D. F., 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.
145. Song, F., and Goodman, R.M., 2002. OsBIMK1, a rice MAP kinase gene involved in disease resistance responses. Planta, 215: 997-1005.
146. Spoel, S. H., Koornneef, A., Claessens, S. M., Korzelius, J. P., Van Pelt, J.A., Mueller, M. J., Buchala, A. J., Metraux, J. P., Brown, R., Kazan, K., Van Loon, L. C., Dong, X., and Pieterse, C. M., 2003. NPR1 modulates cross-talk between salicylate- And jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell, 15: 760-770.
147. Sticher, L., Mauch-Mani, B., and Metraux, J. P., 1997. Systemic acquired resistance. Annu. Rev. Phytopath., 35: 235-270.
148. Sticher, L., Penel, C., and Greppin, H., 1981. Calcium requirement for the secretion of peroxidases by plant cell suspensions. J. Cell Sci., 48: 345-353.
149. Tenhaken, R., and Rübel, 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.
150. Torres, M. A., Onouchi, H., Hamada, S., Machida, C., Hammond-Kosack, K. E., and Jones, J. D., 1998. Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox). Plant J., 14: 365-370.
151. Turner, J.G., Ellis, C., and Devoto, A., 2002. The jasmonate signal pathway. Plant Cell, 14: S153-S164.
152. Ulm, R., Ichimura, K., Mizoguchi, T., Peck, S.C., Zhu, T., Wang, X., Shinozaki, K., and Paszkowski, J., 2002. Distinct regulation of salinity and genotoxic stress responses by Arabidopsis MAP kinase phosphatase 1. EMBO J., 21: 6483-6493.
153. Uquillas, C., Letelier, I., Blanco, F., Jordana, X., and Holoigue, L., 2004. NPR1-independent activation of immediate early salicylic acid-responsive genes in Arabidopsis.Mol. Plant- Microbe Interact., 17: 34-42.
154. Utoguchi, N., Watanabe, Y., Takase, Y., Suzuki, T., and Matsumoto, M., 1999. Carriermediated absorption of salicylic acid from hamster cheek pouch mucosa. J. Pharmacol. Sci., 88: 142-146.
155. Van Dongen, J. T., Schurr, U., Pfister, M., and Geigenberger, P., 2003. Phloem metabolism and function have to cope with low internal oxygen. Plant Physiol., 131: 1529-1543.
156. Van Tegelen, L. J., Moreno, P. R., Croes, A. F., Verpoorte, R., and Wullems, G. J., 1999. Purification and cDNA cloning of isochorismate synthase from elicited cell cultures of Catharanthus roseus. Plant Physiol., 119: 705-712.
157. 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.
158. Vane, J. R., and Botting, R. M., 2003. The mechanism of action of aspirin. Thromb. Res., 110: 255-258.
159. Verberne, M. C., Verpoorte, R., Bol, J. F., Mercado-Blanco, J., and Linthorst, H. J., 2000. Overproduction of salicylic acid in plants by bacterial transgenes enhances pathogen resistance. Nature Biotech., 18: 779-783.
160. 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.
161. Ward, E. R., Uknes, S. J., Williams, S. C., Dincher, S. S., Wielderhol, D. L., Alexander, D. C., Ahl-Goy, P., Métraux, J. P., and Ryals, J., 1991. Coodinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell, 3: 1085-1094.
162. Weissman, G., 1991. Aspirin. Sci. Amer., 264: 84-90.
163. White, P. J., Bowen, H. C., Demidchik, V., Nichols, C., and Davies, J. M., 2002. Genes for calcium-permeable channels in the plasma membrane of plant root cells. Biochem. Biophys. Acta, 1564: 299-309.
164. White, R. F., 1979. Acetylsalicylic acid induces resistance to tobacco mosaic virus in tobacco. Virology, 99: 410-412.
165. White-Stevens, R. H., and Kamin, H., 1972. Studies of a flavoprotein, salicylate hydroxylase. J. Biol. Chem., 247: 2358-2370.
166. Wildermuth, M. C., Dewdney, J., Wu, G., and Ausubel, F. M., 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defense. Nature, 414: 562-565.
167. Xiao, S. Y., Ellwood, S., Calis, O., Patrick, E., Li, T. X., Coleman, M., and Turner, J. G., 2001. Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science, 291: 118-120.
168. Xiao, S., Brown, S., Patrick, E., Brearley, C., and Turner, J. G., 2003. Enhanced transcription of the Arabidopsis disease resistance genes RPW8.1 and RPW8.2 via a salicylic aciddependent amplification circuit is required for hypersensitive cell death. Plant Cell, 15: 33-45.
169. Xu, L., Liu, F., Lechner, E., Genschik, P., Crosby, W. L., Ma, H., Peng, W., Huang, D., and Xie, D., 2002. The SCFCOI1 ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell, 14: 1919-1935.
170. Yalpani, N., Siverman, 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.
171. Yamakawa, H., Katou, S., Seo, S., Mitsuhara, I., Kamada, H., and Ohashi, Y., 2004. Plant MAPK phosphatase interacts with calmodulins. J. Biol. Chem., 279: 928-936.
172. Yamakawa, H., Mitsuhara, I., Ito, N., Seo, S., Kamada, H., and Ohashi, Y., 2001. Transcriptionally and post-transcriptionally regulated response of 13 calmodulin genes to tobacco mosaic virus-induced cell death and wounding in tobacco plant. Eur. J. Biochem., 268: 3916-3929.
173. Yang, K. Y., Liu, Y., and Zhang, S., 2001. Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc. Natl. Acad. Sci. USA., 98: 741-746.
174. Yokawa, K. 2005. A computational model of plant signaling mechanism involved in environmental responses: Construction of an artificial plant cell with calcium homeostasis. Abstract book, Xiamen 2005, 2nd International Workshop on Environmental and Metabolic Biochemistry of Plants and Microorganisms, Xiamen Univ., China. pp.24-25.
175. 2 accumulation and resistance to Phytophthora infestans. Plant Cell, 15: 706-718.
176. Yoshioka, H., Sugie, K., Park, H. J., Maeda, H., Tsuda, N., Kawakita, K., and Doke, N., 2001b. Induction of plant gp91phox homolog by fungal cell wall, arachidonic acid, and salicylic acid in potato. Mol. Plant Microbe Interact., 14: 725-736.
177. Yoshioka, K., Nakashita, H., Klessig, D.F., and Yamaguchi, I., 2001a. Probenazole induces systemic acquired resistance in Arabidopsis with a novel type of action. Plant J., 25: 149- 57.
178. Yuasa, T., Ichimura, K., Mizoguchi, T., and Shinozaki, K., 2001. Oxidative stress activates ATMPK6, an Arabidopsis homologue of MAP kinase. Plant Cell Physiol., 42: 1012-1016.
179. Zhang, S., and Liu, Y., 2001. Activation of salicylic acid-induced protein kinase, a mitogenactivated protein kinase, induces multiple defense responses in tobacco. Plant Cell, 13: 1877-1889.
180. Zhang, S., and Klessig., D. F., 1997. Salicylic acid activates a 48-kD MAP kinase in tobacco. Plant Cell, 9: 809-824.
181. Zhang, Y., Fan, W., Kinkema, M., Li, X., and Dong, X., 1999. Interaction of NPR1 with basic leucine sipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proc. Natl. Acad. Sci. USA., 96: 6523-6528.