Salicylic Acid and its Function in Plant Immunity

Journal of Integrative Plant Biology

Volumn 53, Issue 6, 2011, Pages 412-428

  An, Chuanfu ^a   Mou, Zhonglin ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

Crosstalk; NPR1; Plant defense; SA biosensor; Salicylic acid (SA); Systemic acquired resistance

Indexed keywords

PHYTOHORMONE; SALICYLIC ACID;

BIOCHEMISTRY; GENETIC ANALYSIS; IMMUNE RESPONSE; MOLECULAR ANALYSIS; PHENOLIC COMPOUND; PHYSIOLOGICAL RESPONSE; PLANT DEFENSE; SALICYLIC ACID; SIGNALING;

IMMUNOLOGY; METABOLISM; PLANT IMMUNITY; REVIEW; SIGNAL TRANSDUCTION;

PLANT GROWTH REGULATORS; PLANT IMMUNITY; SALICYLIC ACID; SIGNAL TRANSDUCTION;

EID: 79958700714     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/j.1744-7909.2011.01043.x     Document Type: Review

References (206)

1. Aarts N, Metz M, Holub E, Staskawica BJ, Daniels MJ, Parker JE (1998) Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc. Natl. Acad. Sci. USA 95, 10306-10311.
2. Aboul-Soud MAM, Cook K, Loake GJ (2004) Measurement of salicylic acid by a high-performance liquid chromatography procedure based on ion-exchange. Chromatographia 59, 129-133.
3. Achard P, Renou JP, Berthome R, Harberd NP, Genschik P (2008) Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Curr. Biol. 18, 656-660.
4. Achuo EA, Prinsen E, Hofte M (2006) Influence of drought, salt stress and abscisic acid on the resistance of tomato to Botrytis cinerea and Oidium neolycopersici. Plant Pathol. 55, 178-186.
5. Adie BA, Pérez-Pérez J, Pérez-Pérez MM, Godoy M, Sánchez-Serrano J, Schmelz EA, Solano R (2007) ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 19, 1665-1681.
6. Alonso-Ramírez A, Rodríguez D, Reyes D, Jiménez JA, Nicolás G, López-Climent M, Gómez-Cadenas A, Nicolás C (2009) Cross-talk between gibberellins and salicylic acid in early stress responses in Arabidopsis thaliana seeds. Plant Signal. Behav. 4, 750-751.
7. Anderson JP, Badruzsaufari E, Schenk PM, Manneres JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16, 3460-3479.
8. Asselbergh B, Achuo AE, Hofte M, Van Gijsegem F (2008) Abscisic acid deficiency leads to rapid activation of tomato defense responses upon infection with Erwinia chrysanthemi. Mol. Plant. Pathol. 9, 11-24.
9. Audenaert K, De Meyer GB, Hofte MM (2002) Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiol. 128, 491-501.
10. Bari R, Jones JDG (2009) Role of plant hormones in plant defense response. Plant Mol. Biol. 69, 473-488.
11. Bender J, Fink GR (1998) A Myb homologue, ATR1, activates tryptophan gene expression in Arabidopsis. Proc. Natl. Acad. Sci. USA 95, 5655-5660.
12. Bi D, Cheng Y, Li X, Zhang Y (2010) Activation of plant immune responses by a gain-of-function mutation in an atypical receptor-like kinase. Plant Physiol. 153, 1771-1779.
13. Brodersen P, Petersen M, Nielsen HB, Zhu S, Newman MA, Shokat KM, Rietz S, Parker J, Mundy J (2006) Arabidopsis MAP kinase 4 regulates salicylic acid- and jasmonic acid/ethylene-dependent responses via EDS1 and PAD4. Plant J. 47, 532-549.
14. Cao H, Bowling, SA, Gordon AS, Dong X (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6, 1583-1592.
15. Cao H, Glazebrook J, Clarke JD, Volko S, Dong X (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88, 57-63.
16. Cao H, Li X, Dong X (1998) Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. Proc. Natl. Acad. Sci. USA 95, 6531-6536.
17. Catinot J, Buchala A, Abou-Mansour E, Métraux JP (2008) Salicylic acid production in response to biotic and abiotic stress depends on isochorismate in Nicotiana benthamiana. FEBS Lett. 582, 473-478.
18. Century KS, Shapiro AD, Repetti PP, Dahlbeck D, Holub E, Staskawicz BJ (1997) NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science 278, 1963-1965.
19. Chadha KC, Brwon SA (1974) Biosynthesis of phenolic acids in tomato plants infected with Agrobacterium tumefaciens. Can. J. Bot. 52, 2041-2047.
20. Chandra-Shekara AC, Navarre D, Kachroo A, Kang HG, Klessig D, Kachroo P (2004) Signaling requirements and role of salicylic acid in HRT-and rrt-mediated resistance to turnip crinkle virus in Arabidopsis. Plant J. 40, 647-659.
21. Chen F, D'Auria JC, Tholl D, Ross JR, Gerzhenzon J, Noel JP, Pichersky E (2003) An Arabidopsis thaliana gene for methylsalicylate biosynthesis, identified by a biochemical genomics approach, has a role in defense. Plant J. 36, 577-588.
22. Chen Z, Agnew JL, Cohen JD, He P, Shan P, Sheen J, Kunkel BN (2007) Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. Proc. Natl. Acad. Sci. USA 104, 20131-20136.
23. Chen Z, Zhang H, Jablonowski D, Zhou X, Ren X, Hong X, Schaffrath R, Zhu JK, Gong Z (2006) Mutation in ABO1/ELO2, a subunit of Holo-Elongator, increase abscisic acid sensitivity and drought tolerance in Arabidopsis thaliana. Mol. Cell Biol. 26, 6902-6912.
24. Chen Z, Zheng Z, Huang J, Lai Z, Fan B (2009) Biosynthesis of salicylic acid in plants. Plant Signal. Behav. 4, 493-496.
25. Chern MS, Fitzgerald HA, Canlas PE, Navarre DA, Ronald PC (2005) Overexpression of a rice NPR1 homolog leads to constitutive activation of defense response and hypersensitivity to light. Mol. Plant-Microbe Interact. 18, 511-520.
26. Chern MS, Fitzgerald HA, Yadav RC, Canlas PE, Dong X (2001) Evidence for a disease-resistance pathway in rice similar to the NPR1-mediated signaling pathway in Arabidopsis. Plant J. 27, 101-113.
27. Clarke JD, Liu Y, Klessig DF, Dong X (1998) Uncoupling PR gene expression from NPR1 and bacterial resistance: Characterization of the dominant Arabidopsis cpr6-1 mutant. Plant Cell 10, 557-569.
28. Clarke JD, Volko SM, Ledford H, Ausubel FM, Dong X (2000) Role of salicylic acid, jasmonic acid, and ethylene in cpr-induced resistance in Arabidopsis. Plant Cell 12, 2175-2190.
29. Clarke SM, Mur LAJ, Wood JE, Scott IM (2004) Salicylic acid dependent signaling promotes basal theromtolerance but is not essential for acquired thermotolerance in Arabidopsis thaliana. Plant J. 38, 432-437.
30. Close P, Hawkes N, Cornez I, Creppe C, Lambert CA, Rogister B, Siebenlist U, Merville MP, Slaugenhaupt SA, Bours V, Svejstrup JQ, Chariot A (2006) Transcription impairment and cell migration defects in Elongator-depleted cells: Implication for familial dysautonomia. Mol. Cell 22, 521-531.
31. Coppinger P, Repetti PP, Day B, Dahlbeck D, Mehlert A, Staskawicz BJ (2004) Overexpression of the plasma membrane-localized NDR1 protein results in enhanced bacterial disease resistance in Arabidopsis thaliana. Plant J. 40, 225-237.
32. Coquoz JL, Buchala A, Metraux JP (1998) The biosynthesis of salicylic acid in potato plants. Plant Physiol. 117, 1095-1101.
33. De Vos M, Zaanen WV, Koornneef A, Korzelius JP, Dicke M, Van Loon LC, Pieterse CMJ (2006) Herbivore-induced resistance against microbial pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Physiol. 142, 352-363.
34. Dean JV, Mills JD (2004) Uptake of salicylic acid 2-O-β-D-glucose into soybean tonoplast vesicles by an ATP-binding cassette transporter-type mechanism. Physiol. Plant. 120, 603-612.
35. Dean JV, Mohammed LA, Fitzpatrick T (2005) The formation, vacuolar localization, and tonoplast transport of salicylic acid glucose conjugates in tobacco cell suspension cultures. Planta 221, 287-296.
36. DeFraia CT, Schmelz EA, Mou Z (2008) A rapid biosensor-based method for quantification of free and glucose-conjugated salicylic acid. Plant Meth. 4, 28.
37. DeFraia CT, Zhang X, Mou Z (2010) Elongator subunits 2 is an accelerator of immune responses in Arabidopsis thaliana. Plant J. 64, 511-523.
38. DeFraia CT, Mou Z (2011) The role of the Elongator complex in plants. Plant Signal. Behav. 6, 19-22.
39. Delaney TP, Friedrich L, E, Ryals J (1995) Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc. Natl. Acad. Sci. USA 92, 6602-6606.
40. Delaney TP, Uknes S, Vernooij B, Friedrich L, Weymann K, Negrotto D, Gaffney T, Gut-Rella M, Kessmann H, Ward E, Ryals J (1994) A central role of salicylic acid in plant disease resistance. Science 266, 1247-1250.
41. Després C, DeLong C, Glaze S, Liu E, Fobert PR (2000) The Arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors. Plant Cell 12, 279-290.
42. Desveaux D, Allard J, Brisson N, Sygusch J (2002) A new family of plant transcription factors displays a novel ssDNA-binding surface. Nat. Str. Biol. 9, 512-517.
43. Desveaux D, Subramaniam R, Després C, Mess JN, Lévesque CL, Fobert PR, Dangl JL, Brisson N (2004) A "Whirly" transcription factor is required for salicylic acid-dependent disease resistance in Arabidopsis. Dev. Cell 6, 229-240.
44. Devadas SK, Enyedi A, Raina R (2002) The Arabidopsis hrl1 mutation reveals novel overlapping roles for salicylic acid, jasmonic acid and ethylene signaling in cell death and defense against pathogens. Plant J. 30, 467-480.
45. Dong X (2004) NPR1, all things considered. Curr. Opin. Plant Biol. 7, 547-552.
46. Durrant WE, Dong X (2004) Systemic acquired resistance. Annu. Rev. Phytopathol. 42, 185-209.
47. El-Basyouni SZ, Chen D, Ibrahim RK, Neish AC, Towers GHN (1964) The biosynthesis of hydroxybenzoic acids in higher plants. Phytochemistry 3, 485-492.
48. Elkind Y, Edwards R, Mavandad M, Hedrick SA, Ribak O, Dixon RA, Lamb CJ (1990) Abnormal plant development and downregulation of phenylpropanoid biosynthesis in transgenic tobacco containing a heterologous phenylalanine ammonia-lyase gene. Proc. Natl. Acad. Sci. USA 87, 9057-9061.
49. Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5, 199-206.
50. Falk A, Feys BJ, Frost LN, Jones JD, Daniels MJ, Parker JE (1999) EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryoti lipases. Proc. Natl. Acad. Sci. USA 96, 3292-3297.
51. Fan W, 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.
52. Feys BJ, Benedetti CE, Penfold CN, Turner JG (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6, 751-759.
53. Feys BJ, Moisan LJ, Newman MA, Parker JE (2001) Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO J. 20, 5400-5411.
54. Feys BJ, Wiermer M, Bhat RA, Moisan LJ, Medina-Escobar N, Neu C Cabral A, Parker JE (2005) Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. Plant Cell 17, 2601-2613.
55. Flors V, Ton J, van Doorn R, Jakab G, García-Agustín P, Mauch-Mani B (2008) Interplay between JA, SA and ABA signaling during basal and induced resistance against Pseudomonas syringae and Alternaria brassicicola. Plant J. 54, 81-92.
56. Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H, Ryals J (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261, 754-756.
57. Garcion C, Lohmann A, Lamodière E, Catinot J, Buchala A, Doermann P, Métraux JP (2008) Characterization and biological function of the Isochorismate Synthase 2 gene of Arabidopsis. Plant Physiol. 147, 1279-1287.
58. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205-227.
59. Gorlach J, Volrath S, Knauf-Beiter G, Hengy G, Beckhove U, Kogel KH, Oostendorop M, Staub T, Ward E, Kessmann H, Ryals J (1996) Benzothiadiazole, a novel class of inducers of systemic acquired resistance, activates gene expression and disease resistance in wheat. Plant Cell 8, 629-643.
60. Grant MR, Jones JDG (2009) Hormone (dis)harmony moulds plant health and disease. Science 324, 750-752.
61. Gupta V, Willits MG, Glazebrook J (2000) Arabidopsis thaliana EDS4 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.
62. Hennig J, Malamy J, Grynkiewicz G, Indulski J, Klessig DF (1993) Interconversion of the salicylic acid signal and its glucoside in tobacco. Plant J. 4, 593-600.
63. Hernandez-Blanco C, Feng DX, Hu J, Sánchez-Vallet A, Deslandes L, Llorente F, Berrocal-Lobo M, Keller H, Barlet X, Sánchez-Rodríguez C, Anderson LK, Somerville S, Marco Y, Molina A (2007) Impairment of cellulose synthases required for Arabidopsis secondary cell wall formation enhances disease resistance. Plant Cell 19, 890-903.
64. Huang J, Gu M, Lai Z, Fan B, Shi K, Zhou YH, Yu JQ, Chen Z (2010) Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress. Plant Physiol. 153, 1526-1538.
65. Huang WE, Huang L, Preston GM, Martin N, Carr JP, Li Y, Singer AC, Whiteley AS, Wang H (2006) Quantitative in situ assay of salicylic acid in tobacco leaves using a genetically modified biosensor strain of Acinetoacter sp. ADP1. Plant J. 46, 1073-1083.
66. Ishihara T, Sekine K-T, Hase S, Kanayama Y, Seo S, Ohashi Y, Kusano T, Shibata D, Shah J Takahashi H (2008) Overexpression of the Arabidopsis thaliana EDS5 gene enhances resistance to viruses. Plant Biol. 10, 451-461.
67. Jagadeeswaran G, Raina S, Acharya BR, Maqbool AB, Mosher SL, Appel HM, Schultz JC, Klessig DF, Raina R (2007) Arabidopsis GH3-LIKE DEFENSE GENE 1 is required for accumulation of salicylic acid, activation of defense responses and resistance to Pseudomonas syringae. Plant J. 51, 234-246.
68. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444, 323-329.
69. Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT (2009) Priming in systemic plant immunity. Science 324, 89-91.
70. Kachroo A, Lapchyk L, Fukushige H, Hildebrand D, Klessig D, Kachroo P (2003) Plastidial fatty acid signaling modulates salicylic acid- and jasmonic acid-mediated defense pathways in the Arabidopsis ssi2 mutant. Plant Cell 15, 2952-2965.
71. Kachroo P, Shanklin J, Shah J, Whittle EJ, Klessig DF (2001) A fatty acid desaturease modulates the activation of defense signaling pathways in plants. Proc. Natl. Acad. Sci. USA 98, 9448-9453.
72. Kachroo P, Yoshioka K, Shah J, Dooner HK, Klessig DF (2000) Resistance to turnip crinkle virus in Arabidopsis is regulated by two host genes and is salicylic acid dependent but NPR1, ethylene, and jasmonate independent. Plant Cell 12, 677-690.
73. Klambt HD (1962) Conversion in plants of benzoic acid to salicylic acid and its β-D-glucoside. Nature 196, 491.
74. Kloek AP, Verbsky ML, Sharma SB, Schoelz JE, Vogel J, Klessig DF Kunkel BN (2001) Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana corontine-insensitive (coi1) mutation occurs through two distinct mechanisms. Plant J. 26, 509-522.
75. Koga H, Dohi K, Mori M (2004) Abscisic acid and low temperatures suppress the whole plant-specific resistance reaction of rice plants to the infection of Magnaporthe grisea. Physiol. Mol. Plant Pathol. 65, 3-9.
76. Kopp E, Ghosh S (1994) Inhibition of NF-kappa B by sodium salicylate and aspirin. Science 265, 956-959.
77. Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr. Opin. Plant Biol. 5, 325-331.
78. Lebel E, Heifetz P, Thorne L, Uknes S, Ryals J, Ward E (1998) Functional analysis of regulatory sequences controlling PR-1 gene expression in Arabidopsis. Plant J. 16, 223-233.
79. Lee HI, León J, Raskin I (1995) Biosynthesis and metabolism of salicylic acid. Proc. Natl. Acad. Sci. USA 92, 4076-4079.
80. Lee MW, Lu H, Jung HW, Greenberg JT (2007). A key role for the Arabidopsis WIN3 protein in disease resistance triggered by Pseudomonas syringae that secrete AvrRpt2. Mol. Plant-Microbe Interact. 20, 1192-1200.
81. Lee JS (1998) The mechanism of stomatal closing by salicylic acid in Commelina communis L. J. Plant Biol. 41, 97-102.
82. Leon J, Shulaev V, Yalpani N, Lawton MA, Raskin I (1995) Benzoic acid 2-hydroxylase, a soluble oxygenase from tobacco, catalyzes salicylic acid biosynthesis. Proc. Natl. Acad. Sci. USA 92, 10413-10417.
83. Li J, Brader G, Palva ET (2004) The WRKY70 transcription factor: A node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16, 319-331.
84. Li M, Duan M, Wei C, Li Y (2007) WRKY62 transcription factor acts downstream of cytosolic NPR1 and negatively regulates jamonate-responsive gene expression. Plant Cell Physiol. 48, 833-842.
85. Li X, Clarke JD, Zhang Y, Dong X (2001) Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance. Mol. Plant-Microbe Interact. 14, 1131-1139.
86. Li X, Zhang Y, Clarke JD, Li Y, Dong X (1999) Identification and cloning of a negative regulator of systemic acquired resistance, SNI1, through a screen for suppressors of npr1-1. Cell 98, 329-339.
87. Lin WC, Lu CF, Wu JW, Cheng ML, Lin YM, Yang NS, Black L, Green SK, Wang JF, Cheng CP (2004) Transgenic tomato plants expressing the Arabidopsis NPR1 gene display enhanced resistance to a spectrum of fungal and bacterial diseases. Transgenic Res. 13, 567-581.
88. Lorrain S, Lin B, Auriac MC, Kroj T, Saindrenan P, Nicole M, Balagué C, Roby D (2004) Vascular associated death1, a novel GRAM domain-containing protein, is a regulator of cell death and defense responses in vascular tissues. Plant Cell 16, 2217-2232.
89. Lorrain S, Vailleau F, Balague C, Roby D (2003) Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci. 8, 263-271.
90. Lu H, Rate DN, Song JT, Greenberg JT (2003) ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response. Plant Cell 15, 2408-2420.
91. Makandar R, Essig JS, Schapaugh MA, Trick HN, Shah J (2006) Genetically engineered resistance to Fusarium head blight in wheat by expression of Arabidopsis NPR1. Mol. Plant-Microbe Interact. 19, 123-129.
92. Malamy J, Carr JP, Klessig DF, Raskin I (1990) Salicylic acid: A likely endogenous signal in the resistance response of tobacco to viral infection. Science 250, 1002-1004.
93. Malamy J, Klessig DF (1992) Salicylic acid and plant disease resistance. Plant J. 2, 643-654.
94. Malnoy M, Jin Q, Borejsza-Wysocka EE, He SY, Aldwinckle HS (2007) Overexpression of the apple MpNPR1 gene confers increased disease resistance in Malus×domestica. Mol. Plant-Microbe Interact. 20, 1568-1580.
95. Manthe B, Schulz M, Schnabl H (1992) Effects of salicylic acid on growth and stomatal movement of Vicia faba L.: Evidence for salicylic acid metabolization. J. Chem. Ecol. 18, 1525-1539.
96. Marek G, Carver R, Ding Y, Sathyanarayan D, Zhang X, Mou Z (2010) A high-throughput method for isolation of salicylic acid metabolic mutants. Plant Meth. 6, 21.
97. Mauch-Mani B, Slusarenko AJ (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.
98. McCarty MF, Block KI (2006) Preadministration of high-dose salicylates, suppressors of NF-κB activation, may increase the chemosensitivity of many cancers: an example of proapoptotic signal modulation therapy. Integr. Cancer Ther. 5, 252-268.
99. Métraux JP, Signer H, Ryals JA, Ward E, Wyss-Benz, M Raschdorf GK, Schmid E, Blum W, Inverardi B (1990) Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250, 1004-1006.
100. Meuwly P, Mölders W, Buchala A, Métraux JP (1995) Local and systemic biosynthesis of salicylic acid in infected cucumber plants. Plant Physiol. 109, 1107-1114.
101. Mitchell JA, Akarasereenont P, Thiemermann C, Flower RJ, Vane JR (1990) Selectivity of nonsteroidal anti-inflammatory drugs as inhibitors of constitutive and inducible cyclooxygenase. Proc. Natl. Acad. Sci. USA 90, 11693-11697.
102. Moeder W, Yoshioka K (2008) Lesion mimic mutants-a classical, yet still fundamental approach to study programmed cell death. Plant Signal. Behav. 3, 764-767.
103. Mohr PG, Cahill DM (2001) Relative roles of glyceollin, lignin and the hypersensitive response and the influence of ABA in compatible and in compatible interactions of soybeans with Phytophthora sojae. Physiol. Mol. Plant Pathol. 58, 31-41.
104. Mohr PG, Cahill DM (2003) Abscisic acid influences the susceptibility of Arabidopsis thaliana to Pseudomonas syringae pv. tomato and Peronospora parasitica. Funct. Plant Biol. 30, 461-469.
105. Monaghan J, Germain H, Weihmann T, Li X (2010) Dissecting plant defense signal transduction: Modifiers of snc1 in Arabidopsis. Can. J. Plant Pathol. 32, 35-42.
106. Morris K, MacKerness SA, Page T, John CF, Murphy AM, Carr JP, Buchanan-Wollaston V (2000) Salicylic acid has a role in regulating gene expression during leaf senescence. Plant J. 23, 677-685.
107. Morris SW, Vernooij B, Titatarn S, Starrett M, Thomas S, Wiltse CC, Frederiksen RA, Bhandhufalck A, Hulbert S, Ukness S (1998) Induced resistance response in maize. Mol. Plant-Microbe Interact. 11, 643-658.
108. Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113, 935-944.
109. Mur LAJ, Kenton P, Atzorn R, Miersch O, Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol. 140, 249-262.
110. Murray SL, Thomson C, Chini A, Read ND, Loake GJ (2002) Characterization of a novel, defense-related Arabidopsis mutant, cir1, isolated by luciferase imaging. Mol. Plant-Microbe Ineract. 15, 557-566.
111. Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guilfoyle TJ, Hagen G, Alonso JM, Cohen JD, Farmer EE, Ecker JR, Reed JW (2005) Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132, 4107-4118.
112. Navarro L, Bari R, Achard P, Lison P, Nemri A, Harberd NP, Jones JD (2008) DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr. Biol. 18, 650-655.
113. Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinet O, Jones JD (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312, 436-439.
114. Nawrath C, Heck S, Parinthawong N, Métraux JP (2002) EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell 14, 275-286.
115. Nawrath C, Métraux JP (1999) Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11, 1393-1404.
116. Ndamukong I, Abdallat AA, Thurow C, Fode B, Zander M, Weigel R, Gatz C (2007) SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA-responsive PDF1.2 transcription. Plant J. 50, 128-139.
117. Nelissen H, De Groeve S, Fleury D, Neyt P, Bruno L, Bitonti MB, Vandenbussche F, Van Der Straeten D, Yamaguchi T, Tsukaya H, Witters E, De Jaeger G, Houben A, Van Lijsebettens M (2010) Plant Elongator regulates auxin-related genes during RNA polymerase II transcription elongation. Proc. Natl. Acad. Sci. USA 107, 1678-1683.
118. Nelissen H, Fleury D, Bruno L, Robles P, De Veylder L, Trass J, Micol JL, Van Montagu M, Inze D, Van Lijsebettens M (2005) The elongata mutants identify a functional Elongator complex in plants with a role in cell proliferation during organ growth. Proc. Natl. Acad. Sci. USA 102, 7754-7759.
119. Nobuta K, Okrent RA, Stoutemyer M, Rodibaugh N, Kempema L, Wildermuth MC, Innes RW (2007) The GH3 acyl adenylase family member PBS3 regulates salicylic acid-dependent defense responses in Arabidopsis. Plant Physiol. 144, 1144-1156.
120. Norman C, Howell KA, Millar AH, Whelan JM, Day DA (2004) Salicylic acid is an uncoupler and inhibitor of mitochondrial electron transport. Plant Physiol. 134, 492-501.
121. Pallas JA, Paiva NL, Lamb C, Dixon RA (1996) Tobacco plants epigenetically suppressed in phenylalanine ammonia-lyase expression do not develop systemic acquired resistance in response to infection by tobacco mosaic virus. Plant J. 10, 281-293.
122. Park JE, Park JY, Kim YS, Staswick PE, Jeon J, Yun J, Kim SY, Kim J, Lee YH, Park CM (2007) GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J. Biol. Chem. 282, 10036-10046.
123. Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318, 113-116.
124. Parker JE, Holub EB, Frost LN, Falk A, Gunn ND, Daniel MJ (1996) Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell 8, 2033-2046.
125. Parkhi V, Kumar V, Campbell LM, Bell AA, Shah J, Rathore KS (2010) Resistance against various fungal pathogens and reniform nematode in transgenic cotton plants expressing Arabidopsis NPR1. Transgenic Res. 19, 959-975.
126. Pasquer F, Isidore E, Zarn J, Keller B (2005) Specific patterns of changes in wheat gene expression after treatment with three antifungal compounds. Plant Mol. Biol. 57, 693-707.
127. Petersen M, Brodersen P, Naested H, Andreasson E, Lindhart U, Johansen B, Nielsen HB, Lacy M, Austin MJ, Parker JE, Sharma SB, Klessig DF, Martienssen R, Mattsson O, Jensen AB, Mundy J (2000) Arabidopsis map kinase 4 negatively regulates systemic acquired resistance. Cell 103, 1111-1120.
128. Pierpoint WS (1994) Salicylic acid and its derivatives in plants: Medicines, metabolites and messenger molecules. Adv. Bot. Res. 20, 163-235.
129. Pieterse CM, Leon-Reyes A, Van Der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nature Chem. Biol. 5, 308-316.
130. Pieterse CMJ, Van Loon LC (2004) NPR1: The spider in the web of induced resistance signaling pathways. Curr. Opin. Plant Biol. 7, 456-464.
131. Potlakayala SD, DeLong C, Sharpe A, Robert PR (2007) Conservation of NON-EXPRESSOR OF PATHOGENESIS-RELATED GENES1 function between Arabidopsis thaliana and Brassica napus. Physiol. Mol. Plant Pathol. 71, 174-183.
132. Pridham JB (1965) Low molecular weight phenols in higher plants. Annu. Rev. Plant Physiol. 6, 13-36.
133. Raffaele S, Rivas S, Roby D (2006) An essential role for salicylic acid in AtMYB30-mediated control of the hypersensitive cell death program in Arabidopsis. FEBS Lett. 580, 3498-3504.
134. Rainsford KD (1984) Aspirin and The Salicylates. Butterworth, London
135. Rajou L. Belghazi M, Huguet R. Robin C, Moreau A, Job C, Job D (2006) Proteomic investigation of the effect of salicylic acid on Arabidopsis seed germination and establishment of early defense mechanisms. Plant Physiol. 141, 910-923.
136. Rao MV, Davis KR (2001) The physiology of ozone-induced cell death. Planta 213, 682-690.
137. Rao MV, Lee HI, Davis KR (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.
138. Raridan GJ, Delaney TP (2002) Role of salicylic acid and NIM1/NPR1 in race-specific resistance in Arabidopsis. Genetics 29, 439-451.
139. Raskin I (1992a) Role of salicylic acid in plants. Annu. Rev. Plant Physiol. 43, 438-463.
140. Raskin I (1992b) Salicylate, a new plant hormone. Plant Physiol. 99, 799-803.
141. Raskin I, Ehmann A, Melander WR, Meeuse BJD (1987) Salicylic acid: A natural inducer of heat production in Arum lilies. Science 237, 1601-1602.
142. Rate DN, Cuenca JV, Bowman GR, Guttman DS, Greenberg JT (1999) The gain-of-function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death, defense, and cell growth. Plant Cell 11, 1695-1708.
143. Robert-Seilaniantz A, Navarro L, Bari R, Jones JDG (2007) Pathological hormone imbalances. Curr. Opin. Plant Biol. 10, 372-379.
144. Rochon A, Boyle P, Wignes T, Fobert PR, Despré C (2006) The coactivator function of Arabidopsis NPR1 requires the core of its BTB/POZ domain and the oxidation of C-terminal cysteines. Plant Cell 18, 3670-3685.
145. Rustérucci C, Aviv DH, Holt BF, Dangl JL, Parker JE (2001) The disease resistance signaling components EDS1 and PAD4 are essential regulators of the cell death pathway controlled by LSD1 in Arabidopsis. Plant Cell 13, 2211-2224.
146. Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD (1996) Systemic acquired resistance. Plant Cell 8, 1809-1819.
147. Sawada H, Shim IS, Usui K (2006) Induction of benzoic acid 2-hydroxylase and salicylic acid biosynthesis-modulation by salt stress in rice seedlings. Plant Sci. 171, 263-270.
148. Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc. Natl. Acad. Sci. USA 97, 11655-11660.
149. Schmelz EA, Engelberth J, Alborn HT, O'Donnell P, Sammons M, Toshima H, Tumlinson JH (2003) Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants. Proc. Natl. Acad. Sci. USA 100, 10552-10557.
150. Serino L, Reimmann C, Baur H, Beyeler M, Visca P, Haas D (1995) Structural genes for salicylate biosyntesis from chorismate in Pseudomonas aeruginosa. Mol. Gen. Genet. 249, 217-228.
151. Shah J, Tsui F, Klessig DF (1997) Characterization of a salicylic acid-insensitive mutant (sai1) if Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Mol. Plant-Microbe Interact. 10, 69-78.
152. Shah J, Kachroo P, Klessig DF (1999) The Arabidopsis ssi1 mutation restores pathogenesis-related gene expression in npr1 plants and renders defensin gene expression salicylic acid dependent. Plant Cell 11, 191-206.
153. Shah J, Kachroo P, Nandi A, Klessig DF (2001). A recessive mutation in the Arabidopsis SSI2 gene confers SA- and NPR1-independent expression of PR genes and resistance against bacterial and oomycete pathogens. Plant J. 25, 563-574.
154. Shah J, Klessig DF (1999) Salicylic acid: Signal perception and transduction. In: Hooykaas PPJ, Hall MA, Libbega KR eds. Biochemistry and Molecular Biology of Plant Hormones. Amsterdam, Netherlands Elsevier. pp. 513-541.
155. Shapiro AD, Zhang C (2001) The role of NDR1 in avirulence gene-directed signaling and control of programmed cell death in Arabidopsis. Plant Physiol. 127, 1089-1101.
156. Shirano Y, Kachroo P, Shah J, Klessig DF (2002) A gain-of-function mutation in an Arabidopsis toll interleukiin1 receptor-nucleotide binding site-leucine-rich repeat type R gene triggers defense responses and results in enhanced disease resistance. Plant Cell 14, 3149-3162.
157. Shulaev V, Silverman P, Raskin I (1997) Airborne signaling by methyl salicylate in plant pathogen resistance. Nature 385, 718-721.
158. Silverman P. Seskar M, Kanter D, Schweizer P, Metraux JP, Raskin I (1995) Salicylic acid in rice: biosynthesis, conjugation and possible role. Plant Physiol. 108, 633-639.
159. Song JT, Lu H, McDowell JM, Greeberg JT (2004) A key role for ALD1 in activation of local and systemic defenses in Arabidopsis. Plant J. 40, 200-212.
160. Spoel SH, Koornneef A, Claessens SMC, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Métraux JP, Brown R, Kazan K, Van Loon LC, Dong X, Pieterse CM (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15, 760-770.
161. Stacey G, McAlvin CB, Kim SY, Olivares J, Soto MJ (2006) Effects of endogenous salicylic acid on nodulation in the model legumes Lotus japonicas and Medicago truncatula. Plant Physiol. 141, 1473-1481.
162. Sticher L, Mauch-Mani B, Métraux JP (1997) Systemic acquired resistance. Annu. Rev. Phytopathol. 35, 235-270.
163. Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Dong X (2008) Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science 321, 952-956.
164. Takahashi H, Miller J, Nozaki Y, Sukamoto, Takeda M, Shah J, Hase S, Ikegami M, Ehara Y, Dinesh-Kumar SP (2002) RCY1, an Arabidopsis thaliana RPP8/HRT family resistance gene, conferring resistance to cucumber mosaic virus requires salicylic acid, ethylene and a novel signal transduction mechanism. Plant J. 32, 655-667.
165. Tanaka N, Matsuoka M, Kitano H, Asano T, Kaku H, Komatsu S (2006) gid1, a gibberellin-insensitive dwarf mutant, shows altered regulation of probenazole-inducible protein (PBZ1) in response to cold stress and pathogen attack. Plant Cell Environ. 29, 619-631.
166. Tang D, Christiansen KM, Innes RW (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.
167. Thaler JS, Bostock RM (2004) Interactions between abscisic-acid-mediated responses and plant resistance to pathogens and insects. Ecology 85, 48-58.
168. Tiryaki I, Staswick PE (2002) An Arabidopsis mutant defective in jasmonate response is allelic to auxin-signaling mutant axr1. Plant Physiol. 130, 887-894.
169. Ton J, Flors V, Mauch-Mani B (2009) The multifaceted role of ABA in disease resistance. Trends Plant Sci. 14, 310-317.
170. Torres MA, Jones JDG, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141, 373-378.
171. de Torres-Zabala M, Truman W, Bennett MH, Lafforgue G, Mansfield JW, Egea PR, Bögre L, Grang M (2007) Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signaling pathway to cause disease. EMBO J. 26, 1434-1443.
172. Traw MB, Bergelson J (2003) Interactive effects of jasmonic acid, salicylic acid, and gibberellin on induction of trichomes in Arabidopsis. Plant Physiol. 133, 1367-1375.
173. Truman W, Bennett MH, Kubigsteltig I, Turnbull C, Grant M (2007) Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc. Natl. Acad. Sci. USA 104, 1075-1080.
174. Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F (2009) Network properties of robust immunity in plants. Plos Genet. 5, e1000772.
175. Uppalapati SR, Ishiga Y, Wangdi T, Kunkel BN, Anand A, Mysore KS, Bender CL (2007) The phytotoxin coronatine contributes to pathogen fitness and is required for suppression of salicylic acid accumulation in tomato inoculated with Pseudomonas syringae pv. tomato DC3000. Mol. Plant-Microbe Interact. 20, 955-965.
176. Vanacker H, Lu H, Rate DN, Greenberg JT (2001) A role for salicylic acid and NPR1 in regulating cell growth in Arabidopsis. Plant J. 28, 209-216.
177. Verberne MC, Brouwer N, Delbianco F, Linthorst HJ, Bol JF, Verpoorte R (2002) Method for the extraction of the volatile compound salicylic acid from tobacco leaf material. Phytochem. Anal. 13, 45-50.
178. Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic acid, a multifaceted hormone to combat disease. Ann. Rev. Phytopathol. 47, 177-206.
179. Wang D, Amornisripanitch N, Dong X (2006) A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. Plos Pathog. 2, e123.
180. Wang D, Pajerowska-Mukhtar K, Culler AH, Dong X (2007) Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr. Biol. 17, 1784-1790.
181. Wasternack C, Atzorn R, Jarosch B, Kogel KH (1994) Induction of a thionin, the jasmonate-induced 6 kDa protein of barley by 2, 6-dichloroisonicotinic acid. J. Phytopath. 140, 280-284.
182. van Wees SCM, De Swart EAM, Van Pelt JA, Van Loon LC, Pieterse CMJ (2000) Enhancement of induced disease resistance by simultaneous activation of salicylate- and jasmonate-dependent defense pathways in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 97, 8711-8716.
183. Weigel RR, Bäuscher C, Pfitzner AJP, Pritzner UM (2001). NIMIN-1, NIMIN-2 and NIMIN-3, members of a novel family of proteins from Arabidopsis that interact with NPR1/NIM1, a key regulator of systemic acquired resistance in plants. Plant Mol. Biol. 46, 143-160.
184. Weigel RR, Pfitzner UM, Gatz C (2005) Interaction of NIMIN1 with NPR1 modulates PR gene expression in Arabidopsis. Plant Cell 17, 1279-1291.
185. Weissman G (1991) Aspirin. Scient. Amer. 264, 84-90.
186. Whenham RJ, Fraser RSS, Brown LP, Payne JA (1986) Tobacco-mosaic-virus-induced increase in abscisic-acid concentration in tobacco leaves-intracellular location in light and dark-green areas, and relationship to symptom development. Planta 168, 592-598.
187. Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defense. Nature 414, 562-565.
188. Winkler GS, Kristjuhan A, Erdjument-Bromage H, Tempst P, Svejstrup JQ (2002) Elongator is a histone H3 and H4 acetyltransferase important for normal histone acetylation levels in vivo. Proc. Natl. Acad. Sci. USA 99, 3517-3522.
189. Xiao S, Calis O, Patrick E, Zhang G, Charoenwattana P, Muskett P, Parker JE, Turner JG (2005) The atypical resistance gene, RPW8, recruits components of basal defense for powdery mildew resistance in Arabidopsis. Plant J. 42, 95-110.
190. Xie D, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280, 1091-1094.
191. 2 production via AtMPK6-coupled signaling in Arabidopsis. Plant J. 54, 440-451.
192. Yalpani N, Leon J, Lawton MA, Raskin I (1993) Pathway of salicylic acid biosynthesis in healthy and virus-inoculated tobacco. Plant Physiol. 103, 315-321.
193. Yamada T (1993) The role of auxin in plant-disease development. Annu. Rev. Phytopathol. 31, 253-273.
194. Yang DL, Li Q, Deng YW, Lou YG, Wang MY, Zhou GX, Zhang YY, He ZH (2008) Altered disease development in the eui mutants and eui overexpressors indicates that gibberellins negatively regulate rice basal disease resistance. Mol. Plant 1, 528-537.
195. Yang YO, Klessig DF (1996) Isolation and characterization of a tobacco mosaic virus-inducible Myb oncogene homolog from tobacco. Proc. Natl. Acad. Sci. USA 93, 14972-14977.
196. Yasuda M, Ishikawa A, Jikumaru Y, Seki M, Umezawa T, Asami T, Maruyama-Nakashita A, Kudo T, Shinozaki K, Yoshida S, Nakashita H (2008) Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. Plant Cell 20, 1678-1692.
197. Yu D, Chen C, Chen Z (2001) Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression. Plant Cell 13, 1527-1540.
198. Yuan Y, Zhong S, Zhu Z, Lou Y, Wang J, Wang M, Li Q, Yang D, He Z (2007) Functional analysis of rice NPR1-like genes reveals the OsNPR1/NH1 is the rice orthologue conferring disease resistance with enhanced herbivore susceptibility. Plant Biotechnol. J. 5, 313-324.
199. Zhang X, Francis MI, Dawson WO, Graham JH, Orbović V, Triplett EW, Mou Z (2010) Overexpression of the Arabidopsis NPR1 gene in citrus in crease resistance to citrus canker. Eur. J. Plant Pathol. 128, 91-100.
200. Zhang Y, Tessaro MJ, Lassner M, Li X (2003) Knockout analysis of Arabidopsis transcription factors TGA2, TGA5, and TGA6 reveals their redundant and essential roles in systemic acquired resistance. Plant Cell 15, 2647-2653.
201. Zhang Y, Yang Y, Fang B, Gannon P, Ding P, Li X, Zhang Y (2010) Arabidopsis snc2-1D activates receptor like tein-mediated immunity transduced through WRKY70. Plant Cell 22, 3153-3163.
202. Zhang Z, Li Q, Li Z, Staswick PE, Wang M, Zhu Y, He Z (2007) Dual regulation role of GH3.5 in salicylic acid and auxin signaling during Arabidopsis-Pseudomonas syringae interaction. Plant Physiol. 145, 450-464.
203. Zheng Z, Qualley A, Fan B, Dudareva N, Chen Z (2009) An important role of a BAHD acyl transferase-like protein in plant innate immunity. Plant J. 57, 1040-1053.
204. Zhou N, Tootle TL, Tsui F, Klessig DF, Glazebrook J (1998) PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis. Plant Cell 10, 1021-1030.
205. Zhou X, Hua D, Chen Z, Zhou Z, Gong Z (2009) Elongator mediates ABA responses, oxidative stress resistance and anthocyanin biosynthesis in Arabidopsis. Plant J. 60, 79-90.
206. Zhu S, Cao X, Cao X, Chen M, Ye G, Wei C, Li Y (2005) The rice dwarf virus P2 protein interacts with ent-kaurene oxidases in vivo, leading to reduced biosynthesis of gibberellins and rice dwarf symptoms. Plant Physiol. 139, 1935-1945.