1932

Abstract

Salicylic acid (SA) is an essential plant defense hormone that promotes immunity against biotrophic and semibiotrophic pathogens. It plays crucial roles in basal defense and the amplification of local immune responses, as well as the establishment of systemic acquired resistance. During the past three decades, immense progress has been made in understanding the biosynthesis, homeostasis, perception, and functions of SA. This review summarizes the current knowledge regarding SA in plant immunity and other biological processes. We highlight recent breakthroughs that substantially advanced our understanding of how SA is biosynthesized from isochorismate, how it is perceived, and how SA receptors regulate different aspects of plant immunity. Some key questions in SA biosynthesis and signaling, such as how SA is produced via another intermediate, benzoic acid, and how SA affects the activities of its receptors in the transcriptional regulation of defense genes, remain to be addressed.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-081320-092855
2021-06-17
2024-05-13
Loading full text...

Full text loading...

/deliver/fulltext/arplant/72/1/annurev-arplant-081320-092855.html?itemId=/content/journals/10.1146/annurev-arplant-081320-092855&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Abreu ME, Munne-Bosch S. 2009. Salicylic acid deficiency in NahG transgenic lines and sid2 mutants increases seed yield in the annual plant Arabidopsis thaliana. J. Exp. Bot. 60:1261–71
    [Google Scholar]
  2. 2. 
    Attaran E, Zeier TE, Griebel T, Zeier J. 2009. Methyl salicylate production and jasmonate signaling are not essential for systemic acquired resistance in Arabidopsis. Plant Cell 21:954–71
    [Google Scholar]
  3. 3. 
    Baek D, Pathange P, Chung J-S, Jiang J, Gao L et al. 2010. A stress-inducible sulphotransferase sulphonates salicylic acid and confers pathogen resistance in Arabidopsis. Plant Cell Environ 33:1383–92
    [Google Scholar]
  4. 4. 
    Birkenbihl RP, Kracher B, Somssich IE. 2016. Induced genome-wide binding of three Arabidopsis WRKY transcription factors during early MAMP-triggered immunity. Plant Cell 29:20–38
    [Google Scholar]
  5. 5. 
    Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO et al. 2005. Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42:567–85
    [Google Scholar]
  6. 6. 
    Bussell JD, Reichelt M, Wiszniewski AA, Gershenzon J, Smith SM. 2014. Peroxisomal ATP-binding cassette transporter COMATOSE and the multifunctional protein abnormal INFLORESCENCE MERISTEM are required for the production of benzoylated metabolites in Arabidopsis seeds. Plant Physiol 164:48–54
    [Google Scholar]
  7. 7. 
    Caillaud M-C, Asai S, Rallapalli G, Piquerez S, Fabro G, Jones JD. 2013. A downy mildew effector attenuates salicylic acid–triggered immunity in Arabidopsis by interacting with the host mediator complex. PLOS Biol 11:e1001732
    [Google Scholar]
  8. 8. 
    Canet JV, Dobon A, Roig A, Tornero P. 2010. Structure-function analysis of npr1 alleles in Arabidopsis reveals a role for its paralogs in the perception of salicylic acid. Plant Cell Environ 33:1911–22
    [Google Scholar]
  9. 9. 
    Canet JV, Dobón A, Tornero P. 2012. Non-recognition-of-BTH4, an Arabidopsis mediator subunit homolog, is necessary for development and response to salicylic acid. Plant Cell 24:4220–35
    [Google Scholar]
  10. 10. 
    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 6:1583–92
    [Google Scholar]
  11. 11. 
    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
    [Google Scholar]
  12. 12. 
    Chandran D, Rickert J, Huang Y, Steinwand MA, Marr SK, Wildermuth MC. 2014. Atypical E2F transcriptional repressor DEL1 acts at the intersection of plant growth and immunity by controlling the hormone salicylic acid. Cell Host Microbe 15:506–13
    [Google Scholar]
  13. 13. 
    Chen H, Chen J, Li M, Chang M, Xu K et al. 2017. A bacterial type III effector targets the master regulator of salicylic acid signaling, NPR1, to subvert plant immunity. Cell Host Microbe 22:777–88.e7
    [Google Scholar]
  14. 14. 
    Chen H, Xue L, Chintamanani S, Germain H, Lin H et al. 2009. ETHYLENE INSENSITIVE3 and ETHYLENE INSENSITIVE3-LIKE1 repress SALICYLIC ACID INDUCTION DEFICIENT2 expression to negatively regulate plant innate immunity in Arabidopsis. Plant Cell 21:2527–40
    [Google Scholar]
  15. 15. 
    Chen J, Mohan R, Zhang Y, Li M, Chen H et al. 2019. NPR1 promotes its own and target gene expression in plant defense by recruiting CDK8. Plant Physiol 181:289–304
    [Google Scholar]
  16. 16. 
    Chen L, Wang W-S, Wang T, Meng X-F, Chen T-T et al. 2019. Methyl salicylate glucosylation regulates plant defense signaling and systemic acquired resistance. Plant Physiol 180:2167–81
    [Google Scholar]
  17. 17. 
    Chen Y, Shen H, Wang M, Li Q, He Z 2013. Salicyloyl-aspartate synthesized by the acetyl-amido synthetase GH3.5 is a potential activator of plant immunity in Arabidopsis. Acta Biochim. Biophys. Sin. 45:827–36
    [Google Scholar]
  18. 18. 
    Chen Y-C, Holmes EC, Rajniak J, Kim J-G, Tang S et al. 2018. N-hydroxy-pipecolic acid is a mobile metabolite that induces systemic disease resistance in Arabidopsis. PNAS 115:E4920–29Identified NHP as a mobile signal for SAR that induces the expression of genes involved in SA biosynthesis.
    [Google Scholar]
  19. 19. 
    Chen Z, Silva H, Klessig DF. 1993. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262:1883–86
    [Google Scholar]
  20. 20. 
    Cleland CF, Tanaka O. 1979. Effect of daylength on the ability of salicylic acid to induce flowering in the long-day plant Lemna gibba G3 and the short-day plant Lemna paucicostata 6746. Plant Physiol 64:421–24
    [Google Scholar]
  21. 21. 
    Cui H, Gobbato E, Kracher B, Qiu J, Bautor J, Parker JE. 2017. A core function of EDS1 with PAD4 is to protect the salicylic acid defense sector in Arabidopsis immunity. New Phytol 213:1802–17
    [Google Scholar]
  22. 22. 
    Dean JV, Delaney SP. 2008. Metabolism of salicylic acid in wild-type, ugt74f1 and ugt74f2 glucosyltransferase mutants of Arabidopsis thaliana. Physiol. Plant. 132:417–25
    [Google Scholar]
  23. 23. 
    Delaney TP, Friedrich L, Ryals JA 1995. Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. PNAS 92:6602–6
    [Google Scholar]
  24. 24. 
    Delaney TP, Uknes S, Vernooij B, Friedrich L, Weymann K et al. 1994. A central role of salicylic acid in plant disease resistance. Science 266:1247–50
    [Google Scholar]
  25. 25. 
    Dempsey DA, Vlot AC, Wildermuth MC, Klessig DF. 2011. Salicylic acid biosynthesis and metabolism. Arabidopsis Book 9:e0156
    [Google Scholar]
  26. 26. 
    Devadas SK, Raina R 2002. Preexisting systemic acquired resistance suppresses hypersensitive response-associated cell death in Arabidopsis hrl1 Mutant. Plant Physiol 128:1234–44
    [Google Scholar]
  27. 27. 
    Ding Y, Dommel M, Mou Z. 2016. Abscisic acid promotes proteasome-mediated degradation of the transcription coactivator NPR1 in Arabidopsis thaliana. Plant J 86:20–34
    [Google Scholar]
  28. 28. 
    Ding Y, Sun T, Ao K, Peng Y, Zhang Y et al. 2018. Opposite roles of salicylic acid receptors NPR1 and NPR3/NPR4 in transcriptional regulation of plant immunity. Cell 173:1454–67.e15Provided an updated model on how SA is perceived and how SA receptors regulate defense gene expression.
    [Google Scholar]
  29. 29. 
    Du L, Ali GS, Simons KA, Hou J, Yang T et al. 2009. Ca2+/calmodulin regulates salicylic-acid-mediated plant immunity. Nature 457:1154–58
    [Google Scholar]
  30. 30. 
    Duan L, Liu H, Li X, Xiao J, Wang S 2014. Multiple phytohormones and phytoalexins are involved in disease resistance to Magnaporthe oryzae invaded from roots in rice. Physiol. Plant. 152:486–500
    [Google Scholar]
  31. 31. 
    Durner J, Klessig DF 1995. Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defense responses. PNAS 92:11312–16
    [Google Scholar]
  32. 32. 
    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 14:1377–89
    [Google Scholar]
  33. 33. 
    Fu ZQ, Yan S, Saleh A, Wang W, Ruble J et al. 2012. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486:228–32
    [Google Scholar]
  34. 34. 
    Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G et al. 1993. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754–56
    [Google Scholar]
  35. 35. 
    Gao X, Chen X, Lin W, Chen S, Lu D et al. 2013. Bifurcation of Arabidopsis NLR immune signaling via Ca2+-dependent protein kinases. PLOS Pathog 9:e1003127
    [Google Scholar]
  36. 36. 
    Garcion C, Lohmann A, Lamodiere E, Catinot J, Buchala A et al. 2008. Characterization and biological function of the ISOCHORISMATE SYNTHASE2 gene of Arabidopsis. Plant Physiol 147:1279–87
    [Google Scholar]
  37. 37. 
    Glazebrook J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43:205–27
    [Google Scholar]
  38. 38. 
    Groszmann M, Gonzalez-Bayon R, Lyons RL, Greaves IK, Kazan K et al. 2015. Hormone-regulated defense and stress response networks contribute to heterosis in Arabidopsis F1 hybrids. PNAS 112:E6397–406
    [Google Scholar]
  39. 39. 
    Guo P, Li Z, Huang P, Li B, Fang S et al. 2017. A tripartite amplification loop involving the transcription factor WRKY75, salicylic acid, and reactive oxygen species accelerates leaf senescence. Plant Cell 29:2854–70
    [Google Scholar]
  40. 40. 
    Hartmann M, Zeier T, Bernsdorff F, Reichel-Deland V, Kim D et al. 2018. Flavin monooxygenase-generated N-hydroxypipecolic acid is a critical element of plant systemic immunity. Cell 173:456–69.e16Identified NHP as a signaling molecule for SAR and an inducer of genes involved in SA biosynthesis.
    [Google Scholar]
  41. 41. 
    He J, Liu Y, Yuan D, Duan M, Liu Y et al. 2020. An R2R3 MYB transcription factor confers brown planthopper resistance by regulating the phenylalanine ammonia-lyase pathway in rice. PNAS 117:271–77
    [Google Scholar]
  42. 42. 
    Huang J, Gu M, Lai Z, Fan B, Shi K et al. 2010. Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress. Plant Physiol 153:1526–38
    [Google Scholar]
  43. 43. 
    Huang J, Sun Y, Orduna AR, Jetter R, Li X. 2019. The Mediator kinase module serves as a positive regulator of salicylic acid accumulation and systemic acquired resistance. Plant J 98:842–52
    [Google Scholar]
  44. 44. 
    Huang P, Dong Z, Guo P, Zhang X, Qiu Y et al. 2020. Salicylic acid suppresses apical hook formation via NPR1-mediated repression of EIN3 and EIL1 in Arabidopsis. Plant Cell 32:612–29
    [Google Scholar]
  45. 45. 
    Huang W, Wang Y, Li X, Zhang Y. 2020. Biosynthesis and regulation of salicylic acid and N-hydroxypipecolic acid in plant immunity. Mol. Plant 13:31–41
    [Google Scholar]
  46. 46. 
    Huang X-X, Zhu G-Q, Liu Q, Chen L, Li Y-J, Hou B-K. 2018. Modulation of plant salicylic acid-associated immune responses via glycosylation of dihydroxybenzoic acids. Plant Physiol 176:3103–19
    [Google Scholar]
  47. 47. 
    Ishihama N, Choi S-W, Noutoshi Y, Saska I, Asai S et al. 2020. Oxicam-type nonsteroidal anti-inflammatory drugs inhibit NPR1-mediated salicylic acid pathway. bioRxiv 2020.09.25.311100. https://doi.org/10.1101/2020.09.25.311100
    [Crossref]
  48. 48. 
    Jacob F, Kracher B, Mine A, Seyfferth C, Blanvillain-Baufumé S et al. 2018. A dominant-interfering camta3 mutation compromises primary transcriptional outputs mediated by both cell surface and intracellular immune receptors in Arabidopsis thaliana. New Phytol 217:1667–80
    [Google Scholar]
  49. 49. 
    Jagadeeswaran G, Raina S, Acharya BR, Maqbool SB, Mosher SL et al. 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 51:234–46
    [Google Scholar]
  50. 50. 
    Jin H, Choi SM, Kang MJ, Yun SH, Kwon DJ et al. 2018. Salicylic acid-induced transcriptional reprogramming by the HAC–NPR1–TGA histone acetyltransferase complex in Arabidopsis. Nucleic Acids Res 46:11712–25
    [Google Scholar]
  51. 51. 
    Jin JB, Jin YH, Lee J, Miura K, Yoo CY et al. 2008. The SUMO E3 ligase, AtSIZ1, regulates flowering by controlling a salicylic acid-mediated floral promotion pathway and through affects on FLC chromatin structure. Plant J 53:530–40
    [Google Scholar]
  52. 52. 
    Kim Y, Park S, Gilmour SJ, Thomashow MF. 2013. Roles of CAMTA transcription factors and salicylic acid in configuring the low-temperature transcriptome and freezing tolerance of Arabidopsis. Plant J 75:364–76
    [Google Scholar]
  53. 53. 
    Klessig DF, Tian M, Choi HW. 2016. Multiple targets of salicylic acid and its derivatives in plants and animals. Front. Immunol. 7:206
    [Google Scholar]
  54. 54. 
    Kloek AP, Verbsky ML, Sharma SB, Schoelz JE, Vogel J et al. 2001. Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana coronatine-insensitive (coi1) mutation occurs through two distinct mechanisms. Plant J 26:509–22
    [Google Scholar]
  55. 55. 
    Kong Q, Sun T, Qu N, Ma J, Li M et al. 2016. Two redundant receptor-like cytoplasmic kinases function downstream of pattern recognition receptors to regulate activation of SA biosynthesis. Plant Physiol 171:1344–54
    [Google Scholar]
  56. 56. 
    Lee HJ, Park YJ, Seo PJ, Kim JH, Sim HJ et al. 2015. Systemic immunity requires SnRK2.8-mediated nuclear import of NPR1 in Arabidopsis. Plant Cell 27:3425–38
    [Google Scholar]
  57. 57. 
    Lee MW, Lu H, HW Jung, 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. 20:1192–200
    [Google Scholar]
  58. 58. 
    Leon J, Shulaev V, Yalpani N, Lawton MA, Raskin I 1995. Benzoic acid 2-hydroxylase, a soluble oxygenase from tobacco, catalyzes salicylic acid biosynthesis. PNAS 92:10413–17
    [Google Scholar]
  59. 59. 
    Li J, Brader G, Kariola T, Palva ET. 2006. WRKY70 modulates the selection of signaling pathways in plant defense. Plant J 46:477–91
    [Google Scholar]
  60. 60. 
    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 16:319–31
    [Google Scholar]
  61. 61. 
    Li W, Nishiyama R, Watanabe Y, Van Ha C, Kojima M et al. 2018. Effects of overproduced ethylene on the contents of other phytohormones and expression of their key biosynthetic genes. Plant Physiol. Biochem. 128:170–77
    [Google Scholar]
  62. 62. 
    Liu L, Sonbol F-M, Huot B, Gu Y, Withers J et al. 2016. Salicylic acid receptors activate jasmonic acid signalling through a non-canonical pathway to promote effector-triggered immunity. Nat. Commun. 7:13099
    [Google Scholar]
  63. 63. 
    Liu T, Song T, Zhang X, Yuan H, Su L et al. 2014. Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis. Nat. Commun. 5:4686
    [Google Scholar]
  64. 64. 
    Liu Y, Sun T, Sun Y, Zhang Y, Radojičić A et al. 2020. Diverse roles of the salicylic acid receptors NPR1 and NPR3/NPR4 in plant immunity. Plant Cell 32:4002–16Showed the diverse roles of SA receptors in PTI, ET, and SAR and feedback regulation of SA accumulation.
    [Google Scholar]
  65. 65. 
    Lolle S, Greeff C, Petersen K, Roux M, Jensen MK et al. 2017. Matching NLR immune receptors to autoimmunity in camta3 mutants using antimorphic NLR alleles. Cell Host Microbe 21:518–29.e4
    [Google Scholar]
  66. 66. 
    Lowe-Power TM, Jacobs JM, Ailloud F, Fochs B, Prior P, Allen C 2016. Degradation of the plant defense signal salicylic acid protects Ralstonia solanacearum from toxicity and enhances virulence on tobacco. mBio 7:e00656–16
    [Google Scholar]
  67. 67. 
    Mackelprang R, Okrent RA, Wildermuth MC. 2017. Preference of Arabidopsis thaliana GH3.5 acyl amido synthetase for growth versus defense hormone acyl substrates is dictated by concentration of amino acid substrate aspartate. Phytochemistry 143:19–28
    [Google Scholar]
  68. 68. 
    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 250:1002–4
    [Google Scholar]
  69. 69. 
    Manohar M, Tian M, Moreau M, Park S-W, Choi HW et al. 2015. Identification of multiple salicylic acid-binding proteins using two high throughput screens. Front. Plant Sci. 5:777
    [Google Scholar]
  70. 70. 
    Mao P, Duan M, Wei C, Li Y. 2007. WRKY62 transcription factor acts downstream of cytosolic NPR1 and negatively regulates jasmonate-responsive gene expression. Plant Cell Physiol 58:833–42
    [Google Scholar]
  71. 71. 
    Martínez C, Pons E, Prats G, León J. 2004. Salicylic acid regulates flowering time and links defence responses and reproductive development. Plant J 37:209–17
    [Google Scholar]
  72. 72. 
    Mateo A, Mühlenbock P, Rustérucci C, Chang CC-C, Miszalski Z et al. 2004. LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy. Plant Physiol 136:2818–30
    [Google Scholar]
  73. 73. 
    Mauch-Mani B, Slusarenko AJ. 1996. Production of salicylic acid precursors is a major function of phe-nylalanine ammonia-lyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell 8:203–12
    [Google Scholar]
  74. 74. 
    Melotto M, Underwood W, Koczan J, Nomura K, He SY. 2006. Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–80
    [Google Scholar]
  75. 75. 
    Mercado-Blanco J, van der Drift KM, Olsson PE, Thomas-Oates JE, van Loon LC, Bakker PA. 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. 183:1909–20
    [Google Scholar]
  76. 76. 
    Metraux JP, Signer H, Ryals J, Ward E, Wyss-Benz M et al. 1990. Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250:1004–6
    [Google Scholar]
  77. 77. 
    Miao Y, Zentgraf U. 2007. The antagonist function of Arabidopsis WRKY53 and ESR/ESP in leaf senescence is modulated by the jasmonic and salicylic acid equilibrium. Plant Cell 19:819–30
    [Google Scholar]
  78. 78. 
    Mohan R, Tai T, Chen A, Arnoff T, Fu Z-Q. 2016. Overexpression of Arabidopsis NIMIN1 results in salicylate intolerance. Plant Signal. Behav. 11:e1211222
    [Google Scholar]
  79. 79. 
    Monaghan J, Zipfel C. 2012. Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 15:349–57
    [Google Scholar]
  80. 80. 
    Morris K, Mackerness SAH, Page T, John CF, Murphy AM et al. 2000. Salicylic acid has a role in regulating gene expression during leaf senescence. Plant J 23:677–85
    [Google Scholar]
  81. 81. 
    Mou Z, Fan W, Dong X 2003. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–44
    [Google Scholar]
  82. 82. 
    Mur LA, 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 140:249–62
    [Google Scholar]
  83. 83. 
    Nawrath C, Heck S, Parinthawong N, Metraux 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 14:275–86
    [Google Scholar]
  84. 84. 
    Nawrath C, Metraux 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 11:1393–404
    [Google Scholar]
  85. 85. 
    Ndamukong I, Abdallat AA, Thurow C, Fode B, Zander M et al. 2007. SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA-responsive PDF1.2 transcription. Plant J 50:128–39
    [Google Scholar]
  86. 86. 
    Nickstadt A, Thomma BP, Feussner I, Kangasjärvi J, Zeier J et al. 2004. The jasmonate-insensitive mutant jin1 shows increased resistance to biotrophic as well as necrotrophic pathogens. Mol. Plant Pathol. 5:425–34
    [Google Scholar]
  87. 87. 
    Nobuta K, Okrent RA, Stoutemyer M, Rodibaugh N, Kempema L et al. 2007. The GH3 acyl adenylase family member PBS3 regulates salicylic acid-dependent defense responses in Arabidopsis. Plant Physiol 144:1144–56
    [Google Scholar]
  88. 88. 
    Noutoshi Y, Okazaki M, Kida T, Nishina Y, Morishita Y et al. 2012. Novel plant immune-priming compounds identified via high-throughput chemical screening target salicylic acid glucosyltransferases in Arabidopsis. Plant Cell 24:3795–804
    [Google Scholar]
  89. 89. 
    Ogawa D, Nakajima N, Seo S, Mitsuhara I, Kamada H, Ohashi Y. 2006. The phenylalanine pathway is the main route of salicylic acid biosynthesis in Tobacco mosaic virus-infected tobacco leaves. Plant Biotechnol 23:395–98
    [Google Scholar]
  90. 90. 
    Park J-E, Park J-Y, Kim Y-S, Staswick PE, Jeon J et al. 2007. GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J. Biol. Chem. 282:10036–46
    [Google Scholar]
  91. 91. 
    Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF. 2007. Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318:113–16
    [Google Scholar]
  92. 92. 
    Peng Y, van Wersch R, Zhang Y. 2017. Convergent and divergent signaling in PAMP-triggered immunity and effector-triggered immunity. Mol. Plant Microbe Interact. 31:403–9
    [Google Scholar]
  93. 93. 
    Qi G, Chen J, Chang M, Chen H, Hall K et al. 2018. Pandemonium breaks out: disruption of salicylic acid-mediated defense by plant pathogens. Mol. Plant 11:1427–39
    [Google Scholar]
  94. 94. 
    Qin J, Wang K, Sun L, Xing H, Wang S et al. 2018. The plant-specific transcription factors CBP60g and SARD1 are targeted by a Verticillium secretory protein VdSCP41 to modulate immunity. eLife 7:e34902
    [Google Scholar]
  95. 95. 
    Radojicic A, Li X, Zhang Y. 2018. Salicylic acid: a double-edged sword for programed cell death in plants. Front. Plant Sci. 9:1133
    [Google Scholar]
  96. 96. 
    Rajjou L, Belghazi M, Huguet R, Robin C, Moreau A et al. 2006. Proteomic investigation of the effect of salicylic acid on Arabidopsis seed germination and establishment of early defense mechanisms. Plant Physiol 141:910–23
    [Google Scholar]
  97. 97. 
    Rasmussen JB, Hammerschmidt R, Zook MN. 1991. Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv. syringae. Plant Physiol 97:1342–47
    [Google Scholar]
  98. 98. 
    Rate DN, Greenberg JT. 2001. The Arabidopsis aberrant growth and death2 mutant shows resistance to Pseudomonas syringae and reveals a role for NPR1 in suppressing hypersensitive cell death. Plant J 27:203–11
    [Google Scholar]
  99. 99. 
    Rayapuram C, Baldwin IT. 2007. Increased SA in NPR1-silenced plants antagonizes JA and JA-dependent direct and indirect defenses in herbivore-attacked Nicotiana attenuata in nature. Plant J 52:700–15
    [Google Scholar]
  100. 100. 
    Rekhter D, Ludke D, Ding Y, Feussner K, Zienkiewicz K et al. 2019. Isochorismate-derived biosynthesis of the plant stress hormone salicylic acid. Science 365:498–502Revealed how SA is biosynthesized from isochorismate in the ICS pathway in Arabidopsis.
    [Google Scholar]
  101. 101. 
    Richmond TA, Bleecker AB. 1999. A defect in β-oxidation causes abnormal inflorescence development in Arabidopsis. Plant Cell 11:1911–23
    [Google Scholar]
  102. 102. 
    Rivas-San Vicente M, Plasencia J. 2011. Salicylic acid beyond defence: its role in plant growth and development. J. Exp. Bot. 62:3321–38
    [Google Scholar]
  103. 103. 
    Robatzek S, Somssich IE. 2002. Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes Dev 16:1139–49
    [Google Scholar]
  104. 104. 
    Rochon A, Boyle P, Wignes T, Fobert PR, Despres 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 18:3670–85
    [Google Scholar]
  105. 105. 
    Ryals J, Weymann K, Lawton K, Friedrich L, Ellis D et al. 1997. The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor IκB. Plant Cell 9:425–39
    [Google Scholar]
  106. 106. 
    Saleh A, Withers J, Mohan R, Marques J, Gu Y et al. 2015. Posttranslational modifications of the master transcriptional regulator NPR1 enable dynamic but tight control of plant immune responses. Cell Host Microbe 18:169–82
    [Google Scholar]
  107. 107. 
    Seguel A, Jelenska J, Herrera-Vasquez A, Marr SK, Joyce MB et al. 2018. PROHIBITIN3 forms complexes with ISOCHORISMATE SYNTHASE1 to regulate stress-induced salicylic acid biosynthesis in Arabidopsis. Plant Physiol 176:2515–31
    [Google Scholar]
  108. 108. 
    Serrano M, Wang B, Aryal B, Garcion C, Abou-Mansour E et al. 2013. Export of salicylic acid from the chloroplast requires the multidrug and toxin extrusion-like transporter EDS5. Plant Physiol 162:1815–21
    [Google Scholar]
  109. 109. 
    Shah J, Tsui F, Klessig DF. 1997. Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Mol. Plant Microbe Interact. 10:69–78
    [Google Scholar]
  110. 110. 
    Shine MB, Yang J-W, El-Habbak M, Nagyabhyru P, Fu D-Q et al. 2016. Cooperative functioning between phenylalanine ammonia lyase and isochorismate synthase activities contributes to salicylic acid biosynthesis in soybean. New Phytol 212:627–36
    [Google Scholar]
  111. 111. 
    Skelly MJ, Furniss JJ, Grey H, Wong K-W, Spoel SH. 2019. Dynamic ubiquitination determines transcriptional activity of the plant immune coactivator NPR1. eLife 8:e47005
    [Google Scholar]
  112. 112. 
    Spoel SH, Koornneef A, Claessens SMC, Korzelius JP, Van Pelt JA et al. 2003. NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–70
    [Google Scholar]
  113. 113. 
    Spoel SH, Mou Z, Tada Y, Spivey NW, Genschik P, Dong X. 2009. Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 137:860–72
    [Google Scholar]
  114. 114. 
    Staswick PE. 2008. JAZing up jasmonate signaling. Trends Plant Sci 13:66–71
    [Google Scholar]
  115. 115. 
    Sun T, Busta L, Zhang Q, Ding P, Jetter R, Zhang Y. 2018. TGACG-BINDING FACTOR 1 (TGA1) and TGA4 regulate salicylic acid and pipecolic acid biosynthesis by modulating the expression of SYSTEMIC ACQUIRED RESISTANCE DEFICIENT 1 (SARD1) and CALMODULIN-BINDING PROTEIN 60g (CBP60g). New Phytol 217:344–54
    [Google Scholar]
  116. 116. 
    Sun T, Huang J, Xu Y, Verma V, Jing B et al. 2020. Redundant CAMTA transcription factors negatively regulate the biosynthesis of salicylic acid and N-hydroxypipecolic acid by modulating the expression of SARD1 and CBP60g. Mol. Plant 13:144–56
    [Google Scholar]
  117. 117. 
    Sun T, Liang W, Zhang Y, Li X. 2018. Negative regulation of resistance protein-mediated immunity by master transcription factors SARD1 and CBP60g. J. Integr. Plant Biol. 60:1023–27
    [Google Scholar]
  118. 118. 
    Sun T, Zhang Y, Li Y, Zhang Q, Ding Y, Zhang Y. 2015. ChIP-seq reveals broad roles of SARD1 and CBP60g in regulating plant immunity. Nat. Commun. 6:10159
    [Google Scholar]
  119. 119. 
    Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J et al. 2008. Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–56
    [Google Scholar]
  120. 120. 
    Tan S, Abas M, Verstraeten I, Glanc M, Molnár G et al. 2020. Salicylic acid targets protein phosphatase 2A to attenuate growth in plants. Curr. Biol. 30:381–95.e8
    [Google Scholar]
  121. 121. 
    Torrens-Spence MP, Bobokalonova A, Carballo V, Glinkerman CM, Pluskal T et al. 2019. PBS3 and EPS1 complete salicylic acid biosynthesis from isochorismate in Arabidopsis. Mol. Plant 12:1577–86Showed how SA is produced from isochorismate in the ICS pathway.
    [Google Scholar]
  122. 122. 
    Tsuda K, Sato M, Glazebrook J, Cohen JD, Katagiri F. 2008. Interplay between MAMP-triggered and SA-mediated defense responses. Plant J 53:763–75
    [Google Scholar]
  123. 123. 
    Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F. 2009. Network properties of robust immunity in plants. PLOS Genet 5:e1000772
    [Google Scholar]
  124. 124. 
    van Verk MC, Bol JF, Linthorst HJ. 2011. WRKY transcription factors involved in activation of SA biosynthesis genes. BMC Plant Biol 11:89
    [Google Scholar]
  125. 125. 
    van Wersch R, Li X, Zhang Y 2016. Mighty dwarfs: Arabidopsis autoimmune mutants and their usages in genetic dissection of plant immunity. Front. Plant Sci. 7:1717
    [Google Scholar]
  126. 126. 
    van Wersch S, Tian L, Hoy R, Li X. 2020. Plant NLRs: the whistleblowers of plant immunity. Plant Commun 1:100016
    [Google Scholar]
  127. 127. 
    Volz R, Kim SK, Mi J, Mariappan KG, Guo X et al. 2018. The Trihelix transcription factor GT2-like 1 (GTL1) promotes salicylic acid metabolism, and regulates bacterial-triggered immunity. PLOS Genet 14:e1007708
    [Google Scholar]
  128. 128. 
    Wang D, Amornsiripanitch 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
    [Google Scholar]
  129. 129. 
    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. 17:1784–90
    [Google Scholar]
  130. 130. 
    Wang G-F, Seabolt S, Hamdoun S, Ng G, Park J, Lu H. 2011. Multiple roles of WIN3 in regulating disease resistance, cell death, and flowering time in Arabidopsis. Plant Physiol 156:1508–19
    [Google Scholar]
  131. 131. 
    Wang L, Tsuda K, Sato M, Cohen JD, Katagiri F, Glazebrook J. 2009. Arabidopsis CaM binding protein CBP60g contributes to MAMP-induced SA accumulation and is involved in disease resistance against Pseudomonas syringae. PLOS Pathog 5:e1000301
    [Google Scholar]
  132. 132. 
    Wang L, Tsuda K, Truman W, Sato M, Nguyen LV et al. 2011. CBP60g and SARD1 play partially redundant critical roles in salicylic acid signaling. Plant J 67:1029–41
    [Google Scholar]
  133. 133. 
    Wang W, Withers J, Li H, Zwack PJ, Rusnac D-V et al. 2020. Structural basis of salicylic acid perception by Arabidopsis NPR proteins. Nature 586:311–16Revealed how SA is bound to its receptors by crystal structure analysis.
    [Google Scholar]
  134. 134. 
    Wang X, Gao J, Zhu Z, Dong X, Wang X et al. 2015. TCP transcription factors are critical for the coordinated regulation of ISOCHORISMATE SYNTHASE 1 expression in Arabidopsis thaliana. Plant J 82:151–62
    [Google Scholar]
  135. 135. 
    Wang X, Sager R, Cui W, Zhang C, Lu H, Lee J-Y. 2013. Salicylic acid regulates plasmodesmata closure during innate immune responses in Arabidopsis. Plant Cell 25:2315–29
    [Google Scholar]
  136. 136. 
    Wang Y, Guo H. 2019. On hormonal regulation of the dynamic apical hook development. New Phytol 222:1230–34
    [Google Scholar]
  137. 137. 
    Weigel RR, Pfitzner UM, Gatz C. 2005. Interaction of NIMIN1 with NPR1 Modulates PR Gene Expression in Arabidopsis. Plant Cell 17:1279–91
    [Google Scholar]
  138. 138. 
    White RF. 1979. Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. Virology 99:410–12
    [Google Scholar]
  139. 139. 
    Wildermuth MC, Dewdney J, Wu G, Ausubel FM. 2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–65Revealed that pathogen-induced SA is mainly produced from the ICS pathway in Arabidopsis.
    [Google Scholar]
  140. 140. 
    Wu Y, Zhang D, Chu JY, Boyle P, Wang Y et al. 2012. The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep 1:639–47
    [Google Scholar]
  141. 141. 
    Xu L, Zhao H, Ruan W, Deng M, Wang F et al. 2017. ABNORMAL INFLORESCENCE MERISTEM1 functions in salicylic acid biosynthesis to maintain proper reactive oxygen species levels for root meristem activity in rice. Plant Cell 29:560–74
    [Google Scholar]
  142. 142. 
    Yalpani N, León J, Lawton MA, Raskin I. 1993. Pathway of salicylic acid biosynthesis in healthy and virus-inoculated tobacco. Plant Physiol 103:315–21
    [Google Scholar]
  143. 143. 
    Yang L, Li B, Zheng X-Y, Li J, Yang M et al. 2015. Salicylic acid biosynthesis is enhanced and contributes to increased biotrophic pathogen resistance in Arabidopsis hybrids. Nat. Commun. 6:7309
    [Google Scholar]
  144. 144. 
    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 13:1527–40
    [Google Scholar]
  145. 145. 
    Yuan H-M, Liu W-C, Lu Y-T. 2017. CATALASE2 coordinates SA-mediated repression of both auxin accumulation and JA biosynthesis in plant defenses. Cell Host Microbe 21:143–55
    [Google Scholar]
  146. 146. 
    Zavaliev R, Mohan R, Chen T, Dong X 2020. Formation of NPR1 condensates promotes cell survival during the plant immune response. Cell 182:1093–108.e18
    [Google Scholar]
  147. 147. 
    Zeilmaker T, Ludwig NR, Elberse J, Seidl MF, Berke L et al. 2015. DOWNY MILDEW RESISTANT 6 and DMR 6-LIKE OXYGENASE 1 are partially redundant but distinct suppressors of immunity in Arabidopsis. Plant J 81:210–22
    [Google Scholar]
  148. 148. 
    Zhang K, Halitschke R, Yin C, Liu C-J, Gan S-S 2013. Salicylic acid 3-hydroxylase regulates Arabidopsis leaf longevity by mediating salicylic acid catabolism. PNAS 110:14807–12
    [Google Scholar]
  149. 149. 
    Zhang X, Liu C-J. 2015. Multifaceted regulations of gateway enzyme phenylalanine ammonia-lyase in the biosynthesis of phenylpropanoids. Mol. Plant 8:17–27
    [Google Scholar]
  150. 150. 
    Zhang X, Wang C, Zhang Y, Sun Y, Mou Z. 2012. The Arabidopsis Mediator complex subunit16 positively regulates salicylate-mediated systemic acquired resistance and jasmonate/ethylene-induced defense pathways. Plant Cell 24:4294–309
    [Google Scholar]
  151. 151. 
    Zhang X, Yao J, Zhang Y, Sun Y, Mou Z. 2013. The Arabidopsis Mediator complex subunits MED14/SWP and MED16/SFR6/IEN1 differentially regulate defense gene expression in plant immune responses. Plant J 75:484–97
    [Google Scholar]
  152. 152. 
    Zhang Y, Cheng YT, Qu N, Zhao Q, Bi D, Li X. 2006. Negative regulation of defense responses in Arabidopsis by two NPR1 paralogs. Plant J 48:647–56
    [Google Scholar]
  153. 153. 
    Zhang Y, Fan W, Kinkema M, Li X, Dong X 1999. Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. PNAS 96:6523–28
    [Google Scholar]
  154. 154. 
    Zhang Y, Goritschnig S, Dong X, Li X 2003. A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1-1, constitutive 1. Plant Cell 15:2636–46
    [Google Scholar]
  155. 155. 
    Zhang Y, Li X. 2019. Salicylic acid: biosynthesis, perception, and contributions to plant immunity. Curr. Opin. Plant Biol. 50:29–36
    [Google Scholar]
  156. 156. 
    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 15:2647–53
    [Google Scholar]
  157. 157. 
    Zhang Y, Xu S, Ding P, Wang D, Cheng YT et al. 2010. Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. PNAS 107:18220–25Identified SARD1 and CBP60g as two key transcription factors for controlling SA biosynthesis during pathogen infection.
    [Google Scholar]
  158. 158. 
    Zhang Y, Yang Y, Fang B, Gannon P, Ding P, Li X. 2010. Arabidopsis snc2-1D activates receptor-like protein-mediated immunity transduced through WRKY70. Plant Cell 22:3153–63
    [Google Scholar]
  159. 159. 
    Zhang Y, Zhao L, Zhao J, Li Y, Wang J et al. 2017. S5H/DMR6 encodes a salicylic acid 5-hydroxylase that fine-tunes salicylic acid homeostasis. Plant Physiol 175:1082–93
    [Google Scholar]
  160. 160. 
    Zheng XY, Spivey NW, Zeng W, Liu PP, Fu ZQ et al. 2012. Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 11:587–96
    [Google Scholar]
  161. 161. 
    Zheng XY, Zhou M, Yoo H, Pruneda-Paz JL, Spivey NW et al. 2015. Spatial and temporal regulation of biosynthesis of the plant immune signal salicylic acid. PNAS 112:9166–73
    [Google Scholar]
  162. 162. 
    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 57:1040–53
    [Google Scholar]
  163. 163. 
    Zhou JM, Zhang Y. 2020. Plant immunity: danger perception and signaling. Cell 181:978–89
    [Google Scholar]
  164. 164. 
    Zhou M, Lu Y, Bethke G, Harrison BT, Hatsugai N et al. 2018. WRKY70 prevents axenic activation of plant immunity by direct repression of SARD1. New Phytol 217:700–12
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-081320-092855
Loading
/content/journals/10.1146/annurev-arplant-081320-092855
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error