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Salicylic Acid Signaling in Plant Innate Immunity

  • P. Vidhyasekaran
Chapter
Part of the Signaling and Communication in Plants book series (SIGCOMM, volume 2)

Abstract

Plants are endowed with innate immune system to protect against invading pathogens. The innate immune system serves as a surveillance system against possible attack by viral, bacterial, fungal, and oomycete pathogens. The innate immune system is a sleeping giant to fight against pathogens, and specific signals are needed to activate them. The pathogen’s signature, pathogen-associated molecular pattern (PAMP), switches on the plant innate immune system. The PAMPs are perceived as alarm signals by plant pattern recognition receptors (PRRs), which have a “receptor” and a “signaling domain” in one molecule to perceive and transduce the PAMP signal. Several second messengers are involved in delivering the message generated by the PAMP/PRR signaling complex to plant hormone signals. Salicylic acid (SA) is the important endogenous plant hormone signal in delivering the extracellular PAMP message into the plant cell to initiate the transcription of defense genes. PAMP signaling system generates specific Ca2+ signature in the cytosol, which triggers SA biosynthesis. The information encoded in calcium signature is decoded by an array of calmodulins. A calmodulin-binding protein, CBP60g, has been shown to be involved in activating SA biosynthesis. Calcium signature signals transduced to calmodulin-binding protein CBP60g trigger activation of isochorismate synthase in SA biosynthesis pathway. ROS also acts upstream of SA accumulation. H2O2 causes an intracellular accumulation of benzoic acid (BA), and the conversion of BA to SA is catalyzed by benzoic acid 2-hydroxylase (BA2H), an inducible enzyme that is synthesized de novo in response to increased BA level. Nitric oxide (NO) activates SA biosynthesis pathway, by inducing phenylalanine ammonia lyase (PAL) which is a key enzyme in biosynthesis of salicylic acid. Several MAP kinase cascades have been shown to act upstream of SA signaling system. SA signaling induces increased expression of transcription factors to activate SA-responsive defense-related genes. NPR1 is a master regulator of the SA-mediated induction of defense genes. NPR1 directly binds SA and binding of SA occurs through Cys521/529 via the transition metal copper. Nuclear localization of NPR1 protein is essential for its function. In the absence of pathogen challenge, NPR1 is retained in the cytoplasm. Without induction, NPR1 protein forms an oligomer and is excluded from the nucleus. Pathogen/PAMP exposure induces SA accumulation, and the induced SA controls the nuclear translocation of NPR1 through cellular redox changes. In the absence of pathogen challenge, NPR1 is continuously cleared from the nucleus by proteasome, which restricts its co-activator activity to prevent untimely activation of defense responses. Two NPR1 paralogues, NPR3 and NPR4, have been identified as adaptor proteins of the CUL3 E3 ligase, and they target NPR1 degradation in an SA concentration-dependent manner. At increased SA concentration after infection, SA binds to NPR4, and NPR1, freed from NPR4 binding, activates transcription of defense genes. NPR1 is a cofactor of TGA transcription factors, and it enhances binding of TGA transcription factors to the promoter of PR1 gene to activate transcription of PR1 gene. Systemic acquired resistance (SAR) is a salicylic acid-dependent heightened state of defense against a broad spectrum of pathogens activated throughout a plant following a local infection. Methyl salicylate, methyl salicylate esterase, a lipid transfer protein (DIR1), a lipid-derived molecule (glycerol-3-phosphate)-dependent factor, azelaic acid, dehydroabietinal, and pipecolic acid have been suggested to be the systemic mobile signal molecules involved in SAR. Some Mediators have been shown to be involved in triggering SA-mediated SAR. Mediator is a multiprotein complex that functions as a transcriptional coactivator. SAR is associated with priming of defense, and the priming results in a faster and stronger induction of defense mechanisms after pathogen attack. Some dormant MAPKs have been suggested to be important components required for priming. Pipecolic acid is an endogenous mediator of defense priming. SAR involves extensive reprogramming of transcription. SA mediates changes in the expression pattern of about 1,000–2,000 genes. Such a broad effect on gene transcription may be associated with extensive chromatin remodeling. The chromatin remodeling may involve substitution of canonical histones in the octamer by histone variants, in a process known as histone replacement. Chromatin structure is important for the regulation of gene expression, and chromatin states could control cellular memory. The primed genes may be poised for enhanced activation of gene expression by the histone modification in chromatin. There may be a tight correlation between histone modification patterns and gene priming, and also there may be a histone memory for information storage in the plant stress response. NPR1 may be involved in the chromatin modification-induced priming. NPR1 plays important role in inducing high levels of chromatin modification on promoters of the transcription factor genes. Chromatin remodeling may be instrumental for priming of SA-responsive loci to enable their enhanced reactivation upon subsequent pathogen attack. The priming can be inherited epigenetically from disease-exposed plants, and descendants of primed plants exhibit next-generation systemic acquired resistance. The descendants of primed plants showed a faster and higher accumulation of transcripts of defense-related genes in salicylic acid signaling pathway and enhanced disease resistance upon challenge inoculation with virulent pathogens. The transgenerational SAR was found to be sustained over one stress-free generation, indicating an epigenetic basis of the phenomenon. DNA methylation may also play an important role in transgenerational SAR. The transgenerational SAR is transmitted by hypomethylated genes that direct priming of SA-dependent defenses in the following generations.

References

  1. Adie BA, Perez-Perez J, Godoy M, Sanchez-Serrano JJ, Schmelz EA, Solano R (2007) ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and activation of defenses in Arabidopsis. Plant Cell 19:1665–1681PubMedPubMedCentralGoogle Scholar
  2. Ahmad S, Gordon-Weeks R, Pickett J, Ton J (2010) Natural variation in priming of basal resistance: from evolutionary origin to agricultural exploitation. Mol Plant Pathol 11:817–827PubMedGoogle Scholar
  3. Ahn I-P, Kim S, Lee Y-H, Suh S-C (2007) Vitamin B1-induced priming is dependent on hydrogen peroxide and the NPR1 gene in Arabidopsis. Plant Physiol 143:838–848PubMedPubMedCentralGoogle Scholar
  4. Alamillo JM, Saénz P, Garcia JA (2006) Salicylic acid-mediated and RNA-silencing defense mechanisms cooperate in the restriction of systemic spread of plum pox virus in tobacco. Plant J 48:217–227PubMedGoogle Scholar
  5. Allen GJ, Chu SP, Schumacher K, Shimazaki CT, Vafeados D, Kemper A, Hawke SD, Tallman G, Tsien RY, Harper JF, Chory J, Schroeder JI (2000) Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science 289:2338–2342PubMedGoogle Scholar
  6. Alvarado VY, Scholthof HB (2009) Plant responses against invasive nucleic acids: RNA silencing and its suppression by plant viral pathogens. Semin Cell Dev Biol 20:1032–1040PubMedPubMedCentralGoogle Scholar
  7. Alvarez ME, Nota F, Cambiagno DA (2010) Epigenetic control of plant immunity. Mol Plant Pathol 11:563–576PubMedGoogle Scholar
  8. Amzalek E, Cohen Y (2007) Comparative efficacy of systemic acquired resistance-inducing compounds against rust infection in sunflower plants. Phytopathology 97:179–186PubMedGoogle Scholar
  9. An C, Mou Z (2013) The function of the Mediator complex in plant immunity. Plant Signal Behav 8:e23182PubMedPubMedCentralGoogle Scholar
  10. Anand A, Uppalapati SR, Ryu C-M, Allen SN, Kang L, Tang Y, Mysore KS (2008) Salicylic acid and systemic acquired resistance play a role in attenuating crown gall disease caused by Agrobacterium tumefaciens. Plant Physiol 146:703–715PubMedPubMedCentralGoogle Scholar
  11. Andreasson E, Jenkins T, Brodersen P, Thorgrimsen S, Petersen NHT, Zhu S, Qiu J-L, Micheelsen P, Rocher A, Petersen M, Newman A, Nielsen HB, Hirt H, Somssich I, Mattsson O, Mundy J (2005) The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO J 24:2579–2589PubMedCentralGoogle Scholar
  12. Anfoka GH (2000) Benzo-(1,2,3)-thiadiazole-7-carbothioic acid-S-methyl ester induces systemic resistance in tomato (Lycopersicon esculentum Mill. cv. volledung) to cucumber mosaic virus. Crop Prot 19:401–405Google Scholar
  13. Argueso CT, Ferreira FJ, Epple P, To JPC, Hutchison CE, Schaller GE, Dangl JL, Kieber JJ (2012) Two-component elements mediate interactions between cytokinin and salicylic acid in plant immunity. PLoS Genet 8(1):e1002448PubMedPubMedCentralGoogle Scholar
  14. Arif M, Selvi BR, Kundu TK (2010) Lysine acetylation: the tale of a modification from transcription regulation to metabolism. ChemBioChem 11:1501–1504Google Scholar
  15. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396PubMedPubMedCentralGoogle Scholar
  16. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu W-L, Gómez-Gómez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977–983PubMedGoogle Scholar
  17. Atsumi G, Kagaya U, Kitazawa H, Nakahara KS, Uyeda I (2009) Activation of the salicylic acid signaling pathway enhances Clover yellow vein virus virulence in susceptible pea cultivars. Mol Plant-Microbe Interact 22:166–175PubMedGoogle Scholar
  18. 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 21:954–971PubMedPubMedCentralGoogle Scholar
  19. Audenaert K, De Meyer GB, Höfte MM (2002) Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid- dependent signaling mechanisms. Plant Physiol 128:491–501PubMedPubMedCentralGoogle Scholar
  20. Azevedo C, Sadanandom A, Kitagawa K, Freialdenhoven A, Shirasu K, Schulze-Lefert P (2002) The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295:2073–2076PubMedGoogle Scholar
  21. Azevedo C, Betsuyaku S, Peart J, Takahashi A, Noel L, Sadanandom A, Casals C, Parker J, Shirasu K (2006) Role of SGT1 in resistance protein accumulation in plant immunity. EMBO J 25:2007–2016PubMedPubMedCentralGoogle Scholar
  22. Bartetzko V, Sonnewald S, Vogel F, Hartner K, Stadler R, Hammes UZ, Bornke F (2009) The Xanthomonas campestris pv. vesicatoria type III effector protein XopJ inhibits protein secretion: evidence for interference with cell wall-associated defense responses. Mol Plant-Microbe Interact 22:655–664Google Scholar
  23. Bartsch M, Gobbato E, Bednarek P, Debey S, Schultze J, Bautor J, Parker JE (2006) Salicylic acid-independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the nudix hydrolase NUDT7. Plant Cell 18:1038–1051PubMedPubMedCentralGoogle Scholar
  24. Beckers GJM, Conrath U (2007) Priming for stress resistance: from the lab to the field. Curr Opin Plant Biol 10:425–431PubMedGoogle Scholar
  25. Beckers GJM, Jaskiewicz M, Liu Y, Underwood WR, He SY, Zhang S, Conrath U (2009) Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21:944–953PubMedPubMedCentralGoogle Scholar
  26. Beffa R, Szell M, Meuwly P, Pay A, Vogeli-Lange R, Metraux JP, Neuhaus G, Meins F, Ferenc N (1995) Cholera toxin elevates pathogen resistance and induces pathogenesis-related gene expression in tobacco. EMBO J 14:5753–5761PubMedPubMedCentralGoogle Scholar
  27. Bellin D, Asai DM, Yoshioka H (2013) Nitric oxide as a mediator for defense responses. Mol Plant Microbe Interact 26:271–277PubMedGoogle Scholar
  28. Bender J (2004) Chromatin-based silencing mechanisms. Curr Opin Plant Biol 7:521–526PubMedGoogle Scholar
  29. Benhar M, Forrester MT, Hess DT, Stamler JS (2008) Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins. Science 320:1050–1054PubMedPubMedCentralGoogle Scholar
  30. Berger SL (2002) Histone modifications in transcriptional regulation. Curr Opin Genet Dev 2:142–148Google Scholar
  31. Berrocal-Lobo M, Molina A, Solano R (2002) Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J 29:23–32PubMedGoogle Scholar
  32. Block A, Alfano JR (2011) Plant targets for Pseudomonas syringae type III effectors: virulence targets or guarded decoys? Curr Opin Microbiol 14:39–46PubMedCentralGoogle Scholar
  33. Block A, Li G, Fu ZQ, Alfano JR (2008) Phytopathogen type III effector weaponry and their plant targets. Curr Opin Plant Biol 11:396–403PubMedPubMedCentralGoogle Scholar
  34. Boller T, He SY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742–744PubMedPubMedCentralGoogle Scholar
  35. Bolwell GP, Butt VS, Davies DR, Zimmerlin A (1995) The origin of the oxidative burst in plants. Free Radical Res 23:517–532Google Scholar
  36. Bolwell GP, Davies DR, Gerrish C, Auh C-K, Murphy TM (1998) Comparative biochemistry of the oxidative burst produced by rose and French bean cells reveals two distinct mechanisms. Plant Physiol 116:1379–1385PubMedPubMedCentralGoogle Scholar
  37. Bouché N, Scharlat A, Snedden WA, Bouchez D, Fromm H (2002) A novel family of calmodulin-binding transcription activators in multicellular organisms. J Biol Chem 277:21851–21861PubMedGoogle Scholar
  38. Boursiac Y, Lee SM, Romanowsky S, Blank R, Stadek C, Chung WS, Harper JF (2010) Disruption of the vacuolar calcium-ATPase in Arabidopsis results in the activation of a salicylic acid-dependent programmed cell death pathway. Plant Physiol 154:1158–1171PubMedPubMedCentralGoogle Scholar
  39. Britton LM, Gonzales-Cope M, Zee BM, Garcia BA (2011) Breaking the histone code with quantitative mass spectrometry. Expert Rev Proteomics 8:631–643PubMedPubMedCentralGoogle Scholar
  40. Brodersen P, Petersen M, Bjorn Nielsen H, 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 47:532–546PubMedGoogle Scholar
  41. Brooks DM, Bender CL, Kunkel BN (2005) The Pseudomonas syringae phytotoxin coronatine promotes virulence by overcoming salicylic acid-dependent defenses in Arabidopsis thaliana. Mol Plant Pathol 6:629–639PubMedGoogle Scholar
  42. Camañes G, Pastor V, Cerezo M, Garcia-Andrade J, Vicedo B, Garcia-Agustin P, Flors V (2012) A deletion in NRT2.1 attenuates Pseudomonas syringae-induced hormonal perturbation, resulting in primed plant defenses. Plant Physiol 158:1054–1066PubMedPubMedCentralGoogle Scholar
  43. 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 24:4220–4235PubMedPubMedCentralGoogle Scholar
  44. Cao H, Glazebrook J, Clarke J, Volko S, Dong X (1997) The Arabidopsis npr1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57–63PubMedGoogle Scholar
  45. Cao X, Aufsatz W, Zilberman D, Mette MF, Jacobsen SE (2003) Role of the DRM and CMT3 methyltransferases in RNA-directed DNA methylation. Curr Biol 13:2212–2217PubMedGoogle Scholar
  46. Carr JP, Lewsey MG, Palukaitis P (2010) Signaling in induced resistance. Adv Virus Res 76:57–121PubMedGoogle Scholar
  47. 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 582:473–478PubMedGoogle Scholar
  48. Cevik V, Kidd BN, Zhang P, Hill C, Kiddle S, Denby KJ, Holub EB, Cahill DM, Manners JM, Schenk PM, Beynon J, Kazan K (2012) MEDIATOR25 acts as an integrative hub for the regulation of jasmonate-responsive gene expression in Arabidopsis. Plant Physiol 160:541–555PubMedPubMedCentralGoogle Scholar
  49. Chadha KC, Brown SA (1974) Biosynthesis of phenolic acids in tomato plants infected with Agrobacterium tumefaciens. Can J Bot 52:2041–2047Google Scholar
  50. Chanda B, Xia Y, Mandal MK, Yu K, Sekine K-T, Gao Q-M, Selote D, Hu Y, Stromberg A, Navarre D, Kachroo A, Kachroo P (2011) Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nat Genet 43:421–427PubMedGoogle Scholar
  51. Chaturvedi R, Krothapalli K, Makandar R, Nandi A, Sparks AA, Roth MR, Welti R, Shah J (2008) Plastid omega3-fatty acid desaturase-dependent accumulation of a systemic acquired resistance inducing activity in petiole exudates of Arabidopsis thaliana is independent of jasmonic acid. Plant J 54:106–117PubMedGoogle Scholar
  52. Chaturvedi R, Venables B, Petros RA, Nalam V, Li M, Wang X, Takemoto LJ, Shah J (2012) An abietane diterpenoid is a potent activator of systemic acquired resistance. Plant J 71:161–172PubMedGoogle Scholar
  53. Chellappan P, Vanitharani R, Ogbe F, Fauquet CM (2005) Effect of temperature on Geminivirus-induced RNA silencing in plants. Plant Physiol 138:1828–1841PubMedPubMedCentralGoogle Scholar
  54. Chen C, Chen Z (2002) Potentiation of developmentally regulated defense response by AtWRKY18, a pathogen-induced Arabidopsis transcription factor. Plant Physiol 129:706–716PubMedPubMedCentralGoogle Scholar
  55. Chen Z, Klessig DF (1991) Identification of a soluble salicylic acid-binding protein that may function in signal transduction in the plant disease resistance response. Proc Natl Acad Sci U S A 90:9533–9537Google Scholar
  56. Chen ZX, Ricigliano JW, Klessig DF (1993) Purification and characterization of a soluble salicylic acid-binding protein that may function in signal from tobacco. Proc Natl Acad Sci U S A 90:9533–9537PubMedPubMedCentralGoogle Scholar
  57. Chen Z, Zheng Z, Huang J, Lai Z, Fan B (2009) Biosynthesis of salicylic acid in plants. Plant Signal Behav 4:493–496PubMedPubMedCentralGoogle Scholar
  58. Chen X, Hu Y, Zhou DX (2011) Epigenetic gene regulation by plant Jumonji group of histone demethylase. Biochim Biophys Acta 1809:421–426PubMedGoogle Scholar
  59. Chen R, Jiang H, Li L, Zhai Q, Qi L, Zhou W, Liu X, Li H, Zheng W, Sun J, Li C (2012) The Arabidopsis mediator subunit MED25 differentially regulates jasmonate and abscisic acid signaling through interacting with MYC2 and ABI5 transcription factors. Plant Cell 24:2898–2916PubMedPubMedCentralGoogle Scholar
  60. Cheong YH, Moon BC, Kim JK, Kim CY, Kim MC, Kim IH, Park CY, Kim JC, Park BO, Koo SC, Yoon HW, Chung WS, Lim CO, Lee SY, Cho MJ (2003) BWMK1, a rice mitogen-activated protein kinase, locates in the nucleus and mediates pathogenesis-related gene expression by activation of a transcription factor. Plant Physiol 132:1961–1972PubMedPubMedCentralGoogle Scholar
  61. Chern M-S, Fitzgerald H, Yadav RC, Canlas PE, Dong X, Ronald PC (2001) Evidence for a disease-resistance pathway in rice similar to the NPR1-mediated signaling pathway in Arabidopsis. Plant J 27:101–113PubMedGoogle Scholar
  62. Chern M, 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 18:511–520PubMedGoogle Scholar
  63. Chern M, Canlas PE, Ronald PC (2008) Strong suppression of systemic acquired resistance in Arabidopsis by NRR is dependent on its ability to interact with NPR1 and its putative repressive domain. Mol Plant 1:552–559PubMedGoogle Scholar
  64. Chini A, Fonseca S, Fernández G, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, Lόpez-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signaling. Nature 448:666–671PubMedGoogle Scholar
  65. Chini A, Fonseca S, Chico JM, Fernández-Calvo P, Solano R (2009) The ZIM domain mediates homo- and heteromeric interactions between Arabidopsis JAZ proteins. Plant J 59:77–87PubMedGoogle Scholar
  66. Chivasa S, Murphy AM, Naylor M, Carr JP (1997) Salicylic acid interferes with tobacco mosaic virus replication as a novel salicylhydroxamic acid-sensitive mechanism. Plant Cell 9:547–557PubMedPubMedCentralGoogle Scholar
  67. Choi J, Huh SU, Kojima M, Sakakibara H, Paek K-H, Hwang I (2010) The cytokinin-activated transcription factor ARR2 promotes plant immunity via TGA3/NPR1-dependent salicylic acid signaling in Arabidopsis. Dev Cell 19:284–295PubMedGoogle Scholar
  68. Choi J, Choi D, Lee R, Ryu CM, Hwang I (2011) Cytokinins and plant immunity: old foes or new friends. Trends Plant Sci 16:388–394Google Scholar
  69. Chong J, Pierrel M-A, Atanassova R, Werck-Reichhart D, Fritig B, Saindrenan PS (2001) Free and conjugated benzoic acid in tobacco plants and cell cultures. Induced accumulation upon elicitation of defense responses and role as salicylic acid precursors. Plant Physiol 125:318–328PubMedCentralGoogle Scholar
  70. Chun HJ, Park HC, Koo SC, Lee JH, Park CY, Choi MS, Kang CH, Baek D, Cheong YH, Yun DJ, Chung WS, Cho MJ, Kim MC (2012) Constitutive expression of mammalian nitric oxide synthase in tobacco plants triggers disease resistance to pathogens. Mol Cells 34:463–471PubMedPubMedCentralGoogle Scholar
  71. Clark D, Durner J, Navarre DA, Klessig DF (2000) Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol Plant-Microbe Interact 13:1380–1384PubMedGoogle Scholar
  72. Clarke JD, Volko SM, Ledford H, Ausubel FM, Dong X (2000) Roles of salicylic acid, jasmonic acid, and ethylene in cpr-induced resistance in Arabidopsis. Plant Cell 12:2175–2190PubMedPubMedCentralGoogle Scholar
  73. Conaway RC, Conaway JW (2011a) Function and regulation of the Mediator complex. Curr Opin Genet Dev 21:225–230PubMedPubMedCentralGoogle Scholar
  74. Conaway RC, Conaway JW (2011b) Origin and activity of the Mediator complex. Semin Cell Dev Biol 22:729–734PubMedPubMedCentralGoogle Scholar
  75. Conrath U (2009) Priming of induced plant defense responses. Adv Bot Res 51:361–395Google Scholar
  76. Conrath U (2011) Molecular aspects of defence priming. Trends Plant Sci 16:524–531PubMedGoogle Scholar
  77. Conrath U, Chen Z, Ricigliano JR, Klessig DF (1995) Two inducers of plant defense responses, 2,6-dichloroisonicotinic acid and salicylic acid, inhibit catalase activity in tobacco. Proc Natl Acad Sci U S A 92:7143–7147PubMedPubMedCentralGoogle Scholar
  78. Conrath U, Klessig DF, Bachmair A (1998) Tobacco plants perturbed in the ubiquitin-dependent protein degradation system accumulate callose, salicylic acid, and pathogenesis-related protein 1. Plant Cell Rep 17:876–880Google Scholar
  79. Conrath U, Thulke O, Katz V, Schwindling S, Kohler A (2001) Priming as a mechanism in induced systemic resistance of plants. Eur J Plant Pathol 107:113–119Google Scholar
  80. Conrath U, Pieterse CMJ, Mauch-Mani B (2002) Priming in plant-pathogen interactions. Trends Plant Sci 7:210–216PubMedGoogle Scholar
  81. Conrath U, Beckers GJM, Flors V, Garcia-Agustin P, Jakab G, Mauch F, Newman M-A, Pieterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B (2006) Priming: getting ready for battle. Mol Plant-Microbe Interact 19:1062–1071PubMedGoogle Scholar
  82. Cools HJ, Ishii H (2002) Pre-treatment of cucumber plants with acibenzolar-S-methyl systemically primes a phenylalanine ammonia lyase gene (PAL1) for enhanced expression upon attack with a pathogenic fungus. Physiol Mol Plant Pathol 61:273–280Google Scholar
  83. Daudi A, Cheng Z, O’Brein JA, Mammarella N, Khan S, Ausubel FM, Bolwell GP (2012) The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity. Plant Cell 24:275–287PubMedPubMedCentralGoogle Scholar
  84. de Jonge R, Thomma BPHJ (2009) Fungal LysM effectors: extinguishers of host immunity? Trends Microbiol 17:151–157PubMedGoogle Scholar
  85. de Jonge R, van Esse HP, Kombrink A, Shinya T, Desaki Y, Bours R, van der Krol S, Shibuya N, Joosten MHAJ, Thomma BPHJ (2010) Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329:953–955PubMedGoogle Scholar
  86. de Torres M, Mansfield JW, Grabov N, Brown IR, Ammouneh H, Tsiamis G, Forsyth A, Robatzek S, Grant M, Boch J (2006) Pseudomonas syringae effector AvrPtroB suppresses basal defence in Arabidopsis. Plant J 47:368–382PubMedGoogle Scholar
  87. de Torres-Zabala M, Bennett MH, Truman WH, Grant MR (2009) Antagonism between salicylic and abscisic acid reflects early host-pathogen conflict and moulds plant defense responses. Plant J 59:375–386PubMedGoogle Scholar
  88. De Vleeschauwer D, Van Buyten E, Satoh K, Balidion J, Mauleon R, Choi I-R, Vera-Cruz C, Kikuchi S, Höfte M (2012) Brassinosteroids antagonize gibberellin- and salicylate-mediated root immunity in rice. Plant Physiol 158:1833–1846Google Scholar
  89. Dean JV, Mohammed LA, Fitzpatrick T (2005) The formation, vacuolar localization, and tonoplast transport salicylic acid glucose conjugates in tobacco cell suspension cultures. Planta 221:287–296PubMedGoogle Scholar
  90. DebRoy S, Thilmony R, Kwack Y-B, Nomura K, He S-Y (2004) A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants. Proc Natl Acad Sci U S A 101:9927–9932PubMedPubMedCentralGoogle Scholar
  91. Deepak SA, Ishii A, Park P (2006) Acibenzolar-S-methyl primes cell wall strengthening genes and reactive oxygen species forming/scavenging enzymes in cucumber after fungal pathogen attack. Physiol Mol Plant Pathol 69:52–61Google Scholar
  92. DeFalco TA, Bender KW, Snedden WA (2010) Breaking the code: Ca2+ sensors in plant signalling. Biochem J 425:27–40Google Scholar
  93. Dellagi A, Helibronn J, Avrova AO, Montesano M, Palva ET, Stewart HE, Toth IK, Cooke DE, Lyon GD, Birch PR (2000) A potato gene encoding a WRKY-like transcription factor is induced in interactions with Erwinia carotovora subsp. atroseptica and Phytophthora infestans and is coregulated with a class I endochitinase expression. Mol Plant-Microbe Interact 13:1092–1101PubMedGoogle Scholar
  94. Dempsey DA, Vlot AC, Wildermuth MC, Klessig DF (2011) Salicylic acid biosynthesis and metabolism. Arabidopsis Book 9:e0156. doi: 10.1199/tab.0156 PubMedPubMedCentralGoogle Scholar
  95. Denancé N, Sánchez-Vallet A, Goffner D, Molina A (2013) Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front Plant Sci 4:1–12, Article 155Google Scholar
  96. 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 12:279–290PubMedPubMedCentralGoogle Scholar
  97. Després C, Chubak C, Rochon A, Clark R, Bethune T, Desveaux D, Fobert PR (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 15:2181–2191PubMedPubMedCentralGoogle Scholar
  98. Desveaux D, Subramaniam R, Després C, Mess J-N, Lévesque C, Fobert PR, Dangl JL, Brisson N (2004) A ‘Whirly’ transcription factor is required for salicylic acid-dependent disease resistance in Arabidopsis. Dev Cell 6:229–240PubMedGoogle Scholar
  99. Devadas SK, Enyedi A, Raina R (2002) The Arabidopsis hrl1 mutation reveals novel overlapping roles for salicylic acid, jasmonic acid and ethylene signalling in cell death and defense against pathogens. Plant J 30:467–480PubMedGoogle Scholar
  100. Diaz-Pendon JA, Li F, Li WX, Ding SW (2007) Suppression of antiviral silencing by cucumber mosaic virus 2b protein in Arabidopsis is associated with drastically reduced accumulation of three classes of viral small interfering RNAs. Plant Cell 19:2053–2063PubMedPubMedCentralGoogle Scholar
  101. Ding S-W (2010) RNA-based antiviral immunity. Nat Rev Immunol 10:632–644PubMedGoogle Scholar
  102. Ding S-W, Voinnet O (2007) Antiviral immunity directed by small RNAs. Cell 130:413–426PubMedPubMedCentralGoogle Scholar
  103. Doares SH, Narvaez-Vasquez J, Conconi A, Ryan CA (1995) Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol 108:1741–1746PubMedPubMedCentralGoogle Scholar
  104. Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61:593–620PubMedGoogle Scholar
  105. Dong J, Chen C, Chen Z (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol 51:21–37PubMedGoogle Scholar
  106. Dreher K, Callis J (2007) Ubiquitin, hormones and biotic stress in plants. Ann Bot 99:787–822PubMedPubMedCentralGoogle Scholar
  107. Du H, Klessig DF (1997) Identification of a soluble, high-affinity salicylic acid-binding protein in tobacco. Plant Physiol 113:1319–1327PubMedPubMedCentralGoogle Scholar
  108. Du H, Zhang L, Liu L, Tang X-F, Yang W-J, Wu Y-M, Huang Y-B, Tang Y-X (2009) Biochemical and molecular characterization of plant MYB transcription factor family. Biochemistry (Moscow) 74:1–11Google Scholar
  109. Du Q, Zhu W, Zhao Z, Qian X, Xu Y (2012) Novel benzo-1,2,3-thiadiazole-7-carboxylate derivatives as plant activators and the development of their agricultural applications. J Agric Food Chem 60:346–353PubMedGoogle Scholar
  110. Durner J, Klessig DF (1995) Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defense responses. Proc Natl Acad Sci U S A 92:11312–11316PubMedPubMedCentralGoogle Scholar
  111. Durner J, Klessig DF (1996) Salicylic acid is a modulator of tobacco and mammalian catalases. J Biol Chem 271:28492–28501PubMedGoogle Scholar
  112. Durner J, Klessig DF (1999) Nitric oxide as a signal in plants. Curr Opin Plant Biol 2:369–374PubMedGoogle Scholar
  113. Durner J, Shah J, Klessig DF (1997) Salicylic acid and disease resistance in plants. Trends Plant Sci 2:266–274Google Scholar
  114. Durner J, Wendehenne D, Klessig DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP ribose. Proc Natl Acad Sci U S A 95:10328–10333PubMedPubMedCentralGoogle Scholar
  115. Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209PubMedGoogle Scholar
  116. Eberharter A, Becker PB (2002) Histone acetylation: a switch between repressive and permissive chromatin. EMBO Rep 3:224–229PubMedPubMedCentralGoogle Scholar
  117. Edgar CI, McGrath KC, Dombrecht B, Manners JM, Maclean DC, Schenk PM, Kazan K (2006) Salicylic acid mediates resistance to the vascular wilt pathogen Fusarium oxysporum in the model host Arabidopsis thaliana. Australasian Plant Pathol 35:581–591Google Scholar
  118. El Rahman TA, El Oirdi M, Gonzalez-Lamothe R, Bouarab K (2012) Necrotrophic pathogens use salicylic acid signaling pathway to promote disease development in tomato. Mol Plant-Microbe Interact 25:1584–1593PubMedGoogle Scholar
  119. Enyedi AJ, Yalpani N, Silverman P, Raskin I (1992) Localization, conjugation, and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. Proc Natl Acad Sci U S A 89:2480–2484PubMedPubMedCentralGoogle Scholar
  120. Espunya C, De Michele R, Gomez-Cadenas AA, Martinez MC (2012) S-Nitrosoglutathione is a component of wound- and salicylic acid-induced systemic responses in Arabidopsis thaliana. J Exp Bot 63:3219–3227PubMedPubMedCentralGoogle Scholar
  121. Eulgem T, Rushton PJ, Schmelzer E, Hahlbrock K, Somssich IE (1999) Early nuclear events in plant defence signaling: rapid gene activation by WRKY transcription factors. EMBO J 18:4689–4699PubMedPubMedCentralGoogle Scholar
  122. Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206PubMedGoogle Scholar
  123. Eulgem T, Weighman VJ, Chang H-S, McDowell JM, Holub EB, Glazebrook J, Zhu T, Dangl JL (2004) Gene expression signatures from three genetically separable resistance gene signaling pathways for downy mildew resistance. Plant Physiol 135:1129–1144PubMedPubMedCentralGoogle Scholar
  124. Fabro G, Di Rienzo JA, Voigt CA, Savchenko T, Dehesh K, Somerville S, Alvarez ME (2008) Genome-wide expression profiling Arabidopsis at the stage of Golovinomyces cichoracearum haustorium formation. Plant Physiol 146:1421–1439PubMedPubMedCentralGoogle Scholar
  125. 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 14:1377–1389PubMedPubMedCentralGoogle Scholar
  126. Farmer EE, Almeras E, Krishnamurthy V (2003) Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr Opin Plant Biol 6:372–378PubMedGoogle Scholar
  127. Ferrari S, Plotnokova JM, De Lorenzo G, Ausubel FM (2003) Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J 35:193–205PubMedGoogle Scholar
  128. Feys BJ, Moisan LJ, Newman MA, Parker JE (2001) Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO J 20:5400–5411PubMedPubMedCentralGoogle Scholar
  129. Fitzgerald HA, Chern M-S, Navarre R, Ronald PC (2004) Overexpression of (At) NPR1 in rice leads to a BTH- and environment-induced lesion-mimic/cell death phenotype. Mol Plant Microbe Interact 17:140–151PubMedGoogle Scholar
  130. Fitzgerald HA, Canlas PE, Chern M-S, Ronald PC (2005) Alteration of TGA factor activity in rice results in enhanced tolerance to Xanthomonas oryzae pv. oryzae. Plant J 43:335–347PubMedGoogle Scholar
  131. Flors V, Ton J, van Doorn R, Garcia-Agustin P, Mauch-Mani B (2008) Interplay between JA, SA, and ABA signalling during basal and induced resistance against Pseudomonas syringae and Alternaria brassicicola. Plant J 54:81–92PubMedGoogle Scholar
  132. Foissner L, Wendehenne D, Langebartels C, Durner J (2000) In vivo imaging of an elicitor-induced nitric oxide burst in tobacco. Plant J 23:817–824PubMedGoogle Scholar
  133. Forouhar F, Yang Y, Kumar D, Chen Y, Fridman E, Park SW, Chiang Y, Acton TB, Montelione GT, Pichersky E, Klessig DF, 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 U S A 102:1773–1778PubMedPubMedCentralGoogle Scholar
  134. Friedrich L, Lawton K, Reuss W, Masner P, Specker N, Gut Rella M, Meier B, Dincher S, Staub T, Uknes S, Metraux JP, Kessmann H, Ryals J (1996) A benzothiadiazole derivative induces systemic acquired resistance in tobacco. Plant J 10:61–70Google Scholar
  135. Frye CA, Tang D, Innes RW (2001) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc Natl Acad Sci U S A 98:373–378PubMedPubMedCentralGoogle Scholar
  136. Fu ZQ, Guo M, Jeong BR, Tian F, Elthon TE, Cerny RL, Staiger D, Alfano JR (2007) A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature 447:284–288Google Scholar
  137. Fu DQ, Ghabrial S, Kachroo A (2009) GmRAR1 and Gm SGT1 are required for basal, R gene-mediated and systemic acquired resistance in soybean. Mol Plant-Microbe Interact 22:86–95PubMedGoogle Scholar
  138. Fu L-J, Shi K, Gu M, Zhou Y-H, Dong D-K, Liang W-S, Song F-M, Yu J-Q (2010) Systemic induction and role of mitochondrial alternative oxidase and nitric oxide in a compatible tomato-Tobacco mosaic virus interaction. Mol Plant-Microbe Interact 23:39–48PubMedGoogle Scholar
  139. Fu ZQ, Yang S, Saleh A, Wang W, Ruble J, Oka N, Mohan R, Spoel SH, Tada Y, Zheng N, Dong X (2012) NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486:228–232PubMedCentralGoogle Scholar
  140. Fujiwara M, Umemura K, Kawasaki T, Shimamoto K (2006) Proteomics of Rac GTPase signaling reveals its predominant role in elicitor-induced defense response of cultured rice cells. Plant Physiol 140:734–745PubMedPubMedCentralGoogle Scholar
  141. Fung RWM, Gonzalo M, Fekete C, Kovacs LG, He Y, Marsh E, McIntyre LM, Schchtman DP, Qiu W (2008) Powdery mildew induces defense-oriented reprogramming of the transcriptome in a susceptible but not in a resistant grapevine. Plant Physiol 146:236–249PubMedPubMedCentralGoogle Scholar
  142. Gaille C, Kast P, Hass D (2002) Salicylate biosynthesis in Pseudomonas aeruginosa. Purification and characterization of PchB, a novel bifunctional enzyme displaying isochorismate pyruvate-lyase and chorismate mutase activities. J Biol Chem 277:21768–21775PubMedGoogle Scholar
  143. Gaille C, Reimmann C, Haas D (2003) Isochorismate synthase (PchA), the first and rate-limiting enzyme in salicylate biosynthesis of Pseudomonas aeruginosa. J Biol Chem 278:16893–16898PubMedGoogle Scholar
  144. Galon Y, Aloni R, Nachmias D, Snir O, Feldmesser E, Scrase-Field S, Boyce JM, Bouché N, Knight MR, Fromm H (2010) Calmodulin-binding transcription activator 1 mediates auxin signaling and responds to stresses in Arabidopsis. Planta 232:165–178PubMedGoogle Scholar
  145. Gao M, Liu J, Zhang Z, Cheng F, Chen S, Zhang Y (2008) MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res 18:1190–1198PubMedGoogle Scholar
  146. Gao Q, Liu Y, Wang M, Zhang J, Gai Y, Zhu C, Guo N (2009) Molecular cloning and characterization of an inducible RNA-dependent RNA polymerase gene, GhRdRP, from cotton (Gossypium hirsutum L.). Mol Biol Rep 36:47–56PubMedGoogle Scholar
  147. Garcia-Brugger A, Lamotte O, Vandelle E, Bourque S, Lecourieux D, Poinssot B, Wendehenne D, Pugin A (2006) Early signaling events induced by elicitors of plant defenses. Mol Plant-Microbe Interact 19:711–724PubMedGoogle Scholar
  148. Garcia-Ruiz H, Takeda A, Chapman EJ, Sullivan CM, Fahlgren N, Brempelis KJ, Carrington JC (2010) Arabidopsis RNA-dependent RNA polymerases and dicer-like proteins in antiviral defense and small interfering RNA biogenesis during Turnip mosaic virus infection. Plant Cell 22:481–496PubMedPubMedCentralGoogle Scholar
  149. Garcion C, Métraux J-P (2006) Salicylic acid. In: Hedden P, Thomas SG (eds) Plant hormone signaling, vol 24, Annual reviews. Blackwell Press, Oxford, pp 229–257Google Scholar
  150. Garcion C, Lohmann A, Lamodiere E, Catinot J, Buchala A, Doermann P, Métraux J-P (2008) Characterization and biological function of the ISOCHORISMATE SYNTHASE2 gene of the Arabidopsis. Plant Physiol 147:1279–1287PubMedPubMedCentralGoogle Scholar
  151. Gelli A, Higgins VJ, Blumwald E (1997) Activation of plant plasma membrane Ca2+-permeable channels by race-specific fungal elicitors. Plant Physiol 113:269–279PubMedPubMedCentralGoogle Scholar
  152. Genger RK, Jurkowski GI, McDowell JM, Lu H, Jung HW, Greenberg JT, Bent AF (2008) Signaling pathways that regulate the enhanced disease resistance of Arabidopsis “Defense, No death” mutants. Mol Plant-Microbe Interact 21:1285–1296PubMedPubMedCentralGoogle Scholar
  153. Gilliland A, Singh DP, Hayward JM, Moore CA, Murphy AM, York CJ, Slator J, Carr JP (2003) Genetic modification of alternative respiration has differential effects on antimycin A-induced versus salicylic acid-induced resistance to Tobacco mosaic virus. Plant Physiol 132:1518–1528PubMedPubMedCentralGoogle Scholar
  154. Gimenez-Ibanez S, Solano R (2013) Nuclear jasmonate and salicylate signaling and crosstalk in defense against pathogens. Front Plant Sci 4:Article 72/1Google Scholar
  155. Glazebrook J, Chen W, Estes B, Chang HS, Nawrath C, Metraux JP, Zhu T, Katagiri F (2003) Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. Plant J 34:217–228PubMedGoogle Scholar
  156. Göhre V, Spallek T, Häweker H, Mersmann S, Mentzel T, Boller T, de Torres M, Mansfield JW, Robatzek S (2008) Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr Biol 18:1824–1832PubMedGoogle Scholar
  157. Greenberg MVC, Ausin I, Chan SWL, Cokus SJ, Cuperus JT, Feng S, Law JA, Chu C, Pellegrini M, Carrington JC, Jacobsen SE (2011) Identification of genes required for de novo DNA methylation in Arabidopsis. Epigenetics 6:344–354PubMedPubMedCentralGoogle Scholar
  158. Grennan AK (2008) Ethylene response factors in jasmonate signaling and defense response. Plant Physiol 146:1457–1458PubMedPubMedCentralGoogle Scholar
  159. Gudesblat GE, Torres PS, Vojnov AA (2009) Xanthomonas campestris overcomes Arabidopsis stomatal innate immunity through a DSF cell-to-cell signal-regulated virulence factor. Plant Physiol 149:1017–1027PubMedPubMedCentralGoogle Scholar
  160. 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 13:503–511PubMedGoogle Scholar
  161. Hamada H, Kurusu T, Okuma E, Nokajima H, Kiyoduka M, Koyano T, Sugiyama Y, Okada K, Koga J, Saji H, Miyao A, Hirochika H, Yamane H, Murata Y, Kuchitsu K (2012) Regulation of a proteinaceous elicitor-induced Ca2+ influx and production of phytoalexins by a putative voltage-gated cation channel, OsTPC1, in cultured rice cells. J Biol Chem 287:9931–9939PubMedPubMedCentralGoogle Scholar
  162. Hamiduzzaman MM, Jakeb G, Barnavon L, Neuhaus JM, Mauch-Mani B (2005) β-Aminobutyric acid-induced resistance against downy mildew in grapevine acts through the potentiation of callose formation and jasmonic acid signaling. Mol Plant-Microbe Interact 18:819–829PubMedGoogle Scholar
  163. Hammerschmidt R (2009) Systemic acquired resistance. Adv Bot Res 51:173–222Google Scholar
  164. Harms K, Ramirez I, Peńa-Cortés H (1998) Inhibition of wound-induced accumulation of allene oxide synthase transcripts in flax leaves by aspirin and salicylic acid. Plant Physiol 118:1057–1065PubMedCentralGoogle Scholar
  165. Hashimoto K, Eckert C, Anschūtz U, Scholz M, Held K, Waadt R, Reyer A, Hippler M, Becker D, Kudla J (2012) Phosphorylation of calcineurin B-like (CBL) calcium sensor proteins by their CBL-interacting protein kinases (CIPKs) is required for full activity of CBL-CIPK complexes toward their target proteins. J Biol Chem 287:7956–7968PubMedPubMedCentralGoogle Scholar
  166. Hauck P, Thilmony R, He SY (2003) A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc Natl Acad Sci U S A 100:8577–8582PubMedPubMedCentralGoogle Scholar
  167. Henderson IR, Deleris A, Wong W, Zhong X, Chin HG, Horwitz GA, Kelly KA, Pradhan S, Jacobsen SE (2010) The de novo cytosine methyltransferase DRM2 requires intact UBA domains and a catalytically mutated paralog DRM3 during RNA-directed DNA methylation in Arabidopsis thaliana. PLoS Genet 6:e1001182PubMedPubMedCentralGoogle Scholar
  168. Hennig J, Malamy J, Grynkiewicz G, Indulski J, Klessig DF (1993) Interconversion of salicylic acid signal and its glucoside in tobacco. Plant J 4:593–600PubMedGoogle Scholar
  169. Hermann M, Maier F, Masroor A, Hirth S, Pfitzner AJ, Pfitzner UM (2013) The Arabidopsis NIMIN proteins affect NPR1 differentially. Front Plant Sci 4:88PubMedPubMedCentralGoogle Scholar
  170. Hettenhausen C, Baldwin IT, Wu J (2012) Silencing MPK4 in Nicotiana attenuata enhances photosynthesis and seed production but compromises abscisic acid-induced stomatal closure and guard cell-mediated resistance to Pseudomonas syringae pv. tomato DC3000. Plant Physiol 158:759–776PubMedPubMedCentralGoogle Scholar
  171. Hirt H (2000) Connecting oxidative stress, auxin, and cell cycle regulation through a plant mitogen-activated protein kinase pathway. Proc Natl Acad Sci U S A 97:2405–2407PubMedPubMedCentralGoogle Scholar
  172. Hondo D, Hase S, Kanayama Y, Yoshikawa N, Takenaka S, Takahashi H (2007) The LeATL6-associated ubiquitin/proteasome system may contribute to fungal elicitor-activated defense response via the jasmonic acid-dependent signaling pathway in tomato. Mol Plant-Microbe Interact 20:72–81PubMedGoogle Scholar
  173. Huang J, Wang H, Xie X, Zhang D, Liu Y, Guo G (2010) Roles of DNA methyltransferases in Arabidopsis development. Afr J Biotechnol 9:8506–8514Google Scholar
  174. Hukkanen AT, Kokko HI, Buchala AJ, McDougall GJ, Stewart D, Kárenlampi SO, Karjalainen RO (2007) Benzothiadiazole induces the accumulation of phenolics and improves resistance to powdery mildew in strawberries. J Agric Food Chem 55:1862–1870PubMedGoogle Scholar
  175. Ichimura K, Shinozaki K, Tena G, Sheen J, Henry Y (2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci 7:301–308Google Scholar
  176. Iwai T, Seo S, Mitsuhara I, Ohashi Y (2007) Probenazole-induced accumulation of salicylic acid confers resistance to Magnaporthe grisea in adult rice plants. Plant Cell Physiol 48:915–924PubMedGoogle Scholar
  177. Jakob K, Kniskern JM, Bergelson J (2007) The role of pectate lyase and the jasmonic acid defense response in Pseudomonas viridiflava virulence. Mol Plant-Microbe Interact 20:146–158PubMedGoogle Scholar
  178. Jakoby M, Weisshaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111PubMedGoogle Scholar
  179. Jaskiewicz M, Conrath U, Peterhänsel C (2011) Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep 12:50–55PubMedPubMedCentralGoogle Scholar
  180. Jaubert M, Bhattacharjee S, Mello AF, Perry KL, Moffett P (2011) ARGONAUTE2 mediates RNA silencing anti-viral defenses against Potato virus X in Arabidopsis. Plant Physiol 156:1556–1564PubMedPubMedCentralGoogle Scholar
  181. Jelenska J, Yao N, Vinatzer BA, Wright CM, Brodsky JL, Greenberg JT (2007) A J domain virulence effector of Pseudomonas syringae remodels host chloroplasts and suppresses defenses. Curr Biol 17:499–508PubMedPubMedCentralGoogle Scholar
  182. Ji L-H, Ding S-W (2001) The suppressor of transgene RNA silencing encoded by Cucumber mosaic virus interferes with salicylic acid-mediated virus resistance. Mol Plant-Microbe Interact 14:715–724PubMedGoogle Scholar
  183. Jing B, Xu S, Xu M, Li Y, Li S, Ding J, Zhang Y (2011) Brush and spray: a high-throughput systemic acquired resistance assay suitable for large-scale genetic screening. Plant Physiol 157:973–980PubMedPubMedCentralGoogle Scholar
  184. Jirage D, Tootle TL, Reuber TL, Frost LN, Feys BJ, Parker JE (1999) Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc Natl Acad Sci U S A 96:13583–13588PubMedPubMedCentralGoogle Scholar
  185. Johnson C, Boden E, Arias J (2003) Salicylic acid and NPR1 induce the recruitment of trans-activating TGA factors to a defense gene promoter in Arabidopsis. Plant Cell 15:1846–1858PubMedPubMedCentralGoogle Scholar
  186. Johnson C, Mhatre A, Arias J (2008) NPR1 preferentially binds to the DNA-inactive form of Arabidopsis TGA2. Biochim Biophys Acta 1779:583–589PubMedGoogle Scholar
  187. Journot-Catalino N, Somssich IE, Roby D, Kroj T (2006) The transcription factors WRKY11 and WRKY17 act as negative regulators of basal resistance in Arabidopsis thaliana. Plant Cell 18:3289–3302PubMedPubMedCentralGoogle Scholar
  188. Jovel J, Walker M, Sanfacon H (2011) Salicylic acid-dependent restriction of Tomato ringspot virus spread in tobacco is accompanied by a hypersensitive response, local RNA silencing, and moderate systemic resistance. Mol Plant-Microbe Interact 24:706–718Google Scholar
  189. Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT (2009) Priming in systemic plant immunity. Science 324:89–91PubMedGoogle Scholar
  190. 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 12:677–690PubMedPubMedCentralGoogle Scholar
  191. Kachroo P, Shanklin J, Shah J, Whittle EJ, Klessig DF (2001) A fatty acid desaturase modulates the activation of defense signaling pathways in plants. Proc Natl Acad Sci U S A 98:9448–9453PubMedPubMedCentralGoogle Scholar
  192. Kachroo P, Kachroo A, Lapchyk L, Hildebrand D, Klessig DF (2003a) Restoration of defective cross talk in ssi2 mutants: role of salicylic acid, jasmonic acid, and fatty acids in SSI2-mediated signaling. Mol Plant-Microbe Interact 16:1022–1029Google Scholar
  193. Kachroo A, Lapchyk L, Fukushige H, Hildebrand D, Klessig D, Kachroo P (2003b) Plastidial fatty acid signaling modulates salicylic acid- and jasmonic acid-mediated defense pathways in the Arabidopsis ssi2 mutant. Plant Cell 15:2952–2965PubMedPubMedCentralGoogle Scholar
  194. Kachroo A, Venugopal SC, Lapchyk L, Falcone D, Hildebrand D, Kachroo P (2004) Oleic acid levels regulated by glycerolipid metabolism modulate defense gene expression in Arabidopsis. Proc Natl Acad Sci U S A 101:5152–5157PubMedPubMedCentralGoogle Scholar
  195. Kalde M, Barth M, Somssich IE, Lippok B (2003) Members of the Arabidopsis WRKY group III transcription factors are part of different plant defense signaling pathways. Mol Plant-Microbe Interact 16:295–305PubMedGoogle Scholar
  196. Kallenbach M, Alagna F, Baldwin IT, Bonaventure G (2010) Nicotiana attenuata SIPK, WIPK, NPR1, and fatty acid-amino acid conjugates participate in the induction of jasmonic acid biosynthesis by affecting early enzymatic steps in the pathway. Plant Physiol 152:98–106Google Scholar
  197. Kamakka RT, Biggins S (2005) Histone variants: deviants? Genes Dev 19:295–310Google Scholar
  198. Kang CH, Jung WY, Kang YH, Kim JY, Kim DG, Jeong JC, Baek DW, Jin JB, Lee JY, Kim MO, Chung WS, Mengiste T, Koiwa H, Kwak SS, Bahk JD, Lee SY, Nam JS, Yun DJ, Cho MJ (2006) AtBAG6, a novel calmodulin-binding protein, induces programmed cell death in yeast and plants. Cell Death Differ 13:84–95PubMedGoogle Scholar
  199. Katiyar-Agarwal S, Jin H (2010) Role of small RNAs in host-microbe interactions. Annu Rev Phytopathol 48:225–246PubMedPubMedCentralGoogle Scholar
  200. Katsir L, Schilmiller A, Staswick P, He SY, Howe GA (2008) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci U S A 105:7100–7105PubMedPubMedCentralGoogle Scholar
  201. Kesarwani M, Joo J, Dong X (2007) Genetic interactions of TGA transcription factors in the regulation of pathogenesis-related genes and disease resistance in Arabidopsis. Plant Physiol 144:336–346PubMedPubMedCentralGoogle Scholar
  202. Khang CH, Berruyer R, Giraldo MC, Kankanala P, Park SY, Czymmek K, Kang S, Valent B (2010) Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 22:1388–1403PubMedPubMedCentralGoogle Scholar
  203. Kidd BN, Cahill DM, Manners JM, Schenk PM, Kazan K (2011) Diverse roles of the Mediator complex in plants. Semin Cell Dev Biol 22:741–748PubMedGoogle Scholar
  204. Kim HS, Delaney TP (2002) Overexpression of TGA5, which encodes a bZIP transcription factor that interacts with NIM1/NPR1, confers SAR-independent resistance in Arabidopsis thaliana to Peronospora parasitica. Plant J 32:151–163Google Scholar
  205. Kim KC, Fan B, Chen Z (2006) Pathogen-induced Arabidopsis WRKY7 is a transcriptional repressor and enhances susceptibility to Pseudomonas syringae. Plant Physiol 142:1180–1192PubMedPubMedCentralGoogle Scholar
  206. Kim S-Y, Kim Y-C, Seong ES, Lee Y-H, Park M, Choi D (2007) The chili pepper CaATL1: an AT-hook motif-containing transcription factor implicated in defence responses against pathogens. Mol Plant Pathol 8:761–771PubMedGoogle Scholar
  207. Kim K-C, Lai Z, Fan B, Chen Z (2008) Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense. Plant Cell 20:2357–2371PubMedPubMedCentralGoogle Scholar
  208. Kinkema M, Fan W, Dong X (2000) Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12:2339–2350PubMedCentralGoogle Scholar
  209. Klessig DF, Durner J, Noad R, Navarre DA, Wendehenne D, Kumar D, Zhou JM, Shah J, Zhang S, Kachroo P, Trifa Y, Pontier D, Lam E, Silva H (2000) Nitric oxide and salicylic acid signalling in plant defense. Proc Natl Acad Sci U S A 97:8849–8855PubMedPubMedCentralGoogle Scholar
  210. Kloek AP, Verbsky ML, Sharma SB, Schoelz JE, Vogel J, Klessig DF, Kunkel BN (2001) Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana coronatine-insensitive (coi) mutation occurs through two distinct mechanisms. Plant J 26:509–522PubMedGoogle Scholar
  211. Knoth C, Ringler J, Dangl JL, Eulgem T (2007) Arabidopsis WRKY70 is required for full RPP4-mediated disease resistance and basal defense against Hyaloperonospora parasitica. Mol Plant-Microbe Interact 20:120–128PubMedGoogle Scholar
  212. Kobayashi M, Seo S, Hirai K, Yamamoto-Katou A, Katou S, Seto H, Meshi T, Mitsuhara I, Ohashi Y (2010) Silencing of WIPK and SIPK mitogen-activated protein kinases reduces Tobacco mosaic virus accumulation but permits systemic viral movement in tobacco possessing the N resistance gene. Mol Plant-Microbe Interact 23:1032–1041PubMedGoogle Scholar
  213. Kohler A, Schwindling S, Conrath U (2002) Benzothiadiazole-induced priming for potentiated responses to pathogen infection, wounding, and infiltration of water into leaves requires the NPR1/NIM1 gene in Arabidopsis. Plant Physiol 128:1046–1056PubMedPubMedCentralGoogle Scholar
  214. Koo YJ, Kim MA, Kim EH, Song JT, Jung CK, Moon JK, Kim JH, Seo HS, Song SL, Kim JK, Lee JS, Cheong JJ, Choi YD (2007) Overexpression of salicylic acid carboxyl methyltransferase reduces salicylic acid-mediated pathogen resistance in Arabidopsis thaliana. Plant Mol Biol 64:1–15PubMedGoogle Scholar
  215. Koornneef A, Pieterse CMJ (2008) Cross talk in defense signaling. Plant Physiol 146:839–844PubMedPubMedCentralGoogle Scholar
  216. Korolev N, David DR, Elad Y (2008) The role of phytohormones in basal resistance in Trichoderma-induced systemic resistance to Botrytis cinerea in Arabidopsis thaliana. Biocontrol 53:667–683Google Scholar
  217. Krečič-Stres C, Vučak C, Ravnikar M, Kovač M (2005) Systemic Potato virus Y NTN infection and levels of salicylic and gentisic acids in different potato genotypes. Plant Pathol 54:441–447Google Scholar
  218. Krinke O, Ruelland E, Valentová O, Vergnolle C, Renou J-P, Taconnat L, Flemr M, Burketova L, Zachowski A (2007) Phosphatidylinositol 4-kinase activation is an early response to salicylic acid in Arabidopsis suspension cells. Plant Physiol 144:1347–1359PubMedCentralGoogle Scholar
  219. Kudla J, Batistić O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22:541–563PubMedPubMedCentralGoogle Scholar
  220. Kumar D, Klessig DF (2000) Differential induction of tobacco MAP kinases by the defense signals nitric oxide, salicylic acid, ethylene, and jasmonic acid. Mol Plant-Microbe Interact 13:347–351PubMedGoogle Scholar
  221. Kumar D, Klessig DF (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 U S A 100:16101–16106PubMedPubMedCentralGoogle Scholar
  222. Kumar D, Klessig DF (2008) The search for the salicylic acid receptor led to discovery of the SAR signal receptor. Plant Signal Behav 3:691–692PubMedPubMedCentralGoogle Scholar
  223. Kumar D, Gustafsson C, Klessig DF (2006) Validation of RNAi silencing specificity using synthetic genes: salicylic acid-binding protein 2 is required for innate immunity in plants. Plant J 45:863–868PubMedGoogle Scholar
  224. Kwaaitaal M, Huisman R, Maintz J, Reinstädler A, Panstruga R (2011) Ionotropic glutamate receptor (iGluR)-like channels mediate MAMP-induced calcium influx in Arabidopsis thaliana. Biochem J 440:355–365PubMedGoogle Scholar
  225. Kwon C (2010) Plant defense responses coming to shape. Plant Pathol J 26:115–120Google Scholar
  226. Kwon S, Hamada K, Matsuyama A, Yasuda M, Nakashita H, Yamakawa T (2009) Biotic and abiotic stresses induce AbSAMT1, encoding S-adenosyl-L-methionine: salicylic acid carboxyl methyltransferase, in Atropa belladonna. Plant Biotechnol 26:207–215Google Scholar
  227. Lamotte O, Gould K, Lecourieux D, Sequeira-Legrand A, Lebrun-Garcia A, Durner J, Pugin A, Wendehenne D (2004) Analysis of nitric oxide signaling functions in tobacco cells challenged by the elicitor cryptogein. Plant Physiol 135:516–529PubMedPubMedCentralGoogle Scholar
  228. Laquitaine L, Gomès E, Francois J, Marchive C, Pascal S, Hamdi S, Atanassova R, Delrot S, Coutos-Thévenot P (2006) Molecular basis of ergosterol-induced protection of grape against Botrytis cinerea: induction of type 1 LTP promoter activity, WRKY, and stilbene synthase gene expression. Mol Plant-Microbe Interact 19:1103–1112PubMedGoogle Scholar
  229. Laudert D, Weiler EW (1998) Allene oxide synthase: a major control point in Arabidopsis thaliana octadecanoid signaling. Plant J 15:675–684PubMedGoogle Scholar
  230. Latunde-Dada AO, Lucas JA (2001) The plant defense activator acibenzalor-S-methyl primes cowpea [Vigna unguiculata (L.) Walp.] seedlings for rapid induction of resistance. Physiol Mol Plant Pathol 58:199–208Google Scholar
  231. Laurie-Berry N, Joardar V, Street JH, Kunkel BN (2006) The Arabidopsis thaliana JASMONATE INSENSITIVE 1 gene is required for suppression of salicylic acid-dependent defenses during infection by Pseudomonas syringae. Mol Plant-Microbe Interact 19:789–800PubMedGoogle Scholar
  232. Lawton K, Weymann K, Friedrich L, Vernooij B, Uknes S, Ryals J (1995) Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Mol Plant Microbe Interact 8:863–870PubMedGoogle Scholar
  233. Lecourieux D, Ranjeva R, Pugin A (2006) Calcium in plant defence-signalling pathways. New Phytol 171:249–269Google Scholar
  234. Lee H-L, Raskin I (1999) Purification, cloning, and expression of a pathogen inducible UDP-glucose: salicylic acid glucosyltransferase from tobacco. J Biol Chem 274:36637–36642PubMedGoogle Scholar
  235. Lee H-I, León J, Raskin I (1995) Biosynthesis and mechanism of salicylic acid. Proc Natl Acad Sci U S A 92:4076–4079PubMedPubMedCentralGoogle Scholar
  236. Lee DE, Lee IJ, Han O, Baik MG, Han SS, Back K (2004) Pathogen resistance of transgenic rice expressing mitogen-activated protein kinase 1, MK1, from Capsicum annuum. Mol Cells 17:81–85PubMedGoogle Scholar
  237. Lee J, Nam J, Park HC, Na G, Miura K, Jin JB, Yoo CY, Baek D, Kim DH, Jeong JC, Kim D, Lee SY, Salt DE, Mengiste T, Gong Q, Ma S, Bohnert HJ, Kwak S-S, Bressan RA, Hasegawa PM, Yun D-J (2007) Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. Plant J 49:79–90PubMedGoogle Scholar
  238. Lee DH, Choi HW, Hwang BK (2011a) The pepper E3 ubiquitin ligase RING1 gene, CaRING1, is required for cell death and the salicylic acid-dependent defense response. Plant Physiol. doi: 10.1104/pp. 111.177568 (On Line first)Google Scholar
  239. Lee W-S, Fu S-F, Verchot-Lubicz J, Carr JP (2011b) Genetic modification of alternative respiration in Nicotiana benthamiana affects basal and salicylic acid-induced resistance to potato virus X. BMC Plant Biol 11:41PubMedPubMedCentralGoogle Scholar
  240. Lehtonen NT, Akita M, Frank W, Reski R, Valkonen JPT (2012) Involvement of a class III peroxidase and the mitochondrial protein TSPO in oxidative burst upon treatment of moss plants with a fungal elicitor. Mol Plant-Microbe Interact 25:363–371PubMedGoogle Scholar
  241. Leibman D, Wolf D, Saharan V, Zelcer A, Arazi T, Yoel S, Gaba V, Gal-On A (2011) A high level of transgenic viral small RNA is associated with broad potyvirus resistance in cucurbits. Mol Plant-Microbe Interact 24:1220–1238PubMedGoogle Scholar
  242. León J, Yalpani N, Raskin I, Lawton MA (1993) Induction of benzoic acid 2-hydroxylase in virus-inoculated tobacco. Plant Physiol 103:323–328PubMedPubMedCentralGoogle Scholar
  243. León J, Lawton MA, Raskin I (1995) Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol 108:1673–1678PubMedPubMedCentralGoogle Scholar
  244. Leon-Reyes A, Du Y, Koornneef A, Proietti S, Körbes AP, Memelink J, Pieterse CMJ, Ritsema T (2010a) Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic acid. Mol Plant-Microbe Interact 23:187–197PubMedGoogle Scholar
  245. Leon-Reyes A, Van der Does D, De Lange ES, Delker C, Wasternack C, Van Wees SCM, Ritsema T, Pieterse CMJ (2010b) Salicylate-mediated suppression of jasmonate-responsive gene expression in Arabidopsis is targeted downstream of the jasmonate biosynthesis pathway. Planta 232:1423–1432PubMedPubMedCentralGoogle Scholar
  246. Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593PubMedGoogle Scholar
  247. Lewsey MG, Murphy AM, MacLean D, Dalchau N, Westwood JH, Macaulay K, Bennett M, Moulin M, Hanke DE, Powell G, Smith AG, Carr JP (2010) Disruption of two signaling pathways by a viral RNA silencing suppressor. Mol Plant-Microbe Interact 23:835–845PubMedGoogle Scholar
  248. 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 16:319–331PubMedPubMedCentralGoogle Scholar
  249. Li J, Brader G, Kariola T, Tapio Palva E (2006) WRKY70 modulates the selection of signaling pathways in plant defense. Plant J 46:477–491PubMedGoogle Scholar
  250. Li C, Bonnema G, Che D, Dong L, Lindhout P, Visser R, Bai Y (2007) Biochemical and molecular mechanisms involved in monogenic resistance responses to tomato powdery mildew. Mol Plant-Microbe Interact 20:1161–1172PubMedGoogle Scholar
  251. Li G, Meng X, Wang R, Mao G, Han L, Liu Y, Zhang S (2012) Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLoS Genet 8(6):e1002767. doi: 10.1371/journal.pgen.1002767 PubMedPubMedCentralGoogle Scholar
  252. Lim E-K, Doucet CJ, Li Y, Elias L, Worrall D, Spencer SP, Ross J, Bowles DJ (2002) Arabidopsis glycosyltransferases toward salicylic acid, 4-hydroxybenzoic acid and other benzoates. J Biol Chem 277:586–592PubMedGoogle Scholar
  253. Lindermayr C, Sell S, Müller B, Leister D, Dumer J (2010) Redox regulation of NPR1-TGA1 system of Arabidopsis thaliana by nitric oxide. Plant Cell 22:2894–2907PubMedPubMedCentralGoogle Scholar
  254. Lippok B, Birkenbihl RP, Rivory G, Brummer J, Schmelzer E, Logemann E, Somssich IE (2007) Expression of AtWRKY33 encoding a pathogen- or PAMP-responsive WRKY transcription factor is regulated by a composite DNA motif containing W box elements. Mol Plant-Microbe Interact 20:420–429PubMedGoogle Scholar
  255. Liu J-J, Ekramoddoullah AKM, Yu X (2003) Differential expression of multiple PR10 proteins in western white pine following wounding, fungal infection and cold-hardening. Physiol Plant 119:544–553Google Scholar
  256. Liu X, Bai X, Wang X, Chu C (2007) OsWRKY71, a rice transcription factor, is involved in rice defense response. J Plant Physiol 164:969–979PubMedGoogle Scholar
  257. Liu P-P, Yang Y, Pichersky E, Klessig DF (2010) Altering expression of benzoic acid/salicylic acid carboxyl methyltransferase 1 compromises systemic acquired resistance and PAMP-triggered immunity in Arabidopsis. Mol Plant-Microbe Interact 23:82–90PubMedGoogle Scholar
  258. Liu P-P, von Dahl CC, Klessig DF (2011a) The extent to which methyl salicylate is required for signaling systemic acquired resistance is dependent on exposure to light after infection. Plant Physiol 157:2216–2226PubMedPubMedCentralGoogle Scholar
  259. Liu P-P, von Dahl CC, Park S-W, Klessig DF (2011b) Interconnection between methyl salicylate and lipid-based long-distance signaling during the development of systemic acquired resistance in Arabidopsis and tobacco. Plant Physiol 155:1762–1768PubMedPubMedCentralGoogle Scholar
  260. Lorenc-Kukula K, Chaturvedi R, Roth M, Welti R, Shah J (2012) Biochemical and molecular-genetic characterization of SFD1’s involvement in lipid metabolism and defense signaling. Front Plant Sci 3:26PubMedPubMedCentralGoogle Scholar
  261. Lorkovic ZJ (2009) Role of plant RNA-binding proteins in development, stress response and genome organization. Trends Plant Sci 14:229–236PubMedGoogle Scholar
  262. Love AJ, Yun B-W, Laval V, Loake GJ, Milner JL (2005) Cauliflower mosaic virus, a compatible pathogen of Arabidopsis, engages three distinct defense-signaling pathways and activates rapid systemic generation of reactive oxygen species. Plant Physiol 139:935–948PubMedCentralGoogle Scholar
  263. Luan S, Kudla J, Rodriguez-Concepcion M, Yalovsky S, Gruissem W (2002) Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell 14:S389–S400PubMedPubMedCentralGoogle Scholar
  264. Luna E, Bruce TJA, Roberts MR, Flors V, Ton J (2012) Next generation systemic acquired resistance. Plant Physiol 158:844–853PubMedCentralGoogle Scholar
  265. Ma W, Berkowitz GA (2007) The grateful dead: calcium and cell death in plant innate immunity. Cell Microbiol 9:2571–2585PubMedGoogle Scholar
  266. Maeo K, Hayashi S, Kojima-Suzuki H, Morikami A, Nakamura D (2001) Role of conserved residues of the WRKY domain in the DNA-binding of tobacco WRKY family proteins. BioSci Biotechnol Biochem 65:2428–2436PubMedGoogle Scholar
  267. Maier F, Zwicker S, Hückelhoven A, Meissner M, Funk J, Pfitzner AJ, Pfitzner UM (2011) NONEXPRESSOR OF PATHOGENESIS-RELATED PROTEINS1 (NPR1) and some NPR1-related proteins are sensitive to salicylic acid. Mol Plant Pathol 12:73–91PubMedGoogle Scholar
  268. Malamy J, Hennig J, Klessig DF (1992) Temperature-dependent induction of salicylic acid and its conjugates during the resistance response to tobacco mosaic virus infection. Plant Cell 4:359–366PubMedPubMedCentralGoogle Scholar
  269. Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK (2002) A putative lipid transfer protein involved in systemic acquired resistance in potato. Mol Plant-Microbe Interact 23:82–90Google Scholar
  270. Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26:403–410PubMedGoogle Scholar
  271. Malik SI, Hussain A, Yun BW, Spoel SH, Loake GJ (2011) GSNOR-mediated de-nitrosylation in the plant defence response. Plant Sci 181:540–544Google Scholar
  272. Mandal B, Mandal S, Csinos AS, Martinez N, Culbreath AK, Pappu HR (2008) Biological and molecular analyses of the acibenzolar-S-methyl-induced systemic acquired resistance in flue-cured tobacco against Tomato spotted wilt virus. Phytopathology 98:196–204PubMedGoogle Scholar
  273. Manosalva PM, Park S-W, Forouhar F, Tong L, Fry WE, Klessig DF (2010) Methyl Esterase 1 (StMES1) is required for systemic acquired resistance in potato. Mol Plant-Microbe Interact 23:1151–1163PubMedGoogle Scholar
  274. 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 48:833–842PubMedGoogle Scholar
  275. March-Diaz R, Garcia-Domỉnguez M, Lozano-Juste J, Leόn J, Florencio FJ, Reyes JC (2008) Histone H2A.Z and homologues of components of the SWR1 complex are required to control immunity in Arabidopsis. Plant J 53:475–487PubMedGoogle Scholar
  276. Marchive C, Mzid R, Deluc L, Barrieu F, Pirrello J, Gauthier A, Corio-Costet M-F, Regard F, Cailleteau B, Hamdi S, Lauvergeat V (2007) Isolation and characterization of a Vitis vinifera transcription factor, VvWRKY1, and its effect on responses to fungal pathogens in transgenic tobacco plants. J Exp Bot 58:1999–2010PubMedGoogle Scholar
  277. Mateo A, Muhlenbock P, Rustérucci C, Chang CC, Miszalski Z, Karpinska B, Parker JE, Mullineaux PM, Karpinski S (2004) LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy. Plant Physiol 136:2818–2830PubMedPubMedCentralGoogle Scholar
  278. 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 8:203–212PubMedPubMedCentralGoogle Scholar
  279. Maxwell DP, Wang Y, McIntosh L (1999) The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci U S A 96:8271–8276PubMedPubMedCentralGoogle Scholar
  280. Mayers CN, Lee KC, Moore CA, Wong SM, Carr JP (2005) Salicylic acid-induced resistance to Cucumber mosaic virus in squash and Arabidopsis thaliana: contrasting mechanisms of induction and antiviral action. Mol Plant-Microbe Interact 18:428–434PubMedGoogle Scholar
  281. McAinsh MR, Pittman JK (2009) Shaping the calcium signature. New Phytol 181:275–294PubMedGoogle Scholar
  282. McGrath KC, Dombrecht B, Manners JM, Schenk PM, Edgar CI, Maclean DJ, Scheible W-R, Udvardi MK, Kazan K (2005) Repressor- and activator-type ethylene response factors functioning in jasmonate signaling and disease resistance identified via a genome-wide screen of Arabidopsis transcription factor gene expression. Plant Physiol 139:949–959PubMedPubMedCentralGoogle Scholar
  283. Meldau S, Ullman-Zeunert L, Govind G, Bartram S, Baldwin IT (2012) MAPK-dependent JA and SA signalling in Nicotiana attenuata affects plant growth and fitness during competition with conspecifics. BMC Plant Biol 12(213):u7Google Scholar
  284. Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126:969–980Google Scholar
  285. Mengiste T, Chen X, Salmeron J, Dietrich R (2003) The Botrytis Susceptible 1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell 15:2551–2565PubMedPubMedCentralGoogle Scholar
  286. Menke FLH, Kang H-G, Chen Z, Mee Park J, Kumar D, Klessig DF (2005) Tobacco transcription factor WRKY1 is phosphorylated by the MAP kinase SIPK and mediates HR-like cell death in tobacco. Mol Plant-Microbe Interact 10:1027–1034Google Scholar
  287. Mészáros T, Helfer A, Hatzimasoura E, Magyar Z, Serazetdinova L, Rios G, Bardόczy V, Teige M, Koncz C, Peck S, Bögre L (2006) The Arabidopsis MAP kinase kinase MKK1 participates in defence responses to the bacterial elicitor flagellin. Plant J 48:485–495PubMedGoogle Scholar
  288. Metraux J-P (2002) Recent breakthroughs in the study of salicylic acid biosynthesis. Trends Plant Sci 7:332–334PubMedGoogle Scholar
  289. Metz M, Dahlbeck D, Morales CQ, Al Sady B, Clark ET, Staskawicz BJ (2005) The conserved Xanthomonas campestris pv. vesicatoria effector protein XopX is a virulence factor and suppresses host defense in Nicotiana benthamiana. Plant J 41:801–814PubMedGoogle Scholar
  290. Meur G, Budatha M, Gupta AD, Prakash S, Kirti PB (2006) Differential induction of NPR1 during defense responses in Brassica juncea. Physiol Mol Plant Pathol 68:128–137Google Scholar
  291. 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 19:819–830PubMedPubMedCentralGoogle Scholar
  292. Midoh N, Iwata M (1996) Cloning and characterization of a probenazole-inducible gene for an intracellular pathogenesis-related protein in rice. Plant Cell Physiol 37:9–18PubMedGoogle Scholar
  293. Mikami K, Sakamoto A, Iwabuchi M (1994) The HBP-1 family of wheat basic/leucine zipper proteins interacts with overlapping cis-acting hexamer motifs of plant histone genes. J Biol Chem 269:9974–9985PubMedGoogle Scholar
  294. Mishina TE, Zeier J (2006) The Arabidopsis flavin-dependent monooxygenase FMO1 is an essential component of biologically induced systemic acquired resistance. Plant Physiol 141:1666–1675PubMedPubMedCentralGoogle Scholar
  295. Mitsuhara I, Iwai T, Seo S, Yanagawa Y, Kawahigasi H, Hirose S, Ohkawa Y, Ohashi Y (2008) Characteristic expression of twelve PR1 family genes in response to pathogen infection, wounding, and defense-related signal compounds. Mol Genet Genomics 279:415–427PubMedPubMedCentralGoogle Scholar
  296. Moeder W, Urguhart W, Ung H, Yoshioka K (2011) The role of cyclic nucleotide-gated ion channels in plant immunity. Mol Plant 4:442–452PubMedGoogle Scholar
  297. Mohr PG, Cahill DM (2007) Suppression by ABA of salicylic acid and lignin accumulation and the expression of multiple genes, in Arabidopsis infected with Pseudomonas syringae pv. tomato. Funct Integr Genomics 7:181–191PubMedGoogle Scholar
  298. Momol MT, Olson SM, Funderburk JE, Stavisky J, Marois JJ (2004) Integrated management of tomato spotted wilt on field-grown tomatoes. Plant Dis 88:882–890Google Scholar
  299. Moreau M, Tian M, Klessig DF (2012) Salicylic acid binds NPR3 and NPR4 to regulate NPR1-dependent defense responses. Cell Res. doi: 10.1038/cr 2012.100 PubMedPubMedCentralGoogle Scholar
  300. Mosher RA, Durrant WE, Wang D, Song J, Dong X (2006) A comprehensive structure-function analysis of Arabidopsis SNI1defines essential regions and transcriptional repressor activity. Plant Cell 18:1750–1765PubMedPubMedCentralGoogle Scholar
  301. Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944PubMedGoogle Scholar
  302. Mucha E, Fricke I, Schaefer A, Wittinghofer A, Berken A (2011) Rho proteins of plants-functional cycle and regulation of cytoskeletal dynamics. Eur J Cell Biol 90:934–943Google Scholar
  303. Mukherjee M, Larrimore KE, Ahmed NJ, Bedick TS, Barghouthi NT, Traw MB, Barth C (2010) Ascorbic acid deficiency in Arabidopsis induces constitutive priming that is dependent on hydrogen peroxide, salicylic acid, and the NPR1 gene. Mol Plant-Microbe Interact 23:340–351PubMedGoogle Scholar
  304. Mur LAJ, Bi YM, Darby RM, Firek S, Draper J (1997) Compromising early salicylic acid accumulation delays the hypersensitive response and increases viral dispersal during lesion development in TMV-infected tobacco. Plant J 12:1113–1126PubMedGoogle Scholar
  305. 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 140:249–262PubMedPubMedCentralGoogle Scholar
  306. Murphy AM, Chivasa S, Singh DP, Carr JP (1999) Salicylic acid-induced resistance to viruses and other pathogens: a parting of ways? Trends Plant Sci 4:155–160PubMedGoogle Scholar
  307. Murphy AM, Gilliland A, York CJ, Hyman B, Carr JP (2004) High-level expression of alternative oxidase protein sequences enhances the spread of viral vectors in resistant and susceptible plants. J Gen Virol 85:3777–3786PubMedGoogle Scholar
  308. Nakashita H, Yasuda M, Nishioka M, Hasegawa S, Arai Y, Uramoto M, Yoshida S, Yamaguchi I (2002) Chloroisonicotinamide derivative induces a broad range of disease resistance in rice and tobacco. Plant Cell Physiol 43:823–831PubMedGoogle Scholar
  309. Nakashita H, Yasuda M, Okage R, Nishioka M, Arie T, Yoshida S (2003) A pyrazole derivative induces systemic acquired resistance with a new type of action. Plant Cell Physiol 44:S179–S179Google Scholar
  310. Nandi A, Krothapalli K, Buseman C, Li M, Welti R, Enyedi A, Shah J (2003) The Arabidopsis thaliana sid mutants affect plastidic lipid composition and suppress dwarfing, cell death and the enhanced disease resistance phenotypes resulting from the deficiency of a fatty acid desaturase. Plant Cell 15:2383–2398PubMedPubMedCentralGoogle Scholar
  311. Nandi A, Welti R, Shah J (2004) The Arabidopsis thaliana dihydroxyacetone phosphate reductase gene SUPPRESSOR OF FATTY ACID DESATURASE DEFICIENCY1 is required for glycerolipid metabolism and for the activation of systemic acquired resistance. Plant Cell 16:465–477PubMedPubMedCentralGoogle Scholar
  312. Nandi A, Moeder W, Kachroo P, Klessig DF, Shah J (2005) Arabidopsis ssi-2 conferred susceptibility to Botrytis cinerea is dependent on EDS5 and PAD4. Mol Plant-Microbe Interact 18:363–370PubMedGoogle Scholar
  313. Nandi D, Tahiliani P, Kumar A, Chandu D (2006) The Ubiquitin-Proteasome system. J Biosci 31:137–155PubMedGoogle Scholar
  314. Naumann U, Daxinger L, Kanno T, Eun C, Long Q, Lorkovic ZJ, Matzke M, Matzke AJM (2011) Genetic evidence that DNA methyltransferase DRM2 has a direct catalytic role in RNA-directed DNA methylation in Arabidopsis thaliana. Genetics 187:977–979PubMedCentralGoogle Scholar
  315. Návarová H, Bernsdorff F, Döring A-C, Zeier J (2012) Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell 24:5123–5141PubMedPubMedCentralGoogle Scholar
  316. Navarre DA, Mayo D (2004) Differential characteristics of salicylic acid-mediated signaling in potato. Physiol Mol Plant Pathol 64:179–188Google Scholar
  317. 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 MATE transporter family. Plant Cell 14:275–286PubMedPubMedCentralGoogle Scholar
  318. Naylor M, Murphy AM, Berry JO, Carr JP (1998) Salicylic acid can induce resistance in plant virus movement. Mol Plant Microbe Interact 11:860–868Google Scholar
  319. 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 50:128–139PubMedGoogle Scholar
  320. Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signaling molecules in plants. J Exp Bot 53:1237–1247PubMedGoogle Scholar
  321. Neill S, Bright J, Desikan R, Hancock J, Harrison J, Wilson I (2008) Nitric oxide evolution and perception. J Exp Bot 59:25–35PubMedGoogle Scholar
  322. Nie X (2006) Salicylic acid suppresses Potato virus Y isolate N:O-induced symptoms in tobacco plants. Phytopathology 96:255–263PubMedGoogle Scholar
  323. Niki T, Mitsuhara I, Seo S, Ohtsubo N, Ohasshi 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 39:500–507Google Scholar
  324. Nishioka M, Nakashita H, Yasuda M, Yoshida S, Yamaguchi I (2005) Induction of resistance against rice bacterial blight by 3-chloro-1-methyl-1H-pyrazole-5-carboxylic acid. J Pest Sci 30:47–49Google Scholar
  325. 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 144:1144–1156PubMedPubMedCentralGoogle Scholar
  326. Nürnberger T, Küfner I (2011) The role of the plant plasma membrane in microbial sensing and innate immunity: the plant plasma membrane. Plant Cell Monogr 19:471–483Google Scholar
  327. O’Brein JA, Daudi A, Finch P, Butt VS, Whitelegge JP, Souda P, Ausubel FM, Bolwell GP (2012) A peroxidase-dependent apoplastic oxidative burst in cultured Arabidopsis cells functions in MAMP-elicited defense. Plant Physiol 158:2013–2027Google Scholar
  328. 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 23:395–398Google Scholar
  329. Oki K, Inaba N, Kitagawa K, Fujioka S, Kitano H, Fujisawa Y, Kato H, Iwasaki Y (2009) Function of the α subunit of rice heterotrimeric G protein in brassinosteroid signaling. Plant Cell Physiol 50:161–172PubMedGoogle Scholar
  330. Olszak B, Malinovsky FG, Brodersen P, Grell M, Giese H, Petersen M, Mundy J (2006) A putative flavin-containing mono-oxygenase as a marker for certain defense and cell death pathways. Plant Sci 170:614–623Google Scholar
  331. Oostendorp M, Kunz W, Dietrich B, Staub T (2001) Induced disease resistance in plants by chemicals. Eur J Plant Pathol 107:19–28Google Scholar
  332. Ouyang J, Gill G (2009) SUMO engages multiple corepressors to regulate chromatin structure and transcription. Epigenetics 4:440–444Google Scholar
  333. Pandey S, Wang R-S, Wilson L, Li S, Zhao Z, Gookin TE, Assmann SM, Albert R (2010) Boolean modeling of transcriptome data reveals novel modes of heterotrimeric G-protein action. Mol Syst Biol 6:372PubMedPubMedCentralGoogle Scholar
  334. Papaefthimiou I, Hamilton A, Denti M, Baulcombe D, Tsagris M, Tabler M (2001) Replicating Potato spindle tuber viroid RNA is accompanied by short RNA fragments that are characteristic of post-transcriptional gene silencing. Nucleic Acids Res 29:2395–2400PubMedPubMedCentralGoogle Scholar
  335. Park J, Choi HJ, Lee S, Lee T, Yang Z, Lee Y (2000) Rac-related GTP-binding protein in elicitor-induced reactive oxygen generation by suspension-cultured soybean cells. Plant Physiol 124:725–732PubMedPubMedCentralGoogle Scholar
  336. Park CY, Heo WD, Yoo JH, Lee JH, Kim MC, Chun HJ, Moon BC, Kim IH, Park HC, Choi MS, Ok HM, Cheong MS, Lee SM, Kim HS, Lee KH, Lim CO, Chung WS, Cho MJ (2004) Pathogenesis-related gene expression by specific calmodulin isoforms is dependent on NIM1, a key regulator of systemic acquired resistance. Mol Cells 18:207–213PubMedGoogle Scholar
  337. Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318:113–116PubMedGoogle Scholar
  338. Park SW, Liu PP, Forouhar F, Vlot AC, Tong L, Tietjen K, Klessig DF (2009) Use of synthetic salicylic acid analog to investigate the roles of methyl salicylate and its esterases in plant disease resistance. J Biol Chem 284:7307–7317PubMedPubMedCentralGoogle Scholar
  339. Pastor V, Luna E, Mauch-Mani B, Ton J, Flors V (2013a) Primed plants do not forget. Environ Exp Bot 94:46–56Google Scholar
  340. Pastor V, Luna E, Ton J, Cerezo M, Garcia-Agustin P, Flors V (2013b) Fine tuning of ROS homeostasis regulates primed immune responses in Arabidopsis. Plant-Microbe Interact 26:1334–1344Google Scholar
  341. Pauwels L, Goossens A (2011) The JAZ proteins: a crucial interface in the jasmonate signaling cascade. Plant Cell 23:3089–3100PubMedCentralGoogle Scholar
  342. Pedley KF, Martin GB (2005) Role of mitogen-activated protein kinases in plant immunity. Curr Opin Plant Biol 8:541–547PubMedGoogle Scholar
  343. Peňa-Cortés HT, Albrecht T, Prat S, Weiler EW, Willmitzer L (1993) Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis. Planta 191:123–128Google Scholar
  344. Perchepied L, Balagué C, Riou C, Claudel-Renard C, Riviére N, Grezes-Besset B, Roby D (2010) Nitric oxide participates in the complex interplay of defense-related signaling pathways controlling disease resistance to Sclerotinia sclerotiorum in Arabidopsis thaliana. Mol Plant-Microbe Interact 23:846–860PubMedGoogle Scholar
  345. Peters JM, Franke WW, Kleinschmidt JA (1994) Distinct 19S and 20S subcomplexes of the 26S proteasome and their distribution in the nucleus and the cytoplasm. J Biol Chem 269:7709–7718PubMedGoogle Scholar
  346. 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 103:1111–1120PubMedGoogle Scholar
  347. Petrov VD, van Breusegem F (2012) Hydrogen peroxide – a central hub for information flow in plant cells. AOB Plants 2012:pls014. doi: 10.1093/aobpla/pls014
  348. Pickart CM, Eddins MJ (2004) Ubiquitin: structures, functions, mechanisms. Biochim Biophys Acta 1695:55–72PubMedGoogle Scholar
  349. Pieterse CMJ (2012) Prime time for transgenerational defense. Plant Physiol 158:545PubMedPubMedCentralGoogle Scholar
  350. Pieterse CMJ, Dicke M (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci 12:564–569PubMedGoogle Scholar
  351. Pieterse CMJ, Leon-Reyes A, van der Does D, Verhage A, Koornneef A, van Pelt JA, van Wees SCM (2012) Networking by small-molecule hormones in plant immunity. Induced resistance against insects and diseases. IOBC-WPRS Bull 83:77–80Google Scholar
  352. Pitzschke A, Djamei A, Bitton F, Hirt H (2009) A major role of the MEKK1-MKK1/2-MPK4 pathway in ROS signalling. Mol Plant 2:120–137PubMedCentralGoogle Scholar
  353. Potlakayala SD, Reed DW, Covello PS, Fobert PR (2007) Systemic acquired resistance in canola is linked with pathogenesis-related gene expression and requires salicylic acid. Phytopathology 97:794–802PubMedGoogle Scholar
  354. Po-Wen C, Singh P, Zimmerli L (2013) Priming of the Arabidopsis pattern-triggered immunity response upon infection by necrotrophic Pectobacterium carotovorum bacteria. Mol Plant Pathol 14:58–70PubMedGoogle Scholar
  355. Pré M, Atallah M, Champion A, De Vos M, Pieterse CMJ, Memelink J (2008) The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol 147:1347–1357PubMedPubMedCentralGoogle Scholar
  356. Price MB, Jelesko J, Okumoto S (2012) Glutamine receptor homologs in plants: functions and evolutionary origins. Front Plant Sci 3:Article 235. doi: 10.3389/fpls.2012.00235
  357. Probst AV, Fransz PF, Paszkowski J, Mittelsten Scheid O (2003) Two means of transcriptional reactivation within heterochromatin. Plant J 33:743–749PubMedGoogle Scholar
  358. Probst AV, Fagard M, Proux F, Mourrain P, Boutet S, Earley K, Lawrence RJ, Pikaard CS, Murfett J, Furner I, Vaucheret H, Scheid OM (2004) Arabidopsis histone deacetylase HDA6 is required for maintenance of transcriptional gene silencing and determines nuclear organization of rDNA repeats. Plant Cell 16:1021–1034PubMedPubMedCentralGoogle Scholar
  359. Qi X, Bao FS, Xie Z (2009) Small RNA deep sequencing reveals role for Arabidopsis thaliana RNA-dependent RNA polymerases in viral siRNA biogenesis. PLoS One 4:e4971PubMedPubMedCentralGoogle Scholar
  360. Qi Y, Tsuda K, Joe A, Sato M, Nguyen LV, Glazebrook J, Alfano JR, Cohen JD, Katagiri F (2010) A putative RNA-binding protein positively regulates salicylic acid-mediated immunity in Arabidopsis. Mol Plant-Microbe Interact 23:1573–1583PubMedGoogle Scholar
  361. Qiu D, Xiao J, Ding X, Xiong M, Cai M, Cao Y, Li X, Xu C, Wang S (2007) OsWRKY13 mediates rice disease resistance by regulating defense-related genes in salicylate- and jasmonate-dependent signaling. Mol Plant-Microbe Interact 20:492–499PubMedGoogle Scholar
  362. Qiu JL, Fiil BK, Petersen K, Nielsen HB, Botanga CJ, Thorgrimsen S, Palma K, Suarez-Rodriguez MC, Sandbech-Clausen S, Lichota J, Brodersen P, Grasser KD, Mattson O, Glazebrook J, Mundy J, Petersen M (2008a) Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J 27:2214–2221PubMedPubMedCentralGoogle Scholar
  363. Qiu JL, Zhou L, Yun B, Nielsen H, Fiil BK, Petersen K, MacKinlay J, Loake GJ, Mundy J, Morris PC (2008b) Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1. Plant Physiol 148:212–222PubMedPubMedCentralGoogle Scholar
  364. Qu F, Morris TJ (2005) Suppressors of RNA silencing encoded by plant viruses and their role in viral infection. FEBS Lett 579:5958–5964PubMedGoogle Scholar
  365. Quilis J, Peñas G, Messeguer J, Brugidou C, Segundo BS (2008) The Arabidopsis AtNPR1 inversely modulates defense responses against fungal, bacterial, or viral pathogens while conferring hypersensitivity to abiotic stresses in transgenic rice. Mol Plant-Microbe Interact 21:1215–1231Google Scholar
  366. 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 580:3498–3504PubMedGoogle Scholar
  367. Rakshandehroo F, Takeshita M, Squires J, Palukaitis P (2009) The influence of RNA-dependent RNA polymerase 1 on potato virus Y infection and on other antiviral response genes. Mol Plant-Microbe Interact 22:1312–1318Google Scholar
  368. Ranf S, Eschen-Lippold L, Pecher P, Lee J, Scheel D (2011) Interplay between calcium signaling and early signaling elements during defense responses to microbe- or damage-associated molecular patterns. Plant J 68:100–113PubMedGoogle Scholar
  369. Reddy ASN, Ali GS, Celesnik H, Day IS (2011) Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell 23:2010–2032PubMedCentralGoogle Scholar
  370. Ren D, Yang K-Y, Li G-J, Liu Y, Zhang S (2006) Activation of Ntf4, a tobacco mitogen-activated protein kinase, during plant defense and its involvement in hypersensitive response-like cell death. Plant Physiol 141:1482–1493PubMedPubMedCentralGoogle Scholar
  371. Ribnicky DM, Shulaev V, Raskin I (1998) Intermediates of salicylic acid biosynthesis in tobacco. Plant Physiol 118:565–572PubMedPubMedCentralGoogle Scholar
  372. Robert-Seilaniantz A, Grant MR, Jones JDG (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49:2621–2627Google Scholar
  373. Rocher F, Chollet J-F, Jousse C, Bonnemain J-L (2006) Salicylic acid, an ambimobile molecule exhibiting a high ability to accumulate in the phloem. Plant Physiol 141:1684–1693PubMedCentralGoogle Scholar
  374. Rochon A, Boyle P, Wignes T, Fobert PR, Després 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 18:3670–3685PubMedPubMedCentralGoogle Scholar
  375. Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258PubMedGoogle Scholar
  376. 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 13:2211–2224PubMedCentralGoogle Scholar
  377. Ruthenburg AJ, Allis CD, Wysocka J (2007) Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. Mol Cell 25:15–30PubMedGoogle Scholar
  378. Ryals JA, Weymann K, Lawton K, Friedrich L, Ellis D, Steiner H-Y, Johnson J, Delaney TP, Jesse T, Vos P, Uknes S (1997) The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor IkB. Plant Cell 9:425–439PubMedPubMedCentralGoogle Scholar
  379. Sagi M, Fluhr R (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol 141:336–340PubMedPubMedCentralGoogle Scholar
  380. Sänchez G, Gerhardt N, Siciliano F, Vojnov A, Malcuit I, Marono MR (2010) Salicylic acid is involved in the Nb-mediated defense responses to Potato virus X in Solanum tuberosum. Mol Plant-Microbe Interact 23:394–405PubMedGoogle Scholar
  381. Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the cross-roads of signaling. Plant Cell 14:S401–S417PubMedPubMedCentralGoogle Scholar
  382. Sano H, Seo S, Orudgev S, Youssefian K, Ishizuka K, Ohashi Y (1994) Expression of the gene for a small GTP binding protein in transgenic tobacco elevates endogenous cytokinin levels, abnormally induces salicylic acid in response to wounding, and increases resistance to tobacco mosaic virus infection. Proc Natl Acad Sci U S A 91:10556–10560PubMedPubMedCentralGoogle Scholar
  383. Sasaki Y, Asamizu E, Shibata D, Nakamura Y, Kaneko T, Awai K, Amagi M, Kuwata C, Tsugane T, Masuda T, Shimada H, Takamiya K, Ohta H, Tabata S (2001) Monitoring of methyl jasmonate-responsive genes in Arabidopsis by cDNA microarray: Self-activation of jasmonic acid biosynthesis and crosstalk with other phytohormone signaling pathways. DNA Res 8:153–161PubMedGoogle Scholar
  384. 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 171:263–270Google Scholar
  385. Segonzac C, Zipfel C (2011) Activation of plant pattern-recognition receptors by bacteria. Curr Opin Microbiol 14:54–61PubMedGoogle Scholar
  386. Seo PJ, Park C-M (2010) MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis. New Phytol 186:471–483PubMedGoogle Scholar
  387. Seo S, Okamoto M, Settee H, Ishizuka K, Sano H, Ohashi Y (1995) Tobacco MAP kinase: a possible mediator in wound signal transduction pathways. Science 270:1988–1992PubMedGoogle Scholar
  388. Seo S, Katou S, Seto H, Gomi K, Ohashi Y (2007) The mitogen-activated protein kinases WIPK and SIPK regulate the levels of jasmonic and salicylic acids in wounded tobacco plants. Plant J 49:899–909PubMedGoogle Scholar
  389. Seskar M, Shulaev V, Raskin I (1998) Endogenous methyl salicylate in pathogen-inoculated tobacco plants. Plant Physiol 116:387–392PubMedCentralGoogle Scholar
  390. Shah J (2009) Plants under attack: systemic signals in defence. Curr Opin Plant Biol 12:459–464PubMedGoogle Scholar
  391. Shah J, Zeier J (2013) Long-distance communication and signal amplification in systemic acquired resistance. Front Plant Sci 4:30. doi: 10.3389/fpls.2013.00030
  392. Shapiro AD, Gutsche AT (2003) Capillary electrophoresis-based profiling and quantitation of total salicylic acid and related phenolics for analysis of early signaling in Arabidopsis disease resistance. Anal Biochem 320:223–233PubMedGoogle Scholar
  393. Shen X, Yuan B, Liu H, Li X, Xu C, Wang S (2010) Opposite functions of a rice mitogen-activated protein kinase during the process of resistance against Xanthomonas oryzae. Plant J 64:86–99PubMedGoogle Scholar
  394. Shen W, Yan P, Gao L, Pan X, Wu J, Zhou P (2010b) Helper component-proteinase (HC-Pro) protein of Papaya ringspot virus interacts with papaya calreticulin. Mol Plant Pathol 11:335–346PubMedGoogle Scholar
  395. Shi L, Fang Y (2011) Histone variants: making structurally divergent nucleosomes and linkers in chromatin. Front Biol 6:93–101Google Scholar
  396. Shi J, An HL, Zhang L, Gao Z, Guo XQ (2010) GhMPK7, a novel multiple stress-responsive cotton group C MAPK gene, has a role in broad spectrum disease resistance and plant development. Plant Mol Biol 74:1–17PubMedGoogle Scholar
  397. Shimono M, Sugano S, Nakayama A, Jiang C-J, Ono K, Toki S, Takatsuji H (2007) Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell 19:2064–2076PubMedPubMedCentralGoogle Scholar
  398. Shoresh M, Gal-On A, Leibman D, Chet I (2006) Characterization of a mitogen-activated protein kinase gene from cucumber required for Trichoderma-conferred plant resistance. Plant Physiol 142:1169–1179PubMedPubMedCentralGoogle Scholar
  399. Shulaev V, Silverman P, Raskin I (1997) Airborne signaling by methyl salicylate in plant pathogen resistance. Nature 385:718–727Google Scholar
  400. Silverman P, Seskar M, Kanter D, Schweizer P, Métraux JP, Raskin I (1995) Salicylic acid in rice – biosynthesis, conjugation, and possible role. Plant Physiol 108:633–639PubMedPubMedCentralGoogle Scholar
  401. Sklodowska M, Gajewski E, Kuzniak E, Mikiciński A, Sobiczewski P (2010) BTH-mediated antioxidant system responses in apple leaf tissues. Scientia Hort 125:34–40Google Scholar
  402. Slaughter A, Daniel X, Flors V, Luna E, Hohn B, Mauch-Mani B (2012) Descendants of primed Arabidopsis plants exhibit resistance to biotic stress. Plant Physiol 158:835–843PubMedPubMedCentralGoogle Scholar
  403. Slaymaker DH, Navarre DA, Clark D, del Pozo O, Martin GB, Klessig DF (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 U S A 99:11640–11645PubMedPubMedCentralGoogle Scholar
  404. Snedden WA, Fromm H (2001) Calmodulin as a versatile calcium signal transducer in plants. New Phytol 151:35–66Google Scholar
  405. Song JT (2006) Induction of a salicylic acid glucosyltransferase, AtSGT1, is an early disease response in Arabidopsis thaliana. Mol Cells 22:233–238PubMedGoogle Scholar
  406. Song F, Goodman RM (2001) Molecular biology of disease resistance in rice. Physiol Mol Plant Pathol 59:1–11Google Scholar
  407. Song C, Yang B (2010) Mutagenesis of 18 type II effectors reveals virulence function of XopZPxo99 in Xanthomonas oryzae pv oryzae. Mol Plant-Microbe Interact 23:893–902PubMedGoogle Scholar
  408. Song JT, Lu H, Greenberg JT (2004a) Divergent roles in Arabidopsis thaliana development and defense of two homologous genes, aberrant growth and death2 and AGO2-LIKE DEFENSE RESPONSE PROTEIN1, encoding novel aminotransferases. Plant Cell 16:353–366PubMedPubMedCentralGoogle Scholar
  409. Song JT, Lu H, McDowell JM, Greenberg JT (2004b) A key role for ALD1 in activation of local and systemic defenses in Arabidopsis. Plant J 40:200–212PubMedGoogle Scholar
  410. Song JT, Koo YJ, Seo HS, Kim MC, Choi YD, Kim JH (2008) Overexpression of AtSGT1, an Arabidopsis salicylic acid glucosyltransferase, leads to increased susceptibility to Pseudomonas syringae. Phytochemistry 69:1128–1134PubMedGoogle Scholar
  411. Spoel SH, Dong X (2008) Making sense of hormone crosstalk during plant immune response. Cell Host Microbe 3:348–351PubMedGoogle Scholar
  412. Spoel SH, Dong X (2012) How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol 12:89–100PubMedGoogle Scholar
  413. Spoel SH, Koornneef A, Claessens SMC, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Metraux J-P, Brown R, Kazan K, Van Loon LC, Dong X, Pieterse CMJ (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770PubMedPubMedCentralGoogle Scholar
  414. Spoel SH, Johnson JS, Dong X (2007) Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci U S A 104:18842–18847PubMedPubMedCentralGoogle Scholar
  415. Spoel SH, Mou Z, Tada Y, Spivey NW, Genschik P, Dong X (2009) Proteasome-mediated coactivator NPR1 plays dual roles in regulating plant immunity. Cell 137:860–872PubMedPubMedCentralGoogle Scholar
  416. Stael S, Wurzinger B, Mair A, Mehlmer N, Vothknecht UC, Teige M (2012) Plant organellar calcium signaling: an emerging field. J Exp Bot 63:1525–1542PubMedPubMedCentralGoogle Scholar
  417. Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117–2127PubMedPubMedCentralGoogle Scholar
  418. Stein M, Dittgen J, Sanchez-Rodriquez C, Hou BH, Molina A, Schulze-Lefert P, Lipka V, Somerville S (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to non-host resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18:731–746PubMedPubMedCentralGoogle Scholar
  419. Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4:447–456PubMedGoogle Scholar
  420. Strawn MA, Marr SK, Inoue K, Inada N, Zubieta C, Wildermuth MC (2007) Arabidopsis isochorismate synthase functional in pathogen-induced salicylate biosynthesis exhibits properties consistent with a role in diverse stress responses. J Biol Chem 282:5919–5933PubMedGoogle Scholar
  421. Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R (2011) Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol 14:691–699PubMedGoogle Scholar
  422. Szczesny R, Buttner B, Escolar L, Schulze S, Seiferth A, Bonas U (2010) Suppression of the AvrBs1-specific hypersensitive response by the YopJ effector homolog AvrBsT from Xanthomonas depends on a SNF1-related kinase. New Phytol 187:1058–1074PubMedGoogle Scholar
  423. 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 thioredoxin. Science 321:952–956PubMedGoogle Scholar
  424. Takabatake R, Karita E, Seo S, Mitsuhara I, Kuchitsu K, Ohashi Y (2007) Pathogen-induced calmodulin isoforms in basal resistance against bacterial and fungal pathogens in tobacco. Plant Cell Physiol 48:414–423PubMedGoogle Scholar
  425. Takahashi H, Miller J, Nozaki Y, Takeda M, Shah J, Hase S, Ikegami M, Ehara Y, Dinesh-Kumar SP, Sukamoto (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 32:655–657PubMedGoogle Scholar
  426. Takahashi Y, Uehara Y, Berberich T, Ito A, Saitoh H, Miyazaki A, Terauchi R, Kusano T (2004) A subset of hypersensitive response marker genes, including HSR203J, is the downstream target of a spermine signal transduction pathway in tobacco. Plant J 40:586–595PubMedGoogle Scholar
  427. Teige M, Scheikl E, Eulgem T, Doczi R, Ichimura K, Shinozaki K, Dangl JL, Hirt H (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell 15:141–152PubMedGoogle Scholar
  428. Thaler JS, Bostock RM (2004) Interactions between abscisic acid-mediated responses and plant resistance to pathogens and insects. Ecology 85:48–58Google Scholar
  429. Thibaud-Nissen F, Wu H, Richmond T, Redman JC, Johnson C, Green R, Arias J, Town CD (2006) Development of Arabidopsis whole-genome microarrays and their application to the discovery of binding sites for the TGA2 transcription factor in salicylic acid-treated plants. Plant J 47:152–162PubMedGoogle Scholar
  430. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF:COI1 complex during jasmonate signaling. Nature 448:661PubMedGoogle Scholar
  431. Thomma B, Penninckx I, Broekaert WF, Cammue BPA (2001) The complexity of disease signaling in Arabidopsis. Curr Opin Immunol 13:63–68PubMedGoogle Scholar
  432. Thomma BPHJ, Nürnberger T, Joosten MHAJ (2011) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4–15PubMedPubMedCentralGoogle Scholar
  433. Tischner R, Koltermann M, Haesse H, Plath M (2010) Early responses of Arabidopsis thaliana to infection by Verticillium longisporum. Physiol Mol Plant Pathol 74:419–427Google Scholar
  434. Torres MA, Jones JDG, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141:373–378PubMedPubMedCentralGoogle Scholar
  435. Tripathi D, Jiang Y-L, Kumar D (2010) SABP2, a methyl salicylate esterase is required for the systemic acquired resistance induced by acibenzolar-S-methyl in plants. FEBS Lett 584:3458–3463PubMedGoogle Scholar
  436. Truman G, Glazebrook J (2012) Coexpression analysis identifies putative targets for CBP60g and SARD1 regulation. BMC Plant Biol 12:216PubMedPubMedCentralGoogle Scholar
  437. 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 U S A 104:1075–1080PubMedPubMedCentralGoogle Scholar
  438. Tsuda K, Sato M, Glazebrook J, Cohen JD, Katagiri F (2008) Interplay between MAMP-triggered and SA-mediated defense responses. Plant J 53:763–775PubMedGoogle Scholar
  439. Umemura K, Satou J, Iwata M, Uozumi N, Koga J, Kawano T, Koshiba T, Anzai H, Mitomi M (2009) Contribution of salicylic acid glucosyltransferase, OsSGT1, to chemically induced disease resistance in rice plants. Plant J 57:463–472PubMedGoogle Scholar
  440. Uppalapati SR, Toyoda K, Yasuhiro I, Ichinose Y, Shiraishi T (2004) Differential regulation of MBP kinases by a glycoprotein elicitor and a polypeptide suppressor from Mycosphaerella pinodes in pea. Physiol Mol Plant Pathol 64:17–25Google Scholar
  441. 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 20:955–965PubMedGoogle Scholar
  442. Vaistij FE, Jones L (2009) Compromised virus-induced gene silencing in RDR6-deficient plants. Plant Physiol 149:1399–1407PubMedPubMedCentralGoogle Scholar
  443. Valent B, Khang CH (2010) Recent advances in rice blast effector research. Curr Opin Plant Biol 13:434–441PubMedGoogle Scholar
  444. Vatsa P, Chiltz A, Bourgue S, Wendehenne D, Garcia-Brugger A, Pugin A (2011) Involvement of putative glutamate receptors in plant defence signaling and NO production. Biochimie 93:2095–2101PubMedGoogle Scholar
  445. van den Burg HA, Takken FLW (2009) Does chromatin remodeling mark systemic acquired resistance? Trends Plant Sci 14:286–294PubMedGoogle Scholar
  446. van den Burg HA, Takken FLW (2010) SUMO-, MAPK- and resistance protein-signaling converge at transcription complexes that regulate plant innate immunity. Plant Signal Behav 5:1507–1601Google Scholar
  447. Van der Does D, Leon-Reyes A, Koornneef A, Van Verk MC, Rodenburg N, Pauwels L, Goossens A, Körbes AP, Memelink J, Ritsema T, Van Wees SCM, Pieterse CMJ (2013) Salicylic acid suppresses jasmonic acid signaling downstream of SCFCOI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59. Plant Cell 25:744–751PubMedPubMedCentralGoogle Scholar
  448. Van der Ent S, Verhagen BWM, Van Doorn R, Bakker D, Verlaan MG, Pel MJC, Joosten RG, Proveniers MCG, Van Loon LC, Ton J, Pieterse CMJ (2008) MYB72 is required in early signaling steps of rhizobacteria-induced systemic resistance in Arabidopsis. Plant Physiol 146:1293–1304PubMedPubMedCentralGoogle Scholar
  449. van Hulten M, Pelser M, van Loon LC, Pieterse CMJ, Ton J (2006) Costs and benefits of priming for defense in Arabidopsis. Proc Natl Acad Sci U S A 103:5602–5607PubMedPubMedCentralGoogle Scholar
  450. van Verk MC, Bol JF, Linthorst HJM (2011) WRKY transcription factors involved in activation of SA biosynthesis genes. BMC Plant Biol 11:89. doi: 10.1186/1471-2229-11-89 PubMedPubMedCentralGoogle Scholar
  451. van Verk MC, Pappaaioannou D, Neeleman L, Bol JF, Linthorst HJM (2008) A novel WRKY transcription factor is required for induction of PR-1a gene expression by salicylic acid and bacterial elicitors. Plant Physiol 140:1983–1995Google Scholar
  452. Vernooij B, Friedrich L, Morse A, Resist R, Kolditz-Jawhar R, Ward E, Uknes S, Kessmann H, Ryals J (1994) Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell 6:959–965PubMedPubMedCentralGoogle Scholar
  453. Vicente J, Cascón T, Vicedo B, Garcia-Agustin P, Hamberg M, Castresana C (2012) Role of 9-lipoxygenase and α-dioxygenase oxylipin pathways as modulators of local and systemic defense. Mol Plant 5:914–928PubMedGoogle Scholar
  454. Vidhyasekaran P (2007) Fungal pathogenesis in plants and crops: molecular biology and host defense mechanisms, 2nd edn. CRC Press/Taylor Francis Group, Boca Raton, p 510Google Scholar
  455. Vidhyasekaran P (2014) PAMP signals in plant innate immunity: signal perception and transduction. Springer, Dordrecht, p 442Google Scholar
  456. Vincill ED, Bieck AM, Spalding EP (2012) Ca2+ conduction by an amino acid-gated ion channel related to glutamate receptors. Plant Physiol 159:40–46PubMedPubMedCentralGoogle Scholar
  457. Vlot AC, Klessig DF, Park S-W (2008a) Systemic acquired resistance: the elusive signal(s). Curr Opin Plant Biol 11:436–442PubMedGoogle Scholar
  458. Vlot AC, Liu P-P, Cameron RK, Park S-W, Yang Y, Kumar D, Zhou F, Padukkavidana T, Gustafsson C, Pichersky E, Klessig DF (2008b) Identification of likely orthologs of tobacco salicylic acid-binding protein 2 and their role in systemic acquired resistance in Arabidopsis thaliana. Plant J 56:445–456PubMedGoogle Scholar
  459. Voinnet O (2008) Post-transcriptional RNA silencing in plant-microbe interactions: a touch of robustness and versatility. Curr Opin Plant Biol 11:464–470PubMedGoogle Scholar
  460. Waller F, Müller A, Chung K-M, Yap Y-K, Nakamura K, Weiler E, Sano H (2006) Expression of a WIPK-activated transcription factor results in increase of endogenous salicylic acid and pathogen resistance in tobacco plants. Plant Cell Physiol 47:1169–1174PubMedGoogle Scholar
  461. Wan D, Li R, Zou B, Zhang X, Cong J, Wang R, Xia Y, Li G (2012) Calmodulin-binding protein CBP60g is a positive regulator of both disease resistance and drought tolerance in Arabidopsis. Plant Cell Rep 31:1269–1281PubMedGoogle Scholar
  462. Wang ZP, Yang PZ, Fan BF, Chen ZX (1998) An oligo selection procedure for identification of sequence-specific DNA-binding activities associated with the plant defense response. Plant J 16:515–522PubMedGoogle Scholar
  463. 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:e123PubMedPubMedCentralGoogle Scholar
  464. 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 17:1784–1790PubMedGoogle Scholar
  465. Wang Y, Gao M, Li Q, Wang L, Jeon J-S, Qu N, Zhang Y, He Z (2008) OsRAR1 and OsSGT1 physically interact and function in rice basal disease resistance. Mol Plant-Microbe Interact 21:294–303PubMedGoogle Scholar
  466. 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(2):e1000301. doi: 10.1371/journal.ppat.1000301 PubMedPubMedCentralGoogle Scholar
  467. Wang X-B, Wu Q, Ito T, Cillo F, Li W-X, Chen X, Yu J-L, Ding S-W (2010) RNAi-mediated viral immunity requires amplification of virus-derived siRNAs in Arabidopsis thaliana. Proc Natl Acad Sci U S A 107:484–489PubMedPubMedCentralGoogle Scholar
  468. Wang L, Tsuda K, Truman W, Sato M, le Nguyen V, Katagiri F, Glazebrook J (2011) CBP60g and SARD1 play partially redundant critical roles in salicylic acid signaling. Plant J 67:1029–1041PubMedGoogle Scholar
  469. Wang W-H, Yi X-Q, Han A-D, Liu T-W, Chen J, Wu F-H, Dong X-J, He J-X, Pei Z-M, Pei Z-M, Zheng H-L (2012) Calcium-sensing receptor regulates stomatal closure through hydrogen peroxide and nitric oxide in response to extracellular calcium in Arabidopsis. J Exp Bot 63:177–190PubMedPubMedCentralGoogle Scholar
  470. Ward JM, Maser P, Schroeder JI (2009) Plant ion channels: gene families, physiology and functional genomic analyses. Annu Rev Physiol 71:59–82PubMedGoogle Scholar
  471. Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot (Lond) 100:681–697Google Scholar
  472. Wathugala DL, Hemsley PA, Moffat CS, Cremelie P, Knight MR, Knight H (2012) The Mediator subunit SFR6/MED16 controls defence gene expression mediated by salicylic acid and jasmonate responsive pathways. New Phytol 195:217–230PubMedGoogle Scholar
  473. Weigel RR, Pfitzner UM, Gatz C (2005) Interaction of NIMIN1 with NPR1 modulates PR gene expression in Arabidopsis. Plant Cell 17:1279–1291PubMedPubMedCentralGoogle Scholar
  474. Wendehenne D, Durner J, Chen Z, Klessig DF (1998) Benzothiadiazole, an inducer of plant defenses, inhibits catalase and ascorbate peroxidases. Phytochemistry 47:651–657Google Scholar
  475. Wiermer M, Feys BJ, Parker JE (2005) Plant immunity: the EDS1 regulatory node. Curr Opin Plant Biol 8:383–389PubMedGoogle Scholar
  476. Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthesis is required to synthesize salicylic acid for plant defense. Nature 414:562–565PubMedGoogle Scholar
  477. Willmann MR, Endres MW, Cook RT, Gregory BD (2011) The functions of RNA-dependent RNA polymerases in Arabidopsis. Arabidopsis Book 9:e0146. doi: 10.1199/tab.0146 PubMedPubMedCentralGoogle Scholar
  478. Wong CE, Carson RA, Carr JP (2002) Chemically induced virus resistance in Arabidopsis thaliana is independent of pathogenesis-related protein expression and the NPR1 gene. Mol Plant-Microbe Interact 15:75–81PubMedGoogle Scholar
  479. Wu S, Lu D, Kabbage M, Wei H-L, Swingle B, Records AR, Dickman M, He P, Shan L (2011) Bacterial effector HopF2 suppresses Arabidopsis innate immunity at the plasma membrane. Mol Plant-Microbe Interact 24:585–593PubMedPubMedCentralGoogle Scholar
  480. Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, Brindle ID, De Luca V, Desprѐs C (2012) The Arabidopsis NPR1 protein is a receptor to the plant defense hormone salicylic acid. Cell Rep 1:639–647PubMedGoogle Scholar
  481. Wypijewski K, Hornyik C, Shaw JA, Stephens J, Goraczniak R, Gunderson SI, Lacomme C (2009) Ectopic 5’ splice sites inhibit gene expression by engaging RNA surveillance and silencing pathways in plants. Plant Physiol 151:955–965PubMedPubMedCentralGoogle Scholar
  482. Xia Y, Suzuki H, Borevitz J, Blount J, Guo Z, Patel K, Dixon RA, Lamb C (2004) An extracellular aspartic protease functions in Arabidopsis disease resistance signaling. EMBO J 23:980–988PubMedPubMedCentralGoogle Scholar
  483. Xiao S, Brown S, Patrick E, Brearley C, Turner J (2003) Enhanced transcription of the Arabidopsis disease resistance genes RPW81 and RPW82 via salicylic acid-dependent amplification circuit is required for hypersensitive cell death. Plant Cell 15:33–45PubMedPubMedCentralGoogle Scholar
  484. Xie Z, Fan B, Chen C, Chen Z (2001) An important role of an inducible RNA-dependent RNA polymerase in plant antiviral defense. Proc Natl Acad Sci U S A 98:6516–6521PubMedPubMedCentralGoogle Scholar
  485. Xie Z, Kasschau KD, Carrinton JC (2003) Negative feedback regulation of Dicer-Like1 in Arabidopsis by microRNA-guided mRNA degradation. Curr Biol 13:784–789PubMedGoogle Scholar
  486. Xing D, Chen Z (2006) Effects of mutations and constitutive overexpression of EDS1 and PAD4 on plant resistance to different types of microbial pathogens. Plant Sci 171:251–262Google Scholar
  487. Xing DH, Lai ZB, Zheng ZY, Vinod KM, Fan BF, Chen ZX (2008) Stress- and pathogen-induced Arabidopsis WRKY48 is a transcriptional activator that represses plant basal defense. Mol Plant 1:459–470PubMedGoogle Scholar
  488. Xu X, Chen C, Fan B, Chen Z (2006) Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. Plant Cell 18:1310–1326PubMedPubMedCentralGoogle Scholar
  489. Xu J, Audenaert K, Hofte M, De Vleesschauwer D (2013) Abscisic acid promotes susceptibility to the rice blight pathogen Xanthomonas oryzae pv. oryzae by suppressing salicylic acid-mediated defenses. PLoS One 8(6):e67413PubMedPubMedCentralGoogle Scholar
  490. Yalowsky S, Baluska F, Jones A (2010) Integrated G proteins signaling in plants. Springer, HeidelbergGoogle Scholar
  491. Yalpani N, Silverman P, Wilson TMA, Kleier DA, Raskin I (1991) Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. Plant Cell 3:809–815PubMedPubMedCentralGoogle Scholar
  492. Yalpani N, León J, Lawton MA, Raskin I (1993) Pathway of salicylic acid biosynthesis in healthy and virus-inoculated tobacco. Plant Physiol 103:315–321PubMedPubMedCentralGoogle Scholar
  493. Yang Z (2002) Small GTPases: versatile signaling switches in plants. Plant Cell 14(Suppl):S375–S388PubMedPubMedCentralGoogle Scholar
  494. Yang D-L, Yang Y, He Z (2013) Roles of plant hormones and their interplay in rice immunity. Mol Plant 6:675–685PubMedGoogle Scholar
  495. Yasuda M (2007) Regulation mechanisms of systemic acquired resistance induced by plant activators. J Pest Sci 32:281–282Google Scholar
  496. Yasuda M, Nakashita H, Hasegawa S, Nishioka M, Arai Y, Uramoto M, Yamaguchi I, Yoshida S (2003) N-Cyanomethyl-2-chloroisonicotinamide induces systemic acquired resistance in Arabidopsis without salicylic acid accumulation. Biosci Biotechnol Biochem 67:322–328PubMedGoogle Scholar
  497. Yoda H, Sano H (2003) Activation of hypersensitive response genes in the absence of pathogens in transgenic tobacco plants expressing a small GTPase. Planta 217:993–997PubMedGoogle Scholar
  498. Yoda P, Ogawa M, Yamaguchi Y, Koizumi N, Kusano T, Sano H (2002) Identification of early-responsive genes associated with the hypersensitive response to tobacco mosaic virus and characterization of a WRKY-type transcription factor in tobacco plants. Mol Genet Genomics 267:154–161PubMedGoogle Scholar
  499. Yoshioka K, Sugie K, Park HJ, Maeda H, Tsuda N, Kawakita K, Doke N (2001) Induction of plant gp91 phox homolog by fungal cell wall, arachidonic acid, and salicylic acid in potato. Mol Plant-Microbe Interact 14:725–736PubMedGoogle Scholar
  500. 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 13:1527–1539PubMedPubMedCentralGoogle Scholar
  501. Yu D, Fan B, MacFarlane SA, Chen Z (2003) Analysis of the involvement of an inducible Arabidopsis RNA-dependent RNA polymerase in antiviral defense. Mol Plant-Microbe Interact 16:206–216PubMedGoogle Scholar
  502. Zago E, Morsa S, Dat JF, Alard P, Ferrarini A, Inzé D, Delledonne M, Van Breusegem F (2006) Nitric oxide- and hydrogen peroxide-responsive gene regulation during cell death induction in tobacco. Plant Physiol 141:404–411PubMedPubMedCentralGoogle Scholar
  503. Zahn LM (2009) Secondary messenger. Sci Signal 2:ec123Google Scholar
  504. Zander M, La Camera S, Lamotte O, Metraux JP, Gatz C (2010) Arabidopsis thaliana class-II TGA transcription factors are essential activators of jasmonic acid/ethylene-induced defense responses. Plant J 61:200–210PubMedGoogle Scholar
  505. Zander M, Chen S, Imkampe J, Thurow C, Gatz C (2012) Repression of the Arabidopsis thaliana jasmonic acid/ethylene-induced defense pathway by TGA-interacting glutaredoxins depends on their C-terminal ALWL motif. Mol Plant 5:831–840PubMedGoogle Scholar
  506. Zhang X (2008) The epigenetic landscape of plants. Science 320:489–492PubMedGoogle Scholar
  507. Zhang SQ, Klessig DF (1997) Salicylic acid activates a 48-kD MAP kinase in tobacco. Plant Cell 9:809–824PubMedPubMedCentralGoogle Scholar
  508. Zhang S, Liu Y (2001) Activation of salicylic acid-induced protein kinase, a mitogen-activated protein kinase, induces multiple defense responses in tobacco. Plant Cell 13:1877–1889PubMedPubMedCentralGoogle Scholar
  509. Zhang SQ, Du H, Klessig DF (1998) Activation of the tobacco SIP kinase by both a cell wall-derived carbohydrate elicitor and purified proteinaceous elicitins from Phytophthora spp. Plant Cell 10:435–449PubMedPubMedCentralGoogle Scholar
  510. Zhang Y, Fan M, 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 PR1 gene. Proc Natl Acad Sci U S A 96:6523–6528PubMedPubMedCentralGoogle Scholar
  511. 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 15:2647–2653PubMedPubMedCentralGoogle Scholar
  512. Zhang X, Dai Y, Xiong Y, DeFraia C, Li J, Dong X, Mou Z (2007a) Overexpression of Arabidopsis MAP kinase kinase 7 leads to activation of plant basal and systemic acquired resistance. Plant J 52:1066–1079PubMedGoogle Scholar
  513. Zhang Z, Li Q, Staswick PE, Wang M, Zhu Y, He Z (2007b) Dual regulation role of GH3.5 in salicylic acid and auxin signaling Arabidopsis-Pseudomonas syringae interaction. Plant Physiol 145:450–464PubMedPubMedCentralGoogle Scholar
  514. Zhang Y, Xu S, Ding P, Wang D, Cheng YT, He J, Geo M, Xu F, Li Y, Zhu Z, Li X, Zhang Y (2010) Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors. Proc Natl Acad Sci U S A 107:18220–18225PubMedPubMedCentralGoogle Scholar
  515. Zhang W, Jeon BW, Assmann SM (2011) Heterotrimeric G-protein regulation of ROS signalling and calcium currents in Arabidopsis guard cells. J Exp Bot 62:2371–2379PubMedGoogle Scholar
  516. Zhang L, Li Y, Lu W, Meng F, Wu C, Guo X (2012a) Cotton GhMKK5 affects disease resistance, induces HR-like cell death, and reduces the tolerance to salt and drought stress in transgenic Nicotiana benthamiana. J Exp Bot 63:3935–3952PubMedPubMedCentralGoogle Scholar
  517. Zhang X, Wang C, Zhang Y, Sun Y, Mou Z (2012b) The Arabidopsis mediator complex subunit16 positively regulates salicylate-mediated systemic acquired resistance and jasmonate/ethylene-induced defense pathways. Plant Cell 24:4294–4309PubMedPubMedCentralGoogle Scholar
  518. Zhang Z, Wu Y, Gao M, Zhang J, Kong Q, Liu Y, Ba H, Zhou J, Zhang Y (2012c) Disruption of PAMP-induced MAP kinase cascade by a Pseudomonas syringae effector activates plant immunity mediated by the NB-LRR protein SUMM2. Cell Host Microbe 11:253–263PubMedGoogle Scholar
  519. Zheng Z, Qamar SA, Chen Z, Mengiste T (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J 48:596–605Google Scholar
  520. Zheng Z, Mosher SL, Fan B, Klessig DF, Chen Z (2007) Functional analysis of Arabidopsis WRKY25 transcription factor in plant defense against Pseudomonas syringae. BMC Plant Biol 7:2PubMedPubMedCentralGoogle Scholar
  521. Zheng X, Spivey NW, Zeng W, Liu Po-Pu, Fu ZQ, Klessig DF, He SY, Dong X (2012) Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 11:587–596PubMedPubMedCentralGoogle Scholar
  522. Zhou N, Tootle T, Tsui F, Klessig D, Glazebrook J (1998) PAD4 functions upstream from salicylic acid to control defense responses to Arabidopsis. Plant Cell 10:1021–1030PubMedPubMedCentralGoogle Scholar
  523. Zhou F, Mosher S, Tian M, Sassi G, Parker J, Klessig DF (2008) The Arabidopsis gain-of-function mutant ssi4 requires RAR1 and SGT1b differentially for defense activation and morphological alterations. Mol Plant-Microbe Interact 21:40–49PubMedGoogle Scholar
  524. Zhu YJ, Qiu X, Moore PH, Borth W, Hu J, Ferreira S, Albert HH (2003) Systemic acquired resistance induced by BTH in papaya. Physiol Mol Plant Pathol 63:237–248Google Scholar
  525. Ziadi S, Barbedette S, Godard JF, Monot C, Le Corre D, Silue D (2008) Production of pathogenesis-related proteins in the cauliflower (Brassica oleracea var botrytis)-downy mildew (Peronospora parasitica) pathosystem treated with acibenzolar-S-methyl. Plant Pathol 50:579–586Google Scholar
  526. Zoeller M, Stingl N, Krischke M, Fekete A, Waller F, Berger S, Mueller MJ (2012) Lipid profiling of the Arabidopsis hypersensitive response reveals specific lipid peroxidation and fragmentation processes: biogenesis of pimelic and azelaic acid. Plant Physiol 160:365–378PubMedPubMedCentralGoogle Scholar
  527. Zottini M, Costa A, De Michele R, Ruzzene M, Carimi F, Lo Schiavo F (2007) Salicylic acid activates nitric oxide synthesis in Arabidopsis. J Exp Bot 58:1397–1405PubMedGoogle Scholar
  528. Zwicker S, Mast S, Stos V, Pfitzner AJP, Pfitzner UM (2007) Tobacco NIMIN2 proteins control PR gene induction through transient repression early in systemic acquired resistance. Mol Plant Pathol 8:385–400PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • P. Vidhyasekaran
    • 1
  1. 1.Plant PathologyTamil Nadu Agricultural UniversityCoimbatoreIndia

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