Advertisement

Insights into the Role of WRKY Superfamily of Protein Transcription Factor in Defense Response

  • Preeti Singh
  • Shashi Shekhar
  • Anjana Rustagi
  • Vinay Sharma
  • Deepak Kumar
Chapter

Abstract

Plants are constantly challenged by a variety of biotic and abiotic stresses. To combat these challenges, plants have developed intricate mechanisms to perceive external signals and respond with the proper physiological and morphological changes. Generally, plants regulate the expression of many stress-related genes by activating or repressing their transcription upon signal perception and transduction of the external stimuli. The WRKY transcription factors comprise a large family of plant-specific zinc-finger-type regulatory proteins and regulate many plant defense responses to diverse biotic and abiotic stresses. WRKY proteins possess either one or two WRKY domains, a 60-amino-acid region that contains the amino acid sequence WRKYGQK, and a zinc-finger-like motif. In spite of the strong conservation of their DNA-binding domain, the overall structures of WRKY proteins are highly divergent and can be categorized into distinct groups, which might reflect their different functions. Based on the number of conserved WRKY domains and the features of the zinc-finger motif, the WRKY superfamily can be divided into three distinct groups: I, II, and III. Previous studies have demonstrated that WRKY transcription factors participate in regulating defense gene expression at various levels, partly by directly modulating immediate downstream target genes, by activating or repressing other TF genes, and by regulating WRKY genes. WRKY proteins also seem to be involved in other plant-specific processes, such as trichome development and the biosynthesis of secondary metabolites. In this chapter, we will focus our attention to the role of WRKY TFs in plant defense response.

Keywords

Biotic stress Plant defense Transcription factor WRKY Zinc-finger protein 

References

  1. Abbruscato P, Nepusz T, Mizzi L, Del Corvo M, Morandini P, Fumasoni I, Michel C, Paccanaro A, Guiderdoni E, Schaffrath U, Morel JB, Piffanelli P, Faivre-Rampant O (2012) OsWRKY22, a monocot WRKY gene, plays a role in the resistance response to blast. Mol Plant Pathol 3:828–841CrossRefGoogle Scholar
  2. Adachi H, Nakano T, Miyagawa N, Ishihama N, Yoshioka M, Katou Y et al (2015) WRKY transcription factors phosphorylated by MAPK regulate a plant immune NADPH oxidase in Nicotiana benthamiana. Plant Cell 27:2645–2663PubMedPubMedCentralCrossRefGoogle Scholar
  3. Agarwal P, Reddy MP, Chikara J (2011) WRKY: its structure, evolutionary relationship, DNA-binding selectivity, role in stress tolerance and development of plants. Mol Biol Rep 38:3883–3896PubMedCrossRefGoogle Scholar
  4. Alvarez-Venegas R, Abdallat AA, Guo M, Alfano JR, Avramova Z (2007) Epigenetic control of a transcription factor at the cross section of two antagonistic pathways. Epigenetics 2:106–113PubMedCrossRefGoogle Scholar
  5. Andreasson E, Jenkins T, Brodersen P, Thorgrimsen S, Petersen NHT, Zhu S, Qiu J-L, Micheelsen P, Rocher A, Petersen M, Newman M-A et al (2005) The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO J 24:2579–2589PubMedPubMedCentralCrossRefGoogle Scholar
  6. Ay N, Irmler K, Fischer A, Uhlemann R, Reuter G, Humbeck K (2009) Epigenetic programming via histone methylation at WRKY53 controls leaf senescence in Arabidopsis thaliana. Plant J 58:333–346PubMedCrossRefGoogle Scholar
  7. Bakshi M, Oelmüller R (2014) WRKY transcription factors: Jack of many trades in plants. Plant Signal Behav 9:e27700PubMedPubMedCentralCrossRefGoogle Scholar
  8. Banerjee A, Roychoudhury A (2015) WRKY proteins: signaling and regulation of expression during abiotic stress responses. Sci World J 2015:807560CrossRefGoogle Scholar
  9. Berk AJ, Schmidt MC (1990) How do transcription factors work? Genes Dev 4:151–155Google Scholar
  10. Birkenbihl RP, Diezel C, Somssich IE (2012) Arabidopsis WRKY33 is a key transcriptional regulator of hormonal and metabolic responses toward Botrytiscinerea infection. Plant Physiol 159:266–285PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bostock RM (2005) Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu Rev Phytopathol 43:545–580PubMedCrossRefGoogle Scholar
  12. Chang IF, Curran A, Woolsey R, Quilici D, Cushman JC, Mittler R et al (2009) Proteomic profiling of tandem affinity purified 14-3-3 protein complexes in Arabidopsis thaliana. Proteomics 9:2967–2985PubMedPubMedCentralCrossRefGoogle Scholar
  13. Chen C, Chen Z (2002) Potentiation of developmentally regulated plant defense response by AtWRKY18, a pathogen-induced Arabidopsis transcription factor. Plant Physiol 129:706–716PubMedPubMedCentralCrossRefGoogle Scholar
  14. Chen H, Lai Z, Shi J, Xiao Y, Chen Z, Xu X (2010) Roles of Arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biol 10:281PubMedPubMedCentralCrossRefGoogle Scholar
  15. Chen L, Zhang L, Li D, Wang F, Yu D (2013) WRKY8 transcription factor functions in the TMV-cg defense response by mediating both abscisic acid and ethylene signaling in Arabidopsis. Proc Natl Acad Sci 110:E1963–E1971PubMedPubMedCentralCrossRefGoogle Scholar
  16. Cheng Y, Zhou Y, Yang Y, Chi YJ, Zhou J, Chen JY et al (2012) Structural and functional analysis of VQ motif-containing proteins in Arabidopsis as interacting proteins of WRKY transcription factors. Plant Physiol 159:810–825PubMedPubMedCentralCrossRefGoogle Scholar
  17. Chi Y, Yang Y, Zhou Y, Zhou J, Fan B, Yu JQ et al (2013) Protein-protein interactions in the regulation of WRKY transcription factors. Mol Plant 6:287–300PubMedCrossRefGoogle Scholar
  18. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814PubMedCrossRefGoogle Scholar
  19. Chujo T, Takai R, Akimoto-Tomiyama C, Ando S, Minami E, Nagamura Y, Kaku H, Hibuya N, Yasuda M, Nakashita H, Umemura K, Okada A, Okada K, Nojiri H, Yamane H (2007) Involvement of the elicitor-induced gene OsWRKY53 in the expression of defense-related genes in rice. BBA Gene Struct Expr 1769:497–505CrossRefGoogle Scholar
  20. Dang FF, Wang YN, Yu L, Eulgem T, Lai Y, Liu ZQ, Wang X, Qiu AL, Zhang TX, Lin J, Chen YS, Guan DY, Cai HY, Mou SL, He SL (2013) CaWRKY40, a WRKY protein of pepper, plays an important role in the regulation of tolerance to heat stress and resistance to Ralstonia solanacearum infection. Plant Cell Environ 36:757–774PubMedCrossRefGoogle Scholar
  21. Denison FC, Paul A-L, Zupanska AK, Ferl RJ (2011) 14-3-3 proteins in plant physiology. Semin Cell Dev Biol 22:720–727PubMedCrossRefGoogle Scholar
  22. Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M, Boucher C, Somssich I, Genin S, Marco Y (2003) Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc Natl Acad Sci U S A 100:8024–8029PubMedPubMedCentralCrossRefGoogle Scholar
  23. Duan M-R, Nan J, Liang YH, Mao P, Lu L, Li L, Wei C, Lai L, Li Y, Su XD (2007) DNA binding mechanism revealed by high resolution crystal structure of Arabidopsis thaliana WRKY1 protein. Nucleic Acids Res 35:1145–1154PubMedPubMedCentralCrossRefGoogle Scholar
  24. Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209PubMedCrossRefGoogle Scholar
  25. Encinas-Villarejo S, Maldonado AM, Amil-Ruiz F, de los Santos B, Romero F, Pliego-Alfaro F, Muñoz-Blanco J, Caballero JL (2009) Evidence for a positive regulatory role of strawberry (Fragaria x ananassa) FaWRKY1 and Arabidopsis AtWRKY75 proteins in resistance. J Exp Bot 60:3043–3065PubMedCrossRefGoogle Scholar
  26. Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371PubMedCrossRefGoogle Scholar
  27. Eulgem T, Rushton PJ, Schmelzer E, Hahlbrock K, Somssich IE (1999) Early nuclear events in plant defense signalling: rapid gene activation by WRKY transcription factors. EMBO J 18:4689–4699PubMedPubMedCentralCrossRefGoogle Scholar
  28. Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206PubMedCrossRefGoogle Scholar
  29. Franco-Zorrillaa JM, López-Vidrieroa I, Carrascob JL, Godoya M, Verab P, Solanoc R (2014) DNA-binding specificities of plant transcription factors and their potential to define target genes. PNAS 111(6):2367–2372CrossRefGoogle Scholar
  30. Fu ZQ, Yan 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 theimmune signal salicylic acid in plants. Nature 486:228–232PubMedPubMedCentralGoogle Scholar
  31. Hu J, Barlet X, Deslandes L, Hirsch J, Feng DX, Somssich I, Marco Y (2008) Transcriptional responses of Arabidopsis thaliana during wilt diseasecaused by the soil-borne phytopathogenic bacterium, Ralstonia solanacearum. PLoS One 3:e2589PubMedPubMedCentralCrossRefGoogle Scholar
  32. Hu L, Ye M, Li R, Zhang T, Zhou G, Wang Q et al (2015) The rice transcription factor WRKY53 suppresses herbivore-induced defenses by acting as a negative feedback modulator of mitogen-activated protein kinase activity. Plant Physiol 169:2907–2921PubMedPubMedCentralCrossRefGoogle Scholar
  33. Huangfu J, Li J, Li R, Ye M, Kuai P, Zhang T, Lou Y (2016) The transcription factor OsWRKY45 negatively modulates the resistance of rice to the brown planthopper Nilaparvata lugens. Int J Mol Sci 17:697. https://doi.org/10.3390/ijms17060697 PubMedCentralCrossRefGoogle Scholar
  34. Ishiguro S, Nakamura K (1994) Characterization of a cDNA encoding a novel DNA-binding protein, SPF1, that recognizes SP8 sequences in the 50 upstream regions of genes coding for sporamin and β-amylase from sweet potato. Mol Gen Genet 244:563–571PubMedCrossRefGoogle Scholar
  35. Ishihama N, Yoshioka H (2012) Post-translational regulation of WRKY transcription factors in plant immunity. Curr Opin Plant Biol 15:431–437PubMedCrossRefGoogle Scholar
  36. Jiang Y, Duan Y, Yin J, Ye S, Zhu J, Zhang F, Lu W, Fan D, Luo K (2014) Genome-wide identification and characterization of the Populus WRKY transcription factor family and analysis of their expression in response to biotic and abiotic stresses. J Exp Bot 65:6629–6644PubMedPubMedCentralCrossRefGoogle Scholar
  37. Jiang W, Wu J, Zhang Y, Yin L, Lu J (2015) Isolation of a WRKY30 gene from Muscadinia rotundifolia (Michx) and validation of its function under biotic and abiotic stresses. Protoplasma 252:1361–1374PubMedCrossRefGoogle Scholar
  38. Jiang Y, Guo L, Liu R, Jiao B, Zhao X, Ling Z, Luo K (2016) Overexpression of poplar PtrWRKY89 in transgenic Arabidopsis leads to a reduction of disease resistance by regulating defense-related genes in salicylate- and jasmonate-dependent signaling. PLoS One 28(11):e0149137CrossRefGoogle Scholar
  39. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329PubMedCrossRefGoogle Scholar
  40. 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 18:3289–3302PubMedPubMedCentralCrossRefGoogle Scholar
  41. Kim KC, Fan B, Chen Z (2006) Pathogen-induced Arabidopsis WRKY7 is a transcriptional repressor and enhances plant susceptibility to Pseudomonas syringae. Plant Physiol 142:1180–1192PubMedPubMedCentralCrossRefGoogle Scholar
  42. Kim KC, Lai Z, Fan B, Chen Z (2008) Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense. Plant Cell 20:2357–2371PubMedPubMedCentralCrossRefGoogle Scholar
  43. Kim DY, Kwon SI, Choi C, Lee H, Ahn I, Park SR et al (2013) Expression analysis of rice VQ genes in response to biotic and abiotic stresses. Gene 529:208–214PubMedCrossRefGoogle Scholar
  44. Kim HS, Park YH, Nam H, Lee YM, Song K, Choi C, Ahn I, Park SR, Lee YH, Hwang DJ (2014) Overexpression of the Brassica rapa transcription factor WRKY12 results in reduced soft rot symptoms caused by Pectobacterium carotovorum in Arabidopsis and Chinese cabbage. Plant Biol (Stuttg) 16:973–981CrossRefGoogle Scholar
  45. 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(2):120–128PubMedCrossRefGoogle Scholar
  46. Koo SC, Moon BC, Kim JK, Kim CY, Sung SJ, Kim MC et al (2009) OsBWMK1 mediates SA-dependent defense responses by activating the transcription factor OsWRKY33. Biochem Biophys Res Commun 387:365–370PubMedCrossRefGoogle Scholar
  47. Koornneef A, Pieterse CMJ (2008) Cross talk in defense signaling. Plant Physiol 146:839–844PubMedPubMedCentralCrossRefGoogle Scholar
  48. Kumar K, Srivastava V, Purayannur S, Kaladhar VC, Cheruvu PJ, Verma PK (2016) WRKY domain-encoding genes of a crop legume chickpea (Cicer arietinum): comparative analysis with Medicago truncatula WRKY family and characterization of group-III gene(s). DNA Res 23:225–239PubMedPubMedCentralCrossRefGoogle Scholar
  49. Lai Z, Vinod K, Zheng Z, Fan B, Chen Z (2008) Roles of Arabidopsis WRKY3 and WRKY4 transcription factors in plant responses to pathogens. BMC Plant Biol 8:68PubMedPubMedCentralCrossRefGoogle Scholar
  50. Lai Z, Li Y, Wang F, Cheng Y, Fan B, Yu JQ et al (2011) Arabidopsis sigma factor binding proteins are activators of the WRKY33 transcription factor in plant defense. Plant Cell 23:3824–3841PubMedPubMedCentralCrossRefGoogle Scholar
  51. Lan A, Huang J, Zhao W, Peng Y, Chen Z, Kang D (2013) A salicylic acid-induced rice (Oryza sativa L.) transcription factor OsWRKY77 is involved in disease resistance of Arabidopsis thaliana. Plant Biol (Stuttg) 15:452–461CrossRefGoogle Scholar
  52. 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 16:319–331PubMedPubMedCentralCrossRefGoogle Scholar
  53. Li J, Brader G, Kariola T, Palva ET (2006) WRKY70 modulates the selection of signaling pathways in plant defense. Plant J 46:477–491PubMedCrossRefGoogle Scholar
  54. Li JB, Luan YS, Liu Z (2015) Overexpression of SpWRKY1 promotes resistance to Phytophthora nicotianae and tolerance to salt and drought stress in transgenic tobacco. Physiol Plant 155:248–266PubMedCrossRefGoogle Scholar
  55. Liu XQ, Bai XQ, Qian Q, Wang XJ, Chen MS, Chu CC (2005) OsWRKY03, a rice transcriptional activator that functions in defense signaling pathway upstream of OsNPR1. Cell Res 15:593–603PubMedCrossRefGoogle Scholar
  56. Mangelsen E, Kilian J, Berendzen KW, Kolukisaoglu UH, Harter K, Jansson C, Wanke D (2008) Phylogenetic and comparative gene expression analysis of barley (Hordeum vulgare) WRKY transcription factor family reveals putatively retained functions between monocots and dicots. BMC Genomics 9:194PubMedPubMedCentralCrossRefGoogle Scholar
  57. 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 48:833–842PubMedCrossRefGoogle Scholar
  58. Mao G, Meng X, Liu Y, Zheng Z, Chen Z, Zhang S (2011) Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23:1639–1653PubMedPubMedCentralCrossRefGoogle Scholar
  59. Marchive C, Léon C, Kappel C, Coutos-Thévenot P, Corio-Costet MF, Delrot S, Lauvergeat V (2013) Over-expression of VvWRKY1 in grapevines induces expression of jasmonic acid pathway-related genes and confers higher tolerance to the downy mildew. PLoS One 8:e54185PubMedPubMedCentralCrossRefGoogle Scholar
  60. Murray SL, Ingle RA, Petersen LN, Denby KJ (2007) Basal resistance against Pseudomonas syringae in Arabidopsis involves WRKY53 and a protein with homology to a nematode resistance protein. Mol Plant-Microbe Interact 20:1431–1438PubMedCrossRefGoogle Scholar
  61. Oh SK, Baek KH, Park JM, Yi SY, Yu SH, Kamoun S, Choi D (2008) Capsicum annuum WRKY protein CaWRKY1 is a negative regulator of pathogen defense. New Phytol 177:977–989PubMedCrossRefGoogle Scholar
  62. Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648–1655PubMedPubMedCentralCrossRefGoogle Scholar
  63. Pandey SP, Roccaroz M, Schön M, Logemann E, Somssich IE (2010) Transcriptional reprogramming regulated by WRKY18 and WRKY40 facilitates powdery mildew infection of Arabidopsis. Plant J 64:912–923PubMedCrossRefGoogle Scholar
  64. Park CY, Lee JH, Yoo JH, Moon BC, Choi MS, Kang YH (2005) WRKY Group IId transcription factors interact with calmodulin. FEBS Lett 579:1545–1550PubMedCrossRefGoogle Scholar
  65. Phukan UJ, Jeena GS, Shukla RK (2016) WRKY transcription factors: molecular regulation and stress responses in plants. Front Plant Sci 7:760. https://doi.org/10.3389/fpls.2016.00760 PubMedPubMedCentralCrossRefGoogle Scholar
  66. 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 20:492–499PubMedCrossRefGoogle Scholar
  67. Qiu JL, Fiil BK, Petersen K, Nielsen HB, Botanga CJ, Thorgrimsen S et al (2008) Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J 27:2214–2221PubMedPubMedCentralCrossRefGoogle Scholar
  68. Ramamoorthy R, Jiang SY, Kumar N, Venkatesh PN, Ramachandran S (2008) A comprehensive transcriptional profiling of the WRKY gene family in rice under various abiotic and phytohormone treatments. Plant Cell Physiol 49:865–879PubMedCrossRefGoogle Scholar
  69. Robatzek S, Somssich IE (2001) A new member of the Arabidopsis WRKY transcription factor family, AtWRKY6, is associated with both senescence- and defense-related processes. Plant J 28:123–133PubMedCrossRefGoogle Scholar
  70. Roberts MR (2003) 14-3-3 proteins find new partners in plant cell signalling. Trends Plant Sci 8:218–223PubMedCrossRefGoogle Scholar
  71. Rushton PJ, Torres JT, Parniske M, Wernert P, Hahlbrock K, Somssich IE (1996) Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J 15:5690e700Google Scholar
  72. Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258PubMedCrossRefGoogle Scholar
  73. Ryu H-S, Han M, Lee S-K, Cho JI, Ryoo N, Heu S, Lee YH, Bhoo SH, Wang GL, Hahn TR, Jeon JS (2006) A comprehensive expressionanalysis of the WRKY gene superfamily in rice plants during defense response. Plant Cell Rep 25:836–847PubMedCrossRefGoogle Scholar
  74. Schmutz J, Cannon SB et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183PubMedCrossRefGoogle Scholar
  75. Shan W, Chen JY, Kuang JF, Lu WJ (2016) Banana fruit NAC transcription factor MaNAC5 cooperates with MaWRKYs to enhance the expression of pathogenesis-related genes against Colletotrichum musae. Mol Plant Pathol 17:330–338PubMedCrossRefGoogle Scholar
  76. Shang Y, Yan L, Liu ZQ, Cao Z, Mei C, Xin Q et al (2010) The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell 22:1909–1935PubMedPubMedCentralCrossRefGoogle Scholar
  77. Shen YH, Godlewski J, Bronisz A, Zhu J, Comb MJ, Avruch J et al (2003) Significance of 14–3–3 self-dimerization for phosphorylation-dependent target binding. Mol Biol Cell 14:4721–4733PubMedPubMedCentralCrossRefGoogle Scholar
  78. Shen QH, Saijo Y, Mauch S, Biskup C, Bieri S, Keller B, Seki H, Ulker B, Somssich IE, Schulze-Lefert P (2007) Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315:1098–1103PubMedCrossRefGoogle Scholar
  79. Shi W, Liu D, Hao L, Wu C, Guo X, Li H (2014) GhWRKY39, a member of the WRKY transcription factor family in cotton, has a positive role in disease resistance and salt stress tolerance. Plant Cell Tissue Organ Cult 118:17–32CrossRefGoogle Scholar
  80. Shimono M, Sugano S, Nakayama A, Jiang CJ, Ono K, Toki S, Takatsuji H (2007) Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell 19:2064–2076PubMedPubMedCentralCrossRefGoogle Scholar
  81. Shimono M, Koga H, Akagi A, Hayashi N, Goto S, Sawada M, Kurihara T, Matsushita A, Sugano S, Jiang CJ, Kaku H, Inoue H, Takatsuji H (2012) Rice WRKY45 plays important roles in fungal and bacterial disease resistance. Mol Plant Pathol 13:83–94PubMedCrossRefGoogle Scholar
  82. Skibbe M, Qu N, Galis I, Baldwin IT (2008) Induced plant defenses in the natural environment: Nicotiana attenuate WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell 20:1984–2000PubMedPubMedCentralCrossRefGoogle Scholar
  83. Song Y, Jing S, Yu D (2010) Overexpression of the stress-induced OsWRKY08 improves osmotic stress tolerance in Arabidopsis. Chin Sci Bull 54:4671–4678Google Scholar
  84. Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270PubMedCrossRefGoogle Scholar
  85. Tsuda K, Mine A, Bethke G, Igarashi D, Botanga CJ, Tsuda Y, Glazebrook J, Sato M, Katagiri F (2013) Dual regulation of gene expression mediated by extended MAPK activation and salicylic acid contributes to robust innate immunity in Arabidopsis thaliana. PLoS Genet 9:e1004015PubMedPubMedCentralCrossRefGoogle Scholar
  86. Turck F, Zhou A, Somssich IE (2004) Stimulus-dependent, promoter-specific binding of transcription factor WRKY1 to its native promoter and the defense-related gene PcPR1-1 in parsley. Plant Cell 16:2573–2585PubMedPubMedCentralCrossRefGoogle Scholar
  87. Ulker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 7:491–498PubMedCrossRefGoogle Scholar
  88. 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:e123PubMedPubMedCentralCrossRefGoogle Scholar
  89. Wang H, Hao J, Chen X, Hao Z, Wang X, Lou Y, Peng Y, Guo Z (2007) Overexpression of rice WRKY89 enhances ultraviolet B tolerance and disease resistance in rice plants. Plant Mol Biol 65:799–815PubMedCrossRefGoogle Scholar
  90. Wang JN, Kuang JF, Shan W, Chen J, Xie H, Lu WJ et al (2012) Expression profiles of a banana fruit linker histone H1gene MaHIS1 and its interaction with a WRKY transcription factor. Plant Cell Rep 31:1485–1494PubMedCrossRefGoogle Scholar
  91. Wang Z, Fang H, Chen Y, Chen K, Li G, Gu S, Tan X (2014) Over-expression of BnWRKY33 in oilseed rape enhances resistance to Sclerotinia sclerotiorum. Mol Plant Pathol 15:677–689PubMedCrossRefGoogle Scholar
  92. Wei T, Ou B, Li J, Zhao Y, Guo D, Zhu Y, Chen Z, Gu H, Li C, Qin G, Qu LJ (2013) Transcriptional profiling of rice early response to Magnaporthe oryzae identified OsWRKYs as important regulators in rice blast resistance. PLoS One 8:e59720PubMedPubMedCentralCrossRefGoogle Scholar
  93. Wei W, Hu Y, Han YT, Zhang K, Zhao FL, Feng JY (2016) The WRKY transcription factors in the diploid woodland strawberry Fragaria vesca: identification and expression analysis under biotic and abiotic stresses. Plant Physiol Biochem 105:129–144PubMedCrossRefGoogle Scholar
  94. Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, Brindle ID, De Luca V, Després C (2012) The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep 1:639–647PubMedCrossRefGoogle Scholar
  95. 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 1:459–470PubMedCrossRefGoogle Scholar
  96. 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 18:1310–1326PubMedPubMedCentralCrossRefGoogle Scholar
  97. Yamasaki K, Kigawa T, Inoue M, Tateno M, Yamasaki T, Yabuki T, Aoki M, Seki E, Matsuda T, Tomo Y et al (2005) Solution structure of an Arabidopsis WRKY DNA binding domain. Plant Cell 17:944–956PubMedPubMedCentralCrossRefGoogle Scholar
  98. Yamasaki K, Kigawa T, Watanabe S, Inoue M, Yamasaki T, Seki M, Shinozaki K, Yokoyama S (2012) Structural basis for sequence-specificDNA recognition by an Arabidopsis WRKY transcription factor. J Biol Chem 287:7683–7691PubMedPubMedCentralCrossRefGoogle Scholar
  99. Yamasaki K, Kigawa T, Seki M, Shinozaki K, Yokoyama S (2013) DNA-binding domains of plant-specific transcription factors: structure, function, and evolution. Trends Plant Sci 18:267–276PubMedCrossRefGoogle Scholar
  100. Yan L, Liu Z-Q, Xu Y-H, Lu K, Wang X-F, Zhang D-P (2013) Auto and cross-repression of three Arabidopsis WRKY transcription factors WRKY18, WRKY40, and WRKY60 negatively involved in ABA signaling. J Plant Growth Regul 32:399–416CrossRefGoogle Scholar
  101. Yan Y, Jia H, Wang F, Wang C, Liu S, Guo X (2015) Overexpression of GhWRKY27a reduces tolerance to drought stress and resistance to Rhizoctonia solani infection in transgenic Nicotiana benthamiana. Front Physiol 24(6):265Google Scholar
  102. Yang P, Chen C, Wang Z, Fan B, Chen Z (1999) A pathogen and salicylic acid-induced WRKY DNA-binding activity recognizes the elicitor response element of the tobacco class I chitinase gene promoter. Plant J 18:141–149CrossRefGoogle Scholar
  103. Ye S, Jiang Y, Duan Y, Karim A, Fan D, Yang L, Zhao X, Yin J, Luo K (2014) Constitutive expression of the poplar WRKY transcription factor PtoWRKY60 enhances resistance to Dothiorella gregaria Sacc. in transgenic plants. Tree Physiol 34(10):1118–1129PubMedCrossRefGoogle Scholar
  104. Yu FF, Huaxia YF, Lu WJ, Wu C, Guo XQ (2012) GhWRKY15, a member of the WRKY transcription factor family identified from cotton (Gossypium hirsutum L.), is involved in disease resistance and plant development. BMC Plant Biol 12:144PubMedPubMedCentralCrossRefGoogle Scholar
  105. Zheng Z, Qamar SA, Chen Z, Mengiste T (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J 48:592–605PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Preeti Singh
    • 1
  • Shashi Shekhar
    • 1
  • Anjana Rustagi
    • 2
  • Vinay Sharma
    • 3
  • Deepak Kumar
    • 4
  1. 1.School of Life SciencesJawaharlal Nehru UniversityNew DelhiIndia
  2. 2.Department of BotanyGargi CollegeNew DelhiIndia
  3. 3.Department of Bioscience and BiotechnologyBanasthali UniversityBanasthaliIndia
  4. 4.Department of BotanyCentral University of JammuJammuIndia

Personalised recommendations