WRKY: Its structure, evolutionary relationship, DNA-binding selectivity, role in stress tolerance and development of plants

Molecular Biology Reports

Volumn 38, Issue 6, 2011, Pages 3883-3896

  Agarwal, Parinita ^a   Reddy, M P ^a   Chikara, Jitendra ^a  

^a CSIR CENTRAL SALT AND MARINE CHEMICALS RESEARCH INSTITUTE   (India)

Author keywords

Abiotic; Biotic; DNA binding; Senescence; Transcription factor; WRKY

Indexed keywords

AMINO ACID; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR WRKY; UNCLASSIFIED DRUG;

ABIOTIC STRESS; ARTICLE; BIOTIC STRESS; CONTROLLED STUDY; DNA BINDING; DNA FLANKING REGION; EUKARYOTE; GENE SEQUENCE; GENE STRUCTURE; GENETIC CONSERVATION; HORMONAL REGULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT DEVELOPMENT; PLANT GENE; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SENESCENCE; SIGNAL TRANSDUCTION; WRKY GENE;

DNA, PLANT; EVOLUTION, MOLECULAR; PLANT PROTEINS; PLANTS; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS;

FILICOPHYTA; MAGNOLIOPHYTA; PROTISTA;

EID: 80052509226     PISSN: 03014851     EISSN: 15734978     Source Type: Journal    
DOI: 10.1007/s11033-010-0504-5     Document Type: Article

References (127)

1. Eulgem T (2005) Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci 10:71-78. (Pubitemid 40234482)
2. Köhler C, Hennig L, Spillane C, Pien S, Gruissem W, Grossniklaus U (2003) The Polycomb group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1. Genes Dev 17:1540-1553. (Pubitemid 36734710)
3. Iida K, Seki M, Sakurai T, Satou M, Akiyama K, Toyoda T, Konagaya A, Shinozaki K (2005) RARTF: database and tools for complete sets of Arabidopsis transcription factors. DNA Res 12:247-256.
4. Xiong Y, Liu T, Tian C, Sun S, Li J, Chen M (2005) Transcription factors in rice: a genome-wide comparative analysis between monocots and eudicots. Plant Mol Biol 59:191-203. (Pubitemid 41429429)
5. Mewes HW et al (1997) Overview of the yeast genome. Nature 387:7-65.
6. Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10: 366-371. (Pubitemid 47126955)
7. Ross CA, Liu Y, Shen QJ (2007) The WRKY gene family in rice (Oryza sativa). J Int Plant Biol 49:827-842. (Pubitemid 46993133)
8. Schmutz J, Cannon SB et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178-183.
9. Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648-1655.
10. Johnson CS, Kolevski B, Smyth DR (2002) TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. Plant Cell 14:1359-1375. (Pubitemid 34780437)
11. Luo M, Dennis ES, Berger F, Peacock WJ, Chaudhury A (2005) MINISEED3 (MINI3), a WRKY family gene, and HAIKU2 (IKU2), a leucine-rich repeat (LRR) KINASE gene, are regulators of seed size in Arabidopsis. Proc Natl Acad Sci USA 102:17531-17536. (Pubitemid 41740900)
12. Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247-258.
13. Zhang Y, Wang L (2005) The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evol Biol 5:1-12.
14. 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 9:194.
15. Xie Z, Zhang ZL, Zou X, Huang J, Ruas P, Thompson D, Shen QJ (2005) Annotations and functional analyses of the rice WRKY gene superfamily reveal positive and negative regulators of abscisic acid signaling in aleurone cells. Plant Physiol 137:176-189. (Pubitemid 43034300)
16. Yang B, Jiang Y, Rahman MH, Deyholos MK, Kav NN (2009) Identification and expression analysis of WRKY transcription factor genes in canola (Brassica napus L.) in response to fungal pathogens and hormone treatments. BMC Plant Biol 9:68.
17. 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 65:2428-2436. (Pubitemid 33615705)
18. Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199-206. (Pubitemid 30300843)
19. Yamasaki K, Kigawa T, Inoue M, Tateno M, Yamasaki T, Yabuki T, Aoki M, Seki E, Matsuda T, Tomo Y, Hayami N, Terada T, Shirouzu M, Tanaka A, Seki M, Shinozaki K (2005) Yokoyama S. Solution structure of an Arabidopsis WRKY DNA binding domain. Plant Cell 17:944-956. (Pubitemid 43138232)
20. 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 35:1145-1154. (Pubitemid 46522968)
21. Cormack RS, Eulgem T, Rushton PJ, Kochner P, Hahlbrock K, Somssich IE (2002) Leucine zipper-containing WRKY proteins widen the spectrum of immediate early elicitor-induced WRKY transcription factors in parsley. Biochim Biophys Acta 1576: 92-100. (Pubitemid 34597088)
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 USA 100:8024-8029. (Pubitemid 36760088)
23. Zou X, Seemann JR, Neuman D, Shen QJ (2004) A WRKY gene from creosote bush encodes an activator of the abscisic acid signaling pathway. J Biol Chem 279:55770-55779. (Pubitemid 40066584)
24. Riechmann JL et al (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105-2110. (Pubitemid 32001583)
25. Pan YJ, Cho CC, Kao YY, Sun CH (2009) A novel WRKY-like protein involved in transcriptional activation of cyst wall protein genes in Giardia lamblia. J Biol Chem 284:17975-17988.
26. Glöckner G et al (2002) Sequence and analysis of chromosome 2 of Dictyostelium discoideum. Nature 418:79-85. (Pubitemid 34742574)
27. Liu JJ, Ekramoddoullah AK (2009) Identification and characterization of the WRKY transcription factor family in Pinus monticola. Genome 52:77-88.
28. Wu KL, Guo ZJ, Wang HH, Li J (2005) The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Res 12:9-26. (Pubitemid 40628503)
29. Babu MM, Iyer LM, Balaji S, Aravind L (2006) The natural history of the WRKY-GCM1 zinc fingers and the relationship between transcription factors and transposons. Nucleic Acids Res 34:6505-6520. (Pubitemid 46017946)
30. Ulker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 7:491-498. (Pubitemid 39175145)
31. Ciolkowski I, Wanke D, Birkenbihl RP, Somssich IE (2008) Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function. Plant Mol Biol 68:81-92.
32. 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 b-amylase from sweet potato. Mol Gen Genet 244:563-571.
33. de Pater S, Greco V, Pham K, Memelink J, Kijne J (1996) Characterization of a zinc-dependent transcriptional activator from Arabidopsis. Nucleic Acids Res 24:4624-4631. (Pubitemid 26413337)
34. Eulgem T, Rushton PJ, Schmelzer E, Hahlbrock K, Somssich IE (1999) Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors. EMBO J 18:4689-4699. (Pubitemid 29415523)
35. Mackay JP, Crossley M (1998) Zinc fingers are sticking together. Trends Biochem Sci 23:1-4. (Pubitemid 28093984)
36. Dong J, Chen C, Chen Z (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol 51:21-37. (Pubitemid 36189133)
37. Kalde M, Barth M, Somssich IE, Lippok B (2003) Members of the Arabidopsis WRKY group III transcription factors are part of different plant defence signalling pathways. Mol Plant- Microbe Interact 16:295-305. (Pubitemid 36386449)
38. Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263-1274. (Pubitemid 44786606)
39. Urano K, Kurihara Y, Seki M, Shinozaki K (2010) 'Omics' analyses of regulatory networks in plant abiotic stress responses. Curr Opin Plant Bio 13:132-138.
40. Jiang Y, Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes. BMC Plant Biol 6:25.
41. Xie Z, Zhang Z-L, Zou X, Yang G, Komatsu S, Shen QJ (2006) Interactions of two abscisic-acid induced WRKY genes in repressing gibberellin signaling in aleurone cells. Plant J 46:231-242. (Pubitemid 43773563)
42. Qiu Y, Jing S, Fu J, Li L, Yu D (2004) Cloning and analysis of expression profile of 13 WRKY genes in rice. Chin Sci Bull 49:2159-2168. (Pubitemid 44561128)
43. 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 49:865-879.
44. Zhou QY, Tian AG, Zou HF, Xie ZM, Lei G, Huang J, Wang CM, Wang HW, Zhang JS, Chen SY (2008) Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnol J 6:486-503. (Pubitemid 351670275)
45. Wei W, Zhang Y, Han L, Guan Z, Chai T (2008) A novel WRKY transcriptional factor from Thlaspi caerulescens negatively regulates the osmotic stress tolerance of transgenic tobacco. Plant Cell Rep 27:795-803.
46. Jiang Y, Deyholos MK (2009) Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol Biol 69:91-105.
47. Ren X, Chen Z, Liu Y, Zhang H, Zhang M, Liu Q, Hong X, Zhu J, Gong Z (2010) ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. Plant J 63:417-429.
48. Qiu Y, Yu D (2009) Over-expression of the stress-induced OsWRKY45 enhances disease resistance and drought tolerance in Arabidopsis. Environ and Exp Bot 65:35-47.
49. Wu X, Shiroto Y, Kishitani S, Ito Y, Toriyama K (2009) Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Rep 28:21-30.
50. 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 65:799-815. (Pubitemid 350159807)
51. Zou XL, Shen QJ, Neuman D (2007) An ABA inducible WRKY gene integrates responses of creosote bush Larrea tridentata to elevated CO2 and abiotic stresses. Plant Sci 172:997-1004. (Pubitemid 46517736)
52. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323-329. (Pubitemid 44764102)
53. Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185-209. (Pubitemid 39308511)
54. 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 34:217-228. (Pubitemid 36536683)
55. Katagiri F (2004) A global view of defense gene expression regulation-a highly interconnected signaling network. Curr Opin Plant Biol 7:506-511. (Pubitemid 39175147)
56. Kunkel BN, Brooks DM (2002) Cross talk between signalling pathways in pathogen defence. Curr Opin Plant Biol 5:325-331. (Pubitemid 34695970)
57. 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 13:1527-1539. (Pubitemid 32675718)
58. 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 7:2.
59. Chen C, Chen Z (2002) Potentiation of developmentally regulated plant defense response by AtWRKY18, a pathogeninduced Arabidopsis transcription factor. Plant Physiol 129: 706-716. (Pubitemid 34689157)
60. 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 18:1310-1326. (Pubitemid 43956133)
61. 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 315:1098-1103. (Pubitemid 46328015)
62. Lai Z, Vinod KM, Zheng Z, Fan B, Chen Z (2008) Roles of Arabidopsis WRKY3 and WRKY4 transcription factors in plant responses to pathogens. BMC Plant Biol 8:68.
63. Wang L, Chen S, Kong W, Li S, Archbold DD (2006) Salicylic acid pretreatment alleviates chilling injury and affects the antioxidant system and heat shock proteins of peaches during cold storage. Postharvest Biol Technol 41:244-251. (Pubitemid 44764832)
64. Li J, Brader G, Palva ET (2004) The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16: 319-331. (Pubitemid 38192692)
65. Li J, Brader G, Kariola T, Tapio Palva E (2006) WRKY70 modulates the selection of signaling pathways in plant defense. Plant J 46:477-491.
66. 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(11): 1431-1438. (Pubitemid 47612505)
67. Kim KC, Fan B, Chen Z (2006) Pathogen-induced Arabidopsis WRKY7 is a transcriptional repressor and enhances plant susceptibility to Pseudomonas syringae. Plant Physiol 42: 1180-1192. (Pubitemid 44764641)
68. 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 20:2357-2371. (Pubitemid 352844604)
69. Park CY, Lee JH, Yoo JH, Moon BC, Choi MS, Kang YH, Lee SM, Kim HS, Kang KY, Chung WS et al (2005) WRKY group IId transcription factors interact with calmodulin. FEBS Lett 579:1545-1550. (Pubitemid 40289210)
70. Ryu H-S et al (2006) A comprehensive expression analysis of the WRKY gene superfamily in rice plants during defense response. Plant Cell Rep 25:836-847. (Pubitemid 44078578)
71. 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 15:593-603. (Pubitemid 41679292)
72. 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 jasmonatedependent signaling. Mol Plant-Microbe Interact 20:492-499. (Pubitemid 46641427)
73. Shimono M, Sugano S, Nakayama A, Jiang CJ, Ono K, Toki S (2007) Takatsuji H. Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell 19: 2064-2076. (Pubitemid 47218859)
74. Hara K, Yagi M, Kusano T, Sano H (2000) Rapid systemic accumulation of transcripts encoding a tobacco WRKY transcription factor upon wounding. Mol Gen Genet 263:30-37.
75. Yoda H, Ogawa M, Yamaguchi Y, Koizumi N, Kusano T, Sanop 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 Genom 267:154-161. (Pubitemid 34437990)
76. Skibbe M, Qu N, Galis I, Baldwin IT (2008) Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell 20(7):1984-2000. (Pubitemid 352844545)
77. 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 15:5690-5700. (Pubitemid 26385628)
78. 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 9 ananassa) Fa WRKY1 and Arabidopsis At WRKY75 proteins in resistance. J Exp Bot 60:3043-3065.
79. Levée V, Major I, Levasseur C, Tremblay L, Mackay J, Séguin A (2009) Expression profiling and functional analysis of Populus WRKY23 reveals a regulatory role in defense. New Phytol 184:48-70.
80. Marchive C, Mzid R, Deluc L et al (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 58:1999-2010. (Pubitemid 47216561)
81. Mzid R, Marchive C, Blancard D, Deluc L, Barrieu F, Corio- Costet MF, Drira N, Hamdi S, Lauvergeat V (2007) Overexpression of VvWRKY2 in tobacco enhances broad resistance to necrotrophic fungal pathogens. Physiol Plant 131(3):434-447. (Pubitemid 47508555)
82. Guillaumie S, Mzid R, Méchin V, Léon C, Hichri I, Destrac- Irvine A, Trossat-Magnin C, Delrot S, Lauvergeat V (2010) The grapevine transcription factor WRKY2 influences the lignin pathway and xylem development in tobacco. Plant Mol Biol 72:215-234.
83. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu W-L, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977-983. (Pubitemid 34193435)
84. Liu Y, Schiff M, Dinesh-Kumar SP (2004) Involvement of MEK1 MAPKK, NTF6 MAPK, WRKY/MYB transcription factors, COI1 and CTR1 in N-mediated resistance to tobacco mosaic virus. Plant J 38:800-809. (Pubitemid 38693459)
85. Du L, Chen Z (2000) Identification of genes encoding receptorlike protein kinases as possible targets of pathogen- and salicylic acid-induced WRKY DNA-binding proteins in Arabidopsis. Plant J 24:837-847. (Pubitemid 32100481)
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 16:2573-2585. (Pubitemid 41071347)
87. Yang P, Chen C, Wang Z, Fan B, Chen Z (1999) A pathogenand salicylic acid-induced WRKY DNA-binding activity recognizes the elicitor response element of the tobacco class I chitinase gene promoter. Plant J 18:141-149.
88. Kim CY, Zhang S (2004) Activation of a mitogen-activated protein kinase cascade induces WRKY family of transcription factors and defence genes in tobacco. Plant J 38:142-151. (Pubitemid 38448451)
89. Menke FLH, Kang H-G, Chen Z, Park JM, 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 18:1027-1034. (Pubitemid 41356406)
90. 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 24:2579-2589. (Pubitemid 41076314)
91. Zheng Z, Qamar SA, Chen Z, Mengiste T (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J 48:592-605. (Pubitemid 44673260)
92. Hofmann MG, Sinha AK, Proels RK, Roitsch T (2008) Cloning and characterization of a novel LpWRKY1 transcription factor in tomato. Plant Physiol Biochem 46:533-540.
93. Koller D (1969) The physiology of dormancy and survival of plants in desert environments. Symp Soc Exp Biol 23:449-469.
94. Raven PH, Evert RF, Eichhorn SE (1992) Biology of plants. New York, Worth.
95. Merquiol M, Pnueli L, Cohen M, Simovitch M, Goloubinoff P, Kaplan A, Mittler R (2002) Seasonal and diurnal variations in gene expression in the desert legume Retama raetam. Plant Cell Environ 25:1627-1638. (Pubitemid 35456647)
96. Pnueli L, Hallak-Herr E, Rozenberg M, Cohen M, Goloubinoff P, Kaplan A, Mittler R (2002) Molecular and biochemical mechanisms associated with dormancy and drought tolerance in the desert legume Retama raetam. Plant J 31:319-330. (Pubitemid 34915403)
97. Rushton PJ, Macdonald H, Huttly AK, Lazarus CM, Hooley R (1995) Members of a new family of DNA-binding proteins bind to a conserved cis-element in the promoters of alpha-Amy2 genes. Plant Mol Biol 29:691-702. (Pubitemid 3012894)
98. Zou X, Neuman D, Shen QJ (2008) Interactions of two transcriptional repressors and two transcriptional activators in modulating gibberellin signaling in aleurone cells. Plant Physiol 148:176-186. (Pubitemid 352847594)
99. Jiang W, Yu D (2009) Arabidopsis WRKY2 transcription factor mediates seed germination and post-germination arrest of development by abscisic acid. BMC Plant Biol 22:994-996.
100. Dilkes BP, Spielman M, Weizbauer R, Watson B, Burkart-Waco D, Scott RJ, Comai L (2008) The maternally expressed WRKY transcription factor TTG2 controls lethality in interploidy crosses of Arabidopsis. PLoS Biol 6:2707-2720.
101. Lagace M, Matton DP (2004) Characterization of a WRKY transcription factor expressed in late torpedo-stage embryos of Solanum chacoense. Planta 219:185-189. (Pubitemid 38642149)
102. Robatzek S, Somssich IE (2002) Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes Dev 16:1139-1149. (Pubitemid 34507202)
103. Guo Y, Cai Z, Gan S (2004) Transcriptome of Arabidopsis leaf senescence. Plant Cell Environ 27:521-549. (Pubitemid 38600727)
104. Lin JF, Wu SH (2004) Molecular events in senescing Arabidopsis leaves. Plant J 39:612-628.
105. Hinderhofer K, Zentgraf U (2001) Identification of a transcription factor specifically expressed at the onset of leaf senescence. Planta 213:469-473. (Pubitemid 32682633)
106. Miao Y, Laun T, Smykowski A, Zentgraf U (2007) ArabidopsisMEKK1 can take a short cut: it can directly interact with senescence-related WRKY53 transcription factor on the protein level and can bind to its promoter. Plant Mol Biol 65:63-76.
107. Miao Y, Laun T, Zimmermann P, Zentgraf U (2004) Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol Biol 55:853-867.
108. Ulker B, Shahid Mukhtar M, Somssich IE (2007) The WRKY70 transcription factor of Arabidopsis influences both the plant senescence and defense signaling pathways. Planta 226:125-137. (Pubitemid 46763832)
109. Zhang Z-L, Xie Z, Zou X, Casaretto J, T-hD Ho, Shen QJ (2004) A rice WRKY gene encodes a transcriptional repressor of the gibberellin signaling pathway in aleurone cells. Plant Physiol 134:1500-1513. (Pubitemid 38527360)
110. Sun TP, Gubler F (2004) Molecular mechanism of gibberellins signaling in plants. Annu Rev Plant Physiol Plant Mol Biol 55:197-223. (Pubitemid 38940931)
111. Zhang ZL, Shin M, Zou X, Huang J, Ho TH, Shen QJ (2009) A negative regulator encoded by a rice WRKY gene represses both abscisic acid and gibberellins signaling in aleurone cells. Plant Mol Biol 70:139-151.
112. Traw MB, Bergelson J (2003) Interactive effects of jasmonic acid, salicylic acid, and gibberellin on induction of trichomes in Arabidopsis. Plant Physiol 133:1367-1375. (Pubitemid 37458034)
113. Xie Z, Zhang ZL, Hanzlik S, Cook E, Shen QJ (2007) Salicylic acid inhibits gibberellin-induced alpha-amylase expression and seed germination via a pathway involving an abscisic-acidinducible WRKY gene. Plant Mol Biol 64:293-303. (Pubitemid 46663196)
114. Zhang J, Peng Y, Guo Z (2008) Constitutive expression of pathogen-inducible OsWRKY31 enhances disease resistance and affects root growth and auxin response in transgenic rice plants. Cell Res 18:508-521. (Pubitemid 351498858)
115. Li S, Fu Q, Huang W, Yu D (2009) Functional analysis of an Arabidopsis transcription factor WRKY25 in heat stress. Plant Cell Rep 28:683-693.
116. Higashi K, Ishiga Y, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y (2008) Modulation of defense signal transduction by flagellininduced WRKY41 transcription factor in Arabidopsis thaliana. Mol Genet Genomics 279(3):303-312.
117. 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(4): 977-989. (Pubitemid 351225118)
118. Oh SK, Yi SY, Yu SH, Moon JS, Park JM, Choi D (2006) CaWRKY2, a chili pepper transcription factor, is rapidly induced by incompatible plant pathogens. Mol Cells 22:58-64. (Pubitemid 44323046)
119. Mare C, Mazzucotelli E, Crosatti C, Francia E, Stanca AM (2004) Cattivelli L. Hv-WRKY38: a new transcription factor involved in cold- and drought-response in barley. Plant Mol Biol 55:399-416. (Pubitemid 40660266)
120. Liu X, Bai X, Wang X, Chu C (2007) OsWRKY71, a rice transcription factor, is involved in rice defense response. J Plant Physiol 164:969-979. (Pubitemid 47126082)
121. Ze-Jian G, Yun-Chao K, Xu-Jun C, De-Bao L, Dao-Wen W (2004) Characterization of a rice WRKY gene whose expression is induced upon pathogen attack and mechanical wounding. Acta Botanica Sinica 46:955-964.
122. 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 co-regulated with class I endochitinase expression. Mol Plant-Microbe Interact 13:1092-1101.
123. Sun C, Palmqvist S, Olsson H, Boren M, Ahlandsberg S, Jansson C (2003) A novel WRKY transcription factor, SUSIBA2, participates in sugar signaling in barley by binding to the sugarresponsive elements of the iso1 promoter. Plant Cell 15: 2076-2092. (Pubitemid 37144062)
124. Chen C, Chen Z (2000) Isolation and characterization of two pathogen- and salicylic acid-induced genes encoding WRKY DNA-binding proteins from tobacco. Plant Mol Biol 42: 387-396. (Pubitemid 30213416)
125. Lai Z, Vinod KM, Zheng Z, Fan B, Chen Z (2008) Roles of Arabidopsis WRKY3 and WRKY4 transcription factors in plant responses to pathogens. BMC Plant Biol 8:68.
126. 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 18:3289-3302. (Pubitemid 46013291)
127. Xu YH, Wang JW, Wang S, Wang JY, Chen XY (2004) Characterization of GaWRKY1, a cotton transcription factor that regulates the sesquiterpene synthase gene (+)-delta-cadinene synthase-A. Plant Physiol 135:507-515. (Pubitemid 38653695)