REVIEW PAPER
The role of WRKY transcription factors in plants
Publication date: 2015-10-06
BioTechnologia 2014;95(3):215-233
KEYWORDS
ABSTRACT
The WRKY proteins are one of the largest families of transcriptional regulators in plants. Their biosynthesis is
induced during certain stages of plant development and upon pathogen infection. A single WRKY transcription
factor may be involved in the regulation of several apparently disparate processes. Their hallmark is strong
conservation of the DNA binding domain which contains an invariant WRKYGQK amino acid sequence and a zinc
binding motif. However, the overall sequences of individual representatives are highly divergent. Little is known
about the 3D-structure of the WRKY proteins. Up to date there have only been results of structural strudies of
DNA binding domain available. In this review, the biological function as well the structural studies of the WRKY
proteins have been recapitulated.
induced during certain stages of plant development and upon pathogen infection. A single WRKY transcription
factor may be involved in the regulation of several apparently disparate processes. Their hallmark is strong
conservation of the DNA binding domain which contains an invariant WRKYGQK amino acid sequence and a zinc
binding motif. However, the overall sequences of individual representatives are highly divergent. Little is known
about the 3D-structure of the WRKY proteins. Up to date there have only been results of structural strudies of
DNA binding domain available. In this review, the biological function as well the structural studies of the WRKY
proteins have been recapitulated.
REFERENCES (103)
1.
Alexandrova K.S., Conger B.V. (2002) Isolation of two somatic embryogenesis-related genes from orchardgrass (Dactylis glomerata). Plant Sci. 162: 301-307.
2.
Andreasson E., Jenkins T., Brodersen P., Thorgrimsen S., Petersen N.H.T., Zhu S., Qiu J.-L., Micheelsen P., Rocher A., Petersen M., Newman M.-A., Nielsen H.B., Hirt H., Somssich I., Mattsson O., Mundy J. (2005) The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO J. 24(14): 2579-2589.
3.
Asai T., Tena G., Plotnikova J., Willmann M.R., Chiu W.-L., Gomez- Gomez L., Boller T., Ausubel F.M., Sheen J. (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415(6875): 977-983.
4.
Babitha K.C., Ramu S.V., Pruthvi V., Mahesh P., Nataraja K.N., Udayakumar M. (2013) Co-expression of AtbHLH17 and AtWRKY28 confers resistance to abiotic stress in Arabidopsis. Transgenic Res. 22(2): 327-341.
5.
Bera S.K., Ajay B.C., Singh A.L. (2013) WRKY and Na+/H+ antiporter genes conferring tolerance to salinity in interspecific derivatives of peanut (Arachis hypogaea L.). Austral. J. Crop Sci. 7(8): 1173-1180.
6.
Besseau S., Li J., Palva E.T. (2012) WRKY54 and WRKY70 cooperate as negative regulators of leaf senescence in Arabidopsis thaliana. J. Exp. Bot. 63(7): 2667-2679.
7.
Bhattarai K.K., Atamian H.S., Kaloshian I., Eulgem T. (2010) WRKY72-type transcription factors contribute to basal immunity resistance mediated by the tomato R gene Mi-1. Plant J. 63(2): 229-240.
8.
Birkenbihl R.P., Diezel C., Somssich I.E. (2012) Arabidopsis WRKY33 is a key transcriptional regulator of hormonal and metabolic responses toward Botrytis cinerea infection. Plant Physiol. 159(1): 266-285.
9.
Birnbaum K., Shasha D.E., Wang J.Y., Jung J.W., Lambert G.M., Galbraith D.W., Benfey P.N. (2003) A gene expression map of the Arabidopsis root. Science 302(5652): 1956-1960.
10.
Brotman Y., Landau U., Cuadros-Inostroza A., Tohge T., Fernie A.R., Chet I., Viterbo A., Willmitzer L. (2013) Trichoderma- plant root colonization: escaping early plant defense responses and activation of the antioxidant machinery for saline stress tolerance. PLoS Pathog. 9(3): e1003221. Chang I.F., Curran A., Woolsey R., Quilici D., Cushman J. C., Mittler R., Harmon A., Harper J.F. (2009) Proteomic profiling of tandem affinity purified 14-3-3 protein complexes in Arabidopsis thaliana. Proteomics 9(11): 2967-2985.
11.
Chen C., Chen Z. (2002) Potentiation of developmentally regulated plant defense response by AtWRKY18, a pathogeninduced Arabidopsis transcription factor. Plant Physiol. 129(2): 706-716. 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: 281.
12.
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. USA 110(21): E1963- 1971.
13.
Chen L., Zhang L., Yu D. (2010) Wounding-induced WRKY8 is involved in basal defense in Arabidopsis. Mol. Plant Microbe. Interact. 23(5): 558-565.
14.
Chen W., Provart N.J., Glazebrook J., Katagiri F., Chang H.S., Eulgem T., Mauch F., Luan S., Zou G., Whitham S.A. et al. (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14(3): 559-574. Chen Y.F., Li L.Q., Xu Q., Kong Y.H., Wang H., Wu W.H. (2009) The WRKY6 transcription factor modulates PHOSPHATE1 expression in response to low Pi stress in Arabidopsis. Plant Cell 21(11): 3554-3566.
15.
Cheng Y., Zhou Y., Yang Y., Chi Y.J., Zhou J., Chen J.Y., Wang F., Fan B., Shi K., Zhou Y.-H. et al. (2012) Structural and functional analysis of VQ motif-containing proteins in Arabidopsis as interacting proteins of WRKY transcription factors. Plant Physiol. 159(2): 810-825.
16.
Cheong Y.H., Chang H.S., Gupta R., Wang X., Zhu T., Luan S. (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol. 129(2): 661-677.
17.
Chi Y., Yang Y., Zhou Y., Zhou J., Fan B., Yu J.Q., Chen Z. (2013) Protein-protein interactions in the regulation of WRKY transcription factors. Mol. Plant. 6(2): 287-300.
18.
Chisholm S.T., Coaker G., Day B., Staskawicz B.J. (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124(4): 803-814.
19.
Chujo T., Miyamoto K., Shimogawa T., Shimizu T., Otake Y., Yokotani N., Nishizawa Y., Shibuya N., Nojiri H., Yamane H. (2013) OsWRKY28, a PAMP-responsive transrepressor, negatively regulates innate immune responses in rice against rice blast fungus. Plant Mol. Biol. 82(1-2): 23-37. Ciolkowski I., Wanke D., Birkenbihl R.P., Somssich I.E. (2008) Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function. Plant Mol. Biol. 68(1-2): 81-92.
20.
Consortium A.I.M. (2011) Evidence for network evolution in an Arabidopsis interactome map. Science 333: 601-607.
21.
Contento A.L., Kim S.J., Bassham D.C. (2004) Transcriptome profiling of the response of Arabidopsis suspension culture cells to Suc starvation. Plant Physiol. 135(4): 2330- 2347.
22.
Dang F.-F., Wang Y.-N., Yu L., Eulgem T., Lai Y., Liu Z.-Q., Wang X., Qiu A.-L., Zhang T.-X., Lin J. et al. (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(4): 757-774.
23.
Dangl J.L., Dietrich R.A., Richberg M.H. (1996) Death Don't Have No Mercy: Cell Death Programs in Plant-Microbe Interactions. Plant Cell 8(10): 1793-1807.
24.
de Pater S., Greco V., Pham K., Memelink J., Kijne J. (1996) Characterization of a zinc-dependent transcriptional activator from Arabidopsis. Nucl. Acids Res. 24(23): 4624- 4631.
25.
Dellagi A., Helibronn J., Avrova A.O., Montesano M., Palva E.T., Stewart H.E., Toth I.K., Cooke D.E.L., Lyon G.D., Birch P.R.J. (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 class I endochitinase expression. Mol. Plant Microbe. Interact. 13(10): 1092-1101.
26.
Deslandes L., Olivier J., Theulieres F., Hirsch J., Feng D.X., Bittner-Eddy P., Beynon J., Marco Y. (2002) Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. Proc. Natl Acad. Sci. USA 99(4): 2404-2409.
27.
Dodds P.N., Rathjen J.P. (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11(8): 539-548.
28.
Dong J., Chen C., Chen Z. (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol. Biol. 51(1): 21-37.
29.
Du L., Chen Z. (2000) Identification of genes encoding receptor- like protein kinases as possible targets of pathogenand salicylic acid-induced WRKY DNA-binding proteins in Arabidopsis. Plant J. 24(6): 837-847.
30.
Duan M.R., Nan J., Liang Y.H., Mao P., Lu L., Li L., Wei C., Lai L., Li Y., Su X.D. (2007) DNA binding mechanism re in tomato and Arabidopsis as well as gene-for-gene vealed by high resolution crystal structure of Arabidopsis thaliana WRKY1 protein. Nucl. Acids Res. 35(4): 1145-1154. Eulgem T., Rushton P.J., Robatzek S., Somssich I.E. (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5(5): 199-206.
31.
Eulgem T., Rushton P.J., Schmelzer E., Hahlbrock K., Somssich I.E. (1999) Early nuclear events in plant defence signalling:rapid gene activation by WRKY transcription factors. EMBO J. 18(17): 4689-4699.
32.
Gadjev I., Vanderauwera S., Gechev T.S., Laloi C., Minkov I.N., Shulaev V., Apel K., Inzé D., Mittler R., Van Breusegem F. et al. (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol., 141(2): 436-445.
33.
Gao Q.M., Venugopal S., Navarre D., Kachroo A. (2011) Low oleic acid-derived repression of jasmonic acid-inducible defense responses requires the WRKY50 and WRKY51 proteins. Plant Physiol. 155(1): 464-476.
34.
Gao X., Chen X., Lin W., Chen S., Lu D., Niu Y., Li L., Cheng C., McCormack M., Sheen J. et al. (2013) Bifurcation of Arabidopsis NLR immune signaling via Ca(2)(+)-dependent protein kinases. PLoS Pathog. 9(1): e1003127.
35.
Guillaumie S., Mzid R., Mechin V., Leon 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(1-2): 215-234.
36.
Hammargren J., Rosenquist S., Jansson C., Knorpp C. (2008) A novel connection between nucleotide and carbohydrate metabolism in mitochondria: sugar regulation of the Arabidopsis nucleoside diphosphate kinase 3a gene. Plant Cell Rep. 27(3): 529-534.
37.
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(1): 30-37.
38.
Hinderhofer K., Zentgraf U. (2001) Identification of a transcription factor specifically expressed at the onset of leaf senescence. Planta 213(3): 469-473.
39.
Hu Y., Chen L., Wang H., Zhang L., Wang F., Yu D. (2013) Arabidopsis transcription factor WRKY8 functions antagonistically with its interacting partner VQ9 to modulate salinity stress tolerance. Plant J. 74(5): 730-745.
40.
Inoue H., Hayashi N., Matsushita A., Xinqiong L., Nakayama A., Sugano S. et al. (2013) Blast resistance of CC-NB-LRR protein Pb1 is mediated by WRKY45 through protein-protein interaction. Proc. Natl Acad. Sci. USA 110(23): 9577-9582.
41.
Ishiguro S., Nakamura K. (1994) Characterization of a cDNA encoding a novel DNA-binding protein, SPF1, that recognizes SP8 sequences in the 5N upstream regions of genes coding for sporamin and beta-amylase from sweet potato. Mol. Gen. Genet. 244(6): 563-571.
42.
Ishihama N., Yoshioka H. (2012) Post-translational regulation of WRKY transcription factors in plant immunity. Curr. Opin. Plant Biol. 15(4): 431-437.
43.
Izaguirre M.M., Scopel A.L., Baldwin I.T., Ballare C.L. (2003) Convergent responses to stress. Solar ultraviolet-B radiation and Manduca sexta herbivory elicit overlapping transcriptional responses in field-grown plants of Nicotiana longiflora. Plant Physiol. 132(4): 1755-1767.
44.
Jiang Y., Deyholos M.K. (2009) Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol. Biol. 69(1-2): 91-105.
45.
Jin J., Zhang H., Kong L., Gao G., Luo J. (2014) PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucl. Acids Res. 42: D1182- 1187.
46.
Johnson C.S., Kolevski B., Smyth D.R. (2002) TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. Plant Cell 14(6): 1359-1375.
47.
Journot-Catalino N., Somssich I.E., Roby D., Kroj T. (2006) The transcription factors WRKY11 and WRKY17 act as negative regulators of basal resistance in Arabidopsis thaliana. Plant Cell 18(11): 3289-3302.
48.
Kalde M., Barth M., Somssich I.E., Lippok B. (2003) Members of the Arabidopsis WRKY group III transcription factors are part of different plant defense signaling pathways. Mol. Plant Microb. Interact. 16(4): 295-305.
49.
Kasajima I., Ide Y., Yokota Hirai M., Fujiwara T. (2010) WRKY6 is involved in the response to boron deficiency in Arabidopsis thaliana. Physiol. Plant, 139(1): 80-92.
50.
Kim K.C., Fan B., Chen Z. (2006) Pathogen-induced Arabidopsis WRKY7 is a transcriptional repressor and enhances plant susceptibility to Pseudomonas syringae. Plant Physiol. 142(3): 1180-1192.
51.
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(9): 2357- 2371.
52.
Knoth C., Ringler J., Dangl J.L., Eulgem T. (2007) Arabidopsis WRKY70 is required for full RPP4-mediated disease resistance and basal defense against Hyaloperonospora parasitica. Mol. Plant Microb. Interact. 20(2): 120-128.
53.
Lagace M., Matton D.P. (2004) Characterization of a WRKY transcription factor expressed in late torpedo-stage embryos of Solanum chacoense. Planta 219(1): 185-189.
54.
Lai Z., Li Y., Wang F., Cheng Y., Fan B., Yu J.Q., Chen Z. (2011) Arabidopsis sigma factor binding proteins are activators of the WRKY33 transcription factor in plant defense. Plant Cell 23(10): 3824-3841.
55.
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: 68.
56.
Li J., Brader G., Kariola T., Palva E.T. (2006) WRKY70 modulates the selection of signaling pathways in plant defense. Plant J. 46(3): 477-491.
57.
Li S., Fu Q., Huang W., Yu D. (2009) Functional analysis of an Arabidopsis transcription factor WRKY25 in heat stress. Plant Cell Rep. 28(4): 683-693.
58.
Li S., Zhou X., Chen L., Huang W., Yu D. (2010) Functional characterization of Arabidopsis thaliana WRKY39 in heat stress. Mol. Cell 29(5): 475-483.
59.
Liu J.J., Ekramoddoullah A.K. (2009) Identification and characterization of the WRKY transcription factor family in Pinus monticola. Genome 52(1): 77-88.
60.
Luo M., Dennis E.S., Berger F., Peacock W.J., 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(48): 17531-17536.
61.
Maeo K., Hayashi S., Kojima-Suzuki H., Morikami A., Nakamura K. (2001) Role of conserved residues of the WRKY domain in the DNA-binding of tobacco WRKY family proteins. Biosci. Biotechnol. Biochem. 65(11): 2428-2436.
62.
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(4): 1639-1653.
63.
Mishina T.E., Zeier J. (2007) Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J. 50(3): 500-513.
64.
Mishra S., Triptahi V., Singh S., Phukan U.J., Gupta M.M., Shanker K., Shukla R.K. (2013) Wound induced transcriptional regulation of benzylisoquinoline pathway and characterization of wound inducible PsWRKY transcription factor from Papaver somniferum. PLoS One 8(1): e52784.
65.
Park C.Y., Lee J.H., Yoo J.H., Moon B.C., Choi M.S., Kang Y.H. et al. (2005) WRKY group IId transcription factors interact with calmodulin. FEBS Lett. 579(6): 1545-1550.
66.
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(3): 319-330.
67.
Qiu J.L., Fiil B.K., Petersen K., Nielsen H.B., Botanga C.J., Thorgrimsen S. et al. (2008) Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J. 27(16): 2214-2221.
68.
Rizhsky L., Davletova S., Liang H., Mittler R. (2004) The zinc finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J. Biol. Chem. 279(12): 11736-11743.
69.
Rizhsky L., Liang H., Mittler R. (2002) The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol. 130(3): 1143-1151.
70.
Robatzek S., Somssich I.E. (2001) A new member of the Arabidopsis WRKY transcription factor family, AtWRKY6, is associated with both senescence- and defence-related processes. Plant J. 28(2): 123-133.
71.
Robatzek S., Somssich I. E. (2002) Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes Dev. 16(9): 1139-1149.
72.
Rushton P.J., Macdonald H., Huttly A.K., Lazarus C.M., 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(4): 691-702.
73.
Rushton P.J., Somssich I.E., Ringler P., Shen Q.J. (2010) WRKY transcription factors. Trends Plant Sci. 15(5): 247-258.
74.
Rushton P.J., Torres J.T., Parniske M., Wernert P., Hahlbrock K., Somssich I.E. (1996) Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J. 15(20): 5690-5700.
75.
Schon M., Toller A., Diezel C., Roth C., Westphal L., Wiermer M., Somssich I.E. (2013) Analyses of wrky18 wrky40 plants reveal critical roles of SA/EDS1 signaling and indole- glucosinolate biosynthesis for Golovinomyces orontii resistance and a loss-of resistance towards Pseudomonas syringae pv. tomato AvrRPS4. Mol. Plant Microb. Interact. 26(7): 758-767.
76.
Schoonheim P.J., Sinnige M.P., Casaretto J.A., Veiga H., Bunney T.D., Quatrano R.S., de Boer A.H. (2007) 14-3-3 adaptor proteins are intermediates in ABA signal transduction during barley seed germination. Plant J. 49(2): 289-301.
77.
Shim J.S., Choi Y.D. (2013) Direct regulation of WRKY70 by AtMYB44 in plant defense responses. Plant Signal Behav. 8(6): e20783.
78.
Shim J.S., Jung C., Lee S., Min K., Lee Y.W., Choi Y. et al. (2013) AtMYB44 regulates WRKY70 expression and modulates antagonistic interaction between salicylic acid and jasmonic acid signaling. Plant J. 73(3): 483-495.
79.
Skibbe M., Qu N., Galis I., Baldwin I.T. (2008) Induced plant defenses in the natural environment: Nicotiana attenuate WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell 20(7): 1984-2000.
80.
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 sugar-responsive elements of the iso1 promoter. Plant Cell 15(9): 2076-2092.
81.
Tsuda K., Sato M., Stoddard T., Glazebrook J., Katagiri F. (2009) Network properties of robust immunity in plants. PLoS Genet. 5(12): e1000772.
82.
van Loon L.C., Rep M., Pieterse C.M. (2006) Significance of inducible defense-related proteins in infected plants. Ann. Rev. Phytopathol. 44: 135-162.
83.
Van Loon L.C., Pierpoint W.S., Boller T., Conejero V. (1994) Recommendations for naming plant pathogenesis-related proteins. Plant Mol. Biol. Rep. (12): 245-264.
84.
Vandenabeele S., Van Der Kelen K., Dat J., Gadjev I., Boonefaes T., Morsa S. et al. (2003) A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. Proc. Natl Acad. Sci. USA 100(26): 16113-16118.
85.
Wan J., Zhang X.C., Neece D., Ramonell K.M., Clough S., Kim S.Y. et al. (2008) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20(2): 471-481.
86.
Wang D., Amornsiripanitch N., Dong X. (2006) A genomic approach to identify regulatory nodes in the transcriptio nal network of systemic acquired resistance in plants. PLoS Pathog. 2(11): e123. Wang H.J., Wan A.R., Hsu C.M., Lee K.W., Yu S.M., Jauh G.Y. (2007) Transcriptomic adaptations in rice suspension cells under sucrose starvation. Plant Mol. Biol. 63(4): 441-463.
87.
Wang X., Du B., Liu M., Sun N., Qi X. (2013) Arabidopsis transcription factor WRKY33 is involved in drought by directly regulating the expression of CesA8. Amer. J. Plant Sci. 4(6A): 21-27.
88.
Wang Z., Yang P., Fan B., Chen Z. (1998) An oligo selection procedure for identification of sequence-specific DNA-binding activities associated with the plant defence response. Plant J. 16(4): 515-522.
89.
Willmott R.L., Rushton P.J., Hooley R., Lazarus C.M. (1998) DNase1 footprints suggest the involvement of at least three types of transcription factors in the regulation of alpha-Amy2/A by gibberellin. Plant Mol. Biol. 38(5): 817-825.
90.
Wu K.L., Guo Z.J., Wang H.H., Li J. (2005) The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Res. 12(1): 9-26.
91.
Xie Z., Zhang Z.L., Zou X., Huang J., Ruas P., Thompson D., Shen Q.J. (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(1): 176-189.
92.
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(5): 1310-1326.
93.
Xu Y.H., Wang J.W., Wang S., Wang J.Y., Chen X.Y. (2004) Characterization of GaWRKY1, a cotton transcription factor that regulates the sesquiterpene synthase gene (+)- delta-cadinene synthase-A. Plant Physiol. 135(1): 507-515.
94.
Yamasaki K., Kigawa T., Inoue M., Tateno M., Yamasaki T., Yabuki T. et al. (2005) Solution structure of an Arabidopsis WRKY DNA binding domain. Plant Cell 17(3): 944-956.
95.
Yamasaki K., Kigawa T., Watanabe S., Inoue M., Yamasaki T., Seki M. et al. (2012) Structural basis for sequence-specific DNA recognition by an Arabidopsis WRKY transcription factor. J. Biol. Chem. 287(10): 7683-7691.
96.
Yang P.Z., Chen C.H., Wang Z.P., Fan B.F., Chen Z.X. (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(2):141-149.
97.
Zhang H., Jin J., Tang L., Zhao Y., Gu X., Gao G., Luo J. (2011) PlantTFDB 2.0: update and improvement of the comprehensive plant transcription factor database. Nucl. Acids Res. 39: D1114-1117.
98.
Zhang Z.L., Xie Z., Zou X., Casaretto J., Ho T.H., Shen Q.J. (2004) A rice WRKY gene encodes a transcriptional repressor of the gibberellin signaling pathway in aleurone cells. Plant Physiol. 134(4): 1500-1513.
99.
Zheng Z., Mosher S.L., Fan B., Klessig D.F., Chen Z. (2007) Functional analysis of Arabidopsis WRKY25 transcription factor in plant defense against Pseudomonas syringae. BMC Plant Biol. 7: 2.
100.
Zheng Z., Qamar S.A., Chen Z., Mengiste T. (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J. 48(4): 592-605.
101.
Zipfel C., Kunze G., Chinchilla D., Caniard A., Jones J.D., Boller T., Felix G. (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125(4): 749-760.
102.
Zipfel C., Robatzek S., Navarro L., Oakeley E.J., Jones J.D., Felix G., Boller T. (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428 (6984): 764-767.
103.
Zou C., Jiang W., Yu D. (2010) Male gametophyte-specific WRKY34 transcription factor mediates cold sensitivity of mature pollen in Arabidopsis. J. Exp. Bot. 61(14): 3901- 3914.
Share
RELATED ARTICLE
| eISSN: | 2353-9461 |
| ISSN: | 0860-7796 |
We process personal data collected when visiting the website. The function of obtaining information about users and their behavior is carried out by voluntarily entered information in forms and saving cookies in end devices. Data, including cookies, are used to provide services, improve the user experience and to analyze the traffic in accordance with the Privacy policy. Data are also collected and processed by Google Analytics tool (more).
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
