Elucidating the evolutionary conserved DNA-binding specificities of WRKY transcription factors by molecular dynamics and in vitro binding assays

Nucleic Acids Research

Volumn 41, Issue 21, 2013, Pages 9764-9778

  Brand, Luise H ^a   Fischer, Nina M ^a   Harter, Klaus ^a   Kohlbacher, Oliver ^a   Wanke, Dierk ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN ATWRKY11; PROTEIN ATWRKY33; PROTEIN ATWRKY50; PROTEIN WRKY; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; DNA BINDING MOTIF; ENZYME LINKED IMMUNOSORBENT ASSAY; EUKARYOTE; GENETIC CONSERVATION; IN VITRO STUDY; MOLECULAR DYNAMICS; MONOPHYLY; NONHUMAN; NUCLEOTIDE SEQUENCE; PARAPHYLY; PHYLOGENY; PRIORITY JOURNAL; PROTEIN DNA BINDING; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ARABIDOPSIS PROTEINS; DNA-BINDING PROTEINS; EVOLUTION, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; STRUCTURAL HOMOLOGY, PROTEIN; TRANSCRIPTION FACTORS;

EID: 84890074285     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt732     Document Type: Article

References (83)

1. Kilian, J., Peschke, F., Berendzen, K.W., Harter, K. and Wanke, D. (2012) Prerequisites, performance and profits of transcriptional profiling the abiotic stress response. Biochim. Biophys. Acta, 1819, 166-175.
2. Babu, M.M., Iyer, L.M., Balaji, S. and 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.
3. Eulgem, T., Rushton, P.J., Robatzek, S. and Somssich, I.E. (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci., 5, 199-206.
4. Pandey, S.P. and Somssich, I.E. (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol., 150, 1648-1655.
5. Ramirez, S.R. and Basu, C. (2009) Comparative analyses of plant transcription factor databases. Curr. Genomics, 10, 10-17.
6. Riechmann, J.L., Heard, J., Martin, G., Reuber, L., Jiang, C., Keddie, J., Adam, L., Pineda, O., Ratcliffe, O.J., Samaha, R.R. et al. (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science, 290, 2105-2110.
7. Rushton, P.J., Somssich, I.E., Ringler, P. and Shen, Q.J. (2010) WRKY transcription factors. Trends Plant Sci., 15, 247-258.
8. Ulker, B. and Somssich, I.E. (2004) WRKY transcription factors: from DNA binding towards biological function. Curr. Opin. Plant Biol., 7, 491-498.
9. Wenke, K., Wanke, D., Kilian, J., Berendzen, K., Harter, K. and Piechulla, B. (2012) Volatiles of two growth-inhibiting rhizobacteria commonly engage AtWRKY18 function. Plant J., 70, 445-459.
10. Zhang, Y. and Wang, L. (2005) The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evol. Biol., 5, 1.
11. Ay, N., Irmler, K., Fischer, A., Uhlemann, R., Reuter, G. and Humbeck, K. (2009) Epigenetic programming via histone methylation at WRKY53 controls leaf senescence in Arabidopsis thaliana. Plant J., 58, 333-346.
12. Besseau, S., Li, J. and Palva, E.T. (2012) WRKY54 and WRKY70 co-operate as negative regulators of leaf senescence in Arabidopsis thaliana. J. Exp. Bot., 63, 2667-2679.
13. Dilkes, B.P., Spielman, M., Weizbauer, R., Watson, B., Burkart-Waco, D., Scott, R.J. and Comai, L. (2008) The maternally expressed WRKY transcription factor TTG2 controls lethality in interploidy crosses of Arabidopsis. PLoS Biol., 6, 2707-2720.
14. Garcia, D., Fitz Gerald, J.N. and Berger, F. (2005) Maternal control of integument cell elongation and zygotic control of endosperm growth are coordinated to determine seed size in Arabidopsis. Plant Cell, 17, 52-60.
15. Ishida, T., Hattori, S., Sano, R., Inoue, K., Shirano, Y., Hayashi, H., Shibata, D., Sato, S., Kato, T., Tabata, S. et al. (2007) Arabidopsis TRANSPARENT TESTA GLABRA2 is directly regulated by R2R3 MYB transcription factors and is involved in regulation of GLABRA2 transcription in epidermal differentiation. Plant Cell, 19, 2531-2543.
16. Johnson, C.S., Kolevski, B. and Smyth, D.R. (2002) TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. Plant Cell, 14, 1359-1375.
17. Luo, M., Dennis, E.S., Berger, F., Peacock, W.J. and 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.
18. Miao, Y., Laun, T., Zimmermann, P. and Zentgraf, U. (2004) Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol. Biol., 55, 853-867.
19. Ngo, Q.A., Baroux, C., Guthorl, D., Mozerov, P., Collinge, M.A., Sundaresan, V. and Grossniklaus, U. (2012) The Armadillo repeat gene ZAK IXIK promotes Arabidopsis early embryo and endosperm development through a distinctive gametophytic maternal effect. Plant Cell, 24, 4026-4043.
20. Ishiguro, S. and 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 beta-amylase from sweet potato. Mol. Gen. Genet., 244, 563-571.
21. Rushton, P.J., Macdonald, H., Huttly, A.K., Lazarus, C.M. and 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.
22. Rushton, P.J., Torres, J.T., Parniske, M., Wernert, P., Hahlbrock, K. and Somssich, I.E. (1996) Interaction of elicitor-induced DNAbinding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J., 15, 5690-5700.
23. He, H., Dong, Q., Shao, Y., Jiang, H., Zhu, S., Cheng, B. and Xiang, Y. (2012) Genome-wide survey and characterization of the WRKY gene family in Populus trichocarpa. Plant Cell Rep., 31, 1199-1217.
24. Ling, J., Jiang, W., Zhang, Y., Yu, H., Mao, Z., Gu, X., Huang, S. and Xie, B. (2011) Genome-wide analysis of WRKY gene family in Cucumis sativus. BMC Genomics, 12, 471.
25. Mangelsen, E., Kilian, J., Berendzen, K.W., Kolukisaoglu, U.H., Harter, K., Jansson, C. and 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.
26. Rensing, S.A., Lang, D., Zimmer, A.D., Terry, A., Salamov, A., Shapiro, H., Nishiyama, T., Perroud, P.F., Lindquist, E.A., Kamisugi, Y. et al. (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science, 319, 64-69.
27. Rushton, P.J., Bokowiec, M.T., Han, S., Zhang, H., Brannock, J.F., Chen, X., Laudeman, T.W. and Timko, M.P. (2008) Tobacco transcription factors: novel insights into transcriptional regulation in the Solanaceae. Plant Physiol., 147, 280-295.
28. Ryu, H.S., Han, M., Lee, S.K., Cho, J.I., Ryoo, N., Heu, S., Lee, Y.H., Bhoo, S.H., Wang, G.L., Hahn, T.R. et al. (2006) A comprehensive expression analysis of the WRKY gene superfamily in rice plants during defense response. Plant Cell Rep., 25, 836-847.
29. Tripathi, P., Rabara, R.C., Langum, T.J., Boken, A.K., Rushton, D.L., Boomsma, D.D., Rinerson, C.I., Rabara, J., Reese, R.N., Chen, X. et al. (2012) The WRKY transcription factor family in Brachypodium distachyon. BMC Genomics, 13, 270.
30. Wu, K.L., Guo, Z.J., Wang, H.H. and Li, J. (2005) The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Res., 12, 9-26.
31. Zhang, Z.L., Xie, Z., Zou, X., Casaretto, J., Ho, T.H. and Shen, Q.J. (2004) A rice WRKY gene encodes a transcriptional repressor of the gibberellin signaling pathway in aleurone cells. Plant Physiol., 134, 1500-1513.
32. Giacomelli, J.I., Ribichich, K.F., Dezar, C.A. and Chan, R.L. (2010) Expression analyses indicate the involvement of sunflower WRKY transcription factors in stress responses, and phylogenetic reconstructions reveal the existence of a novel clade in the Asteraceae. Plant Sci., 178, 398-410.
33. Huang, S., Gao, Y., Liu, J., Peng, X., Niu, X., Fei, Z., Cao, S. and Liu, Y. (2012) Genome-wide analysis of WRKY transcription factors in Solanum lycopersicum. Mol. Genet. Genomics, 287, 495-513.
34. Lang, D., Weiche, B., Timmerhaus, G., Richardt, S., Riano-Pachon, D.M., Correa, L.G., Reski, R., Mueller-Roeber, B. and Rensing, S.A. (2010) Genome-wide phylogenetic comparative analysis of plant transcriptional regulation: a timeline of loss, gain, expansion, and correlation with complexity. Genome Biol. Evol., 2, 488-503.
35. Xie, Z., Zhang, Z.L., Zou, X., Huang, J., Ruas, P., Thompson, D. and 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, 176-189.
36. Eulgem, T. and Somssich, I.E. (2007) Networks of WRKY transcription factors in defense signaling. Curr. Opin. Plant Biol., 10, 366-371.
37. Yamasaki, K., Kigawa, T., Seki, M., Shinozaki, K. and Yokoyama, S. (2012) DNA-binding domains of plant-specific transcription factors: structure, function, and evolution. Trends Plant Sci., 18, 267-276.
38. Brand, L.H., Kirchler, T., Hummel, S., Chaban, C. and Wanke, D. (2010) DPI-ELISA: a fast and versatile method to specify the binding of plant transcription factors to DNA in vitro. Plant Methods, 6, 25.
39. Ciolkowski, I., Wanke, D., Birkenbihl, R.P. and Somssich, I.E. (2008) Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function. Plant Mol. Biol., 68, 81-92.
40. Turck, F., Zhou, A. and Somssich, I.E. (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.
41. Joly-Lopez, Z., Forczek, E., Hoen, D.R., Juretic, N. and Bureau, T.E. (2012) A gene family derived from transposable elements during early angiosperm evolution has reproductive fitness benefits in Arabidopsis thaliana. PLoS Genet., 8, e1002931.
42. Duan, M.R., Nan, J., Liang, Y.H., Mao, P., Lu, L., Li, L., Wei, C., Lai, L., Li, Y. and Su, X.D. (2007) DNA binding mechanism revealed by high resolution crystal structure of Arabidopsis thaliana WRKY1 protein. Nucleic Acids Res., 35, 1145-1154.
43. 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, 944-956.
44. Yamasaki, K., Kigawa, T., Watanabe, S., Inoue, M., Yamasaki, T., Seki, M., Shinozaki, K. and Yokoyama, S. (2012) Structural basis for sequence-specific DNA recognition by an Arabidopsis WRKY transcription factor. J. Biol. Chem., 287, 7683-7691.
45. Wang, Q., Wang, M., Zhang, X., Hao, B., Kaushik, S.K. and Pan, Y. (2011) WRKY gene family evolution in Arabidopsis thaliana. Genetica, 139, 973-983.
46. 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, 810-825.
47. de Pater, S., Greco, V., Pham, K., Memelink, J. and Kijne, J. (1996) Characterization of a zinc-dependent transcriptional activator from Arabidopsis. Nucleic Acids Res., 24, 4624-4631.
48. Eulgem, T., Rushton, P.J., Schmelzer, E., Hahlbrock, K. and Somssich, I.E. (1999) Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors. EMBO J., 18, 4689-4699.
49. Maeo, K., Hayashi, S., Kojima-Suzuki, H., Morikami, A. and Nakamura, K. (2001) Role of conserved residues of the WRKY domain in the DNA-binding of tobacco WRKY family proteins. Biosci. Biotechnol. Biochem., 65, 2428-2436.
50. Banks, J.A., Nishiyama, T., Hasebe, M., Bowman, J.L., Gribskov, M., dePamphilis, C., Albert, V.A., Aono, N., Aoyama, T., Ambrose, B.A. et al. (2011) The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science, 332, 960-963.
51. Goujon, M., McWilliam, H., Li, W., Valentin, F., Squizzato, S., Paern, J. and Lopez, R. (2010) A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res., 38, W695-W699.
52. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res., 25, 4876-4882.
53. Felsenstein, J. (1997) An alternating least squares approach to inferring phylogenies from pairwise distances. Syst. Biol., 46, 101-111.
54. Felsenstein, J. (2012) A comparative method for both discrete and continuous characters using the threshold model. Am. Nat., 179, 145-156.
55. Swafford, D.L. (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts. http://www.sinauer.com/paupphylogenetic-analysis-using-parsimony- and-other-methods-4-0-beta.html (9 August 2013, date last accessed).
56. Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N. and Bourne, P.E. (2000) The Protein Data Bank. Nucleic Acids Res., 28, 235-242.
57. Cohen, S.X., Moulin, M., Hashemolhosseini, S., Kilian, K., Wegner, M. and Muller, C.W. (2003) Structure of the GCM domain-DNA complex: a DNA-binding domain with a novel fold and mode of target site recognition. EMBO J., 22, 1835-1845.
58. Holm, L. and Rosenstrom, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res., 38, W545-W549.
59. Hildebrandt, A., Dehof, A.K., Rurainski, A., Bertsch, A., Schumann, M., Toussaint, N.C., Moll, A., Stockel, D., Nickels, S., Mueller, S.C. et al. (2010) BALL-biochemical algorithms library 1.3. BMC Bioinformatics, 11, 531.
60. Case, D., Darden, T.A., Cheatham, T.E., Simmerling, C., Wang, J., Duke, R., Luo, R., Crowley, M., Walker, R., Zhang, W. et al. (2010) Amber 11. University of California, San Francisco.
61. Gordon, J.C., Myers, J.B., Folta, T., Shoja, V., Heath, L.S. and Onufriev, A. (2005) H++: a server for estimating pKas and adding missing hydrogens to macromolecules. Nucleic Acids Res., 33, W368-W371.
62. Hornak, V., Abel, R., Okur, A., Strockbine, B., Roitberg, A. and Simmerling, C. (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins, 65, 712-725.
63. Perez, A., Marchan, I., Svozil, D., Sponer, J., Cheatham, T.E. III, Laughton, C.A. and Orozco, M. (2007) Refinement of the AMBER force field for nucleic acids: improving the description of alpha/ gamma conformers. Biophys. J., 92, 3817-3829.
64. Jorgensen, W.L., Chandrasekhar, J., Madura, J.D., Impey, R.W. and Klein, M.L. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys., 79, 926.
65. Cheatham, T.E. and Kollman, P.A. (1997) Molecular dynamics simulations highlight the structural differences among DNA:DNA, RNA:RNA and DNA:RNA hybrid duplexes. J. Amer. Chem. Soc., 119, 4805-4825.
66. Chiu, S.W., Clark, M., Subramaniam, S. and Jakobsson, E. (2000) Collective motion artifacts arising in long-duration molecular dynamics simulations. J. Comput. Chem., 21, 121-131.
67. Harvey, S.C., Tan, R.K.Z. and Cheatham, T.E. (1998) The flying ice cube: velocity rescaling in molecular dynamics leads to violation of energy equipartition. J. Comput. Chem., 19, 726-740.
68. Darden, T., Pearlman, D. and Pedersen, L.G. (1998) Ionic charging free energies: spherical versus periodic boundary conditions. J. Chem. Phys., 109, 10921.
69. Ryckaert, J.P., Ciccotti, G. and Berendsen, H. (1977) Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys., 23, 327-341.
70. Jacobson, M.P., Friesner, R.A., Xiang, Z. and Honig, B. (2002) On the role of the crystal environment in determining protein sidechain conformations. J. Mol. Biol., 320, 597-608.
71. Jacobson, M.P., Pincus, D.L., Rapp, C.S., Day, T.J., Honig, B., Shaw, D.E. and Friesner, R.A. (2004) A hierarchical approach to all-atom protein loop prediction. Proteins, 55, 351-367.
72. Bailey, T.L., Boden, M., Buske, F.A., Frith, M., Grant, C.E., Clementi, L., Ren, J., Li, W.W. and Noble, W.S. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res., 37, W202-W208.
73. Crooks, G.E., Hon, G., Chandonia, J.M. and Brenner, S.E. (2004) WebLogo: a sequence logo generator. Genome Res., 14, 1188-1190.
74. Ramamoorthy, R., Jiang, S.Y., Kumar, N., Venkatesh, P.N. and 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.
75. Rossberg, M., Theres, K., Acarkan, A., Herrero, R., Schmitt, T., Schumacher, K., Schmitz, G. and Schmidt, R. (2001) Comparative sequence analysis reveals extensive microcolinearity in the lateral suppressor regions of the tomato, Arabidopsis, and Capsella genomes. Plant Cell, 13, 979-988.
76. Sun, C., Palmqvist, S., Olsson, H., Boren, M., Ahlandsberg, S. and 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.
77. Honig, B. and Rohs, R. (2011) Biophysics: flipping Watson and Crick. Nature, 470, 472-473.
78. Rohs, R., Jin, X., West, S.M., Joshi, R., Honig, B. and Mann, R.S. (2010) Origins of specificity in protein-DNA recognition. Annu. Rev. Biochem., 79, 233-269.
79. Lane, W.J. and Darst, S.A. (2006) The structural basis for promoter-35 element recognition by the group IV sigma factors. PLoS Biol., 4, e269.
80. Welner, D.H., Lindemose, S., Grossmann, J.G., Mollegaard, N.E., Olsen, A.N., Helgstrand, C., Skriver, K. and Lo Leggio, L. (2012) DNA binding by the plant-specific NAC transcription factors in crystal and solution: a firm link to WRKY and GCM transcription factors. Biochem. J., 444, 395-404.
81. Ernst, H.A., Olsen, A.N., Larsen, S. and Lo Leggio, L. (2004) Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors. EMBO Rep., 5, 297-303.
82. Lai, Z., Li, Y., Wang, F., Cheng, Y., Fan, B., Yu, J.Q. and Chen, Z. (2011) Arabidopsis sigma factor binding proteins are activators of the WRKY33 transcription factor in plant defense. Plant Cell, 23, 3824-3841.
83. Song, M.J., Hwang, S., Wong, W., Round, J., Martinez-Guzman, D., Turpaz, Y., Liang, J., Wong, B., Johnson, R.C., Carey, M. et al. (2004) The DNA architectural protein HMGB1 facilitates RTA-mediated viral gene expression in gamma-2 herpesviruses. J. Virol., 78, 12940-12950.