bZIPs and WRKYs: Two large transcription factor families executing two different functional strategies

Frontiers in Plant Science

Volumn 5, Issue APR, 2014, Pages

  Llorca, Carles M ^a   Potschin, Maren ^a   Zentgraf, Ulrike ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

BZIPs; DNA binding; G C box accumulation; Heterodimerization; Regulatory mechanisms; W box accumulation; WRKYs

Indexed keywords

EID: 84901041577     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00169     Document Type: Review

References (149)

1. Abe, M., Kobayashi, Y., Yamamoto, S., Daimon, Y., Yamaguchi, A., Ikeda, Y., et al. (2005). FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309, 1052-1056. doi: 10.1126/science.1115983
2. Acharya, A., Ruvinov, S. B., Gal, J., Moll, J. R., and Vinson, C. (2002). A heterodimerizing leucine zipper coiled coil system for examining the specificity of a position interactions: amino acids I, V, L, N, A, and K. Biochemistry 41, 14122-14131. doi: 10.1021/bi020486r
3. Alonso, R., Onate-Sanchez, L., Weltmeier, F., Ehlert, A., Diaz, I., Dietrich, K., et al. (2009). A pivotal role of the basic leucine zipper transcription factor bZIP53 in the regulation of Arabidopsis seed maturation gene expression based on heterodimerization and protein complex formation. Plant Cell 21, 1747-1761. doi: 10.1105/tpc.108.062968
4. Alves, M., Dadalto, S., Gonçalves, A., De Souza, G., Barros, V., and Fietto, L. (2013). Plant bZIP transcription factors responsive to pathogens: a review. Int. J. Mol. Sci. 14, 7815-7828. doi: 10.3390/ijms14047815
5. Amoutzias, G., Veron, A., Weiner, J., Robinson-Rechavi, M., Bornberg-Bauer, E., Oliver, S., et al. (2006). One billion years of bZIP transcription factor evolution: conservation and change in dimerization and DNA-binding site specificity. Mol. Biol. Evol. 24, 827-835. doi: 10.1093/molbev/msl211
6. Amoutzias, G. D., Robertson, D. L., Van De Peer, Y., and Oliver, S. G. (2008). Choose your partners: dimerization in eukaryotic transcription factors. Trends Biochem. Sci. 33, 220-229. doi: 10.1016/j.tibs.2008.02.002
7. Andronis, C., Barak, S., Knowles, S. M., Sugano, S., and Tobin, E. M. (2008). The clock protein CCA1 and the bZIP transcription factor HY5 physically interact to regulate gene expression in Arabidopsis. Mol. Plant 1, 58-67. doi: 10.1093/mp/ssm005
8. Asai, T., Tena, G., Plotnikova, J., Willmann, M. R., Chiu, W. L., Gomez-Gomez, L., et al. (2002). MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977-983. doi: 10.1038/415977a
9. Assunção, A. G. L., Herrero, E., Lin, Y.-F., Huettel, B., Talukdar, S., Smaczniak, C., et al. (2010). Arabidopsis thaliana transcription factors bZIP19 and bZIP23 regulate the adaptation to zinc deficiency. Proc. Natl. Acad. Sci. U.S.A. 107, 10296-10301. doi: 10.1073/pnas.1004788107
10. 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. doi: 10.1111/j.0960-7412.2009.03782.x
11. 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. doi: 10.1093/nar/gkl888
12. Babu Rajendra Prasad, V., Gupta, N., Nandi, A., and Chattopadhyay, S. (2012). HY1 genetically interacts with GBF1 and regulates the activity of the Z-box containing promoters in light signaling pathways in Arabidopsis thaliana. Mech. Dev. 129, 298-307. doi: 10.1016/j.mod.2012.06.004
13. Baena-González, E., Rolland, F., Thevelein, J. M., and Sheen, J. (2007). A central integrator of transcription networks in plant stress and energy signalling. Nature 448, 938-942. doi: 10.1038/nature06069
14. Bensmihen, S., Rippa, S., Lambert, G., Jublot, D., Pautot, V., Granier, F., et al. (2002). The homologous ABI5 and EEL transcription factors function antagonistically to fine-tune gene expression during late embryogenesis. Plant Cell 14, 1391-1403. doi: 10.1105/tpc.000869
15. Berri, S., Abbruscato, P., Faivre-Rampant, O., Brasileiro, A. C., Fumasoni, I., Satoh, K., et al. (2009). Characterization of WRKY co-regulatory networks in rice and Arabidopsis. BMC Plant Biol. 9:120. doi: 10.1186/1471-2229-9-120
16. 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. doi: 10.1093/jxb/err450
17. Birkenbihl, R. P., Diezel, C., and Somssich, I. E. (2012). Arabidopsis WRKY33 is a key transcriptional regulator of hormonal and metabolic responses toward Botrytis cinerea infection. Plant Physiol. 159, 266-285. doi: 10.1104/pp.111.192641
18. Brand, L. H., Fischer, N. M., Harter, K., Kohlbacher, O., and Wanke, D. (2013). Elucidating the evolutionary conserved DNA-binding specificities of WRKY transcription factors by molecular dynamics and in vitro binding assays. Nucleic Acids Res. 41, 9764-9778. doi: 10.1093/nar/gkt732
19. Breeze, E., Harrison, E., Mchattie, S., Hughes, L., Hickman, R., Hill, C., et al. (2011). High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 23, 873-894. doi: 10.1105/tpc.111.083345
20. Cai, M., Qiu, D., Yuan, T., Ding, X., Li, H., Duan, L., et al. (2008). Identification of novel pathogen-responsive cis-elements and their binding proteins in the promoter of OsWRKY13, a gene regulating rice disease resistance. Plant Cell Environ. 31, 86-96.
21. Chae, M. J., Lee, J. S., Nam, M. H., Cho, K., Hong, J. Y., Yi, S. A., et al. (2007). A rice dehydration-inducible SNF1-related protein kinase 2 phosphorylates an abscisic acid responsive element-binding factor and associates with ABA signaling. Plant Mol. Biol. 63, 151-169. doi: 10.1007/s11103-006-9079-x
22. Chen, H., Lai, Z., Shi, J., Xiao, Y., Chen, Z., and 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. doi: 10.1186/1471-2229-10-281
23. Chen, Y.-T., Liu, H., Stone, S., and Callis, J. (2013). ABA and the ubiquitin E3 ligase KEEP ON GOING affect proteolysis of the Arabidopsis thaliana transcription factors ABF1 and ABF3. Plant J. 75, 965-976. doi: 10.1111/tpj.12259
24. Cheng, Y., Zhou, Y., Yang, Y., Chi, Y. J., Zhou, J., Chen, J. Y., 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. doi: 10.1104/pp.112.196816
25. Chi, Y., Yang, Y., Zhou, Y., Zhou, J., Fan, B., Yu, J. Q., et al. (2013). Protein-protein interactions in the regulation of WRKY transcription factors. Mol. Plant 6, 287-300. doi: 10.1093/mp/sst026
26. Cho, Y. H., Hong, J. W., Kim, E. C., and Yoo, S. D. (2012). Regulatory functions of SnRK1 in stress-responsive gene expression and in plant growth and development. Plant Physiol. 158, 1955-1964. doi: 10.1104/pp.111.189829
27. Choi, H. I., Hong, J., Ha, J., Kang, J., and Kim, S. Y. (2000). ABFs, a family of ABA-responsive element binding factors. J. Biol. Chem. 275, 1723-1730. doi: 10.1074/jbc.275.3.1723
28. Chujo, T., Miyamoto, K., Shimogawa, T., Shimizu, T., Otake, Y., Yokotani, N., et al. (2013). OsWRKY28, a PAMP-responsive transrepressor, negatively regulates innate immune responses in rice against rice blast fungus. Plant Mol. Biol. 82, 23-37. doi: 10.1007/s11103-013-0032-5
29. 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. doi: 10.1007/s11103-008-9353-1
30. Deppmann, C. D., Acharya, A., Rishi, V., Wobbes, B., Smeekens, S., Taparowsky, E. J., et al. (2004). Dimerization specificity of all 67 B-ZIP motifs in Arabidopsis thaliana: a comparison to Homo sapiens B-ZIP motifs. Nucleic Acids Res. 32, 3435-3445. doi: 10.1093/nar/gkh653
31. Deppmann, C. D., Alvania, R. S., and Taparowsky, E. J. (2006). Cross-species annotation of basic leucine zipper factor interactions: insight into the evolution of closed interaction networks. Mol. Biol. Evol. 23, 1480-1492. doi: 10.1093/molbev/msl022
32. Deppmann, C. D., Thornton, T. M., Utama, F. E., and Taparowsky, E. J. (2003). Phosphorylation of BATF regulates DNA binding: a novel mechanism for AP-1 (activator protein-1) regulation. Biochem. J. 374, 423-431. doi: 10.1042/BJ20030455
33. Dietrich, K., Weltmeier, F., Ehlert, A., Weiste, C., Stahl, M., Harter, K., et al. (2011). Heterodimers of the Arabidopsis transcription factors bZIP1 and bZIP53 reprogram amino acid metabolism during low energy stress. Plant Cell 23, 381-395. doi: 10.1105/tpc.110.075390
34. Djamei, A., Pitzschke, A., Nakagami, H., Rajh, I., and Hirt, H. (2007). Trojan horse strategy in Agrobacterium transformation: abusing MAPK defense signaling. Science 318, 453-456. doi: 10.1126/science.1148110
35. Dong, J., Chen, C., and Chen, Z. (2003). Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol. Biol. 51, 21-37. doi: 10.1023/A:1020780022549
36. Duan, M. R., Nan, J., Liang, Y. H., Mao, P., Lu, L., Li, L., et al. (2007). DNA binding mechanism revealed by high resolution crystal structure of Arabidopsis thaliana WRKY1 protein. Nucleic Acids Res. 35, 1145-1154. doi: 10.1093/nar/gkm001
37. Dyson, H. J., and Wright, P. E. (2005). Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 6, 197-208. doi: 10.1038/nrm1589
38. Ehlert, A., Weltmeier, F., Wang, X., Mayer, C. S., Smeekens, S., Vicente-Carbajosa, J., et al. (2006). Two-hybrid protein-protein interaction analysis in Arabidopsis protoplasts: establishment of a heterodimerization map of group C and group S bZIP transcription factors. Plant J. 46, 890-900. doi: 10.1111/j.1365-313X.2006.02731.x
39. 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. doi: 10.1016/S1360-1385(00)01600-9
40. 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. doi: 10.1093/emboj/18.17.4689
41. Fong, J., Keating, A., and Singh, M. (2004). Predicting specificity in bZIP coiled-coil protein interactions. Genome Biol. 5, R11. doi: 10.1186/gb-2004-5-2-r11
42. Foster, R., Izawa, T., and Chua, N.-H. (1994). Plant bZIP proteins gather at ACGT elements. FASEB J. 8, 192-200.
43. Fu, Z. Q., and Dong, X. (2013). Systemic acquired resistance: turning local infection into global defense. Annu. Rev. Plant Biol. 64, 839-863. doi: 10.1146/annurev-arplant-042811-105606
44. Fujii, Y., Shimizu, T., Toda, T., Yanagida, M., and Hakoshima, T. (2000). Structural basis for the diversity of DNA recognition by bZIP transcription factors. Nat. Struct. Biol. 7, 889-893. doi: 10.1038/82822
45. Fujita, Y., Fujita, M., Satoh, R., Maruyama, K., Parvez, M. M., Seki, M., et al. (2005). AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17, 3470-3488. doi: 10.1105/tpc.105.035659
46. Gangappa, S. N., Crocco, C. D., Johansson, H., Datta, S., Hettiarachchi, C., Holm, M., et al. (2013). The Arabidopsis B-BOX protein BBX25 interacts with HY5, negatively regulating BBX22 expression to suppress seedling photomorphogenesis. Plant Cell 25, 1243-1257. doi: 10.1105/tpc.113.109751
47. Glawischnig, E. (2007). Camalexin. Phytochemistry 68, 401-406. doi: 10.1016/j.phytochem.2006.12.005
48. Glover, J. N. M., and Harrison, S. C. (1995). Crystal structure of the heterodimeric bZIP transcription factor c-Fos-c-Jun bound to DNA. Nature 373, 257-261. doi: 10.1038/373257a0
49. Hardtke, C. S., Gohda, K., Osterlund, M. T., Oyama, T., Okada, K., and Deng, X. W. (2000). HY5 stability and activity in Arabidopsis is regulated by phosphorylation in its COP1 binding domain. EMBO J. 19, 4997-5006. doi: 10.1093/emboj/19.18.4997
50. Holm, M., Ma, L.-G., Qu, L.-J., and Deng, X.-W. (2002). Two interacting bZIP proteins are direct targets of COP1-mediated control of light-dependent gene expression in Arabidopsis. Genes Dev. 16, 1247-1259. doi: 10.1101/gad.969702
51. Hsieh, T. H., Li, C. W., Su, R. C., Cheng, C. P., Sanjaya, Tsai, Y. C., et al. (2010). A tomato bZIP transcription factor, SlAREB, is involved in water deficit and salt stress response. Planta 231, 1459-1473. doi: 10.1007/s00425-010-1147-4
52. Hu, Y., Dong, Q., and Yu, D. (2012). Arabidopsis WRKY46 coordinates with WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. Plant Sci. 185-186, 288-297. doi: 10.1016/j.plantsci.2011.12.003
53. Huang, S., Gao, Y., Liu, J., Peng, X., Niu, X., Fei, Z., et al. (2012). Genome-wide analysis of WRKY transcription factors in Solanum lycopersicum. Mol. Genet. Genomics 287, 495-513. doi: 10.1007/s00438-012-0696-6
54. Hummel, M., Rahmani, F., Smeekens, S., and Hanson, J. (2009). Sucrose-mediated translational control. Ann. Bot. 104, 1-7. doi: 10.1093/aob/mcp086
55. Ishida, S., Yuasa, T., Nakata, M., and Takahashi, Y. (2008). A tobacco calcium-dependent protein kinase, CDPK1, regulates the transcription factor REPRESSION OF SHOOT GROWTH in response to gibberellins. Plant Cell 20, 3273-3288. doi: 10.1105/tpc.107.057489
56. Ishiguro, S., and Nakamura, K. (1994). Characterization of a cDNA encoding a novel DNA-binding protein, SPF1, that recognizes SP8 sequences in the 5′ upstream regions of genes coding for sporamin and beta-amylase from sweet potato. Mol. Gen. Genet. 244, 563-571. doi: 10.1007/BF00282746
57. Ishihama, N., Yamada, R., Yoshioka, M., Katou, S., and Yoshioka, H. (2011). Phosphorylation of the Nicotiana benthamiana WRKY8 transcription factor by MAPK functions in the defense response. Plant Cell 23, 1153-1170. doi: 10.1105/tpc.110.081794
58. Iwata, Y., Fedoroff, N. V., and Koizumi, N. (2008). Arabidopsis bZIP60 is a proteolysis-activated transcription factor involved in the endoplasmic reticulum stress response. Plant Cell 20, 3107-3121. doi: 10.1105/tpc.108.061002
59. Izawa, T., Foster, R., and Chua, N.-H. (1993). Plant bZIP protein DNA binding specificity. J. Mol. Biol. 230, 1131-1144. doi: 10.1006/jmbi.1993.1230
60. Jakoby, M., Weisshaar, B., Dröge-Laser, W., Vicente-Carbajosa, J., Tiedemann, J., Kroj, T., et al. (2002). bZIP transcription factors in Arabidopsis. Trends Plant Sci. 7, 106-111. doi: 10.1016/S1360-1385(01)02223-3
61. Jiang, Y., and Deyholos, M. K. (2009). Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol. Biol. 69, 91-105. doi: 10.1007/s11103-008-9408-3
62. 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. doi: 10.1105/tpc.001404
63. Journot-Catalino, N., Somssich, I. E., Roby, D., and Kroj, T. (2006). The transcription factors WRKY11 and WRKY17 act as negative regulators of basal resistance in Arabidopsis thaliana. Plant Cell 18, 3289-3302. doi: 10.1105/tpc.106.044149
64. Kagaya, Y., Hobo, T., Murata, M., Ban, A., and Hattori, T. (2002). Abscisic acid-induced transcription is mediated by phosphorylation of an abscisic acid response element binding factor, TRAB1. Plant Cell 14, 3177-3189. doi: 10.1105/tpc.005272
65. Kaminaka, H., Nake, C., Epple, P., Dittgen, J., Schutze, K., Chaban, C., et al. (2006). bZIP10-LSD1 antagonism modulates basal defense and cell death in Arabidopsis following infection. EMBO J. 25, 4400-4411. doi: 10.1038/sj.emboj.7601312
66. Kang, S. G., Price, J., Lin, P. C., Hong, J. C., and Jang, J. C. (2010). The Arabidopsis bZIP1 transcription factor is involved in sugar signaling, protein networking, and DNA binding. Mol. Plant 3, 361-373. doi: 10.1093/mp/ssp115
67. Kim, K. C., Lai, Z., Fan, B., and Chen, Z. (2008). Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense. Plant Cell 20, 2357-2371. doi: 10.1105/tpc.107.055566
68. Kirchler, T., Briesemeister, S., Singer, M., Schütze, K., Keinath, M., Kohlbacher, O., et al. (2010). The role of phosphorylatable serine residues in the DNA-binding domain of Arabidopsis bZIP transcription factors. Eur. J. Cell Biol. 89, 175-183. doi: 10.1016/j.ejcb.2009.11.023
69. Kobayashi, Y., Murata, M., Minami, H., Yamamoto, S., Kagaya, Y., Hobo, T., et al. (2005). Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. Plant J. 44, 939-949. doi: 10.1111/j.1365-313X.2005.02583.x
70. Konig, P., and Richmond, T. J. (1993). The X-ray structure of the GCN4-bZIP bound to ATF/CREB site DNA shows the complex depends on DNA flexibility. J. Mol. Biol. 233, 139-154. doi: 10.1006/jmbi.1993.1490
71. Krylov, D., Mikhailenko, I., and Vinson, C. (1994). A thermodynamic scale for leucine zipper stability and dimerization specificity: e and g interhelical interactions. EMBO J. 13, 2849-2861.
72. Kuo, M.-H., Vom Baur, E., Struhl, K., and Allis, C. D. (2000). Gcn4 activator targets Gcn5 histone acetyltransferase to specific promoters independently of transcription. Mol. Cell. 6, 1309-1320. doi: 10.1016/S1097-2765(00)00129-5
73. Lai, Z., Li, Y., Wang, F., Cheng, Y., Fan, B., Yu, J. Q., et al. (2011). Arabidopsis sigma factor binding proteins are activators of the WRKY33 transcription factor in plant defense. Plant Cell 23, 3824-3841. doi: 10.1105/tpc.111.090571
74. Lee, S., Shuman, J. D., Guszczynski, T., Sakchaisri, K., Sebastian, T., Copeland, T. D., et al. (2010). RSK-mediated phosphorylation in the C/EBP leucine zipper regulates DNA binding, dimerization, and growth arrest activity. Mol. Cell. Biol. 30, 2621-2635. doi: 10.1128/MCB.00782-09
75. Li, W., Jain, M. R., Chen, C., Yue, X., Hebbar, V., Zhou, R., et al. (2005). Nrf2 possesses a redox-insensitive nuclear export signal overlapping with the leucine zipper motif. J. Biol. Chem. 280, 28430-28438. doi: 10.1074/jbc.M410601200
76. Liu, J. X., Srivastava, R., Che, P., and Howell, S. H. (2007a). An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28. Plant Cell 19, 4111-4119. doi: 10.1105/tpc.106.050021
77. Liu, X., Bai, X., Wang, X., and Chu, C. (2007b). OsWRKY71, a rice transcription factor, is involved in rice defense response. J. Plant Physiol. 164, 969-979. doi: 10.1016/j.jplph.2006.07.006
78. Liu, J.-X., Srivastava, R., and Howell, S. H. (2008). Stress-induced expression of an activated form of AtbZIP17 provides protection from salt stress in Arabidopsis. Plant Cell Environ. 31, 1735-1743. doi: 10.1111/j.1365-3040.2008.01873.x
79. Liu, Z. Q., Yan, L., Wu, Z., Mei, C., Lu, K., Yu, Y. T., et al. (2012). Cooperation of three WRKY-domain transcription factors WRKY18, WRKY40, and WRKY60 in repressing two ABA-responsive genes ABI4 and ABI5 in Arabidopsis. J. Exp. Bot. 63, 6371-6392. doi: 10.1093/jxb/ers293
80. Luna, E., Bruce, T. J., Roberts, M. R., Flors, V., and Ton, J. (2012). Next-generation systemic acquired resistance. Plant Physiol. 158, 844-853. doi: 10.1104/pp.111.187468
81. 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. doi: 10.1271/bbb.65.2428
82. Mallappa, C., Singh, A., Ram, H., and Chattopadhyay, S. (2008). GBF1, a transcription factor of blue light signaling in Arabidopsis, is degraded in the dark by a proteasome-mediated pathway independent of COP1 and SPA1. J. Biol. Chem. 283, 35772-35782. doi: 10.1074/jbc.M803437200
83. Mangelsen, E., Kilian, J., Berendzen, K. W., Kolukisaoglu, U. H., Harter, K., Jansson, C., et al. (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. doi: 10.1186/1471-2164-9-194
84. Mao, G., Meng, X., Liu, Y., Zheng, Z., Chen, Z., and Zhang, S. (2011). Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23, 1639-1653. doi: 10.1105/tpc.111.084996
85. Matiolli, C. C., Tomaz, J. P., Duarte, G. T., Prado, F. M., Del Bem, L. E. V., Silveira, A. B., et al. (2011). The Arabidopsis bZIP gene AtbZIP63 is a sensitive integrator of transient abscisic acid and glucose signals. Plant Physiol. 157, 692-705. doi: 10.1104/pp.111.181743
86. Menkens, A. E., and Cashmore, A. R. (1994). Isolation and characterization of a fourth Arabidopsis thaliana G-box-binding factor, which has similarities to Fos oncoprotein. Proc. Natl. Acad. Sci. U.S.A. 91, 2522-2526. doi: 10.1073/pnas.91.7.2522
87. 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. doi: 10.1007/s11103-005-2142-1
88. Miao, Y., Laun, T. M., Smykowski, A., and Zentgraf, U. (2007). Arabidopsis MEKK1 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. doi: 10.1007/s11103-007-9198-z
89. Miller, M. (2009). The importance of being flexible: the case of basic region leucine zipper transcriptional regulators. Curr. Protein Pept. Sci. 10, 244-269. doi: 10.2174/138920309788452164
90. Miller, M., Shuman, J. D., Sebastian, T., Dauter, Z., and Johnson, P. F. (2003). Structural basis for DNA recognition by the basic region leucine zipper transcription factor CCAAT/enhancer-binding protein alpha. J. Biol. Chem. 278, 15178-15184. doi: 10.1074/jbc.M300417200
91. Miotto, B., and Struhl, K. (2006). Differential gene regulation by selective association of transcriptional coactivators and bZIP DNA-binding domains. Mol. Cell. Biol. 26, 5969-5982. doi: 10.1128/MCB.00696-06
92. Moitra, J., Szilák, L., Krylov, D., and Vinson, C. (1997). Leucine is the most stabilizing aliphatic amino acid in the d position of a dimeric leucine zipper coiled coil. Biochemistry 36, 12567-12573. doi: 10.1021/bi971424h
93. Newman, J. R. S., and Keating, K. (2003). Comprehensive identification of human bZIP interactions with coiled-coil arrays. Science 300, 2097-2101. doi: 10.1126/science.1084648
94. Nieva, C., Busk, P. K., Domínguez-Puigjaner, E., Lumbreras, V., Testillano, P. S., Risueño, M.-C., et al. (2005). Isolation and functional characterisation of two new bZIP maize regulators of the ABA responsive gene rab28. Plant Mol. Biol. 58, 899-914. doi: 10.1007/s11103-005-8407-x
95. Nijhawan, A., Jain, M., Tyagi, A. K., and Khurana, J. P. (2007). Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol. 146, 333-350. doi: 10.1104/pp.107.112821
96. Niu, X., Renshaw-Gegg, L., Miller, L., and Guiltinan, M. J. (1999). Bipartite determinants of DNA-binding specificity of plant basic leucine zipper proteins. Plant Mol. Biol. 41, 1-13. doi: 10.1023/A:1006206011502
97. Oliphant, A. R., Brandl, C. J., and Struhl, K. (1989). Defining the sequence specificity of DNA-binding proteins by selecting binding sites from random-sequence oligonucleotides: analysis of yeast GCN4 protein. Mol. Cell. Biol. 9, 2944-2949.
98. Orellana, S., Yanez, M., Espinoza, A., Verdugo, I., Gonzalez, E., Ruiz-Lara, S., et al. (2010). The transcription factor SlAREB1 confers drought, salt stress tolerance and regulates biotic and abiotic stress-related genes in tomato. Plant Cell Environ. 33, 2191-2208. doi: 10.1111/j.1365-3040.2010.02220.x
99. Pandey, S. P., and Somssich, I. E. (2009). The role of WRKY transcription factors in plant immunity. Plant Physiol. 150, 1648-1655. doi: 10.1104/pp.109.138990
100. Petitot, A. S., Barsalobres-Cavallari, C., Ramiro, D., Albuquerque Freire, E., Etienne, H., and Fernandez, D. (2013). Promoter analysis of the WRKY transcription factors CaWRKY1a and CaWRKY1b homoeologous genes in coffee (Coffea arabica). Plant Cell Rep. 32, 1263-1276. doi: 10.1007/s00299-013-1440-3
101. Pontier, D., Privat, I., Trifa, Y., Zhou, J.-M., Klessig, D. F., and Lam, E. (2002). Differential regulation of TGA transcription factors by post-transcriptional control. Plant J. 32, 641-653. doi: 10.1046/j.1365-313X.2002.01461.x
102. Popescu, S. C., Popescu, G. V., Bachan, S., Zhang, Z., Gerstein, M., Snyder, M., et al. (2009). MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev. 23, 80-92. doi: 10.1101/gad.1740009
103. Potschin, M., Schlienger, S., Bieker, S., and Zentgraf, U. (2013). Senescence networking: WRKY18 is an upstream regulator, a downstream target gene, and a protein interaction partner of WRKY53. J. Plant Growth Regul. 33, 106-118. doi: 10.1007/s00344-013-9380-2
104. Ren, D., Liu, Y., Yang, K. Y., Han, L., Mao, G., Glazebrook, J., et al. (2008). A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 105, 5638-5643. doi: 10.1073/pnas.0711301105
105. Robatzek, S., and 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, 123-133. doi: 10.1046/j.1365-313X.2001.01131.x
106. Robatzek, S., and Somssich, I. E. (2002). Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes Dev. 16, 1139-1149. doi: 10.1101/gad.222702
107. Rochon, A., Boyle, P., Wignes, T., Fobert, P. R., and Despres, C. (2006). The coactivator function of Arabidopsis NPR1 requires the core of its BTB/POZ domain and the oxidation of C-terminal cysteines. Plant Cell 18, 3670-3685. doi: 10.1105/tpc.106.046953
108. Rook, F., Weisbeek, P., and Smeekens, S. (1998). The light-regulated Arabidopsis bZIP transcription factor gene ATB2 encodes a protein with an unusually long leucine zipper domain. Plant Mol. Biol. 37, 171-178. doi: 10.1023/A:1005964327725
109. Rushton, D. L., Tripathi, P., Rabara, R. C., Lin, J., Ringler, P., Boken, A. K., et al. (2012). WRKY transcription factors: key components in abscisic acid signalling. Plant Biotechnol. J. 10, 2-11. doi: 10.1111/j.1467-7652.2011.00634.x
110. 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. doi: 10.1007/BF00041160
111. Rushton, P. J., Somssich, I. E., Ringler, P., and Shen, Q. J. (2010). WRKY transcription factors. Trends Plant Sci. 15, 247-258. doi: 10.1016/j.tplants.2010.02.006
112. Rushton, P. J., Torres, J. T., Parniske, M., Wernert, P., Hahlbrock, K., and 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, 5690-5700.
113. Scarpeci, T. E., Zanor, M. I., Mueller-Roeber, B., and Valle, E. M. (2013). Overexpression of AtWRKY30 enhances abiotic stress tolerance during early growth stages in Arabidopsis thaliana. Plant Mol. Biol. 83, 265-277. doi: 10.1007/s11103-013-0090-8
114. Schumacher, M. A., Goodman, R. H., and Brennan, R. G. (2000). The structure of a CREB bZIPmiddle dotSomatostatin CRE complex reveals the basis for selective dimerization and divalent cation-enhanced DNA binding. J. Biol. Chem. 275, 35242-35247. doi: 10.1074/jbc.M007293200
115. Seldeen, K. L., Mcdonald, C. B., Deegan, B. J., and Farooq, A. (2008). Coupling of folding and DNA-binding in the bZIP domains of Jun-Fos heterodimeric transcription factor. Arch. Biochem. Biophys. 473, 48-60. doi: 10.1016/j.abb.2008.02.024
116. Shaikhali, J., Noren, L., de Dios Barajas-Lopez, J., Srivastava, V., Konig, J., Sauer, U. H., et al. (2012). Redox-mediated mechanisms regulate DNA binding activity of the G-group of basic region leucine zipper (bZIP) transcription factors in Arabidopsis. J. Biol. Chem. 287, 27510-27525. doi: 10.1074/jbc.M112.361394
117. Shang, Y., Yan, L., Liu, Z. Q., 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, 1909-1935. doi: 10.1105/tpc.110.073874
118. Shen, H., Cao, K., and Wang, X. (2007). A conserved proline residue in the leucine zipper region of AtbZIP34 and AtbZIP61 in Arabidopsis thaliana interferes with the formation of homodimer. Biochem. Biophys. Res. Commun. 362, 425-430. doi: 10.1016/j.bbrc.2007.08.026
119. Shen, H., Cao, K., and Wang, X. (2008). AtbZIP16 and AtbZIP68, two new members of GBFs, can interact with other G group bZIPs in Arabidopsis thaliana. BMB Rep. 41, 132-138. doi: 10.5483/BMBRep.2008.41.2.132
120. Shen, Y. Y., Wang, X. F., Wu, F. Q., Du, S. Y., Cao, Z., Shang, Y., et al. (2006). The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443, 823-826. doi: 10.1038/nature05176
121. Singh, A., Ram, H., Abbas, N., and Chattopadhyay, S. (2012). Molecular interactions of GBF1 with HY5 and HYH proteins during light-mediated seedling development in Arabidopsis thaliana. J. Biol. Chem. 287, 25995-26009. doi: 10.1074/jbc.M111.333906
122. Sirichandra, C., Davanture, M., Turk, B. E., Zivy, M., Valot, B., Leung, J., et al. (2010). The Arabidopsis ABA-activated kinase OST1 phosphorylates the bZIP transcription factor ABF3 and creates a 14-3-3 binding site involved in its turnover. PLoS ONE 5:e13935. doi: 10.1371/journal.pone.0013935
123. Smykowski, A., Zimmermann, P., and Zentgraf, U. (2010). G-box binding factor1 reduces CATALASE2 expression and regulates the onset of leaf senescence in Arabidopsis. Plant Physiol. 153, 1321-1331. doi: 10.1104/pp.110.157180
124. Suttipanta, N., Pattanaik, S., Kulshrestha, M., Patra, B., Singh, S. K., and Yuan, L. (2011). The transcription factor CrWRKY1 positively regulates the terpenoid indole alkaloid biosynthesis in Catharanthus roseus. Plant Physiol. 157, 2081-2093. doi: 10.1104/pp.111.181834
125. Tsugama, D., Liu, S., and Takano, T. (2012). A bZIP protein, VIP1, is a regulator of osmosensory signaling in Arabidopsis. Plant Physiol. 159, 144-155. doi: 10.1104/pp.112.197020
126. 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. doi: 10.1105/tpc.104.024810
127. Ulker, B., and Somssich, I. E. (2004). WRKY transcription factors: from DNA binding towards biological function. Curr. Opin. Plant Biol. 7, 491-498. doi: 10.1016/j.pbi.2004.07.012
128. Uno, Y., Furihata, T., Abe, H., Yoshida, R., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2000). Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc. Natl. Acad. Sci. U.S.A. 97, 11632-11637. doi: 10.1073/pnas.190309197
129. Vinson, C., Acharya, A., and Taparowsky, E. J. (2006). Deciphering B-ZIP transcription factor interactions in vitro and in vivo. Biochim. Biophys. Acta 1759, 4-12. doi: 10.1016/j.bbaexp.2005.12.005
130. Vinson, C., Myakishev, M., Acharya, A., Mir, A. A., Moll, J. R., and Bonovich, M. (2002). Classification of human B-ZIP proteins based on dimerization properties. Mol. Cell. Biol. 22, 6321-6335. doi: 10.1128/MCB.22.18.6321-6335.2002
131. Wang, C., Deng, P., Chen, L., Wang, X., Ma, H., Hu, W., et al. (2013). A wheat WRKY transcription factor TaWRKY10 confers tolerance to multiple abiotic stresses in transgenic tobacco. PLoS ONE 8:e65120. doi: 10.1371/journal.pone.0065120
132. Wang, D., Amornsiripanitch, N., and Dong, X. (2006). A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathog. 2:e123. doi: 10.1371/journal.ppat.0020123
133. Wang, J. N., Kuang, J. F., Shan, W., Chen, J., Xie, H., Lu, W. J., et al. (2012). Expression profiles of a banana fruit linker histone H1 gene MaHIS1 and its interaction with a WRKY transcription factor. Plant Cell Rep. 31, 1485-1494. doi: 10.1007/s00299-012-1263-7
134. Wei, K., Chen, J., Wang, Y., Chen, Y., Chen, S., Lin, Y., et al. (2012). Genome-wide analysis of bZIP-encoding genes in maize. DNA Res. 19, 463-476. doi: 10.1093/dnares/dss026
135. Weltmeier, F., Ehlert, A., Mayer, C. S., Dietrich, K., Wang, X., Schutze, K., et al. (2006). Combinatorial control of Arabidopsis proline dehydrogenase transcription by specific heterodimerisation of bZIP transcription factors. EMBO J. 25, 3133-3143. doi: 10.1038/sj.emboj.7601206
136. Weltmeier, F., Rahmani, F., Ehlert, A., Dietrich, K., Schütze, K., Wang, X., et al. (2008). Expression patterns within the Arabidopsis C/S1 bZIP transcription factor network: availability of heterodimerization partners controls gene expression during stress response and development. Plant Mol. Biol. 69, 107-119. doi: 10.1007/s11103-008-9410-9
137. Wiese, A., Elzinga, N., Wobbes, B., and Smeekens, S. (2004). A conserved upstream open reading frame mediates sucrose-induced repression of translation. Plant Cell 16, 1717-1729. doi: 10.1105/tpc.019349
138. Williams, M. E., Foster, R., and Chua, N.-H. (1992). Sequences flanking the hexameric G-box core CACGTG affect the specificity of protein binding. Plant Cell 4, 485-496. doi: 10.1105/tpc.4.4.485
139. Xu, X., Chen, C., Fan, B., and Chen, Z. (2006). Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. Plant Cell 18, 1310-1326. doi: 10.1105/tpc.105.037523
140. Yamada, Y., and Sato, F. (2013). Transcription factors in alkaloid biosynthesis. Int. Rev. Cell Mol. Biol. 305, 339-382. doi: 10.1016/B978-0-12-407695-2.00008-1
141. 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, 944-956. doi: 10.1105/tpc.104.026435
142. 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, 7683-7691. doi: 10.1074/jbc.M111.279844
143. Yang, Z., Patra, B., Li, R., Pattanaik, S., and Yuan, L. (2013). Promoter analysis reveals cis-regulatory motifs associated with the expression of the WRKY transcription factor CrWRKY1 in Catharanthus roseus. Planta. doi: 10.1007/s00425-013-1949-2 [Epub ahead of print].
144. Zentgraf, U., Laun, T., and Miao, Y. (2010). The complex regulation of WRKY53 during leaf senescence of Arabidopsis thaliana. Eur. J. Cell Biol. 89, 133-137. doi: 10.1016/j.ejcb.2009.10.014
145. Zhang, Y., and Wang, L. (2005). The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evol. Biol. 5:1. doi: 10.1186/1471-2148-5-1
146. 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. doi: 10.1104/pp.103.034967
147. Zheng, Z., Qamar, S. A., Chen, Z., and Mengiste, T. (2006). Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J. 48, 592-605. doi: 10.1111/j.1365-313X.2006.02901.x
148. Zhou, X., Jiang, Y., and Yu, D. (2011). WRKY22 transcription factor mediates dark-induced leaf senescence in Arabidopsis. Mol. Cells 31, 303-313. doi: 10.1007/s10059-011-0047-1
149. Zou, M., Guan, Y., Ren, H., Zhang, F., and Chen, F. (2007). Characterization of alternative splicing products of bZIP transcription factors OsABI5. Biochem. Biophys. Res. Commun. 360, 307-313. doi: 10.1016/j.bbrc.2007.05.226