WRKY transcription factor

WRKY transcription factors (pronounced ‘worky’) are proteins that bind DNA. They are transcription factors that regulate many processes in plants and algae (Viridiplantae), such as the responses to biotic and abiotic stresses, senescence, seed dormancy and seed germination and some developmental processes[1][2] but also contribute to secondary metabolism.[3]

Like many transcription factors, WRKY transcription factors are defined by the presence of a DNA-binding domain; in this case, it is the WRKY domain. The WRKY domain was named in 1996 after the almost invariant WRKY amino acid sequence at the N-terminus and is about 60 residues in length. In addition to containing the ‘WRKY signature’, WRKY domains also possess an atypical zinc-finger structure at the C-terminus (either Cx4-5Cx22-23HxH or Cx7Cx23HxC). Most WRKY transcription factors bind to the W-box promoter element that has a consensus sequence of TTGACC/T.

Individual WRKY proteins do appear in the human protozoan parasite Giardia lamblia and slime mold Dictyostelium discoideum.[4]

Structural diversity

WRKY transcription factors are denoted by a 60-70 amino acid WRKY protein domain composed of a conserved WRKYGQK motif and a zinc-finger region.[5] Based on the amino acid sequence WRKY transcription factors are classified into three major categories, group I, group II, and group III. Group I WRKY proteins are primarily denoted by the presence of two WRKY protein domains, whereas both groups II and III each possess only one domain. Group III WRKY proteins have a C2HC zinc finger instead of the C2H2 motif of group I and II factors. The structure of several plant WRKY domains has been elucidated using crystallography[6] and nuclear magnetic resonance spectroscopy.[7]

The different groups of WRKY Domains in flowering plants

As soon as the WRKY domain was characterized, it was suggested that it contained a novel zinc finger structure and the first evidence to support this came from studies with 2-phenanthroline that chelates zinc ions. Addition of 2-phenenthroline[check spelling] to gel retardation assays that contained E. coli expressed WRKY proteins resulted in a loss of binding to the W-box target sequence. The other suggestion was that the WRKY signature amino acid sequence at the N-terminus of the WRKY domain directly binds to the W-box sequence in the DNA of target promoters. These suggestions were shown to be correct by publication of the solution structure of the C-terminal WRKY domain of the Arabidopsis WRKY4 protein. The WRKY domain was found to form a four-stranded β-sheet.[8] Soon afterwards, a crystal structure of the C-terminal WRKY domain of the Arabidopsis WRKY1 protein was reported. This showed a similar result to the solution structure except that it may contain an additional β-strand at the N-terminus of the domain.[9] From these two studies it appears that the conserved WRKYGQK signature amino acid sequence enters the major groove of the DNA to bind to the W-Box. Recently, the first structural determination of the WRKY domain complexed with a W-Box was reported. The NMR solution structure of the WRKY DNA-binding domain of Arabidopsis WRKY4 in complex with W Box DNA revealed that part of a four-stranded β-sheet enters the major groove of DNA in an atypical mode that the authors named the β-wedge, where this sheet is almost perpendicular to the DNA helical axis. As initially predicted, amino acids in the conserved WRKYGQK signature motif contact the W Box DNA bases mainly through extensive apolar contacts with thymine methyl groups. These structural data explain the conservation of both the WRKY signature sequence at the N-terminus of the WRKY domain and the conserved cysteine and histidine residues. It also provides the molecular basis for the previously noted remarkable conservation of both the WRKY amino acid signature sequence and the W Box DNA sequence.[10]

History

In 1994 and 1995, the first two reports of WRKY transcription factors appeared. They described newly discovered but as yet ill-defined DNA binding proteins that played potential roles in the regulation of gene expression by sucrose (SPF1) [11] or during germination (ABF1 and ABF2).[12] A third report appeared in 1996 that identified WRKY1, WRKY2 and WRKY3 from parsley. The authors named the new transcription factor family the WRKY family (pronounced ‘worky’) after a conserved amino acid sequence at the N-terminus of the DNA-binding domain.[13] The parsley WRKY proteins also provided the first evidence that WRKY transcription factors play roles in regulating plant responses to pathogens. Numerous papers have now shown this to be a major function of WRKY transcription factors. Since these initial publications, it has become clear that the WRKY family is among the ten largest families of transcription factors in higher plants and that these transcription factors play key roles in regulating a number of plant processes including the responses to biotic and abiotic stresses, germination, senescence, and some developmental processes.[14]

Evolution

WRKY transcription factor genes are found throughout the plant lineage and also outside of the plant lineage in some diplomonads, social amoebae, fungi incertae sedis, and amoebozoa.[15] This patchy distribution suggests that lateral gene transfer is responsible. These lateral gene transfer events appear to pre-date the formation of the WRKY groups in flowering plants, where there are seven well-defined groups, Groups I + IIc, Groups IIa + IIb, Groups IId + IIe, and Group III. Flowering plants also contain proteins with domains typical for both resistance (R) proteins and WRKY transcription factors. R protein-WRKY genes have evolved numerous times in flowering plants, each type being restricted to specific flowering plant lineages. These chimeric proteins contain not only novel combinations of protein domains but also novel combinations and numbers of WRKY domains.

Several early reports proposed that a group I WRKY transcription factor was the progenitor of the family.[16] It was thought that a single group I WRKY domain occurred first and then duplicated to form the original ancestral WRKY transcription factor. However, more recent evidence suggests that WRKY transcription factors evolved from a single group IIc-like gene, which then diversified into group I, group IIc, and group IIa+b domains.[17] The original WRKY protein domain has been proposed to have arisen from the GCM1 and FLYWCH zinc finger factors.[18] GCM1 and FLYWCH are proposed ancestral proteins base on their crystal structural similarity to the WRKY domain.[19] Both GCM1 and FLYWCH belong to families of DNA-binding factors found in metazoan. The plant specific NAC transcription factor family also shares a common structural shape and origin with WRKY transcription factors.[20]

During plant evolution the WRKY family has dramatically expanded, which is proposed to be a result of through duplication.[21] Some species including Arabidopsis thaliana, rice (Oryza sativa), and tomato (Solanum lycopersicum) have WRKY groups which dramatically expanded and diversified in recent evolutionary history.[22] However, differences in expression, not variation in gene sequences, have likely lead to the diverse functions of WRKY genes.[23] Such a model is plausible as WRKY family members are part of numerous phytohormone, developmental, and defense signaling transcriptional networks. Furthermore, W-box elements for WRKY binding occur in promoters of many other WRKY transcription factors [24] indicating not simply a hierarchical rank in gene activation, but also which genes may have arisen later during evolution after initial WRKY regulatory networks were established.

Phylogenetic tree of WRKY transcription factors from the plant kingdom and beyond.

Function

Over the last two decades great effort has been invested in characterizing WRKY transcription factors. The results show that WRKY transcription factors function in a diverse array of plant response, both to internal and external cues.

Plant development

Studies have demonstrated the function of WRKY transcription factors in plant development. Successful male gametogenesis and tolerance to interploidy crosses both require WRKY transcription factors.[25] Embryo and root development also require WRKY transcription factors.[26] WRKYs also contribute to determination of seed size and seed coat color in Arabidopsis.[27] Furthermore, WRKY transcription factors have been shown to play key roles in regulation of developmentally programmed leaf senescence.[28]

Abiotic and biotic stresses

One of the most notorious roles of the WRKY transcription factor family is the regulation of plant stress tolerance. WRKYs participate in nearly every aspect of plant defense to abiotic and biotic stressors. WRKYs are known to regulate cold,[29] drought,[30] flooding,[31] heat,[32] heavy metal toxicity,[33] low humidity,[34] osmotic,[35] oxidative,[36] salt [37] and UV [38] stresses. Likewise, WRKY transcription factors play an essential role in plant tolerance to biotic stresses, protecting against innumerable viruses,[39] bacterial [40] and fungal [41] pathogens, as well as insect herbivory.[42] Plants are believed to perceive pathogens via pathogen-associated molecular pattern (PAMP) triggered immunity and effector-triggered immunity. WRKY transcription factors participate in regulating responses to pathogens by targeting PAMP [43] and effector [44] triggered immunity.

Hormone signaling

WRKY transcription factors function through a variety of plant hormone signaling cascades. Over half of Arabidopsis thaliana WRKY transcription factors respond to salicylic acid treatment.[45] At least 25% of WRKY transcription factors from Madagascar periwinkle (Catharanthus roseus) are responsive to jasmonate.[46] Similarly, in grape (Vitis vinifera) 63%, 73%, 76%, and 81% or WRKY transcription factors are responsive to salicylic acid, ethylene, abscisic acid, and jasmonate treatment, respectively.[47] In Arabidopsis thaliana, two important WRKY transcription factors are WRKY57 and WRKY70. WRKY57 mediates crosstalk between jasmonate and auxin signaling cascades,[48] whereas WRKY70 moderates signaling between the jasmonate and salicylic acid pathways.[49] Arabidopsis thaliana WRKY23 functions downstream of auxin signaling to positively activate expression of flavonols, which function as polar auxin transport inhibitors, to negatively feedback and suppress further auxin responses.[50] Several WRKY transcription factors also respond to gibberellin treatment.[51]

Primary and secondary metabolism

Due to difficulty in measuring phenotypes, less is known about the roles of WRKY transcription factors in plant metabolism.[52] The earliest reports identified WRKYs based on their ability to regulate β-amylase, a gene involved in catabolism of starch into sugars.[53] Since then, WRKY transcription factors have also been shown to regulate phosphate acquisition[54] and tolerance to arsenic.[55] Additionally, WRKYs are needed for proper expression of lignin biosynthetic pathway genes, which form products necessary for cell wall and xylem formation.[56] Analysis of WRKY transcription factors from numerous plant species indicates the importance of the family in regulating secondary metabolism.[57] WRKY transcription factors also play a role in regulating pathways for the biosynthesis of pharmaceutically valuable plant-specialized metabolites.[58] Efforts to use WRKY transcription factors to improve production of the valuable anti-malarial drug artemisinin have been successful.[59]

Mode of action

A long-standing question of in the field of transcriptional regulation is how large families of regulators binding a consensus DNA sequences dictate expression of different target genes. The WRKY transcription factor family has long exemplified this problem. Plant species contain numerous WRKY transcription factors which predominantly recognize a conserved cis-element. Only recently has it begun to be revealed how different WRKY transcription factors regulate unique sets of target genes.

Variation in cis-element recognition

Early work indicated that the WRKY family could bind W-box (T/A)TGAC(T/A).[60] Later, a barley (Hordeum vulgare) WRKY transcription factor, SUSIBA2, was found to bind the Sugar Response Element (TAAAGATTACTAATAGGAA), illustrating some diversity exists in DNA sequence which WRKYs could recognize.[61] Since then, WRKYs have been found to bind a more generic GAC core cis-element with flanking sequences dictating DNA-protein interactions.[62] On the protein side differences in the consensus motif and downstream arginine or lysine residues dictate the exact flanking sequence recognized.[63] Additionally, contrary to early reports, both WRKY domains of group I family members can bind DNA.[64] Implications of these results are still being resolved.

Protein-protein interactions

One mechanism for determining WRKY binding activity is by protein-protein interactions. WRKY transcription factors have been found to interact with a variety of proteins, some of which occur by a group specific manner. Recent evidence suggests that VQ protein family is an important regulator of group I and group IIc WRKY transcription factors.[65] VQ proteins appear to bind the WRKY domain, thus inhibiting protein-DNA interactions. At least one WRKY transcription factor, Arabidopsis WRKY57, interacts with jasmonate ZIM-domain (JAZ) and auxin/indole acetic acid (AUX/IAA) repressor of the jasmonate and auxin signaling cascade, respectively, indicating a point of crosstalk between these phytohormones.[66] Other WRKYs interact with histone deacetylases.[67] Group IIa WRKY factors form homodimers and heterodimers within the subgroup and with other group II subgroups.[68] Group IId WRKY transcription factors typically possess a domain allowing interaction with calcium bound calmodulin.[69]

Phosphorylation

Protein phosphorylation is a common method to regulate protein activity and WRKY transcription factors are no exception. WRKY gene involved in plant defense,[70] hormone signaling,[71] and secondary metabolism [72] are regulated by phosphorylation via mitogen-activated protein kinase (MAPK) cascades. Additionally, a MAPK can phosphorylate a VQ protein, freeing the WRKY transcription factor for target gene activation.[73] While kinases phosphorylating WRKY transcription factors are known, phosphatases removing phosphate groups have yet to be identified.

Proteasomeal degradation

Protein degradation via the proteasome is a common feature in plant regulatory networks to limit the duration of activation or repression by transcription factors. WRKY transcription factors have also been found to be regulated by proteasomal degradation mechanisms. In Chinese grapevine (Vitis pseudoreticulata) ERYSIPHE NECATOR-INDUCED RING FINGER PROTEIN1 targets WRKY11 for degradation leading to enhanced powdery mildew resistance.[74] In rice, WRKY45 is degraded by the proteasome although the E3 ubiquitin ligase responsible remains unknown [75]

References

  1. ^ Rushton PJ, Somssich IE, Ringler P, Shen QJ: WRKY transcription factors. Trends in plant science 2010, 15(5):247-258
  2. ^ Bakshi and Oelmüller (2014) WRKY transcription factors: Jack of many trades in plants. Plant Signaling & Behavior. 9(1). e27700
  3. ^ Schluttenhofer and Yuan (2014) Regulation of Specialized Metabolism by WRKY Transcription Factors. Plant Physiology.
  4. ^ Wu, Guo, Wang and Li (2005) The WRKY Family of Transcription Factors in Rice and Arabidopsis and Their Origins. DNA Research. 12(1). 9-26
  5. ^ Eulgem, Rushton, Robatzek and Somssich (2000) The WRKY superfamily of plant transcription factors. Trends in Plant Science. 5(5). 199-206
  6. ^ Duan, Nan, Liang, Mao, Lu, et al. (2007) DNA binding mechanism revealed by high resolution crystal structure of Arabidopsis thaliana WRKY1 protein. Nucleic Acids Research. 35(4). 1145-1154
  7. ^ Yamasaki, Kigawa, Inoue, Tateno, Yamasaki, et al. (2005) Solution Structure of an Arabidopsis WRKY DNA Binding Domain. The Plant Cell. 17(3). 944-956, Yamasaki, Kigawa, Watanabe, Inoue, Yamasaki, et al. (2012) Structural Basis for Sequence-specific DNA Recognition by an Arabidopsis WRKY Transcription Factor. Journal of Biological Chemistry. 287(10). 7683-7691
  8. ^ 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
  9. ^ Duan MR, Nan J, Liang YH, Mao P, Lu L, Li L, Wei C, Lai L, Li Y and Su XD (2007) DNA binding mechanism revealed by high resolution crystal structure of Arabidopsis thaliana WRKY1 protein. Nucleic Acids Res. 35:1145-1154
  10. ^ Eulgem T, Rushton PJ, Robatzek S and Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199-206
  11. ^ 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
  12. ^ Rushton, P.J. et al. (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
  13. ^ 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
  14. ^ Eulgem, T. and Somssich, I.E. (2007) Networks of WRKY transcription factors in defense signaling. Curr. Opin. Plant Biol. 10, 366–371, Ulker, B. and Somssich, I.E. (2004) WRKY transcription factors: from DNA binding towards biological function. Curr. Opin. Plant Biol. 7, 491–498
  15. ^ Charles I. Rinerson, Roel C. Rabara, Prateek Tripathi Qingxi J Shen, and Paul J. Rushton (2015) Structure and evolution of WRKY transcription factors. In Plant Transcription Factors: Evolutionary, Structural and Functional Aspects Edited by: Daniel H. Gonzalez. Elsevier
  16. ^ Wu, Guo, Wang and Li (2005) The WRKY Family of Transcription Factors in Rice and Arabidopsis and Their Origins. DNA Research. 12(1). 9-26, Zhang and Wang (2005) The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evolutionary Biology. 5(1). 1
  17. ^ Brand, Fischer, Harter, Kohlbacher and Wanke (2013) Elucidating the evolutionary conserved DNA-binding specificities of WRKY transcription factors by molecular dynamics and in vitro binding assays. Nucleic Acids Research. 41(21). 9764-9778
  18. ^ Babu, Iyer, Balaji and Aravind (2006) The natural history of the WRKY–GCM1 zinc fingers and the relationship between transcription factors and transposons. Nucleic Acids Research. 34(22). 6505-6520
  19. ^ Babu, Iyer, Balaji and Aravind (2006) The natural history of the WRKY–GCM1 zinc fingers and the relationship between transcription factors and transposons. Nucleic Acids Research. 34(22). 6505-6520
  20. ^ Welner, Lindemose, Grossmann, Møllegaard, Olsen, et al. (2012) DNA binding by the plant-specific NAC transcription factors in crystal and solution: a firm link to WRKY and GCM transcription factors. Biochemical Journal. 444(3). 395-404
  21. ^ Wu, Guo, Wang and Li (2005) The WRKY Family of Transcription Factors in Rice and Arabidopsis and Their Origins. DNA Research. 12(1). 9-26
  22. ^ Wu, Guo, Wang and Li (2005) The WRKY Family of Transcription Factors in Rice and Arabidopsis and Their Origins. DNA Research. 12(1). 9-26, Eulgem, Rushton, Robatzek and Somssich (2000) The WRKY superfamily of plant transcription factors. Trends in Plant Science. 5(5). 199-206, Zhang and Wang (2005) The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evolutionary Biology. 5(1). 1, Huang, Gao, Liu, Peng, Niu, et al. (2012) Genome-wide analysis of WRKY transcription factors in Solanum lycopersicum. Molecular Genetics and Genomics. 287(6). 495-513
  23. ^ Babu, Iyer, Balaji and Aravind (2006) The natural history of the WRKY–GCM1 zinc fingers and the relationship between transcription factors and transposons. Nucleic Acids Research. 34(22). 6505-6520
  24. ^ Dong, Chen and Chen (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Molecular Biology. 51(1). 21-37
  25. ^ Guan, Meng, Khanna, Lamontagne, Liu, et al. (2014) Phosphorylation of a WRKY Transcription Factor by MAPKs Is Required for Pollen Development and Function in Arabidopsis. PLoS Genet. 10(5). e1004384, Dilkes, Spielman, Weizbauer, Watson, Burkart-Waco, et al. (2008) The maternally expressed WRKY transcription factor TTG2 controls lethality in interploidy crosses of Arabidopsis. PLoS biology. 6(12).
  26. ^ Grunewald, De Smet, Lewis, Löfke, Jansen, et al. (2012) Transcription factor WRKY23 assists auxin distribution patterns during Arabidopsis root development through local control on flavonol biosynthesis. Proceedings of the National Academy of Sciences. 109(5). 1554-1559, Grunewald, De Smet, De Rybel, Robert, Van De Cotte, et al. (2013) Tightly controlled WRKY23 expression mediates Arabidopsis embryo development. EMBO Reports. 14(12). 1136-1142, Devaiah, Karthikeyan and Raghothama (2007) WRKY75 Transcription Factor Is a Modulator of Phosphate Acquisition and Root Development in Arabidopsis. Plant Physiology. 143(4). 1789-1801
  27. ^ Johnson, Kolevski and Smyth (2002) TRANSPARENT TESTA GLABRA2, a Trichome and Seed Coat Development Gene of Arabidopsis, Encodes a WRKY Transcription Factor. The Plant Cell. 14(6). 1359-1375, Luo, Dennis, Berger, Peacock and Chaudhury (2005) MINISEED3 (MINI3), a WRKY family gene, and HAIKU2 (IKU2), a leucine-rich repeat (LRR) KINASE gene, are regulators of seed size in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America. 102(48). 17531-17536
  28. ^ Robatzek and Somssich (2001) A new member of the Arabidopsis WRKY transcription factor family, AtWRKY6, is associated with both senescence- and defence-related processes. The Plant Journal. 28(2). 123-133, Besseau, Li and Palva (2012) WRKY54 and WRKY70 co-operate as negative regulators of leaf senescence in Arabidopsis thaliana. Journal of Experimental Botany. 63(7). 2667-2679, Miao and Zentgraf (2007) The Antagonist Function of Arabidopsis WRKY53 and ESR/ESP in Leaf Senescence Is Modulated by the Jasmonic and Salicylic Acid Equilibrium. The Plant Cell Online. 19(3). 819-830
  29. ^ Yokotani, Sato, Tanabe, Chujo, Shimizu, et al. (2013) WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance. Journal of Experimental Botany. 64(16). 5085-5097, Niu, Wei, Zhou, Tian, Hao, et al. (2012) Wheat WRKY genes TaWRKY2 and TaWRKY19 regulate abiotic stress tolerance in transgenic Arabidopsis plants. Plant, Cell & Environment. 35(6). 1156-1170, Zhou, Tian, Zou, Xie, Lei, et al. (2008) Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnology Journal. 6(5). 486-503
  30. ^ Niu, Wei, Zhou, Tian, Hao, et al. (2012) Wheat WRKY genes TaWRKY2 and TaWRKY19 regulate abiotic stress tolerance in transgenic Arabidopsis plants. Plant, Cell & Environment. 35(6). 1156-1170, Zhou, Tian, Zou, Xie, Lei, et al. (2008) Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnology Journal. 6(5). 486-503, Ren, Chen, Liu, Zhang, Zhang, et al. (2010) ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. The Plant Journal. 63(3). 417-429
  31. ^ Hsu, Chou, Chou, Li, Peng, et al. (2013) Submergence Confers Immunity Mediated by the WRKY22 Transcription Factor in Arabidopsis. The Plant Cell Online. 25(7). 2699-2713
  32. ^ Li, Fu, Huang and Yu (2009) Functional analysis of an Arabidopsis transcription factor WRKY25 in heat stress. Plant Cell Reports. 28(4). 683-693, Li, Zhou, Chen, Huang and Yu (2010) Functional characterization of Arabidopsis thaliana WRKY39 in heat stress. Molecules and Cells. 29(5). 475-483
  33. ^ Ding, Yan, Xu, Li and Zheng (2013) WRKY46 functions as a transcriptional repressor of ALMT1, regulating aluminum-induced malate secretion in Arabidopsis. The Plant Journal. 76(5). 825-835
  34. ^ Noutoshi, Ito, Seki, Nakashita, Yoshida, et al. (2005) A single amino acid insertion in the WRKY domain of the Arabidopsis TIR–NBS–LRR–WRKY-type disease resistance protein SLH1 (sensitive to low humidity 1) causes activation of defense responses and hypersensitive cell death. The Plant Journal. 43(6). 873-888
  35. ^ Zhou, Tian, Zou, Xie, Lei, et al. (2008) Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnology Journal. 6(5). 486-503, Vanderauwera, Vandenbroucke, Inzé, Van De Cotte, Mühlenbock, et al. (2012) AtWRKY15 perturbation abolishes the mitochondrial stress response that steers osmotic stress tolerance in Arabidopsis. Proceedings of the National Academy of Sciences. 109(49). 20113-20118, Li, Besseau, Törönen, Sipari, Kollist, et al. (2013) Defense-related transcription factors WRKY70 and WRKY54 modulate osmotic stress tolerance by regulating stomatal aperture in Arabidopsis. New Phytologist. 200(2). 457-472
  36. ^ Liu, Hong, Zhang, Li, Huang, et al. (2014) Tomato WRKY transcriptional factor SlDRW1 is required for disease resistance against Botrytis cinerea and tolerance to oxidative stress. Plant Science. 227(0). 145-156, Gong, Hu and Liu (2014) Cloning and characterization of FcWRKY40, A WRKY transcription factor from Fortunella crassifolia linked to oxidative stress tolerance. Plant Cell, Tissue and Organ Culture. 119(1). 197-210
  37. ^ Niu, Wei, Zhou, Tian, Hao, et al. (2012) Wheat WRKY genes TaWRKY2 and TaWRKY19 regulate abiotic stress tolerance in transgenic Arabidopsis plants. Plant, Cell & Environment. 35(6). 1156-1170, Zhou, Tian, Zou, Xie, Lei, et al. (2008) Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnology Journal. 6(5). 486-503, Li, Gao, Xu, Dai, Deng, et al. (2013) ZmWRKY33, a WRKY maize transcription factor conferring enhanced salt stress tolerances in Arabidopsis. Plant Growth Regulation. 70(3). 207-216, Qin, Tian, Han and Yang (2013) Constitutive expression of a salinity-induced wheat WRKY transcription factor enhances salinity and ionic stress tolerance in transgenic Arabidopsis thaliana. Biochemical and Biophysical Research Communications. 441(2). 476-481
  38. ^ Wang, Hao, Chen, Hao, Wang, et al. (2007) Overexpression of rice WRKY89 enhances ultraviolet B tolerance and disease resistance in rice plants. Plant Molecular Biology. 65(6). 799-815
  39. ^ Liu, Schiff and Dinesh-Kumar (2004) Involvement of MEK1 MAPKK, NTF6 MAPK, WRKY/MYB transcription factors, COI1 and CTR1 in N-mediated resistance to tobacco mosaic virus. The Plant Journal. 38(5). 800-809, Yoda, Ogawa, Yamaguchi, Koizumi, Kusano, et al. (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. Molecular Genetics and Genomics. 267(2). 154-161
  40. ^ Zheng, Mosher, Fan, Klessig and Chen (2007) Functional analysis of Arabidopsis WRKY25 transcription factor in plant defense against Pseudomonas syringae. BMC Plant Biology. 7(1). 2, Hu, Dong and Yu (2012) Arabidopsis WRKY46 coordinates with WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. Plant Science. 185(288-297, Deslandes, Olivier, Peeters, Feng, Khounlotham, et al. (2003) Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proceedings of the National Academy of Sciences. 100(13). 8024-8029
  41. ^ Liu, Hong, Zhang, Li, Huang, et al. (2014) Tomato WRKY transcriptional factor SlDRW1 is required for disease resistance against Botrytis cinerea and tolerance to oxidative stress. Plant Science. 227(0). 145-156, Shimono, Sugano, Nakayama, Jiang, Ono, et al. (2007) Rice WRKY45 Plays a Crucial Role in Benzothiadiazole-Inducible Blast Resistance. The Plant Cell Online. 19(6). 2064-2076, Zheng, Qamar, Chen and Mengiste (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. The Plant Journal. 48(4). 592-605
  42. ^ Skibbe, Qu, Galis and Baldwin (2008) Induced Plant Defenses in the Natural Environment: Nicotiana attenuata WRKY3 and WRKY6 Coordinate Responses to Herbivory. Plant Cell. 20(7). 1984-2000, Grunewald, Karimi, Wieczorek, Van De Cappelle, Wischnitzki, et al. (2008) A Role for AtWRKY23 in Feeding Site Establishment of Plant-Parasitic Nematodes. Plant Physiology. 148(1). 358-368
  43. ^ Asai, Tena, Plotnikova, Willmann, Chiu, et al. (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature. 415(6875). 977-983
  44. ^ Deslandes, Olivier, Peeters, Feng, Khounlotham, et al. (2003) Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proceedings of the National Academy of Sciences. 100(13). 8024-8029
  45. ^ Dong, Chen and Chen (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Molecular Biology. 51(1). 21-37
  46. ^ Schluttenhofer, Pattanaik, Patra and Yuan (2014) Analyses of Catharanthus roseus and Arabidopsis thaliana WRKY transcription factors reveal involvement in jasmonate signaling. BMC Genomics. 15(1). 502
  47. ^ Guo, Guo, Xu, Gao, Li, et al. (2014) Evolution and expression analysis of the grape (Vitis vinifera L.) WRKY gene family. Journal of Experimental Botany. 65(6). 1513-1528
  48. ^ Jiang, Liang, Yang and Yu (2014) Arabidopsis WRKY57 Functions as a Node of Convergence for Jasmonic Acid– and Auxin-Mediated Signaling in Jasmonic Acid–Induced Leaf Senescence. The Plant Cell. 26(1). 230-245
  49. ^ Li, Brader and Palva (2004) The WRKY70 Transcription Factor: A Node of Convergence for Jasmonate-Mediated and Salicylate-Mediated Signals in Plant Defense. Plant Cell. 16(2). 319-331
  50. ^ Grunewald, De Smet, Lewis, Löfke, Jansen, et al. (2012) Transcription factor WRKY23 assists auxin distribution patterns during Arabidopsis root development through local control on flavonol biosynthesis. Proceedings of the National Academy of Sciences. 109(5). 1554-1559
  51. ^ Suttipanta, Pattanaik, Kulshrestha, Patra, Singh, et al. (2011) The Transcription Factor CrWRKY1 Positively Regulates the Terpenoid Indole Alkaloid Biosynthesis in Catharanthus roseus. Plant Physiology. 157(4). 2081-2093, Xie, Zhang, Zou, Yang, Komatsu, et al. (2006) Interactions of two abscisic-acid induced WRKY genes in repressing gibberellin signaling in aleurone cells. The Plant Journal. 46(2). 231-242
  52. ^ Schluttenhofer and Yuan (2014) Regulation of Specialized Metabolism by WRKY Transcription Factors. Plant Physiology.
  53. ^ Ishiguro and Nakamura (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 β-amylase from sweet potato. Molecular and General Genetics. 244(6). 563-571
  54. ^ Devaiah, Karthikeyan and Raghothama (2007) WRKY75 Transcription Factor Is a Modulator of Phosphate Acquisition and Root Development in Arabidopsis. Plant Physiology. 143(4). 1789-1801, Wang, Xu, Kong, Chen, Duan, et al. (2014) Arabidopsis WRKY45 Transcription Factor Activates PHOSPHATE TRANSPORTER1;1 Expression in Response to Phosphate Starvation. Plant Physiology. 164(4). 2020-2029
  55. ^ Castrillo, Sánchez-Bermejo, De Lorenzo, Crevillén, Fraile-Escanciano, et al. (2013) WRKY6 Transcription Factor Restricts Arsenate Uptake and Transposon Activation in Arabidopsis. The Plant Cell Online. 25(8). 2944-2957
  56. ^ Wang, Hao, Chen, Hao, Wang, et al. (2007) Overexpression of rice WRKY89 enhances ultraviolet B tolerance and disease resistance in rice plants. Plant Molecular Biology. 65(6). 799-815, Wang, Avci, Nakashima, Hahn, Chen, et al. (2010) Mutation of WRKY transcription factors initiates pith secondary wall formation and increases stem biomass in dicotyledonous plants. Proceedings of the National Academy of Sciences. 107(51). 22338-22343, Guillaumie, Mzid, Méchin, Léon, Hichri, et al. (2010) The grapevine transcription factor WRKY2 influences the lignin pathway and xylem development in tobacco. Plant Molecular Biology. 72(1-2). 215-234
  57. ^ Schluttenhofer and Yuan (2014) Regulation of Specialized Metabolism by WRKY Transcription Factors. Plant Physiology.
  58. ^ Suttipanta, Pattanaik, Kulshrestha, Patra, Singh, et al. (2011) The Transcription Factor CrWRKY1 Positively Regulates the Terpenoid Indole Alkaloid Biosynthesis in Catharanthus roseus. Plant Physiology. 157(4). 2081-2093, Li, Zhang, Zhang, Fu and Yu (2013) Functional analysis of a WRKY transcription factor involved in transcriptional activation of the DBAT gene in Taxus chinensis. Plant Biology. 15(1). 19-26, Ma, Pu, Lei, Ma, Wang, et al. (2009) Isolation and Characterization of AaWRKY1, an Artemisia annua Transcription Factor that Regulates the Amorpha-4,11-diene Synthase Gene, a Key Gene of Artemisinin Biosynthesis. Plant and Cell Physiology. 50(12). 2146-2161, Kato, Dubouzet, Kokabu, Yoshida, Taniguchi, et al. (2007) Identification of a WRKY Protein as a Transcriptional Regulator of Benzylisoquinoline Alkaloid Biosynthesis in Coptis japonica. Plant and Cell Physiology. 48(1). 8-18, Xu, Wang, Wang, Wang and Chen (2004) Characterization of GaWRKY1, a Cotton Transcription Factor That Regulates the Sesquiterpene Synthase Gene (+)-δ-Cadinene Synthase-A. Plant Physiology. 135(1). 507-515
  59. ^ Han, Wang, Lundgren and Brodelius (2014) Effects of overexpression of AaWRKY1 on artemisinin biosynthesis in transgenic Artemisia annua plants. Phytochemistry. 102(0). 89-96
  60. ^ Ishiguro and Nakamura (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 β-amylase from sweet potato. Molecular and General Genetics. 244(6). 563-571, Rushton, Macdonald, Huttly, Lazarus and Hooley (1995) Members of a new family of DNA-binding proteins bind to a conserved cis-element in the promoters of α-Amy2 genes. Plant Molecular Biology. 29(4). 691-702
  61. ^ Sun, Palmqvist, Olsson, Borén, Ahlandsberg, et al. (2003) A Novel WRKY Transcription Factor, SUSIBA2, Participates in Sugar Signaling in Barley by Binding to the Sugar-Responsive Elements of the iso1 Promoter. The Plant Cell Online. 15(9). 2076-2092
  62. ^ Brand, Fischer, Harter, Kohlbacher and Wanke (2013) Elucidating the evolutionary conserved DNA-binding specificities of WRKY transcription factors by molecular dynamics and in vitro binding assays. Nucleic Acids Research. 41(21). 9764-9778
  63. ^ Brand, Fischer, Harter, Kohlbacher and Wanke (2013) Elucidating the evolutionary conserved DNA-binding specificities of WRKY transcription factors by molecular dynamics and in vitro binding assays. Nucleic Acids Research. 41(21). 9764-9778
  64. ^ Brand, Fischer, Harter, Kohlbacher and Wanke (2013) Elucidating the evolutionary conserved DNA-binding specificities of WRKY transcription factors by molecular dynamics and in vitro binding assays. Nucleic Acids Research. 41(21). 9764-9778
  65. ^ Cheng, Zhou, Yang, Chi, Zhou, et al. (2012) Structural and Functional Analysis of VQ Motif-Containing Proteins in Arabidopsis as Interacting Proteins of WRKY Transcription Factors. Plant Physiology. 159(2). 810-825
  66. ^ Jiang, Liang, Yang and Yu (2014) Arabidopsis WRKY57 Functions as a Node of Convergence for Jasmonic Acid– and Auxin-Mediated Signaling in Jasmonic Acid–Induced Leaf Senescence. The Plant Cell. 26(1). 230-245
  67. ^ Kim, Lai, Fan and Chen (2008) Arabidopsis WRKY38 and WRKY62 Transcription Factors Interact with Histone Deacetylase 19 in Basal Defense. The Plant Cell. 20(9). 2357-2371
  68. ^ Xu, Chen, Fan and Chen (2006) Physical and Functional Interactions between Pathogen-Induced Arabidopsis WRKY18, WRKY40, and WRKY60 Transcription Factors. The Plant Cell Online. 18(5). 1310-1326
  69. ^ Park, Lee, Yoo, Moon, Choi, et al. (2005) WRKY group IId transcription factors interact with calmodulin. FEBS Letters. 579(6). 1545-1550
  70. ^ Menke, Kang, Chen, Park, Kumar, et al. (2005) Tobacco Transcription Factor WRKY1 Is Phosphorylated by the MAP Kinase SIPK and Mediates HR-Like Cell Death in Tobacco. Molecular Plant-Microbe Interactions. 18(10). 1027-1034, Ishihama, Yamada, Yoshioka, Katou and Yoshioka (2011) Phosphorylation of the Nicotiana benthamiana WRKY8 Transcription Factor by MAPK Functions in the Defense Response. The Plant Cell. 23(3). 1153-1170
  71. ^ Li, Meng, Wang, Mao, Han, et al. (2012) Dual-Level Regulation of ACC Synthase Activity by MPK3/MPK6 Cascade and Its Downstream WRKY Transcription Factor during Ethylene Induction in Arabidopsis. PLoS Genet. 8(6). e1002767
  72. ^ Mao, Meng, Liu, Zheng, Chen, et al. (2011) Phosphorylation of a WRKY Transcription Factor by Two Pathogen-Responsive MAPKs Drives Phytoalexin Biosynthesis in Arabidopsis. The Plant Cell. 23(4). 1639-1653
  73. ^ Qiu, Fiil, Petersen, Nielsen, Botanga, et al. (2008) Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J. 27(16). 2214-2221
  74. ^ Yu, Xu, Wang, Wang, Yao, et al. (2013) The Chinese wild grapevine (Vitis pseudoreticulata) E3 ubiquitin ligase Erysiphe necator-induced RING finger protein 1 (EIRP1) activates plant defense responses by inducing proteolysis of the VpWRKY11 transcription factor. New Phytologist. 200(3). 834-846
  75. ^ Matsushita, Inoue, Goto, Nakayama, Sugano, et al. (2013) Nuclear ubiquitin proteasome degradation affects WRKY45 function in the rice defense program. The Plant Journal. 73(2). 302-313