Research Progress on Family of Plant WRKY Transcription Factors

doi:10.13560/j.cnki.biotech.bull.1985.2019-0626

Abstract

Abstract: WRKY transcription factors are one of the largest families of transcriptional regulators in plants and form an integral part of signaling webs that modulates many plant processes. WKRY transcription factors have a variety of biological functions and play an important role in plant growth,development and senescence,abiotic and biotic stress and so on. At DNA level,WRKY transcription factors can bind to W-box TTGAC（C/T）in the promoter of its target genes and activate or inhibit the expression of downstream genes to regulate their response by self-regulation or cross-regulation. At protein level,WRKY transcription factors can regulate plant growth and development or various stress responses by interacting with a variety of proteins,including MAP kinases,histone deacetylase,resistant R proteins,and a variety of transcription factors. This paper reviews the research progress on the structure,biological function,regulatory mechanism and network of WRKY transcription factors,which will help us to understand their roles in plants more comprehensively.

Key words: WRKY transcription factor, structural characteristics, biological function, regulatory mechanism, regulatory network

HUANG Xing, DING Feng, PENG Hong-xiang, PAN Jie-chun, HE Xin-hua, XU Jiong-zhi, LI Lin. Research Progress on Family of Plant WRKY Transcription Factors[J]. Biotechnology Bulletin, 2019, 35(12): 129-143.

References

[1] Xue GP.The DNA-binding activity of an Ap2 transcriptional activator Hvcbf2 involved in regulation of low-temperature responsive genes in barley is modulated by temperature[J]. Plant J, 2003, 33(2):373-383.
[2] Riechmann JL, Heard J, Martin G, et al.Arabidopsis transcription factors:genome-wide comparative analysis among eukaryotes[J]. Science, 2000, 290(5499):2105-2110.
[3] Yamasaki K, Kigawa T, Inoue M, et al.Structures and evolutionary origins of plant-specific transcription factor DNA-binding domains[J]. Plant Physiology and Biochemistry, 2008, 46(3):394-401.
[4] Ishiguro S, Nakamura K.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[J]. Molecular and General Genetics, 1994, 244(6):563-571.
[5] Rushton PJ, Macdonald H, Huttly AK, et al.Members of a new family of DNA-binding proteins bind to a conserved Cis-element in the promoters of Α-Amy2 genes[J]. Plant Mole Biol, 1995, 29(4):691-702.
[6] Wen F, Zhu H, Li P, et al.Genome-wide evolutionary characterization and expression analyses of WRKY family genes in Brachypodium distachyon[J]. DNA Research, 2014, 21(3):327-339.
[7] Rinerson CI, Rabara RC, Tripathi P, et al.The evolution of WRKY transcription factors[J]. BMC Plant Biology, 2015, 15(1):66.
[8] Liu D, Lei BK, Zhao P, et al.Phylogenetic analysis of barley WRKY proteins and characterization of Hvwrky1 and-2 as repressors of the pathogen-inducible gene Hvger4c[J]. Molecular Genetics and Genomics, 2014, 289(6):1331-1345.
[9] Li MY, Xu ZS, Tian C, et al.Genomic identification of WRKY transcription factors in carrot(Daucus carota)and analysis of evolution and homologous groups for plants[J]. Scientific Reports, 2016, 6:23101.
[10] Liu JJ, Ekramoddoullah AKJ.Identification and characterization of the WRKY transcription factor family in Pinus monticola[J]. Genome, 2009, 52(1):77-88.
[11] Guo C, Guo R, Xu X, et al.Evolution and expression analysis of the grape(Vitis vinifera L.)WRKY gene family[J]. Journal of Experimental Botany, 2014, 65(6):1513-1528.
[12] Da SEG, Ito TM, Souza SG.‘In silico’genome-wide identification and phylogenetic analysis of the WRKY transcription factor family in sweet orange (Citrus sinensis)[J]. Australian Journal of Crop Science, 2017, 11(6):716.
[13] Meng D, Li Y, Bai Y, et al.Genome-wide identification and characterization of WRKY transcriptional factor family in apple and analysis of their responses to waterlogging and drought stress[J]. Plant Physiology, 2016, 103:71-83.
[14] Yang Y, Zhou Y, Chi Y, et al.Characterization of soybean WRKY gene family and identification of soybean WRKY genes that promote resistance to soybean cyst nematode[J]. Scientific Reports, 2017, 7(1):17804.
[15] Ülker B, Somssich IEJ.WRKY transcription factors:from DNA binding towards biological function[J]. Current Opinion in Plant Biology, 2004, 7(5):491-498.
[16] Mangelsen E, Kilian J, Berendzen KW, et al.Phylogenetic and comparative gene expression analysis of barley(Hordeum vulgare)WRKY transcription factor family reveals putatively retained functions between monocots and dicots[J]. BMC Genomics, 2008, 9(1):194.
[17] Ning P, Liu C, Kang J, et al.Genome-wide analysis of WRKY transcription factors in wheat(Triticum aestivum L.)and differential expression under water deficit condition[J]. Peer J, 2017, 5:e3232.
[18] Xu H, Watanabe KA, Zhang L, et al.WRKY transcription factor genes in wild rice Oryza nivara[J]. DNA Research, 2016, 23(4):311-323.
[19] Rice WRKY Working Group. Nomenclature report on rice WRKY’s-conflict regarding gene names and its solution[J]. Rice, 2012, 5(1):3.
[20] Li L, Mu S, Cheng Z, et al.Characterization and expression analysis of the WRKY gene family in moso bamboo[J]. Scientific Reports, 2017, 7(1):6675.
[21] Wei KF, Chen J, Chen YF, et al.Molecular phylogenetic and expression analysis of the complete WRKY transcription factor family in maize[J]. DNA Research, 2012, 19(2):153-164.
[22] Goel R, Pandey A, Trivedi PK, et al.Genome-wide analysis of the musa WRKY gene family:Evolution and differential expression during development and stress[J]. Front Plant Sci, 2016, 7:299.
[23] Eulgem T, Rushton PJ, Robatzek S, et al.The WRKY superfamily of plant transcription factors[J]. Trends in Plant Science, 2000, 5(5):199-206.
[24] Rushton PJ, Somssich IE, Ringler P, et al.WRKY transcription factors[J]. Trends in Plant Science, 2010, 15(5):247-258.
[25] Maeo K, Hayashi S, Kojima SH, et al.Role of conserved residues of the WRKY domain in the DNA-binding of tobacco WRKY family proteins[J]. Bioscience Biotechnology, 2001, 65(11):2428-2436.
[26] Bakshi M, Oelmüller RJ.WRKY transcription factors:Jack of many trades in plants[J]. Plant Signaling Behavior, 2014, 9(2):e27700.
[27] Yamasaki K, Kigawa T, Inoue M, et al.Solution structure of an Arabidopsis WRKY DNA binding domain[J]. The Plant Cell, 2005, 17(3):944-956.
[28] Zhang Y, Wang LJ.The WRKY transcription factor superfamily:Its origin in eukaryotes and expansion in plants[J]. BMC Evolutionary Biology, 2005, 5(1):1.
[29] Wan Y, Mao M, Wan D, et al.Identification of the WRKY gene family and functional analysis of two genes in Caragana intermedia[J]. BMC Plant Biology, 2018, 18(1):31.
[30] Chen L, Song Y, Li S, et al.The role of WRKY transcription factors in plant abiotic stresses[J]. Biochimica et Biophysica Acta -Gene Regulatory Mechanisms, 2012, 1819(2):120-128.
[31] Park CY, Lee JH, Yoo JH, et al.WRKY group iid transcription factors interact with calmodulin[J]. FEBS Letters, 2005, 579(6):1545-1550.
[32] Bailey TL, Boden M, Buske FA, et al.Meme suite:tools for motif discovery and searching[J]. Nucleic Acids Res, 2009, 37(2):W202-W208.
[33] Vyas J, Gryk MR, Schiller MRJ.VENN, a tool for titrating sequence conservation onto protein structures[J]. Nucleic Acids Res, 2009, 37(18):e124.
[34] Tamura K, Dudley J, Nei M, et al.Mega4:Molecular evolutionary genetics analysis(mega)software version 4. 0[J]. Molecular Biology Evolution, 2007, 24(8):1596-1599.
[35] Ou C, Jiang S, Wang F, et al.An RNA-Seq analysis of the pear(Pyrus communis L.)transcriptome, with a focus on genes associated with dwarf[J]. Plant Gene, 2015, 4:69-77.
[36] Zhang D, Ren L, Yue Jh, et al.RNA-Seq-based transcriptome analysis of stem development and dwarfing regulation in Agapanthus praecox ssp. orientalis(leighton)leighton[J]. Gene, 2015, 565(2):252-267.
[37] Jiang J, Ma S, Ye N, et al.WRKY transcription factors in plant responses to stresses[J]. Journal of Integrative Plant Biology, 2017, 59(2):86-101.
[38] Cai Y, Chen X, Xie K, et al.Dlf1, a WRKY transcription factor, is involved in the control of flowering time and plant height in rice[J]. PLoS One, 2014, 9(7):e102529.
[39] Guo D, Zhang J, Wang X, et al.The WRKY transcription factor WRKY71/Exb1 controls shoot branching by transcriptionally regulating Rax genes in Arabidopsis[J]. The Plant Cell, 2015, 27(11):3112-3127.
[40] Ma Y, Xue H, Zhang L, et al.Involvement of auxin and brassinosteroid in dwarfism of autotetraploid apple(Malus× domestica)[J]. Scientific Reports, 2016, 6:26719.
[41] Soumelidou K, Morris D, Battey N, et al.Auxin transport capacity in relation to the dwarfing effect of apple rootstocks[J]. Journal of Horticultural Science, 1994, 69(4):719-725.
[42] Michalczuk LJ.Indole-3-acetic acid level in wood, bark and cambial sap of apple rootstocks differing in growth vigour[J]. Acta Physiologiae Plantarum, 2002, 24(2):131-136.
[43] Zhao B, Li JJ.Regulation of brassinosteroid biosynthesis and inactivation[J]. Journal of Integrative Plant Biology, 2012, 54(10):746-759.
[44] Zheng X, Zhao Y, Shan D, et al.Mdwrky9 overexpression confers intensive dwarfing in the M26 rootstock of apple by directly inhibiting brassinosteroid synthetase Mddwf4 expression[J]. New Phytologist, 2018, 217(3):1086-1098.
[45] Xie Z, Zhang ZL, Zou X, et al.Annotations and functional analyses of the rice WRKY gene superfamily reveal positive and negative regulators of abscisic acid signaling in aleurone cells[J]. Plant Physiology, 2005, 137(1):176-189.
[46] Qiu D, Xiao J, Ding X, et al.Oswrky13 mediates rice disease resistance by regulating defense-related genes in salicylate-and jasmonate-dependent signaling[J]. Molecular Plant-Microbe Interactions, 2007, 20(5):492-499.
[47] Zhang J, Peng Y, Guo ZJ.Constitutive expression of pathogen-inducible Oswrky31 enhances disease resistance and affects root growth and auxin response in transgenic rice plants[J]. Cell Research, 2008, 18(4):508.
[48] Wang PT, Xu X, Tang Z, et al.Oswrky28 regulates phosphate and arsenate accumulation, root system architecture and fertility in rice[J], Frontiers in Plant Science, 2018, 9:1330.
[49] Hu Z, Wang R, Zheng M, et al.Ta WRKY 51 promotes lateral root formation through negative regulation of ethylene biosynthesis in wheat(Triticum aestivum L.)[J]. Plant J, 2018, 96(2):372-388.
[50] Cheng Y, Ahammed GJ, Yu J, et al.Putative WRKYs associated with regulation of fruit ripening revealed by detailed expression analysis of the WRKY gene family in pepper[J]. Scientific Reports, 2016, 6. doi:10.1038/srep39000.
[51] Yang X, Li H, Yang Y, et al.Identification and expression analyses of WRKY genes reveal their involvement in growth and abiotic stress response in watermelon(Citrullus lanatus)[J]. PLoS One, 2018, 13(1):e0191308.
[52] Li QL, Bo S, Deng wJ, et al. Avocado fruit pulp transcriptomes in the after-ripening process[J]. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 2019, 47(2):308-319.
[53] Li D, Mou W, Xia R, et al.Integrated analysis of high-throughput sequencing data shows abscisic acid-responsive genes and mirnas in strawberry receptacle fruit ripening[J]. Horticulture Research, 2019, 6(1):26.
[54] Guo Y, Cai Z, et al.Transcriptome of Arabidopsis Leaf senescence[J]. Plant, Cell Environment, 2004, 27(5):521-549.
[55] Robatzek S, Somssich IEJ.A new member of the Arabidopsis WRKY transcription factor family, Atwrky6, is associated with both senescence-and defence-related processes[J]. Plant J, 2001, 28(2):123-133.
[56] Robatzek S, Somssich IEJ.Targets of Atwrky6 regulation during plant senescence and pathogen defense[J]. Gene Development, 2002, 16(9):1139-1149.
[57] Gu L, Wei H, et al.Characterization and functional analysis of Ghwrky42, a group iid WRKY gene, in upland cotton(Gossypium hirsutum L.)[J]. BMC Genetics, 2018, 19(1):48.
[58] Fan ZQ, Tan XL, Shan W, et al.Characterization of a transcriptional regulator, brwrky6, associated with gibberellin-suppressed leaf senescence of chinese flowering cabbage[J]. Journal of Agricultural Food Chemistry, 2018, 66(8):1791-1799.
[59] Gao H, Wang Y, Xu P, et al.Overexpression of a WRKY transcription factor Tawrky2 enhances drought stress tolerance in transgenic wheat[J]. Front Plant Sci, 2018, 9:997.
[60] Wang CT, Ru JN, Liu YW, et al.Maize WRKY transcription factor Zmwrky106 confers drought and heat tolerance in transgenic plants[J]. International Journal of Molecular Sciences, 2018, 19(10):3046.
[61] Li DH, Wang CH, Liu XP, et al.Expression of Gmwrky35, a soybean WRKY gene, in transgenic tobacco confers drought stress tolerances[J]. Soybean Science, 2017, 36(5):685-691.
[62] Lee H, Cha J, Choi C, et al.Rice WRKY11 plays a role in pathogen defense and drought tolerance[J]. Rice, 2018, 11(1):5.
[63] Wang Y, Shu Z, Wang W, et al.Cswrky2, a novel WRKY gene from camellia sinensis, is involved in cold and drought stress responses[J]. Biologia Plantarum, 2016, 60(3):443-451.
[64] Zhu D, Che YM, Xiao PL, et al.Functional analysis of a grape WRKY30 gene in drought resistance[J]. Plant Cell Tissue and Organ Culture, 2018, 132(3):449-459.
[65] Yang G, Zhang W, Liu Z, et al.Both JrWRKY 2 and Jr WRKY 7 of Juglans regia mediate responses to abiotic stresses and abscisic acid through formation of homodimers and interaction[J]. Plant Biology, 2017, 19(2):268-278.
[66] Raineri J, Ribichich KF, Chan RLJ.The sunflower transcription factor Hawrky76 confers drought and flood tolerance to Arabidopsis thaliana plants without yield penalty[J]. Plant Cell Reports, 2015, 34(12):2065-2080.
[67] He L, Wu YH, Zhao Q, et al.Chrysanthemum Dgwrky2 gene enha-nces tolerance to salt stress in transgenic chrysanthemum[J]. International Journal of Molecular Sciences, 2018, 19(7):2062.
[68] Yang G, Zhang W, Sun Y, et al.Two novel WRKY genes from Juglans regia, Jrwrky6 and Jrwrky53, are involved in abscisic acid-dependent stress responses[J]. Biologia Plantarum, 2017, 61(4):611-621.
[69] Wu M, Liu H, Han G, et al.A Moso Bamboo WRKY gene Pewrky83 confers salinity tolerance in transgenic Arabidopsis plants[J]. Scientific Reports, 2017, 7(1):11721.
[70] Ullah A, Sun H, Hakim, et al. A novel cotton WRKY gene, Ghwrky6-like, improves salt tolerance by activating the aba signaling pathway and scavenging of reactive oxygen species[J]. Physiologia Plantarum, 2018, 162(4):439-454.
[71] Pillai SE, Kumar C, Patel HK, et al.Overexpression of a cell wall damage induced transcription factor, Oswrky42, leads to enhanced callose deposition and tolerance to salt stress but does not enhance tolerance to bacterial infection[J]. BMC Plant Biology, 2018, 18(1):177.
[72] Wang CT, Ru JN, Liu YW, et al.The maize WRKY transcription factor Zmwrky40 confers drought resistance in transgenic Arabidopsis[J]. International Journal of Molecular Sciences, 2018, 19(9):2580.
[73] Hong C, Cheng D, Zhang G, et al.The role of Zmwrky4 in regulating maize antioxidant defense under cadmium stress[J]. Biochemical Biophysical Research Communications, 2017, 482(4):1504-1510.
[74] Sheng Y, Yan X, Huang Y, et al.The WRKY transcription factor, WRKY13, activates Pdr8 expression to positively regulate cadmium tolerance in Arabidopsis[J]. Plant, Cell and Environment, 2019, 42(3):891-903.
[75] Li GZ, Wang ZQ, Yokosho K, et al.Transcription factor WRKY 22 promotes aluminum tolerance via activation of Os Frdl 4 expression and enhancement of citrate secretion in rice(Oryza sativa)[J]. New Phytologist, 2018, 219(1):149-162.
[76] Dai X, Wang Y, Zhang WH.Oswrky74, a WRKY transcription factor, modulates tolerance to phosphate starvation in rice[J]. Journal of Experimental Botany, 2015, 67(3):947-960.
[77] Jones JDG, Dangl JL.The plant immune system[J]. Nature, 2006, 444(7117):323-329.
[78] Monaghan J, Zipfel C.Plant pattern recognition receptor complexes at the plasma membrane[J]. Current Opinion in Plant Biology, 2012, 15(4):349-357.
[79] Chisholm ST, Coaker G, Day B, et al.Host-microbe interactions:shaping the evolution of the plant immune response[J]. Cell, 2006, 124(4):803-814.
[80] Wang X, Guo R, Tu M, et al.Ectopic expression of the wild grape WRKY transcription factor Vqwrky52 in Arabidopsis Thaliana enhances resistance to the biotrophic pathogen powdery mildew but not to the necrotrophic pathogen botrytis cinerea[J]. Front Plant Sci, 2017, 8:97.
[81] Arrano SP, Dominguez FJ, Herrera VA, et al.WRKY7, -11 and-17 transcription factors are modulators of the Bzip28 branch of the unfolded protein response during pamp-triggered immunity in Arabidopsis thaliana[J]. Plant Science, 2018, 277:242-250.
[82] Li J, Wang J, Wang N, et al.Ghwrky44, a WRKY transcription factor of cotton, mediates defense responses to pathogen infection in transgenic Nicotiana benthamiana[J]. Plant Cell, Tissue Organ Culture, 2015, 121(1):127-140.
[83] Wang L, Liu F, et al.Expression characteristics and functional analysis of the Scwrky3 gene from sugarcane[J]. International Journal of Molecular Sciences, 2018, 19(12):4059.
[84] Wang H, Meng J, Peng X, et al.Rice WRKY4 acts as a transcrip-tional activator mediating defense responses toward Rhizoctonia solani, the causing agent of rice sheath blight[J]. Plant Mole Biol, 2015, 89(1-2):157-171.
[85] Shuo Y, Liang Z, Miao LY, et al.The expression and binding properties of the rice WRKY68 protein in the Xa21-Mediated resistance response to Xanthomonas Oryzae pv. Oryzae[J]. Journal of Integrative Agriculture, 2016, 15(11):2451-2460.
[86] Hwang SH, Kwon SI, Jang JY, et al.Oswrky51, a rice transcription factor, functions as a positive regulator in defense response against Xanthomonas Oryzae Pv. Oryzae[J]. Plant Cell Reports, 2016, 35(9):1975-1985.
[87] Liu Z, Luan Y, Li JJ.Molecular cloning and expression analysis of Spwrky6 gene from Solanum Pimpinellifolium[J]. Biologia Plantarum, 2016, 60(2):226-234.
[88] Cui Q, Yan X, et al.Analysis of WRKY transcription factors and characterization of two botrytis cinerea-responsive Lrwrky genes from lilium regale[J]. Plant Physiology, 2018, 127:525-536.
[89] Liu F, Li XX, Wang MR, et al.Interactions of Wrky15 and Wrky33 transcription factors and their roles in the resistance of Oilseed rape to Sclerotinia infection[J]. Plant Biotechnology Journal, 2018, 16(4):911-925.
[90] Wang J, Tao F, Tian W, et al.The wheat WRKY transcription factors Tawrky49 and Tawrky62 confer differential high-temperature seedling-plant resistance to Puccinia striiformis F. sp. tritici[J]. PLoS One, 2017, 12(7):e0181963.
[91] Cui J, Xu P, Meng J, et al.Transcriptome signatures of tomato leaf induced by phytophthora infestans and functional identification of transcription factor Spwrky3[J]. Theoretical and Applied Genetics, 2018, 131(4):787-800.
[92] Wei W, Cui MY, Yang H, et al.Ectopic expression of Fvwrky42, a WRKY transcription factor from the diploid woodland strawberry(Fragaria Vesca), enhances resistance to powdery mildew, improves osmotic stress resistance, and increases abscisic acid sensitivity in Arabidopsis[J]. Plant Science, 2018, 275:60-74.
[93] Liu Q, Li X, Yan S, et al.Oswrky67 Positively regulates blast and bacteria blight resistance by direct activation of Pr genes in rice[J]. BMC Plant Biology, 2018, 18(1):257.
[94] Luan Q, Chen C, Liu M, et al.Cswrky50 mediates defense responses to pseudoperonospora cubensis infection in cucumis sativus[J]. Plant Science, 2019, 279:59-69.
[95] Shan W, Chen JY, Kuang JF, et al.Banana fruit nac transcription factor manac5 cooperates with mawrkys to enhance the expression of pathogenesis-related genes against Colletotrichum musae[J]. Molecular Plant Pathology, 2016, 17(3):330-338.
[96] Hu L, Ye M, Li R, et al.Oswrky53, a versatile switch in regulating herbivore-induced defense responses in rice[J]. Plant Signaling, 2016, 11(4):e1169357.
[97] Ifnan KM, Zhang Y, Liu Z, et al.Cawrky40b in pepper acts as a negative regulator in response to ralstonia solanacearum by directly modulating defense genes including Cawrky40[J]. International journal of Molecular Sciences, 2018, 19(5):1403.
[98] Wang Z, Zhu Y, Wang L, et al.A WRKY transcription factor participates in dehydration tolerance in Boea hygrometrica by binding to the W-Box elements of the galactinol synthase(Bhgols1)promoter[J]. Planta, 2009, 230(6):1155-1166.
[99] Hussain RM, Sheikh AH, Haider I, et al.Arabidopsis WRKY50 and tga transcription factors synergistically activate expression of Pr1[J]. Front Plant Sci, 2018, 9:930.
[100] Miao Y, Laun TM, et al.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[J]. Plant Mole Biol, 2007, 65(1-/2):63-76.
[101] Sheikh AH, Eschen LL, et al.Regulation of WRKY46 transcription factor function by mitogen-activated protein kinases in Arabidopsis thaliana[J]. Front Plant Sci, 2016, 7:61.
[102] Pandey SP, Somssich IEJ.The role of WRKY transcription factors in plant immunity[J]. Plant Physiology, 2009, 150(4):1648-1655.
[103] Arraño SP, Domínguez FJ, Herrera VA, et al.WRKY7, -11 and-17 transcription factors are modulators of the Bzip28 branch of the unfolded protein response during pamp-triggered immunity in Arabidopsis thaliana[J]. Plant Science, 2018, 277:242-250.
[104] Çelik Ö, Meriç S, Ayan A, et al.Epigenetic analysis of WRKY transcription factor genes in salt stressed rice(Oryza sativa L.)plants[J]. Environmental Experimental Botany, 2019, 159:121-131.
[105] Pandey N, Pandey RSJ.Deciphering Uv-B-induced variation in DNA methylation pattern and its influence on regulation of Dbr2 expression in Artemisia annua L.[J]. Planta, 2015, 242(4):869-879.
[106] Kim KC, Lai Z, Fan B, et al.Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense[J]. The Plant Cell, 2008, 20(9):2357-2371.
[107] Chakraborty J, Ghosh P, Sen S, et al.Epigenetic and transcriptional control of chickpea WRKY40 promoter activity under fusarium stress and its heterologous expression in Arabidopsis leads to enhanced resistance against bacterial pathogen[J]. Plant Science, 2018, 276:250-267.
[108] Eulgem T, Rushton PJ, Schmelzer E, et al.Early nuclear events in plant defence signalling:Rapid gene activation by WRKY transcription factors[J]. The EMBO Journal, 1999, 18(17):4689-4699.
[109] Rushton PJ, Torres JT, Parniske M, et al.Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley Pr1 genes[J]. EMBO Journal, 1996, 15(20):5690-5700.
[110] Turck F, Zhou A, Somssich IEJ.Stimulus-dependent, promoter-specific binding of transcription factor WRKY1 to its native promoter and the defense-related gene Pcpr1-1 in parsley[J]. The Plant Cell, 2004, 16(10):2573-2585.
[111] Maleck K, Levine A, Eulgem T, et al.The transcriptome of Arabidopsis thaliana during systemic acquired resistance[J]. Nat Genet, 2000, 26(4):403-410.
[112] Mare C, Mazzucotelli E, Crosatti C, et al.Hv-WRKY38:A new transcription factor involved in cold-and drought-response in barley[J]. Plant Mole Biol, 2004, 55(3):399-416.
[113] Cheng X, Zhao Y, Jiang Q, et al.Structural basis of dimerization and Dual W-Box DNA recognition by rice WRKY domain[J]. Nucleic Acids Res, 2019, 47(8):4308-4318.
[114] Colcombet J, Hirt HJ.Arabidopsis Mapks:A complex signalling network involved in multiple biological processes[J]. Biochemical Journal, 2008, 413(2):217-226.
[115] Fiil BK, Petersen K, Petersen M, et al.Gene regulation by map kinase cascades[J]. Current Opinion In Plant Biology, 2009, 12(5):615-621.
[116] Qiu JL, Fiil BK, et al.Arabidopsis map kinase 4 regulates gene expression through transcription factor release in the nucleus[J]. The EMBO Journal, 2008, 27(16):2214-2221.
[117] Mao G, Meng X, Liu Y, et al.Phosphorylation of a WRKY transcription factor by two pathogen-responsive Mapks drives phytoalexin biosynthesis in Arabidopsis[J]. The Plant Cell, 2011, 23(4):1639-1653.
[118] Guan Y, Meng X, Khanna R, et al.Phosphorylation of a WRKY transcription factor by Mapks is required for pollen development and function in Arabidopsis[J]. PLoS Genetics, 2014, 10(5):e1004384.
[119] Hu L, Ye M, Li R, et al.The rice transcription factor WRKY53 suppresses herbivore-induced defenses by acting as a negative feedback modulator of mitogen-activated protein kinase activity[J]. Plant Physiology, 2015, 169(4):2907-2921.
[120] Wang Y, Schuck S, Wu J, et al.A Mpk3/6-Wrky33-Ald1-pipecolic acid regulatory loop contributes to systemic acquired resistance[J]. The Plant Cell, 2018, 30(10):2480-2494.
[121] Sarris PF, Duxbury Z, Huh SU, et al.A plant immune receptor detects pathogen effectors that target WRKY transcription factors[J]. Cell, 2015, 161(5):1089-1100.
[122] Shen QH, Saijo Y, Mauch S, et al.Nuclear activity of Mla immune receptors links isolate-specific and basal disease-resistance responses[J]. Science, 2007, 315(5815):1098-1103.
[123] Deslandes L, Olivier J, Theulières F, et al.Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive Rrs1-R gene, a member of a novel family of resistance genes[J]. Proceedings of the National Academy of Sciences of the USA, 2002, 99(4):2404-2409.
[124] Deslandes L, Olivier J, Peeters N, et al.Physical interaction between Rrs1-R, a protein conferring resistance to bacterial Wilt, and Popp2, a type iii effector targeted to the plant nucleus[J]. Proceedings of the National Academy of Sciences of the USA, 2003, 100(13):8024-8029.
[125] Vannozzi A, Wong DCJ, Höll J, et al.Combinatorial regulation of stilbene synthase genes by WRKY and Myb transcription factors in grapevine(Vitis vinifera L.)[J]. Plant Cell Physiology, 2018, 59(5):1043-1059.
[126] Lahiri A, Venkatasubramani PS, Datta AJ.Bayesian modeling of plant drought resistance pathway[J]. BMC Plant Biology, 2019, 19(1):96.
[127] Chi Y, Yang Y, Zhou Y, et al.Protein-protein interactions in the regulation of WRKY transcription factors[J]. Molecular Plant, 2013, 6(2):287-300.
[128] Jiao Z, Sun J, Wang C, et al.Genome-wide characterization, evolutionary analysis of WRKY genes in cucurbitaceae species and assessment of its roles in resisting to powdery mildew disease[J]. PLoS One, 2018, 13(12):e0199851.
[129] Chen J, Wang H, Li Y, et al.Arabidopsis Vq10 interacts with WRKY8 to Modulate basal defense against botrytis cinerea[J]. Journal of Integrative Plant Biology, 2018, 60(10):956-969.