Role of WRKY Transcription Factor in Plant Response to Stresses

doi:10.13560/j.cnki.biotech.bull.1985.2020-1481

Abstract

Abstract:

WRKY transcription factors（TFs）are one of the most important transcription factor families in plants. It contains a conserved WRKY domain composed of 60 amino acids. The core sequence WRKYGQK of the domain can specifically bind to W-box[（T）（T）TGAC（C/T）]in the promoter region of target genes,thus regulating the expressions of regulatory genes and/or functional genes containing W-box elements in the promoters. When plants are exposed to stresses,WRKY transcription factors are involved in the regulation of the related transcription reprogramming,and play an important role in plant growth and environmental adaptation. This paper reviews the discovery,structural characteristics,classification,regulation,and expression patterns of WRKY transcription factors,as well as the research progress in plant response to abiotic（such as drought,high temperature,low temperature,high salinity,nutrient deficiency and so on）and biological（such as disease and pest）stresses in recent years,and prospects the future research direction.

Key words: WRKY transcription factors, biological stress, abiotic stress, cis-acting element, W-box

ZHANG Tong, LI Zhi-qiang, WU Guo-qiang. Role of WRKY Transcription Factor in Plant Response to Stresses[J]. Biotechnology Bulletin, 2021, 37(10): 203-215.

Figures/Tables 1

References 123

[1]	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. pmid: 16497589
[2]	Shinozaki K, Yamaguchi-Shinozaki K. Gene networks involved in drought stress response and tolerance[J]. J Exp Bot, 2007, 58(2):221-227. pmid: 17075077
[3]	Wang GQ, Shui QZ. Effect of salinity on seed germination, seedling growth, and inorganic and organic solutes accumulationin sunflower(Helianthus annuus L.)[J]. Plant Soil Environ, 2016, 61(No. 5):220-226. doi: 10.17221/PSE URL
[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]. Mol Gen Genet, 1994, 244(6):563-571. doi: 10.1007/BF00282746 URL
[5]	He Y, Mao S, Gao Y, et al. Genome-wide identification and expression analysis of WRKY transcription factors under multiple stresses in Brassica napus[J]. PLoS One, 2016, 11(6):e0157558. doi: 10.1371/journal.pone.0157558 URL
[6]	Yao S, Wu F, Hao QQ, et al. Transcriptome-wide identification of WRKY transcription factors and their expression profiles under different types of biological and abiotic stress in Pinus massoniana lamb[J]. Genes, 2020, 11(11):1386. doi: 10.3390/genes11111386 URL
[7]	Li HL, Guo D, Yang ZP, et al. Genome-wide identification and characterization of WRKY gene family in Hevea brasiliensis[J]. Genomics, 2014, 104(1):14-23. doi: 10.1016/j.ygeno.2014.04.004 URL
[8]	Yao QY, Xia EH, Liu FH, et al. Genome-wide identification and comparative expression analysis reveal a rapid expansion and functional divergence of duplicated genes in the WRKY gene family of cabbage, Brassica oleracea var. capitata[J]. Gene, 2015, 557(1):35-42. doi: 10.1016/j.gene.2014.12.005 URL
[9]	Yu Y, Wang N, Hu R, et al. Genome-wide identification of soybean WRKY transcription factors in response to salt stress[J]. Springerplus, 2016, 5(1):920. doi: 10.1186/s40064-016-2647-x URL
[10]	Song H, Wang P, Lin JY, et al. Genome-wide identification and characterization of WRKY gene family in peanut[J]. Front Plant Sci, 2016, 7:534. doi: 10.3389/fpls.2016.00534 pmid: 27200012
[11]	Yue H, Wang M, Liu S, et al. Transcriptome-wide identification and expression profiles of the WRKY transcription factor family in Broomcorn millet(Panicum miliaceum L.)[J]. BMC Genomics, 2016, 17:343. doi: 10.1186/s12864-016-2677-3 URL
[12]	Bi C, Xu Y, Ye Q, et al. Genome-wide identification and characterization of the MADS-box gene family in Salix suchowensis[J]. PeerJ, 2016, 4:e2437. doi: 10.7717/peerj.2437 URL
[13]	Chen M, Tan Q, Sun M, et al. Genome-wide identification of WRKY family genes in peach and analysis of WRKY expression during bud dormancy[J]. Mol Genet Genomics, 2016, 291(3):1319-1332. doi: 10.1007/s00438-016-1171-6 pmid: 26951048
[14]	Diao WP, Snyder JC, Wang SB, et al. Genome-wide identification and expression analysis of WRKY gene family in Capsicum annuum L[J]. Front Plant Sci, 2016, 7:211.
[15]	Wei Y, Shi H, Xia Z, et al. Genome-wide identification and expression analysis of the WRKY gene family in cassava[J]. Front Plant Sci, 2016, 7:25.
[16]	Li D, Liu P, Yu J, et al. Genome-wide analysis of WRKY gene family in the sesame genome and identification of the WRKY genes involved in responses to abiotic stresses[J]. BMC Plant Biol, 2017, 17(1):152. doi: 10.1186/s12870-017-1099-y URL
[17]	He C, Teixeira da Silva JA, Tan J, et al. A genome-wide identification of the WRKY family genes and a survey of potential WRKY target genes in Dendrobium officinale[J]. Sci Rep, 2017, 7(1):9200. doi: 10.1038/s41598-017-07872-8 URL
[18]	Zhang C, Wang D, Yang C, et al. Genome-wide identification of the potato WRKY transcription factor family[J]. PLoS One, 2017, 12(7):e0181573. doi: 10.1371/journal.pone.0181573 URL
[19]	Lui S, Luo CG, Zhu LM, et al. Identification and expression analysis of WRKY transcription factor genes in response to fungal pathogen and hormone treatments in apple(Malus domestica)[J]. J Plant Biol, 2017, 60(2):215-230. doi: 10.1007/s12374-016-0577-3 URL
[20]	Silva Monteiro de Almeida D, Oliveira Jordão do Amaral D, Del-Bem LE, et al. Genome-wide identification and characterization of cacao WRKY transcription factors and analysis of their expression in response to witches’ broom disease[J]. PLoS One, 2017, 12(10):e0187346. doi: 10.1371/journal.pone.0187346 URL
[21]	Li L, Mu S, Cheng Z, et al. Characterization and expression analysis of the WRKY gene family in moso bamboo[J]. Sci Rep, 2017, 7(1):6675. doi: 10.1038/s41598-017-06701-2 URL
[22]	Jing ZB, Liu ZD. Genome-wide identification of WRKY transcription factors in kiwifruit(Actinidia spp. )and analysis of WRKY expression in responses to biotic and abiotic stresses[J]. Genes Genom, 2018, 40(4):429-446. doi: 10.1007/s13258-017-0645-1 URL
[23]	Yang XZ, Li H, Yang YC, 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. doi: 10.1371/journal.pone.0191308 URL
[24]	Wang P, Yue C, Chen D, et al. Genome-wide identification of WRKY family genes and their response to abiotic stresses in tea plant(Camellia sinensis)[J]. Genes Genomics, 2019, 41(1):17-33. doi: 10.1007/s13258-018-0734-9 URL
[25]	Li Z, Hua X, Zhong W, et al. Genome-wide identification and expression profile analysis of WRKY family genes in the autopolyploid Saccharum spontaneum[J]. Plant Cell Physiol, 2020, 61(3):616-630. doi: 10.1093/pcp/pcz227 URL
[26]	Kumar G, Bajpai R, Sarkar A, et al. Identification, characterization and expression profiles of Fusarium udum stress-responsive WRKY transcription factors in Cajanus cajan under the influence of NaCl stress and Pseudomonas fluorescens OKC[J]. Sci Rep, 2019, 9(1):14344. doi: 10.1038/s41598-019-50696-x URL
[27]	Wu GQ, Li ZQ, Cao H, et al. Genome-wide identification and expression analysis of the WRKY genes in sugar beet(Beta vulgaris L.)under alkaline stress[J]. PeerJ, 2019, 7:e7817. doi: 10.7717/peerj.7817 URL
[28]	Liu XT, Li DD, Zhang SY, et al. Genome-wide characterization of the rose(Rosa chinensis)WRKY family and role of RcWRKY41 in gray mold resistance[J]. BMC Plant Biol, 2019, 19(1):522. doi: 10.1186/s12870-019-2139-6 URL
[29]	Li J, Xiong YC, Li Y, et al. Comprehensive analysis and functional studies of WRKY transcription factors in Nelumbo nucifera[J]. Int J Mol Sci, 2019, 20(20):5006. doi: 10.3390/ijms20205006 URL
[30]	Ding WJ, Ouyang QX, Li YL, et al. Genome-wide investigation of WRKY transcription factors in sweet Osmanthus and their potential regulation of aroma synjournal[J]. Tree Physiol, 2020, 40(4):557-572. doi: 10.1093/treephys/tpz129 URL
[31]	Nan H, Gao LZ. Genome-wide analysis of WRKY genes and their response to hormone and mechanic stresses in carrot[J]. Front Genet, 2019, 10:363. doi: 10.3389/fgene.2019.00363 URL
[32]	Zhang JJ, Yang ED, He Q, et al. Moringa oleifera genome-wide analysis of the WRKY gene family in drumstick(Lam. )[J]. PeerJ, 2019, 7:e7063. doi: 10.7717/peerj.7063 URL
[33]	Bao F, Ding AQ, Cheng TR, et al. Genome-wide analysis of members of the WRKY gene family and their cold stress response in Prunus mume[J]. Genes, 2019, 10(11):E911.
[34]	Yan HF, Li MZ, Xiong YP, et al. Genome-wide characterization, expression profile analysis of WRKY family genes in Santalum album and functional identification of their role in abiotic stress[J]. Int J Mol Sci, 2019, 20(22):5676. doi: 10.3390/ijms20225676 URL
[35]	Waqas M, Azhar MT, et al. Genome-wide identification and expression analyses of WRKY transcription factor family members from chickpea(Cicer arietinum L.)reveal their role in abiotic stress-responses[J]. Genes Genom, 2019, 41(4):467-481. doi: 10.1007/s13258-018-00780-9 URL
[36]	Li Y, Zhang L, Zhu P, et al. Genome-wide identification, characterisation and functional evaluation of WRKY genes in the sweet potato wild ancestor Ipomoea trifida(H. B. K. )G. Don. under abiotic stresses[J]. BMC Genet, 2019, 20(1):90. doi: 10.1186/s12863-019-0789-x URL
[37]	Chen X, Chen RH, Wang YF, et al. Genome-wide identification of WRKY transcription factors in Chinese jujube(Ziziphus jujuba milL.)and their involvement in fruit developing, ripening, and abiotic stress[J]. Genes, 2019, 10(5):E360.
[38]	Yue H, Chang X, Zhi YQ, et al. Evolution and identification of the WRKY gene family in quinoa(Chenopodium quinoa)[J]. Genes, 2019, 10(2):131. doi: 10.3390/genes10020131 URL
[39]	Bankaji I, Sleimi N, et al. Identification and expression of the Cucurbita WRKY transcription factors in response to water deficit and salt stress[J]. Sci Hortic, 2019, 256:108562. doi: 10.1016/j.scienta.2019.108562 URL
[40]	Chanwala J, Satpati S, Dixit A, et al. Genome-wide identification and expression analysis of WRKY transcription factors in pearl millet(Pennisetum glaucum)under dehydration and salinity stress[J]. BMC Genomics, 2020, 21(1):231. doi: 10.1186/s12864-020-6622-0 pmid: 32171257
[41]	Goyal P, Manzoor MM, Vishwakarma RA, et al. A comprehensive transcriptome-wide identification and screening of WRKY gene family engaged in abiotic stress in Glycyrrhiza glabra[J]. Sci Rep, 2020, 10(1):373. doi: 10.1038/s41598-019-57232-x URL
[42]	Xu YH, Sun PW, Tang XL, et al. Genome-wide analysis of WRKY transcription factors in Aquilaria sinensis(Lour. )Gilg[J]. Sci Rep, 2020, 10:3018. doi: 10.1038/s41598-020-59597-w URL
[43]	Chen C, Chen X, Han J, et al. Genome-wide analysis of the WRKY gene family in the cucumber genome and transcriptome-wide identification of WRKY transcription factors that respond to biotic and abiotic stresses[J]. BMC Plant Biol, 2020, 20(1):443. doi: 10.1186/s12870-020-02625-8 URL
[44]	Song YN, Cui HL, et al. Genome-wide identification and functional characterization of the Camelina sativa WRKY gene family in response to abiotic stress[J]. BMC Genom, 2020, 21(1):786. doi: 10.1186/s12864-020-07189-3 URL
[45]	Villano C, Esposito S, D’Amelia V, et al. WRKY genes family study reveals tissue-specific and stress-responsive TFs in wild potato species[J]. Sci Rep, 2020, 10(1):7196. doi: 10.1038/s41598-020-63823-w pmid: 32346026
[46]	Zhang L, Wan X, Xu Y, et al. De novo assembly of transcriptome and genome-wide identification reveal GA₃ stress-responsive WRKY transcription factors involved in fiber formation in jute(Corchorus capsularis)[J]. BMC Plant Biol, 2020, 20(1):403. doi: 10.1186/s12870-020-02617-8 URL
[47]	Wang ZQ, Ni LJ, Guo JB, et al. Phylogenetic and transcription analysis of Hibiscus hamabo sieb. et zucc. WRKY transcription factors[J]. DNA Cell Biol, 2020, 39(7):1141-1154. doi: 10.1089/dna.2019.5254 URL
[48]	Yang X, Zhou Z, Fu M, et al. Transcriptome-wide identification of WRKY family genes and their expression profiling toward salicylic acid in Camellia japonica[J]. Plant Signal Behav, 2021, 16(1):1844508. doi: 10.1080/15592324.2020.1844508 pmid: 33222651
[49]	Baillo EH, Hanif MS, Guo Y, et al. Genome-wide Identification of WRKY transcription factor family members in Sorghum(Sorghum bicolor(L.)moench)[J]. PLoS One, 2020, 15(8):e0236651. doi: 10.1371/journal.pone.0236651 URL
[50]	Zhao N, He M, Li L, et al. Identification and expression analysis of WRKY gene family under drought stress in peanut(Arachis hypogaea L.)[J]. PLoS One, 2020, 15(4):e0231396. doi: 10.1371/journal.pone.0231396 URL
[51]	Yang Y, Liu J, Zhou XH, et al. Identification of WRKY gene family and characterization of cold stress-responsive WRKY genes in eggplant[J]. PeerJ, 2020, 8:e8777. doi: 10.7717/peerj.8777 URL
[52]	Xiu H, Nuruzzaman M, et al. Molecular cloning and expression analysis of eight PgWRKY genes in Panax ginseng responsive to salt and hormones[J]. Int J Mol Sci, 2016, 17(3):319. doi: 10.3390/ijms17030319 URL
[53]	Eulgem T, Rushton PJ, Robatzek S, et al. The WRKY superfamily of plant transcription factors[J]. Trends Plant Sci, 2000, 5(5):199-206. pmid: 10785665
[54]	Barco B, Clay NK. Hierarchical and dynamic regulation of defense-responsive specialized metabolism by WRKY and MYB transcription factors[J]. Front Plant Sci, 2019, 10:1775. doi: 10.3389/fpls.2019.01775 URL
[55]	Lan J, Lin Q, Zhou C, et al. Small grain and semi-dwarf 3, a WRKY transcription factor, negatively regulates plant height and grain size by stabilizing SLR1 expression in rice[J]. Plant Mol Biol, 2020, 104(4/5):429-450. doi: 10.1007/s11103-020-01049-0 URL
[56]	Singh D, Debnath P, Roohi, et al. Expression of the tomato WRKY gene, SlWRKY23, alters root sensitivity to ethylene, auxin and JA and affects aerial architecture in transgenic Arabidopsis[J]. Physiol Mol Biol Plants, 2020, 26(6):1187-1199. doi: 10.1007/s12298-020-00820-3 URL
[57]	Zhao MM, Zhang XW, Liu YW, et al. A WRKY transcription factor, TaWRKY42-B, facilitates initiation of leaf senescence by promoting jasmonic acid biosynjournal[J]. BMC Plant Biol, 2020, 20(1):1-22. doi: 10.1186/s12870-019-2170-7 URL
[58]	Kang G, Yan D, Chen X, et al. HbWRKY82, a novel IIc WRKY transcription factor from Hevea brasiliensis associated with abiotic stress tolerance and leaf senescence in Arabidopsis[J]. Physiol Plant, 2021, 171(1):151-160. doi: 10.1111/ppl.v171.1 URL
[59]	Cui X, Zhao P, et al. A rapeseed WRKY transcription factor phosphorylated by CPK modulates cell death and leaf senescence by regulating the expression of ROS and SA-synjournal-related genes[J]. J Agric Food Chem, 2020, 68(28):7348-7359. doi: 10.1021/acs.jafc.0c02500 URL
[60]	Wang Y, Li Y, He SP, et al. A cotton(Gossypium hirsutum)WRKY transcription factor(GhWRKY22)participates in regulating anther/pollen development[J]. Plant Physiol Biochem, 2019, 141:231-239. doi: 10.1016/j.plaphy.2019.06.005 URL
[61]	Huang Z, Guo HD, Liu L, et al. Heterologous expression of dehydration-inducible MfWRKY17 of Myrothamnus flabellifolia confers drought and salt tolerance in Arabidopsis[J]. Int J Mol Sci, 2020, 21(13):4603. doi: 10.3390/ijms21134603 URL
[62]	苏琦, 尚宇航, 等. 植物WRKY转录因子研究进展[J]. 中国农学通报, 2007, 23(5):94-98.
	Su Q, Shang YH, et al. Progress on plant WRKY transcription factor[J]. Chin Agric Sci Bull, 2007, 23(5):94-98.
[63]	Jiang Y, Duan Y, Yin J, et al. Genome-wide identification and characterization of the Populus WRKY transcription factor family and analysis of their expression in response to biotic and abiotic stresses[J]. J Exp Bot, 2014, 65(22):6629-6644. doi: 10.1093/jxb/eru381 URL
[64]	Zhu H, Zhou YY, Zhai H, et al. A novel sweetpotato WRKY transcription factor, IbWRKY2, positively regulates drought and salt tolerance in transgenic Arabidopsis[J]. Biomolecules, 2020, 10(4):506. doi: 10.3390/biom10040506 URL
[65]	Wang MQ, Huang QX, Lin P, et al. The overexpression of a transcription factor gene VbWRKY32 enhances the cold tolerance in Verbena bonariensis[J]. Front Plant Sci, 2019, 10:1746. doi: 10.3389/fpls.2019.01746 URL
[66]	Li HL, Qu L, Guo D, et al. Histone deacetylase interacts with a WRKY transcription factor to regulate the expression of the small rubber particle protein gene from Hevea brasiliensis[J]. Ind Crop Prod, 2020, 145:111989. doi: 10.1016/j.indcrop.2019.111989 URL
[67]	Rushton PJ, Somssich IE, Ringler P, et al. WRKY transcription factors[J]. Trends Plant Sci, 2010, 15(5):247-258. doi: 10.1016/j.tplants.2010.02.006 pmid: 20304701
[68]	Ma Q, Xia Z, Cai Z, et al. GmWRKY16 enhances drought and salt tolerance through an ABA-mediated pathway in Arabidopsis thaliana[J]. Front Plant Sci, 2018, 9:1979. doi: 10.3389/fpls.2018.01979 URL
[69]	Wei W, Liang DW, Bian XH, et al. GmWRKY54 improves drought tolerance through activating genes in abscisic acid and Ca²⁺ signaling pathways in transgenic soybean[J]. Plant J, 2019, 100(2):384-398. doi: 10.1111/tpj.14449
[70]	Jiang Y, Qiu Y, Hu Y, et al. Heterologous expression of AtWRKY57 confers drought tolerance in Oryza sativa[J]. Front Plant Sci, 2016, 7:145.
[71]	Jaffar M, Song AP, Faheem M, et al. Involvement of CmWRKY10 in drought tolerance of Chrysanthemum through the ABA-signaling pathway[J]. Int J Mol Sci, 2016, 17(5):693. doi: 10.3390/ijms17050693 URL
[72]	Ahammed GJ, Li X, Yang YX, et al. Tomato WRKY81 acts as a negative regulator for drought tolerance by modulating guard cell H₂O₂-mediated stomatal closure[J]. Environ Exp Bot, 2020, 171:103960. doi: 10.1016/j.envexpbot.2019.103960 URL
[73]	Liu Y, Yang T, Lin Z, et al. A WRKY transcription factor PbrWRKY53 from Pyrus betulaefolia is involved in drought tolerance and AsA accumulation[J]. Plant Biotechnol J, 2019, 17(9):1770-1787.
[74]	Munns R, Tester M. Mechanisms of salinity tolerance[J]. Annu Rev Plant Biol, 2008, 59:651-681. doi: 10.1146/annurev.arplant.59.032607.092911 pmid: 18444910
[75]	Xu Z, Raza Q, Xu L, et al. GmWRKY49, a salt-responsive nuclear protein, improved root length and governed better salinity tolerance in transgenic Arabidopsis[J]. Front Plant Sci, 2018, 9:809. doi: 10.3389/fpls.2018.00809 URL
[76]	Wang K, Wu YH, Tian XQ, et al. Overexpression of DgWRKY4 enhances salt tolerance in Chrysanthemum seedlings[J]. Front Plant Sci, 2017, 8:1592. doi: 10.3389/fpls.2017.01592 pmid: 28959270
[77]	Li P, Song A, Gao C, et al. Chrysanthemum WRKY gene CmWRKY17 negatively regulates salt stress tolerance in transgenic Chrysanthemum and Arabidopsis plants[J]. Plant Cell Rep, 2015, 34(8):1365-1378. doi: 10.1007/s00299-015-1793-x URL
[78]	Zhu D, Hou LX, Xiao PL, et al. VvWRKY30, a grape WRKY transcription factor, plays a positive regulatory role under salinity stress[J]. Plant Sci, 2019, 280:132-142. doi: 10.1016/j.plantsci.2018.03.018 URL
[79]	Zhou L, Wang NN, Gong SY, et al. Overexpression of a cotton(Gossypium hirsutum)WRKY gene, GhWRKY34, in Arabidopsis enhances salt-tolerance of the transgenic plants[J]. Plant Physiol Biochem, 2015, 96:311-320. doi: 10.1016/j.plaphy.2015.08.016 URL
[80]	Lv B, Wu Q, Wang A, et al. A WRKY transcription factor, FtWRKY46, from Tartary buckwheat improves salt tolerance in transgenic Arabidopsis thaliana[J]. Plant Physiol Biochem, 2020, 147:43-53. doi: 10.1016/j.plaphy.2019.12.004 URL
[81]	Dong Q, Zheng W, Duan D, et al. MdWRKY30, a group IIa WRKY gene from apple, confers tolerance to salinity and osmotic stresses in transgenic apple callus and Arabidopsis seedlings[J]. Plant Sci, 2020, 299:110611. doi: 10.1016/j.plantsci.2020.110611 URL
[82]	El-Esawi MA, Al-Ghamdi AA, et al. Overexpression of AtWRKY30 transcription factor enhances heat and drought stress tolerance in wheat(Triticum aestivum L.)[J]. Genes, 2019, 10(2):163. doi: 10.3390/genes10020163 URL
[83]	He GH, Xu JY, Wang YX, et al. Drought-responsive WRKY transcription factor genes TaWRKY1 and TaWRKY33 from wheat confer drought and/or heat resistance in Arabidopsis[J]. BMC Plant Biol, 2016, 16(1):116. doi: 10.1186/s12870-016-0806-4 URL
[84]	Li S, Fu Q, Huang W, et al. Functional analysis of an Arabidopsis transcription factor WRKY25 in heat stress[J]. Plant Cell Rep, 2009, 28(4):683-693. doi: 10.1007/s00299-008-0666-y URL
[85]	Li SJ, Fu QT, Chen LG, et al. Arabidopsis thaliana WRKY25, WRKY26, and WRKY33 coordinate induction of plant thermotolerance[J]. Planta, 2011, 233(6):1237-1252. doi: 10.1007/s00425-011-1375-2 URL
[86]	Kim CY, Vo KTX, Nguyen CD, et al. Functional analysis of a cold-responsive rice WRKY gene, OsWRKY71[J]. Plant Biotechnol Rep, 2016, 10(1):13-23. doi: 10.1007/s11816-015-0383-2 URL
[87]	Yokotani N, Sato Y, et al. WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance[J]. J Exp Bot, 2013, 64(16):5085-5097. doi: 10.1093/jxb/ert298 pmid: 24043853
[88]	Martin MH, Marschner H. The mineral nutrition of higher plants[J]. J Ecol, 1988, 76(4):1250.
[89]	Xu L, Jin L, Long L, et al. Overexpression of GbWRKY1 positively regulates the Pi starvation response by alteration of auxin sensitivity in Arabidopsis[J]. Plant Cell Rep, 2012, 31(12):2177-2188. doi: 10.1007/s00299-012-1328-7 URL
[90]	Dai X, Wang Y, Zhang WH. OsWRKY74, a WRKY transcription factor, modulates tolerance to phosphate starvation in rice[J]. J Exp Bot, 2016, 67(3):947-960. doi: 10.1093/jxb/erv515 URL
[91]	Wang H, Xu Q, Kong YH, et al. Arabidopsis WRKY45 transcription factor activates phosphate transporter1;1 expression in response to phosphate starvation[J]. Plant Physiol, 2014, 164(4):2020-2029. doi: 10.1104/pp.113.235077 pmid: 24586044
[92]	Wu TY, Krishnamoorthi S, et al. Crosstalk between heterotrimeric G protein-coupled signaling pathways and WRKY transcription factors modulating plant responses to suboptimal micronutrient conditions[J]. J Exp Bot, 2020, 71(10):3227-3239. doi: 10.1093/jxb/eraa108 URL
[93]	Gao K, Zhou T, Hua Y, et al. Transcription factor WRKY23 is involved in ammonium-induced repression of Arabidopsis primary root growth under ammonium toxicity[J]. Plant Physiol Biochem, 2020, 150:90-98. doi: 10.1016/j.plaphy.2020.02.034 URL
[94]	Chun XL, Jing YY, Jiang YR, et al. A WRKY transcription factor confers aluminum tolerance via regulation of cell wall modifying genes[J]. J Integr Plant Biol, 2020, 62(8):1176-1192. doi: 10.1111/jipb.v62.8 URL
[95]	Li GZ, Wang ZQ, Yokosho K, et al. Transcription factor WRKY22 promotes aluminum tolerance via activation of OsFRDL4 expression and enhancement of citrate secretion in rice(Oryza sativa)[J]. New Phytol, 2018, 219(1):149-162. doi: 10.1111/nph.2018.219.issue-1 URL
[96]	Ye J, Wang X, Hu TX, et al. An InDel in the promoter of alactivated malate transporter9 selected during tomato domestication determines fruit malate contents and aluminum tolerance[J]. Plant Cell, 2017, 29(9):2249-2268. doi: 10.1105/tpc.17.00211 URL
[97]	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 Environ, 2019, 42(3):891-903. doi: 10.1111/pce.v42.3 URL
[98]	Kang GJ, Yan D, Chen XL, et al. Molecular characterization and functional analysis of a novel WRKY transcription factor HbWRKY83 possibly involved in rubber production of Hevea brasiliensis[J]. Plant Physiol Biochem, 2020, 155:483-493. doi: 10.1016/j.plaphy.2020.08.013 URL
[99]	Bi M, Li X, Yan X, et al. Chrysanthemum WRKY15-1 promotes resistance to Puccinia horiana Henn. via the salicylic acid signaling pathway[J]. Hortic Res, 2021, 8(1):6. doi: 10.1038/s41438-020-00436-4 URL
[100]	Zhang F, Wang F, Yang S, et al. MdWRKY100 encodes a group I WRKY transcription factor in Malus domestica that positively regulates resistance to Colletotrichum gloeosporioides infection[J]. Plant Sci, 2019, 286:68-77. doi: S0168-9452(19)30063-9 pmid: 31300143
[101]	Dang F, Wang Y, She J, et al. Overexpression of CaWRKY27, a subgroup IIe WRKY transcription factor of Capsicum annuum, positively regulates tobacco resistance to Ralstonia solanacearum infection[J]. Physiol Plant, 2014, 150(3):397-411. doi: 10.1111/ppl.2014.150.issue-3 URL
[102]	Wang X, Li JJ, Guo J, et al. The WRKY transcription factor PlWRKY65 enhances the resistance of Paeonia lactiflora(herbaceous peony)to Alternaria tenuissima[J]. Hortic Res, 2020, 7:57. doi: 10.1038/s41438-020-0267-7 URL
[103]	Cui XX, Yan Q, Gan SP, et al. GmWRKY40, a member of the WRKY transcription factor genes identified from Glycine max L., enhanced the resistance to Phytophthora sojae[J]. BMC Plant Biol, 2019, 19(1):598. doi: 10.1186/s12870-019-2132-0 URL
[104]	Han X, Zhang L, Zhao L, et al. SnRK1 phosphorylates and destabilizes WRKY3 to enhance barley immunity to powdery mildew[J]. Plant Commun, 2020, 1(4):100083. doi: 10.1016/j.xplc.2020.100083 URL
[105]	Zheng Z, Mosher SL, Fan B, et al. Functional analysis of Arabidopsis WRKY25 transcription factor in plant defense against Pseudomonas syringae[J]. BMC Plant Biol, 2007, 7:2. pmid: 17214894
[106]	Kim KC, Lai Z, Fan B, et al. Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense[J]. Plant Cell, 2008, 20(9):2357-2371. doi: 10.1105/tpc.107.055566 URL
[107]	de Vos M, Kim JH, Jander G. Biochemistry and molecular biology of Arabidopsis-aphid interactions[J]. Bioessays, 2007, 29(9):871-883. doi: 10.1002/(ISSN)1521-1878 URL
[108]	Grunewald W, Karimi M, Wieczorek K, et al. A role for AtWRKY23 in feeding site establishment of plant-parasitic nematodes[J]. Plant Physiol, 2008, 148(1):358-368. doi: 10.1104/pp.108.119131 pmid: 18599655
[109]	Skibbe M, Qu N, Galis I, et al. Induced plant defenses in the natural environment:Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory[J]. Plant Cell, 2008, 20(7):1984-2000. doi: 10.1105/tpc.108.058594 URL
[110]	Atamian HS, Eulgem T, Kaloshian I. SlWRKY70 is required for Mi-1-mediated resistance to aphids and nematodes in tomato[J]. Planta, 2012, 235(2):299-309. doi: 10.1007/s00425-011-1509-6 pmid: 21898085
[111]	Kloth KJ, Wiegers GL, Busscher-Lange J, et al. AtWRKY22 promotes susceptibility to aphids and modulates salicylic acid and jasmonic acid signalling[J]. J Exp Bot, 2016, 67(11):3383-3396. doi: 10.1093/jxb/erw159 URL
[112]	Yin M, Song N, Chen S, et al. NaKTI2, a Kunitz trypsin inhibitor transcriptionally regulated by NaWRKY3 and NaWRKY6, is required for herbivore resistance in Nicotiana attenuata[J]. Plant Cell Rep, 2021, 40(1):97-109. doi: 10.1007/s00299-020-02616-x URL
[113]	Amato A, Cavallini E, Zenoni S, et al. A grapevine TTG2-like WRKY transcription factor is involved in regulating vacuolar transport and flavonoid biosynjournal[J]. Front Plant Sci, 2016, 7:1979.
[114]	Zhou C, Lin Q, Lan J, et al. WRKY transcription factor OsWRKY29 represses seed dormancy in rice by weakening abscisic acid response[J]. Front Plant Sci, 2020, 11:691. doi: 10.3389/fpls.2020.00691 URL
[115]	Yang Y, Wang N, Zhao SJ. Functional characterization of a WRKY family gene involved in somatic embryogenesis in Panax ginseng[J]. Protoplasma, 2020, 257(2):449-458. doi: 10.1007/s00709-019-01455-2 pmid: 31760482
[116]	Huang RW, Liu DF, Huang M, et al. CpWRKY71, a WRKY transcription factor gene of wintersweet(Chimonanthus praecox), promotes flowering and leaf senescence in Arabidopsis[J]. Int J Mol Sci, 2019, 20(21):E5325.
[117]	Hu JF, Fang HC, Wang J, et al. Ultraviolet B-induced MdWRKY72 expression promotes anthocyanin synjournal in apple[J]. Plant Sci, 2020, 292:110377. doi: 10.1016/j.plantsci.2019.110377 URL
[118]	Qu L, Li HL, Guo D, et al. HbWRKY27, a group IIe WRKY transcription factor, positively regulates HbFPS₁ expression in Hevea brasiliensis[J]. Sci Rep, 2020, 10(1):1-8. doi: 10.1038/s41598-019-56847-4 URL
[119]	Xiao Y, Feng J, Li Q, et al. IiWRKY34 positively regulates yield, lignan biosynjournal and stress tolerance in Isatis indigotica[J]. Acta Pharm Sin B, 2020, 10(12):2417-2432. doi: 10.1016/j.apsb.2019.12.020 URL
[120]	Hao X, Xie C, Ruan Q, et al. The transcription factor OpWRKY₂ positively regulates the biosynjournal of the anticancer drug camptothecin in Ophiorrhiza pumila[J]. Hortic Res, 2021, 8(1):7. doi: 10.1038/s41438-020-00437-3 URL
[121]	Wang D, Jiang C, Liu W, et al. The WRKY53 transcription factor enhances stilbene synjournal and disease resistance by interacting with MYB14 and MYB15 in Chinese wild grape[J]. J Exp Bot, 2020, 71(10):3211-3226. doi: 10.1093/jxb/eraa097 pmid: 32080737
[122]	Li XY, He L, An XH, et al. VviWRKY40, a WRKY transcription factor, regulates glycosylated monoterpenoid production by VviGT14 in grape berry[J]. Genes, 2020, 11(5):485. doi: 10.3390/genes11050485 URL
[123]	Yao L, Wang J, Sun JC, et al. A WRKY transcription factor, PgWRKY4X, positively regulates ginsenoside biosynjournal by activating squalene epoxidase transcription in Panax ginseng[J]. Ind Crop Prod, 2020, 154:112671. doi: 10.1016/j.indcrop.2020.112671 URL