Molecular cloning and expression analysis of a WRKY transcription factor gene, GbWRKY20, from Ginkgo biloba

References

• Wei KF, Chen J, Chen YF, Wu LJ, Xie DX. Molecular phylogenetic and expression analysis of the complete WRKY transcription factor family in maize. DNA Res. 2012;19(2):1–9. doi:10.1093/dnares/dsr048.
   PubMed Web of Science ®Google Scholar
• Bao W, Wang X, Chen M, Chai T, Wang H. A WRKY transcription factor, PcWRKY33, from Polygonum cuspidatum reduces salt tolerance in transgenic Arabidopsis thaliana. Plant Cell Rep. 2018;37(7):1033–1048. doi:10.1007/s00299-018-2289-2.
   PubMed Web of Science ®Google Scholar
• Rajappa S, Krishnamurthy P, Kumar PP. Regulation of AtKUP2 Expression by bHLH and WRKY Transcription Factors Helps to Confer Increased Salt Tolerance to Arabidopsis thaliana Plants. Front Plant Sci. 2020;11:1311. doi:10.3389/fpls.2020.01311.
   PubMedGoogle Scholar
• Goyal P, Manzoor MM, Vishwakarma RA, Sharma D, Dhar MK, Gupta SA. A Comprehensive Transcriptome-Wide Identification and Screening of WRKY Gene Family Engaged in Abiotic Stress in Glycyrrhiza glabra. Sci Rep. 2020;10(1). doi:10.1038/s41598-019-57232-x.
   Web of Science ®Google Scholar
• Wang Q, Wang M, Zhang X, Hao B, Kaushik SK, Pan Y. WRKY gene family evolution in Arabidopsis thaliana. Genetica. 2011;139(8):973–983. doi:10.1007/s10709-011-9599-4.
   PubMed Web of Science ®Google Scholar
• Huang S, Gao Y, Liu J, Peng X, Niu X, Fei Z, Cao S, Liu Y. Genome-wide analysis of WRKY transcription factors in Solanum lycopersicum. Mol Genet Genomics. 2012;287(6):495–513. doi:10.1007/s00438-012-0696-6.
   PubMed Web of Science ®Google Scholar
• Imran QM, Hussain A, Mun B-G, Lee SU, Asaf S, Ali MA, Lee I-J, Yun B-W. Transcriptome wide identification and characterization of NO-responsive WRKY transcription factors in Arabidopsis thaliana L. Environ Exp Bot. 2018;148:128–143. doi:10.1016/j.envexpbot.2018.01.010.
   Web of Science ®Google Scholar
• Govardhana M, Kumudini BS. In-silico analysis of cucumber (Cucumis sativus L.) Genome for WRKY transcription factors and cis-acting elements. Comput Biol Chem. 2020;85:107212. doi:10.1016/j.compbiolchem.2020.107212.
   PubMed Web of Science ®Google Scholar
• Li W, Pang S, Lu Z, Jin B. Function and Mechanism of WRKY Transcription Factors in Abiotic Stress Responses of Plants. Plants (Basel). 2020:9. doi:10.3390/plants9111515.
   Google Scholar
• Kanofsky K, Rusche J, Eilert L, Machens F, Hehl R. Unusual DNA-binding properties of the Arabidopsis thaliana WRKY50 transcription factor at target gene promoters. Plant Cell Rep. 2021;40(1):69–83. doi:10.1007/s00299-020-02611-2.
   PubMed Web of Science ®Google Scholar
• Llorca CM, Potschin M, Zentgraf U. bZIPs and WRKYs: two large transcription factor families executing two different functional strategies. Front Plant Sci. 2014;5:169. doi:10.3389/fpls.2014.00169.
   PubMed Web of Science ®Google Scholar
• Zhang M, Chen Y, Nie L, Jin X, Liao W, Zhao S, Fu C, Yu L. Transcriptome-wide identification and screening of WRKY factors involved in the regulation of taxol biosynthesis in Taxus chinensis. Sci Rep. 2018;8(1):5197. doi:10.1038/s41598-018-23558-1.
   PubMedGoogle Scholar
• Jiang C, Shen QJ, Wang B, He B, Xiao S, Chen L, Yu T, Ke X, Zhong Q, Fu J, et al. Transcriptome analysis of WRKY gene family in Oryza officinalis Wall ex Watt and WRKY genes involved in responses to Xanthomonas oryzae pv. oryzae stress. PLoS One. 2017;12(11):e0188742. doi:10.1371/journal.pone.0188742.
   PubMed Web of Science ®Google Scholar
• Qu R, Cao Y, Tang X, Sun L, Wei L, Wang K. Identification and expression analysis of the WRKY gene family in Isatis indigotica. Gene. 2021;783:145561. doi:10.1016/j.gene.2021.145561.
   PubMed Web of Science ®Google Scholar
• Song H, Wang P, Hou L, Zhao S, Zhao C, Xia H, Li P, Zhang Y, Bian X, Wang X. Global Analysis of WRKY Genes and Their Response to Dehydration and Salt Stress in Soybean. Front Plant Sci. 2016;7:9. doi:10.3389/fpls.2016.00009.
   PubMed Web of Science ®Google Scholar
• Dou L, Zhang X, Pang C, Song M, Wei H, Fan S, Yu S. Genome-wide analysis of the WRKY gene family in cotton. Mol Genet Genomics. 2014;289(6):1103–1121. doi:10.1007/s00438-014-0872-y.
   PubMed Web of Science ®Google Scholar
• He H, Dong Q, Shao Y, Jiang H, Zhu S, Cheng B, Xiang Y. Genome-wide survey and characterization of the WRKY gene family in Populus trichocarpa. Plant Cell Rep. 2012;31(7):1199–1217. doi:10.1007/s00299-012-1241-0.
   PubMed Web of Science ®Google Scholar
• Xiong W, Xu X, Zhang L, Wu P, Chen Y, Li M, Jiang H, Wu G. Genome-wide analysis of the WRKY gene family in physic nut (Jatropha curcas L.). Gene. 2013;524(2):124–132. doi:10.1016/j.gene.2013.04.047.
   PubMed Web of Science ®Google Scholar
• Agarwal P, Reddy MP, Chikara J. WRKY: its structure, evolutionary relationship, DNA-binding selectivity, role in stress tolerance and development of plants. Mol Biol Rep. 2011;38(6):3883–3896. doi:10.1007/s11033-010-0504-5.
   PubMed Web of Science ®Google Scholar
• Goel R, Pandey A, Trivedi PK, Asif MH. Genome-Wide Analysis of the Musa WRKY Gene Family: evolution and Differential Expression during Development and Stress. Front Plant Sci. 2016;7:299. doi:10.3389/fpls.2016.00299.
   PubMed Web of Science ®Google Scholar
• Zhang C-Q, Xu Y, Lu Y, Yu H-X, Gu M-H, Liu -Q-Q. The WRKY transcription factor OsWRKY78 regulates stem elongation and seed development in rice. Planta. 2011;234(3):541–554. doi:10.1007/s00425-011-1423-y.
   PubMed Web of Science ®Google Scholar
• Ding ZJ, Yan JY, Li CX, Li GX, Wu YR, Zheng SJ. Transcription factor WRKY46 modulates the development of Arabidopsis lateral roots in osmotic/salt stress conditions via regulation of ABA signaling and auxin homeostasis. Plant J. 2015;84(1):56–69. doi:10.1111/tpj.12958.
   PubMed Web of Science ®Google Scholar
• Shirazi FA, Razi H, Niazi A, Alemzadeh A. Molecular cloning and expression analysis of a stress-responsive WRKY transcription factor gene, BnWRKY57, from Brassica napus. Plant Omics. 2019:37-47. doi:10.21475/poj.12.01.19.pt1792.
   Google Scholar
• Bai Y, Sunarti S, Kissoudis C, Visser RGF, Van Der Linden CG. The Role of Tomato WRKY Genes in Plant Responses to Combined Abiotic and Biotic Stresses. Front Plant Sci. 2018;9:801. doi:10.3389/fpls.2018.00801.
   PubMed Web of Science ®Google Scholar
• Gao H, Wang Y, Xu P, Zhang Z. Overexpression of a WRKY Transcription Factor TaWRKY2 Enhances Drought Stress Tolerance in Transgenic Wheat. Front Plant Sci. 2018;9:997. doi:10.3389/fpls.2018.00997.
   PubMed Web of Science ®Google Scholar
• Zhu D, Hou L, Xiao P, Guo Y, Deyholos MK. VvWRKY30 LX. a grape WRKY transcription factor, plays a positive regulatory role under salinity stress. Plant Sci. 2019;280:132–142. doi:10.1016/j.plantsci.2018.03.018.
   PubMed Web of Science ®Google Scholar
• Li X, Tang Y, Zhou C, Zhang L, Lv JA. Wheat WRKY Transcription Factor TaWRKY46 Enhances Tolerance to Osmotic Stress in transgenic Arabidopsis Plants. Int J Mol Sci. 2020:21. doi:10.3390/ijms21041321.
   Web of Science ®Google Scholar
• Suttipanta N, Pattanaik S, Kulshrestha M, Patra B, Singh SK, Yuan L. The Transcription Factor CrWRKY1 Positively Regulates the Terpenoid Indole Alkaloid Biosynthesis in Catharanthus roseus. Plant Physiol. 2011;157(4):2081–2093. doi:10.1104/pp.111.181834.
   PubMed Web of Science ®Google Scholar
• Xu YH, Wang JW, Wang S, Wang JY, Chen XY. Characterization of GaWRKY1, a Cotton Transcription Factor That Regulates the Sesquiterpene Synthase Gene (+)-δ-Cadinene Synthase-A. Plant Physiol. 2004;135(1):507–515. doi:10.1104/pp.104.038612.
   PubMed Web of Science ®Google Scholar
• Zhang L, Chen C, Xie F, Hua Q, Zhang Z, Zhang R, Chen J, Zhao J, Hu G, Qin YA. Novel WRKY Transcription Factor HmoWRKY40 Associated with Betalain Biosynthesis in Pitaya (Hylocereus monacanthus) through Regulating HmoCYP76AD1. Int J Mol Sci. 2021:22. doi:10.3390/ijms22042171.
   Web of Science ®Google Scholar
• Li X, He L, An X, Yu K, Meng N, Duan CQ, Pan QH. VviWRKY40, a WRKY Transcription Factor, Regulates Glycosylated Monoterpenoid Production by VviGT14 in Grape Berry. Genes (Basel). 2020;11(5):485. doi:10.3390/genes11050485.
   Web of Science ®Google Scholar
• Li W, Yang S, Lu Z, He Z, Ye Y, Zhao B, Wang L, Jin B. Cytological, physiological, and transcriptomic analyses of golden leaf coloration in Ginkgo biloba L. Hortic Res. 2018;5(1):12. doi:10.1038/s41438-018-0015-4.
   PubMedGoogle Scholar
• Chang B, Ma K, Lu Z, Lu J, Cui J, Wang L, Jin B. Physiological, Transcriptomic, and Metabolic Responses of Ginkgo biloba L. to Drought, Salt, and Heat Stresses. Biomolecules. 2020;10(12):1635. doi:10.3390/biom10121635.
   Web of Science ®Google Scholar
• Singh SK, Srivastav S, Castellani RJ, Plascencia-Villa G, Perry G. Neuroprotective and Antioxidant Effect of Ginkgo biloba Extract Against AD and Other Neurological Disorders. Neurotherapeutics. 2019;16(3):666–674. doi:10.1007/s13311-019-00767-8.
   PubMed Web of Science ®Google Scholar
• Yang Y, Li Y, Wang J, Sun K, Tao W, Wang Z, Xiao W, Pan Y, Zhang S, Wang Y. Systematic Investigation of Ginkgo Biloba Leaves for Treating Cardio-cerebrovascular Diseases in an Animal Model. ACS Chem Biol. 2017;12(5):1363–1372. doi:10.1021/acschembio.6b00762.
   PubMed Web of Science ®Google Scholar
• Ni J, Dong L, Jiang Z, Yang X, Chen Z, Wu Y, Xu M, Min XJ. Comprehensive transcriptome analysis and flavonoid profiling of Ginkgo leaves reveals flavonoid content alterations in day-night cycles. PLoS One. 2018;13(3):e0193897. doi:10.1371/journal.pone.0193897.
   PubMed Web of Science ®Google Scholar
• Xu F, Li L, Zhang W, Cheng H, Sun N, Cheng S, Wang Y. Isolation, characterization, and function analysis of a flavonol synthase gene from Ginkgo biloba. Mol Biol Rep. 2012;39(3):2285–2296. doi:10.1007/s11033-011-0978-9.
   PubMed Web of Science ®Google Scholar
• Xu N, Liu S, Lu Z, Pang S, Wang L, Wang L, Li W. Gene Expression Profiles and Flavonoid Accumulation during Salt Stress in Ginkgo biloba Seedlings. Plants (Basel). 2020;9(9). doi:10.3390/plants9091162.
   Google Scholar
• Yang X, Zhou T, Wang M, Li T, Wang G, Fu FF, Cao F. Systematic investigation and expression profiles of the GbR2R3-MYB transcription factor family in ginkgo (Ginkgo biloba L.). Int J Biol Macromol. 2021;172:250–262. doi:10.1016/j.ijbiomac.2021.01.053.
   PubMed Web of Science ®Google Scholar
• Zhou X, Liao Y, Kim S-U, Chen Z, Nie G, Cheng S, Ye J, Xu F. Genome-wide identification and characterization of bHLH family genes from Ginkgo biloba. Sci Rep. 2020;10(1):1–15. doi:10.1038/s41598-019-56847-4.
   PubMedGoogle Scholar
• Yang F, Xu F, Wang X, Liao Y, Chen Q, Meng X. Characterization and functional analysis of a MADS-box transcription factor gene (GbMADS9) from Ginkgo biloba. Sci Hortic (Amsterdam). 2016;212:104–114. doi:10.1016/j.scienta.2016.09.042.
   Web of Science ®Google Scholar
• Jager M, Hassanin A, Manuel M, Le Guyader H, Deutsch J. MADS-box genes in Ginkgo biloba and the evolution of the AGAMOUS family. Mol Biol Evol. 2003;20(5):842–854. doi:10.1093/molbev/msg089.
   PubMed Web of Science ®Google Scholar
• Cheng S, Liu X, Liao Y, Zhang W, Ye J, Rao S, Xu F. Genome-Wide Identification of WRKY Family Genes and Analysis of Their Expression in Response to Abiotic Stress in Ginkgo biloba L. Notulae Botanicae Horti Agrobotanici Cluj-Napoca. 2019;47(4):1100–1115. doi:10.15835/nbha47411651.
   Web of Science ®Google Scholar
• Liao YL, Shen YB, Chang J, Zhang WW, Cheng SY, Xu F. Isolation, Expression, and Promoter Analysis of GbWRKY2: a Novel Transcription Factor Gene from Ginkgo biloba. Int J Genomics. 2015;2015:607185. doi:10.1155/2015/607185.
   PubMed Web of Science ®Google Scholar
• Liao YL, Xu F, Zang WW, Cheng SY, Shen YB, Chang J. Cloning, Characterization and Expression Analysis of GbWRKY11, a Novel Transcription Factor Gene in Ginkgo biloba. International Journal of Agriculture and Biology. 2015;18(1):117–124. doi:10.17957/ijab/15.0072.
   Web of Science ®Google Scholar
• Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 2013;30(12):2725–2729. doi:10.1093/molbev/mst197.
   PubMed Web of Science ®Google Scholar
• Zhou T, Yang X, Fu F, Wang G, Cao F. Selection of Suitable Reference Genes Based on Transcriptomic Data in Ginkgo biloba under Different Experimental Conditions. Forests. 2020;11(11):1217. doi:10.3390/f11111217.
   Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. methods. 2001;25(4):402–408. doi:10.1006/meth.2001.1262.
   PubMed Web of Science ®Google Scholar
• Chen L, Song Y, Li S, Zhang L, Zou C, Yu D. The role of WRKY transcription factors in plant abiotic stresses. Biochim Biophys Acta. 2012;1819(2):120–128. doi:10.1016/j.bbagrm.2011.09.002.
   PubMed Web of Science ®Google Scholar
• Yu Y, Wang L, Chen J, Liu Z, Park CM, Xiang F. WRKY71 Acts Antagonistically Against Salt-Delayed Flowering in Arabidopsis thaliana. Plant Cell Physiol. 2018;59(2):414–422. doi:10.1093/pcp/pcx201.
   PubMed Web of Science ®Google Scholar
• Li D, Liu P, Yu J, Wang L, Dossa K, Zhang Y, Zhou R, Wei X, Zhang X. Genome-wide analysis of WRKY gene family in the sesame genome and identification of the WRKY genes involved in responses to abiotic stresses. BMC Plant Biol. 2017;17(1):152. doi:10.1186/s12870-017-1099-y.
   PubMedGoogle Scholar
• Wang Y, Guo D, Li HL, Peng SQ. Characterization of HbWRKY1, a WRKY transcription factor from Hevea brasiliensis that negatively regulates HbSRPP. Plant Physiol Biochem. 2013;71:283–289. doi:10.1016/j.plaphy.2013.07.020.
   PubMed Web of Science ®Google Scholar
• Wu M, Liu H, Han G, Cai R, Pan F, Xiang Y. A moso bamboo WRKY gene PeWRKY83 confers salinity tolerance in transgenic Arabidopsis plants. Sci Rep. 2017;7(1):11721. doi:10.1038/s41598-017-10795-z.
   PubMedGoogle Scholar
• Zhao K, Zhang D, Lv K, Zhang X, Cheng Z, Li R, Zhou B, Jiang T. Functional characterization of poplar WRKY75 in salt and osmotic tolerance. Plant Sci. 2019;289:110259. doi:10.1016/j.plantsci.2019.110259.
   PubMed Web of Science ®Google Scholar
• Xu M, Wu C, Zhao L, Wang Y, Wang C, Zhou W, Ming Y, Kai G. WRKY transcription factor OpWRKY1 acts as a negative regulator of camptothecin biosynthesis in Ophiorrhiza pumila hairy roots. Plant Cell, Tissue and Organ Culture (PCTOC). 2020;142(1):69–78. doi:10.1007/s11240-020-01833-2.
   Web of Science ®Google Scholar
• Alfieri M, Vaccaro MC, Cappetta E, Ambrosone A, De Tommasi N, Leone A. Coactivation of MEP-biosynthetic genes and accumulation of abietane diterpenes in Salvia sclarea by heterologous expression of WRKY and MYC2 transcription factors. Sci Rep. 2018;8(1):1–13. doi:10.1038/s41598-018-29389-4.
   PubMedGoogle Scholar
• Ma D, Pu G, Lei C, Ma L, Wang H, Guo Y, Chen J, Du Z, Wang H, Li G, et al. 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 Cell Physiol. 2009;50(12):2146–2161. doi:10.1093/pcp/pcp149.
   PubMed Web of Science ®Google Scholar
• Wang Y, Shu Z, Wang W, Jiang X, Li D, Pan J, Li X. CsWRKY2, a novel WRKY gene from Camellia sinensis, is involved in cold and drought stress responses. Biologia Plantarum. 2016;60(3):443–451. doi:10.1007/s10535-016-0618-2.
   Web of Science ®Google Scholar
• Nuruzzaman M, Cao H, Xiu H, Luo T, Li J, Chen X, Luo J, Luo Z. Transcriptomics-based identification of WRKY genes and characterization of a salt and hormone-responsive PgWRKY1 gene in Panax ginseng. Acta Biochim Biophys Sin (Shanghai). 2016;48(2):117–131. doi:10.1093/abbs/gmv122.
   PubMed Web of Science ®Google Scholar
• Li L, Liu Q, Liu T, Cui X, Ning W. Expression of putative luteolin biosynthesis genes and WRKY transcription factors in Taraxacum antungense kitag. Plant Cell, Tissue and Organ Culture (PCTOC). 2021. doi:10.1007/s11240-021-02035-0.
   Web of Science ®Google Scholar
• Lui S, Luo C, Zhu L, Sha R, Qu S, Cai B, Wang S. Identification and expression analysis of WRKY transcription factor genes in response to fungal pathogen and hormone treatments in apple (Malus domestica). Journal of Plant Biology. 2017;60(2):215–230. doi:10.1007/s12374-016-0577-3.
   Web of Science ®Google Scholar
• Sabater-Jara AB, Souliman-Youssef S, Novo-Uzal E, Almagro L, Belchí-Navarro S, Pedreño MA. Biotechnological approaches to enhance the biosynthesis of ginkgolides and bilobalide in Ginkgo biloba. Phytochemistry Reviews. 2013;12(1):191–205. doi:10.1007/s11101-013-9275-7.
   Web of Science ®Google Scholar
• Cheng S-Y, Xu F, Wang Y. Advances in the study of flavonoids in Ginkgo biloba leaves. Journal of Medicinal Plants Research. 2009;3:1248–1252.
   Web of Science ®Google Scholar
• Gong YF, Liao ZH, Guo BH, Sun XF, Tang KX. Molecular Cloning and Expression Profile Analysis of Ginkgo biloba DXS Gene Encoding 1-Deoxy-D-xylulose 5-Phosphate Synthase, the First Committed Enzyme of the 2-C-Methyl-D-erythritol 4-Phosphate Pathway. Planta Med. 2006;72(4):329–335. doi:10.1055/s-2005-916234.
   PubMed Web of Science ®Google Scholar
• Kim SM, Kim SU. Characterization of 1-hydroxy-2-methyl-2-(E)-butenyl-4-diphosphate synthase (HDS) gene from Ginkgo biloba. Mol Biol Rep. 2010;37(2):973–979. doi:10.1007/s11033-009-9771-4.
   PubMed Web of Science ®Google Scholar
• Wang NN, Xu SW, Sun YL, Liu D, Zhou L, Li Y, Li XB. The cotton WRKY transcription factor (GhWRKY33) reduces transgenic Arabidopsis resistance to drought stress. Sci Rep. 2019;9(1):724. doi:10.1038/s41598-018-37035-2..
   PubMedGoogle Scholar
• Yousfi FE, Makhloufi E, Marande W, Ghorbel AW, Bouzayen M, Berges H. Comparative Analysis of WRKY Genes Potentially Involved in Salt Stress Responses in Triticum turgidum L. ssp. durum. Front Plant Sci. 2016;7:2034. doi:10.3389/fpls.2016.02034.
   PubMed Web of Science ®Google Scholar
• Agarwal P, Dabi M, Agarwal PK. Molecular Cloning and Characterization of a Group II WRKY Transcription Factor from Jatropha curcas, an Important Biofuel Crop. DNA Cell Biol. 2014;33(8):503–513. doi:10.1089/dna.2014.2349.
   PubMed Web of Science ®Google Scholar
• Lv B, Wu Q, Wang A, Li Q, Dong Q, Yang J, Zhao H, Wang X, Chen H, Li C. A WRKY transcription factor, FtWRKY46, from Tartary buckwheat improves salt tolerance in transgenic Arabidopsis thaliana. Plant Physiol Biochem. 2020;147:43–53. doi:10.1016/j.plaphy.2019.12.004.
   PubMed Web of Science ®Google Scholar
• Zhu H, Zhou Y, Zhai H, He S, Zhao N, Liu QA. Novel Sweetpotato WRKY Transcription Factor, IbWRKY2, Positively Regulates Drought and Salt Tolerance in Transgenic Arabidopsis. Biomolecules. 2020;10(4):506. doi:10.3390/biom10040506.
   Web of Science ®Google Scholar
• Yang J, Chen H, Yang C, Ding Q, Zhao T, Wang D. A WRKY transcription factor WRKY184 from Brassica napus L. is involved in flowering and secondary wall development in transgenic Arabidopsis thaliana. Plant Growth Regul. 2020;92(2):427–440. doi:10.1007/s10725-020-00652-x.
   Web of Science ®Google Scholar