Genome-Wide Identification of WRKY Family Genes and Analysis of Their Expression in Response to Abiotic Stress in Ginkgo biloba L.
Ginkgo biloba is widely planted, and the extracts of leaves contain flavonoids, terpene esters and other medicinal active ingredients. WRKY proteins are a large transcription factor family in plants, which play an important role in the regulation of plant secondary metabolism and development, as well as the response to biotic and abiotic stress. In our study, we identified 40 genes with conserved WRKY motifs in the G. biloba genome and classified into groups I (groups I-N and -C), II (groups IIa, b, c, d, and e), and III, which include 12, 26, and 2 GbWRKY genes, respectively. Meanwhile, the expression patterns of 10 GbWRKY (GbWRKY2, GbWRKY3, GbWRKY5, GbWRKY7, GbWRKY11, GbWRKY15, GbWRKY23, GbWRKY29, GbWRKY31, GbWRKY32) under different tissue and abiotic stress conditions were analyzed. Under stress treatment, the expression patterns of 10 WRKY genes were changed. 10 ginkgo WRKY transcription factors were induced by ETH and SA, but there are two different induced response modes. The expression of 10 WRKY genes was inhibited under low temperature, high temperature and MeJA hormone induction. Most WRKY genes were up-regulated under the induction of high salt and ABA. GbWRKYs were differentially expressed in various tissues after abiotic stress and plant hormone treatments, thereby indicating their possible roles in biological processes and abiotic stress tolerance and adaptation. Our results provided insight into the genome-wide identification of GbWRKYs, as well as their differential responses to stresses and hormones. These data can also be utilized to identify potential molecular targets to confer tolerance to various stresses in G. biloba.
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Agarwal P, Reddy MP, Chikara J (2011). WRKY: its structure, evolutionary relationship, DNA-binding selectivity, role in stress tolerance and development of plants. Molecular Biology Reports 38(6):3883-3896.
Balvay L, Libri D, Gallego M, Fiszman MY (1992). Intronic sequence with both negative and positive effects on the regulation of alternative transcripts of the chicken beta tropomyosin transcripts. Nucleic Acids Research 20(15):3987-3992.
Blencowe BJ (2006). Alternative splicing: new insights from global analyses. Cell 126(1):37-47.
Chen H, Lai Z, Shi J, Yong X, Chen Z, Xu X (2010). Roles of Arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biology 10(1):443-462.
Chen L, Tong H, Wang M, Zhu J, Zi J, Song L, Yu R (2015). Effect of enzyme inhibitors on terpene trilactones biosynthesis and gene expression profiling in Ginkgo biloba cultured cells. Natural Product Communications 10(12):2033-2035.
Chen Q, Yan J, Meng X, Xu F, Zhang W, Liao Y, Qu J (2017). Molecular cloning, characterization, and functional analysis of acetyl-CoA C-acetyltransferase and mevalonate kinase genes involved in terpene trilactone biosynthesis from Ginkgo biloba. Molecules 22(1):74.
Cheng SY, Li LL, Yuan HH, Xu F, Cheng H (2015). Molecular cloning and characterization of GbMECT and GbMECP gene promoters from Ginkgo biloba. Genetics and Molecular Research 14(4):15112-15122.
Ciolkowski I, Wanke D, Birkenbihl RP, Somssich IE (2008). Studies on dna-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function. Plant Molecular Biology 68(1-2):81-92.
Dai X, Wang Y, Zhang WH (2016). OsWRKY74, a WRKY transcription factor, modulates tolerance to phosphate starvation in rice. Journal of Experimental Botany 67(3):947-960.
Du S, Sang Y, Liu X, Xing S, Li J, Tang H, Sun L (2016). Transcriptome profile analysis from different sex types of Ginkgo biloba L. Frontiers in Plant Science 7:871.
Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000). The WRKY superfamily of plant transcription factors. Trends in Plant Science 5(5):199-206.
Eulgem T, Rushton PJ, Schmelzer E, Hahlbrock K, Somssich IE (1999). Early nuclear events in plant defense signaling: rapid gene activation by WRKY transcription factors. EMBO Journal 18(17):4689-4699.
Finn RD, Coggill P, Eberhardt RF, Eddy SR, Mistry J, Mitchell AL, … Bateman A (2016). The Pfam protein families database: towards a more sustainable future. Nucleic Acids Research 44:D279.
Gong Y, Liao Z, Guo B, Sun X, Tang K (2006). 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 Medica 72(04):329-335.
Gong YF, Liao ZH, Chen M, ZOU K, Gou L, Tan Q, … Tang K (2005). Molecular cloning and characterization of a 1-deoxy-D-xylulose S-phosphate reductoisomerase gene from Ginkgo biloba. DNA Sequence 16(2):111-120.
Guan R, Zhao Y, Zhang H, Fan G, Liu X, Zhou W, … Liang X (2016). Draft genome of the living fossil Ginkgo biloba. Gigascience 5(1):49.
Guo AY, Zhu QH, Chen X, Luo JC (2007). GSDS: a gene structure display server. Hereditas 29(8):1023-1026.
Han J, Wang H, Lundgren A, Brodelius PE (2014). Effects of overexpression of Aawrky1 on artemisinin biosynthesis in transgenic Artemisia annua plants. Phytochemistry 102:89-96.
Han S, Wu Z, Jin Y, Yang W, Shi H (2005). RNA-Seq analysis for transcriptome assembly, gene identification, and SSR mining in ginkgo ( Ginkgo biloba L.). Tree Genetics and Genomes 11(3):37.
He B, Gu Y, Xu M, Wang J, Cao F, Xu LA (2015). Transcriptome analysis of Ginkgo biloba kernels. Frontiers in Plant Science 6:819.
Howe KJ, Ares M (1997). Intron self-complementarity enforces exon inclusion in a yeast pre-mRNA. Proceedings of the National Academy of Sciences 94(23):12467-12472.
Ishiguro S, Nakamura K (1994). Characterization of a cDNA encoding a novel DNA-binding protein, SPF1, that recognizes SP8 sequences in the 5' upstream regions of genes coding for sporamin and β-amylase from sweet potato. Molecular and General Genetics 244(6):563-571.
Jiang Y, Deyholos MK (2006). Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes. BMC Plant Biology 6(1):25.
Jin J, Tian F, Yang DC, Meng YQ, Kong L, … Gao G (2017). Plant TFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Research 45:D1040-D1045.
Journot-Catalino N, Somssich IE, Roby D, Kroj T (2006). The transcription factors WRKY11 and WRKY17 act as negative regulators of basal resistance in Arabidopsis thaliana. The Plant Cell 18(11):3289-3302.
Kang MK, Nargis S, Kim SM, Kim SU (2013). Distinct expression patterns of two Ginkgo biloba 1-hydroxy-2-methyl-2-(E)-butenyl-4-diphosphate reductase/isopentenyl diphospahte synthase (HDR/IDS) promoters in Arabidopsis model. Plant Physiology and Biochemistry 62:47-53.
Kim JH, Lee KI, Chang YJ, Kim SU (2012). Developmental pattern of Ginkgo biloba levopimaradiene synthase (GbLPS) as probed by promoter analysis in Arabidopsis thaliana. Plant Cell Reports 31(6):1119-1127.
Kim SM, Kuzuyama T, Chang YJ, Song KS, Kim SU (2006a). Identification of class 2 1-deoxy-D-xylulose 5-phosphate synthase and 1-deoxy-D-xylulose 5-phosphate reductoisomerase genes from Ginkgo biloba and their transcription in embryo culture with respect to ginkgolide biosynthesis. Planta Medica 72(03):234-240.
Kim SM, Kuzuyama T, Chang YJ, Kwon HJ, Kim SU (2006b). Cloning and functional characterization of 2-C-methyl-D-erythritol 4-phosphate cytidyltransferase (GbMECT) gene from Ginkgo biloba. Phytochemistry 67(14):1435-1441.
Kim SM, Kuzuyama T, Chang YJ, Kim SU (2006c). Cloning and characterization of 2-C-methyl-D-erythritol 2, 4-cyclodiphosphate synthase (MECS) gene from Ginkgo biloba. Plant Cell Reports 25(8):829-835.
Kim SM, Kim YB, Kuzuyama T, SU Kim (2008a). Two copies of 4-(cytidine 5′-diphospho)-2-C-methyl-d-erythritol kinase (CMK) gene in Ginkgo biloba: molecular cloning and functional characterization. Planta 228(6):941-950.
Kim SM, Kuzuyama T, Kobayashi A, Sando T, Chang YJ, Kim SU (2008b). 1-Hydroxy-2-methyl-2-(E)-butenyl 4-diphosphate reductase (IDS) is encoded by multicopy genes in gymnosperms Ginkgo biloba and Pinus taeda. Planta 227(2):287-298.
Kim KC, Lai Z, Fan B, Chen Z (2008c). Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense. The Plant Cell 20(9):2357-2371.
Kim SM, Kim SU (2009). Characterization of 1-hydroxy-2-methyl-2-(E)-butenyl-4-diphosphate synthase (HDS) gene from Ginkgo biloba. Molecular Biology Reports 37(2):973-979.
Lai Z, Vinod K, Zheng Z, Fan B, Chen Z (2008). Roles of Arabidopsis WRKY3 and WRKY4 transcription factors in plant responses to pathogens. BMC Plant Biology 8(1):68.
Letunic I, Doerks T, Bork P (2015). SMART: recent updates, new developments and status in 2015. Nucleic Acids Research 43(D1):D257-D260.
Li J, Brader G, Palva ET (2004). The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. The Plant Cell 16(2):319-331.
Li LQ, Huang LP, Pan G, Liu L, Wang XY, Lu LM (2017). Identifying the genes regulated by AtWRKY6 using comparative transcript and proteomic analysis under phosphorus deficiency. International Journal of Molecular Sciences 18(5):1046.
Li S, Zhou X, Chen L, Huang W, Yu D (2010). Functional characterization of arabidopsis thaliana WRKY39 in heat stress. Molecules and Cells 29(5):475-483.
Li XQ, Ye JB, Wang XH, Zhang WW, Xu F (2016). Molecular Cloning and sequence analysis of GbWRKY31, a novel transcription factor gene from Ginkgo biloba. International Journal of Current Research in Bioscience and Plant Biology 3(7):90-94.
Liao Y, Xu F, Huang X, Zhang W, Cheng H, Li L, … Shen Y (2015a). Promoter analysis and transcriptional profiling of Ginkgo biloba 3-hydroxy-3-methylglutaryl coenzyme a reductase (GbHMGR) gene in abiotic stress responses. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 43(1):25-34.
Liao Y, Xu F, Huang X, Zhang W, Cheng H, Wang X, … Shen Y, (2015b). Characterization and transcriptional profiling of Ginkgo biloba mevalonate diphosphate decarboxylase gene (GbMVD) promoter towards light and exogenous hormone treatments. Plant Molecular Biology Reporter 34(3):566-581.
Liao YL, Shen YB, Chang J, Zhang WW, Cheng SY, Xu F (2015c). Isolation, expression, and promoter analysis of GbWRKY2: a novel transcription factor gene from Ginkgo biloba. International Journal of Genomics 2015(6):1-17.
Liao YL, Xu F, Zang WW, Cheng SY, Shen YB, Chang J (2016). Cloning, characterization and expression analysis of GbWRKY11, a novel transcription factor gene in Ginkgo biloba. International Journal of Agriculture and Biology 18(1):1814-9596.
Liao Z, Chen M, Gong Y, Guo L, Tan Q, Feng X, … Tang K (2004). A new geranylgeranyl diphosphate synthase gene from Ginkgo biloba, which intermediates the biosynthesis of the key precursor for ginkgolides. DNA Sequence 15(2):153-158.
Lin X, Zhang J, Li Y, Luo H, Wu Q, Sun C,… Chen S (2011). Functional genomics of a living fossil tree, Ginkgo, based on next-generation sequencing technology. Physiologia Plantarum 143(3):207-218.
Liu QN, Liu Y, Xin ZZ, Zhang DZ, GeBM, Yang RP, … Zhou CL (2017). Genome-wide identification and characterization of the WRKY gene family in potato (Solanum tuberosum). Biochemical Systematics and Ecology 71:212-218.
Llorca CM, Potschin M, Zentgraf U (2014). bZIPs and WRKYs: two large transcription factor families executing two different functional strategies. Frontiers in Plant Science 5:169.
Lu J, Wu W, Cao S, Zhao H, Zeng H, Lin L, … Tang K (2008). Molecular cloning and characterization of 1-hydroxy-2-methyl-2-(E)-butenyl-4-diphosphate reductase gene from Ginkgo biloba. Molecular Biology Reports 35(3):413-420.
Luo DL, Ba LJ, Shan W, Kuang JF, Lu WJ, Chen JY (2017). Involvement of WRKY transcription factors in abscisic-acid-induced cold tolerance of banana fruit. Journal of Agricultural and Food Chemistry 65(18):3627-3635.
Pan L, Ren L, Chen F, Feng Y, Luo Y (2016). Antifeedant activity of Ginkgo biloba secondary metabolites against Hyphantria cunea larvae: mechanisms and applications. PLoS One 11(5):e0155682.
Pang Y, Shen GA, Bergès T, Cardier H, Wu W, Sun X, Tang K (2006). Molecular cloning, characterization and heterologous expression in Saccharomyces cerevisiae of a mevalonate diphosphate decarboxylase cDNA from Ginkgo biloba. Physiologia Plantarum 127(1):19-27.
Potschin M, Schlienger S, Bieker S, Zentgraf U (2014). Senescence networking: WRKY18 is an upstream regulator, a downstream target gene, and a protein interaction partner of WRKY53. Journal of Plant Growth Regulation 33(1):106-118.
Ramamoorthy R, Jiang SY, Kumar N, Venkatesh PN, Ramachandran S (2008). A comprehensive transcriptional profiling of the WRKY gene family in rice under various abiotic and phytohormone treatments. Plant and Cell Physiology 49(6):865-879.
Rinerson CI, Rabara RC, Tripathi P, Shen QJ, Rushton PJ (2015). The evolution of WRKY transcription factors. BMC Plant Biology 15(1):1-18.
Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010). WRKY transcription factors. Trends in Plant Science 15(5):247-258.
Rushton PJ, Torres JT, Parniske M, Wernert P, Hahlbrock K, Somssich IE (1996). Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO Journal 15(20):5690-5700.
Sakamoto H, Maruyama K, Sakuma Y, Meshi T, Iwabuchi M, Shinozaki K (2004). Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiology 136(1):2734-2746.
Schepmann HG, Pang J, Matsuda SP (2001). Cloning and characterization of Ginkgo biloba levopimaradiene synthase, which catalyzes the first committed step in ginkgolide biosynthesis. Archives of Biochemistry and Biophysics 392(2):263-269.
Schmittgen TD, Livak KJ (2008). Analyzing real-time PCR data by the comparative CT method. Nature Protocols 3(6):1101-1108.
Shen G, Pang Y, Wu W, Liao Z, Zhao L, Sun X, Tang K (2016). Cloning and characterization of a root-specific expressing gene encoding 3-hydroxy-3-methylglutaryl coenzyme A reductase from Ginkgo biloba. Molecular Biology Reports 33(2):117-127.
Spyropoulou EA, Haring MA, Schuurink RC (2014). RNA sequencing on Solanum lycopersicum trichomes identifies transcription factors that activate terpene synthase promoters. BMC Genomics 15(1):402.
Stetter MG, Benz M, Ludewig U (2017). Increased root hair density by loss of WRKY6 in Arabidopsis thaliana. PeerJ 5:e2891.
Sun LJ, Huang L, Li DY, Zhang HJ, Song FM (2014). Comprehensive expression analysis suggests overlapping of rice OsWRKY transcription factor genes during abiotic stress responses. Plant Physiology Journal 50(11):1651-1658.
Wang J, Tao F, An F, Zou Y, Tian W, Chen X, … Hu X (2017). Wheat transcription factor TaWRKY70 is positively involved in high-temperature seedling-plant resistance to Puccinia striiformis f. sp. tritici. Molecular Plant Pathology 18(5):649-661.
Wang P, Liao Z, Guo L, Li W, Chen M, Pi Y, … Tang K (2004). Cloning and functional analysis of a cdna encoding Ginkgo biloba farnesyl diphosphate synthase. Molecules and Cells 18(2):150-156.
Wang YQ, Shen JK, Berglund T, Ohlsson AB, Tang XF, Zhou ZK, … Chen JN (2010). Analysis of expressed sequence tags from Ginkgo, mature foliage in China. Tree Genetics and Genomes 6(3):357-365.
Wei S (2010). Methyl jasmonic acid induced expression pattern of terpenoid indole alkaloid pathway genes in Catharanthus roseus seedlings. Plant Growth Regulation 61(3):243-251.
Wei W, Zhang Y, Han L, Guan Z, Chai T (2008). A novel WRKY transcriptional factor from Thlaspi caerulescens negatively regulates the osmotic stress tolerance of transgenic tobacco. Plant Cell Reports 27(4):795-803.
Wu X, Shiroto Y, Kishitani S, Ito Y, Toriyama K (2009). Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of hsp101 promoter. Plant Cell Reports 28(1):21-30.
Xie Z, Zhang ZL, Zou X, Huang J, Ruas P, Thompson D, Shen QJ (2005). Annotations and functional analyses of the rice WRKY gene superfamily reveal positive and negative regulators of abscisic acid signaling in aleurone cells. Plant Physiology 137(1):176-189.
Xu F, Huang XH, Li LL, Deng G, Cheng H, Rong XF, … Cheng SY (2013). Molecular cloning and characterization of GbDXS and GbGGPPS gene promoters, from Ginkgo biloba. Genetics and Molecular Research 12:293-301.
Xu F, Ning YJ, Zhang WW, Liao YL, Li LL, Cheng H, Cheng SY (2014). An R2R3-MYB transcription factor as a negative regulator of the flavonoid biosynthesis pathway in Ginkgo biloba. Functional and Integrative Genomics 14(1):177-189.
Yang R, Fan X, Cai X, Hu F (2015). The inhibitory mechanisms by mixtures of two endophytic bacterial strains isolated from Ginkgo biloba against pepper phytophthora blight. Biological Control 85:59-67.
Yin G, Xu H, Xiao S, Qin Y, Li Y, Yan Y, Hu Yk (2013). The large soybean (Glycine max) WRKY TF family expanded by segmental duplication events and subsequent divergent selection among subgroups. BMC Plant Biology 13(1):148.
Zhang T, Tan D, Zhang L, Zhang X, Han Z (2017). Phylogenetic analysis and drought-responsive expression profiles of the WRKY transcription factor family in maize. Agri Gene 3:99-108.
Zhang Y, Wang L (2005). The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evolutionary Biology 5(1):1.
Zhou QY, Tian AG, Zou HF, Xie ZM, Lei G, Huang J, … Chen SY (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.
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