Abstract
Methyl jasmonate (MeJA) is one of the most effective inducers of taxol biosynthetic genes, particularly the tasy gene. However, the mechanism underlying the regulation of tasy by MeJA is still unknown. In this study, a 550-bp 5′-flanking sequence was obtained and confirmed as the promoter of the tasy gene. Deletion analysis revealed that the fragment containing a GCC-box from −150 to −131 was the crucial jasmonate (JA)-responsive element, designated as JRE. Using JRE as bait, two binding proteins, namely TcERF12 and TcERF15, were discovered. Sequence alignment and phylogenetic analysis showed that TcERF12 was related to the repressor AtERF3, while TcERF15 was more related to the activator ORA59; these are typical GCC-box-binding ethylene-responsive factors. Both could significantly respond to MeJA for 10 and 4.5 times, respectively, in 0.5 h. When the two TcERFs were overexpressed in Taxus cells, tasy gene expression decreased by 2.1 times in TcERF12-overexpressing cells, but increased by 2.5 times in TcERF15-overexpressing cells. Results indicated that TcERF12 and TcERF15 were negative and positive regulators, respectively, in the JA signal transduction to the tasy gene by binding the GCC-box in the JRE of the tasy promoter. Our results promote further research on regulatory mechanisms of taxol biosynthesis.
Similar content being viewed by others
References
Aharoni A et al (2001) The strawberry FaMYB1 transcription factor suppresses anthocyanin and flavonol accumulation in transgenic tobacco. Plant J Cell Mol Biol 28:319–332
Allen MD, Yamasaki K, Ohme-Takagi M, Tateno M, Suzuki M (1998) A novel mode of DNA recognition by a beta-sheet revealed by the solution structure of the GCC-box binding domain in complex with DNA. EMBO J 17:5484–5496. doi:10.1093/emboj/17.18.5484
Aviles-Arnaut H, Delano-Frier JP (2012) Characterization of the tomato prosystemin promoter: organ-specific expression, hormone specificity and methyl jasmonate responsiveness by deletion analysis in transgenic tobacco plants. J Integr Plant Biol 54:15–32. doi:10.1111/j.1744-7909.2011.01084.x
Bohlmann J, Meyer-Gauen G, Croteau R (1998) Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc Natl Acad Sci USA 95:4126–4133
Boter M, Ruiz-Rivero O, Abdeen A, Prat S (2004) Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis. Genes Dev 18:1577–1591. doi:10.1101/Gad.297704
Chen F, Tholl D, Bohlmann J, Pichersky E (2011) The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J 66:212–229. doi:10.1111/j.1365-313X.2011.04520.x
Dai Y et al (2009) Isolation and characterization of a novel cDNA encoding methyl jasmonate-responsive transcription factor TcAP2 from Taxus cuspidata. Biotechnol Lett 31:1801–1809. doi:10.1007/s10529-009-0068-4
De Boer K et al (2011) APETALA2/ETHYLENE RESPONSE FACTOR and basic helix-loop-helix tobacco transcription factors cooperatively mediate jasmonate-elicited nicotine biosynthesis. Plant J Cell Mol Biol 66:1053–1065. doi:10.1111/j.1365-313X.2011.04566.x
De Geyter N, Gholami A, Goormachtig S, Goossens A (2012) Transcriptional machineries in jasmonate-elicited plant secondary metabolism. Trends Plant Sci 17:349–359. doi:10.1016/j.tplants.2012.03.001
De Sutter V et al (2005) Exploration of jasmonate signalling via automated and standardized transient expression assays in tobacco cells. Plant J Cell Mol Biol 44:1065–1076. doi:10.1111/j.1365-313X.2005.02586.x
Dombrecht B et al (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19:2225–2245. doi:10.1105/tpc.106.048017
Dong Y et al (2015) Enhancing taxane biosynthesis in cell suspension culture of Taxus chinensis by overexpressing the neutral/alkaline invertase gene. Process Biochem 50:651
Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15:573–581
Feller A, Machemer K, Braun EL, Grotewold E (2011) Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J Cell Mol Biol 66:94–116. doi:10.1111/j.1365-313X.2010.04459.x
Fujimoto SY, Ohta M, Usui A, Shinshi H, Ohme-Takagi M (2000) Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 12:393–404. doi:10.2307/3870944
Goossens A et al (2003) A functional genomics approach toward the understanding of secondary metabolism in plant cells. Proc Natl Acad Sci USA 100:8595–8600. doi:10.1073/pnas.1032967100
Guerineau F, Benjdia M, Zhou DX (2003) A jasmonate-responsive element within the A-thaliana vsp1 promoter. J Exp Bot 54:1153–1162. doi:10.1093/Jxb/Erg123
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300
Hong GJ, Xue XY, Mao YB, Wang LJ, Chen XY (2012) Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24:2635–2648. doi:10.1105/tpc.112.098749
Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587. doi:10.1093/nar/gkm259
Howat S, Park B, Oh IS, Jin YW, Lee EK, Loake GJ (2014) Paclitaxel: biosynthesis, production and future prospects. New Biotechnol 31:242–245. doi:10.1016/j.nbt.2014.02.010
Kazan K (2006) Negative regulation of defence and stress genes by EAR-motif-containing repressors. Trends Plant Sci 11:109–112. doi:10.1016/j.tplants.2006.01.004
Kim S-R, Choi J-L, Costa MA, An G (1992) Identification of G-box sequence as an essential element for methyl jasmonate response of potato proteinase inhibitor II promoter. Plant Physiol 99:627–631
Laskaris G, Bounkhay M, Theodoridis G, van der Heijden R, Verpoorte R, Jaziri M (1999) Induction of geranylgeranyl diphosphate synthase activity and taxane accumulation in Taxus baccata cell cultures after elicitation by methyl jasmonate. Plant Sci 147:1–8. doi:10.1016/S0168-9452(99)00078-3
Lescot M et al (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327
Li ST et al (2012) Transcriptional profile of Taxus chinensis cells in response to methyl jasmonate. BMC Genomics 13:295. doi:10.1186/1471-2164-13-295
Li S, Zhang P, Zhang M, Fu C, Yu L (2013) Functional analysis of a WRKY transcription factor involved in transcriptional activation of the DBAT gene in Taxus chinensis. Plant Biol 15:19–26. doi:10.1111/j.1438-8677.2012.00611.x
Liu JY, Osbourn A, Ma PD (2015) MYB transcription factors as regulators of phenylpropanoid metabolism in plants. Mol Plant 8:689–708. doi:10.1016/j.molp.2015.03.012
Ma DM et al (2009) Isolation and characterization of AaWRKY1, an Artemisia annua transcription factor that regulates the amorpha-4,11-diene synthase gene, a key gene of artemisinin biosynthesis. Plant Cell Physiol 50:2146–2161. doi:10.1093/Pcp/Pcp149
Mason HS, DeWald DB, Mullet JE (1993) Identification of a methyl jasmonate-responsive domain in the soybean vspB promoter. Plant Cell 5:241–251. doi:10.1105/tpc.5.3.241
McGarvey DJ, Croteau R (1995) Terpenoid metabolism. Plant Cell 7:1015
Menke FL, Champion A, Kijne JW, Memelink J (1999) A novel jasmonate- and elicitor-responsive element in the periwinkle secondary metabolite biosynthetic gene Str interacts with a jasmonate- and elicitor-inducible AP2-domain transcription factor, ORCA2. EMBO J 18:4455–4463. doi:10.1093/emboj/18.16.4455
Nakata M et al (2013) A bHLH-type transcription factor, ABA-INDUCIBLE BHLH-TYPE TRANSCRIPTION FACTOR/JA-ASSOCIATED MYC2-LIKE1, acts as a repressor to negatively regulate jasmonate signaling in Arabidopsis. Plant Cell 25:1641–1656. doi:10.1105/tpc.113.111112
Nystedt B et al (2013) The Norway spruce genome sequence and conifer genome evolution. Nature 497:579–584. doi:10.1038/nature12211
Ohta M, Matsui K, Hiratsu K, Shinshi H, Ohme-Takagi M (2001) Repression domains of class II ERF transcriptional repressors share an essential motif for active repression. Plant Cell 13:1959–1968
Patil RA, Kolewe ME, Normanly J, Walker EL, Roberts SC (2012) Contribution of taxane biosynthetic pathway gene expression to observed variability in paclitaxel accumulation in Taxus suspension cultures. Biotechnol J 7:418–427. doi:10.1002/biot.201100183
Pre M, Atallah M, Champion A, De Vos M, Pieterse CM, Memelink J (2008) The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol 147:1347–1357. doi:10.1104/pp.108.117523
Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258
Sears MT, Zhang H, Rushton PJ, Wu M, Han S, Spano AJ, Timko MP (2014) NtERF32: a non-NIC2 locus AP2/ERF transcription factor required in jasmonate-inducible nicotine biosynthesis in tobacco. Plant Mol Biol 84:49–66. doi:10.1007/s11103-013-0116-2
Shoji T, Hashimoto T (2011) Tobacco MYC2 regulates jasmonate-inducible nicotine biosynthesis genes directly and by way of the NIC2-locus ERF genes. Plant Cell Physiol 52:1117–1130. doi:10.1093/pcp/pcr063
Shoji T, Kajikawa M, Hashimoto T (2010) Clustered transcription factor genes regulate nicotine biosynthesis in tobacco. Plant Cell 22:3390–3409. doi:10.1105/tpc.110.078543
Su X, Mei X, Gong W, Zhang Z (2000) Effects of the combination of methyl jasmonate with salicylic acid or fungal elicitor on the cell suspension of Taxus chinensis. Biotechnology 11:10–13
Suttipanta N, Pattanaik S, Kulshrestha M, Patra B, Singh SK, Yuan L (2011) The transcription factor CrWRKY1 positively regulates the terpenoid indole alkaloid biosynthesis in Catharanthus roseus. Plant Physiol 157:2081–2093. doi:10.1104/pp.111.181834
Todd AT, Liu EW, Polvi SL, Pammett RT, Page JE (2010) A functional genomics screen identifies diverse transcription factors that regulate alkaloid biosynthesis in Nicotiana benthamiana. Plant J 62:589–600. doi:10.1111/j.1365-313X.2010.04186.x
Turck F, Zhou A, Somssich IE (2004) Stimulus-dependent, promoter-specific binding of transcription factor WRKY1 to Its native promoter and the defense-related gene PcPR1-1 in Parsley. Plant Cell 16:2573–2585. doi:10.1105/tpc.104.024810
van der Fits L, Memelink J (2000) ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. Science 289:295–297
Walker K, Croteau R (2001) Taxol biosynthetic genes. Phytochemistry 58:1–7
Xu B, Sheehan MJ, Timko MP (2004) Differential induction of ornithine decarboxylase (ODC) gene family members in transgenic tobacco (Nicotiana tabacum L. cv. Bright Yellow 2) cell suspensions by methyl-jasmonate treatment. Plant Growth Regul 44:101–116
Yang CQ, Fang X, Wu XM, Mao YB, Wang LJ, Chen XY (2012) Transcriptional regulation of plant secondary metabolism. J Integr Plant Biol 54:703–712. doi:10.1111/j.1744-7909.2012.01161.x
Yazaki K, Takeda K, Tabata M (1997) Effects of methyl jasmonate on shikonin and dihydroechinofuran production in Lithospermum cell cultures. Plant Cell Physiol 38:776–782
Yu ZX, Li JX, Yang CQ, Hu WL, Wang LJ, Chen XY (2012) The jasmonate-responsive AP2/ERF transcription factors AaERF1 and AaERF2 positively regulate artemisinin biosynthesis in Artemisia annua L. Mol Plant 5:353–365. doi:10.1093/mp/ssr087
Zhai Y et al (2013) Isolation and characterization of a novel transcriptional repressor GmERF6 from soybean. Biol Plantarum 57:26–32. doi:10.1007/s10535-012-0146-7
Zhang CH, Mei XG, Liu L, Yu LJ (2000) Enhanced paclitaxel production induced by the combination of elicitors in cell suspension cultures of Taxus chinensis. Biotechnol Lett 22:1561–1564. doi:10.1023/A:1005684901329
Zhang HT et al (2011) The basic helix-loop-helix transcription factor CrMYC2 controls the jasmonate-responsive expression of the ORCA genes that regulate alkaloid biosynthesis in Catharanthus roseus. Plant J 67:61–71. doi:10.1111/j.1365-313X.2011.04575.x
Acknowledgments
This work was supported by the National Natural Science Foundation of China (31270342, J1103514/J0106) and the Specialized Research Fund for the Doctoral Program of Higher Education (No. 20120142130009). There is no conflict of interest concerning the article.
Author information
Authors and Affiliations
Corresponding authors
Electronic supplementary material
Below is the link to the electronic supplementary material.
Table S1
Primer sequences (XLS 10 kb)
Rights and permissions
About this article
Cite this article
Zhang, M., Li, S., Nie, L. et al. Two jasmonate-responsive factors, TcERF12 and TcERF15, respectively act as repressor and activator of tasy gene of taxol biosynthesis in Taxus chinensis . Plant Mol Biol 89, 463–473 (2015). https://doi.org/10.1007/s11103-015-0382-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-015-0382-2