Abstract
Objectives
3-Hydroxy-3-methylglutaryl coenzyme A (HMG-CoA) synthase (HMGS) is an important enzyme in mevalonate (MVA) pathway of isoprenoid biosynthesis, which regulates the rubber biosynthetic pathway in rubber tree (Hevea brasiliensis) in coordination with HMG-CoA reductase (HMGR). However, little information is available about the regulation of HMGS gene expression. To understand the mechanism controlling the HbHMGS1 gene expression, we characterized the HbHMGS1 promoter sequence in transgenic plants with the β-glucuronidase (GUS) reporter gene.
Results
GUS activity analysis of the transgenic plants showed that the HbHMGS1 promoter is active in all organs of the transgenic Arabidopsis plants during various developmental stages (from 6 to 45-day-old). Deletion of different portions of the upstream HbHMGS1 promoter identified sequences responsible for either positive or negative regulation of the GUS expression. Particularly, the − 454 bp HbHMGS1 promoter resulted in a 2.19-fold increase in promoter activity compared with the CaMV 35S promoter, suggesting that the − 454 bp HbHMGS1 promoter is a super-strong near-constitutive promoter. In addition, a number of promoter regions important for the responsiveness to ethylene, methyl jasmonate (MeJA) and gibberellic acid (GA) were identified.
Conclusion
The − 454 bp HbHMGS1 promoter has great application potential in plant transformation studies as an alternative to the CaMV 35S promoter. The HbHMGS1 promoter may play important roles in regulating ethylene-, MeJA- and GA-mediated gene expression. The functional complexity of cis-elements revealed by this study remains to be elucidated.
Similar content being viewed by others
References
Alex D, Bach TJ, Chye ML (2000) Expression of Brassica juncea 3-hydroxy-3-methylglutaryl CoA synthase is developmentally regulated and stress-responsive. Plant J 22:415–426
Bastian R, Dawe A, Meier S, Ludidi N, Bajic VB, Gehring C (2010) Gibberellic acid and cGMP-dependent transcriptional regulation in Arabidopsis thaliana. Plant Signal Behav 5:224–232
Bian C, Ruan Q, Peng Z, Ji H, Jiang L, Li J, Yuan L (2011) Cloning, expression and characterization of the putative nuclear transport factor 2 (NTF2) gene from moss Conocephalum conicum (L.) Dum. Mol Biol Rep 38:2023–2032. https://doi.org/10.1007/s11033-010-0325-6
Breathnach R, Chambon P (1981) Organization and expression of eukaryotic split genes coding for proteins. Annu Rev Biochem 50:349–383
Chen H, Nelson R, Sherwood J (1994) Enhanced recovery of transformants of Agrobacterium tumefaciens after freeze-thaw transformation and drug selection. Biotechniques 16(664–668):670
Choudhury SR, Roy S, Sengupta DN (2009) A comparative study of cultivar differences in sucrose phosphate synthase gene expression and sucrose formation during banana fruit ripening. Postharvest Biol Technol 54:15–24. https://doi.org/10.1016/j.postharvbio.2009.05.003
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
Cornish K (2001) Biochemistry of natural rubber, a vital raw material, emphasizing biosynthetic rate, molecular weight and compartmentalization, in evolutionarily divergent plant species. Nat Prod Rep 18:182–189
Davis W (1997) The rubber industry′s biological nightmare. Fortune 4:86–95
Du H, Zhang Z, Li J (2010) Isolation and functional characterization of a water logging-induced promoter from maize. Plant Cell Rep 29:1269–1275. https://doi.org/10.1007/s00299-010-0913-x
Edelman GM, Meech R, Owens GC, Jones FS (2000) Synthetic promoter elements obtained by nucleotide sequence variation and selection for activity. Proc Natl Acad Sci USA 97:3038–3043. https://doi.org/10.1073/pnas.040569897
Goldstein JL, Brown MS (1990) Regulation of the mevalonate pathway. Nature 343:425–430. https://doi.org/10.1038/343425a0
Gronover CS, Wahler D, Prüfer D (2011) Natural rubber biosynthesis and physiochemical studies on plant derived latex. In: Elnashar M (ed) Biotechnology of biopolymers. Intech Open Acess Publisher, Rijeka, pp 75–88
Gubler F, Jacobsen JV (1992) Gibberellin-responsive elements in the promoter of a barley high-pI alpha-amylase gene. Plant Cell 4:1435–1441
Gubler F, Kalla R, Roberts JK, Jacobsen JV (1995) Gibberellin-regulated expression of a myb gene in barley aleurone cells: evidence for Myb transactivation of a high-pI alpha-amylase gene promoter. Plant Cell 7:1879–1891. https://doi.org/10.1105/tpc.7.11.1879
Gubler F, Raventos D, Keys M, Watts R, Mundy J, Jacobsen JV (1999) Target genes and regulatory domains of the GAMYB transcriptional activator in cereal aleurone. Plant J 17(1):1–9
Hagel JM, Yeung EC, Facchini PJ (2008) Got milk? The secret life of laticifers. Trends Plant Sci 13:631–639. https://doi.org/10.1016/j.tplants.2008.09.005
Hernandez-Garcia CM, Finer JJ (2014) Identification and validation of promoters and cis-acting regulatory elements. Plant Sci 217–218:109–119. https://doi.org/10.1016/j.plantsci.2013.12.007
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300. https://doi.org/10.1093/nar/27.1.297
Itzhaki H, Maxson JM, Woodson WR (1994) An ethylene-responsive enhancer element is involved in the senescence-related expression of the carnation glutathione-S-transferase (GST1) gene. Proc Natl Acad Sci USA 91:8925–8929. https://doi.org/10.1073/pnas.91.19.8925
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907
Kusnetsov V, Landsberger M, Meurer J, Oelmüller R (1999) The assembly of the CAAT-box binding complex at a photosynthesis gene promoter is regulated by light, cytokinin, and the stage of the plastids. J Biol Chem 274:36009–36014
Lee KA, Fink JS, Goodman RH, Green MR (1989) Distinguishable promoter elements are involved in transcriptional activation by E1a and cyclic AMP. Mol Cell Biol 9:4390–4397
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Peer Y, Rouzé P, Rombauts S (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. https://doi.org/10.1093/nar/30.1.325
Mace ES, Buhariwalla HK, Crouch JH (2003) A high-throughput DNA extraction protocol for tropical molecular breeding programs. Plant Mol Biol Rep 21:459–460. https://doi.org/10.1007/BF02772596
Maity SN, Golumbek PT, Karsenty G, de Crombrugghe B (1988) Selective activation of transcription by a novel CCAAT binding factor. Science 241:582–585
Maruyama K, Sakuma Y, Kasuga M, Ito Y, Seki M, Goda H, Shimada Y, Yoshida S, Shinozaki K, Yamaguchi-Shinozaki K (2004) Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. Plant J 38:982–993. https://doi.org/10.1111/j.1365-313X.2004.02100.x
Montgomery J, Goldman S, Deikman J, Margossian L, Fischer RL (1993) Identification of an ethylene-responsive region in the promoter of a fruit ripening gene. Proc Natl Acad Sci USA 90:5939–5943. https://doi.org/10.1073/pnas.90.13.5939
Mooibroek H, Cornish K (2000) Alternative sources of natural rubber. Appl Microbiol Biotechnol 53:355–365
Pieterse CMJ, van Wees SCM, van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, van Loon LC (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1517–1580
Rodríguez-Concepción M, Campos N, Ferrer A, Boronat A (2013) Biosynthesis of isoprenoid precursors in Arabidopsis. In: Bach TJ, Rohmer M (eds) Isoprenoid synthesis in plants and microorganisms: new concepts and experimental approaches. Springer, New York, pp 439–456
Rouster J, Leah R, Mundy J, Cameron-Mills V (1997) Identification of a methyl jasmonate responsive region in the promoter of a lipoxygenase 1 gene expressed in barley grain. Plant J 11:513–523
Sando T, Takaoka C, Mukai Y, Yamashita A, Hattori M (2008) Cloning and characterization of mevalonate pathway genes in natural rubber producing plant, Hevea brasiliensis. Biosci Biotechnol Biochem 72:2049–2060. https://doi.org/10.1271/bbb.80165
Sirinupong N, Suwanmanee P, Doolittle RR, Suvachitanont W (2005) Molecular cloning of a new cDNA and expression of 3-hydroxy-3-methylglutaryl-CoA synthase gene from Hevea brasiliensis. Planta 221:502–512. https://doi.org/10.1007/s00425-004-1463-7
Suwanmanee P, Suvachittanon W, Fincher GB (2002) Molecular cloning and sequencing of a cDNA encoding 3-hydroxy-3-methylglutaryl-CoA synthase from Hevea brasiliensis (HBK) Muell Arg. Sci Asia 28:29–36
Suwanmanee P, Sirinupong N, Suvachittanon W (2013) Regulation of 3-hydroxy-3-methylglutaryl-CoA synthase and 3-hydroxy-3-methylglutaryl-CoA reductase and Rubber biosynthesis of Hevea brasiliensis (B.H.K.) Mull. Arg. In: Bach TJ, Rohmer M (eds) Isoprenoid synthesis in plants and microorganisms: new concepts and experimental approaches. Springer, New York, pp 315–328
Tang C, Yang M, Fang Y, Luo Y, Gao S, Xiao X, An Z, Zhou B, Zhang B, Tan X, Yeang HY, Qin Y, Yang J, Lin Q, Mei H, Montoro P, Long X, Qi J, Hua Y, He Z, Sun M, Li W, Zeng X, Cheng H, Liu Y, Yang J, Tian W, Zhuang N, Zeng R, Li D, He P, Li Z, Zou Z, Li S, Li C, Wang J, Wei D, Lai CQ, Luo W, Yu J, Hu S, Huang H (2016) The rubber tree genome reveals new insights into rubber production and species adaptation. Nat Plants 2:16073. https://doi.org/10.1038/nplants.2016.73
Tapia G, Verdugo I, Yanez M, Ahumada I, Theoduloz C, Cordero C, Poblete F, Gonzalez E, Ruiz-Lara S (2005) Involvement of ethylene in stress-induced expression of the TLC1.1 retrotransposon from Lycopersicon chilense Dun. Plant Physiol 138:2075–2086. https://doi.org/10.1073/pnas.90.13.5939
Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch-Mani B, Vogelsang R, Cammue BPA, Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA 95:15107–15111
van Beilen JB, Poirier Y (2007) Establishment of new crops for the production of natural rubber. Trends Biotechnol 25:522–529. https://doi.org/10.1016/j.tibtech.2007.08.009
Vettakkorumakankav NN, Falk D, Saxena P, Fletcher RA (1999) A crucial role for gibberellins in stress protection of plants. Plant Cell Physiol 40:542–548. https://doi.org/10.1093/oxfordjournals.pcp.a029575
Vranová E, Coman D, Gruissem W (2012) Structure and dynamics of the isoprenoid pathway network. Mol Plant 5:318–333. https://doi.org/10.1093/mp/sss015
Wang H, Nagegowda DA, Rawat R, Bouvier-Navé P, Guo D, Bach TJ, Chye ML (2012) Overexpression of Brassica juncea wild-type and mutant HMG-CoA synthase 1 in Arabidopsis up-regulates genes in sterol biosynthesis and enhances sterol production and stress tolerance. Plant Biotechnol J 10:31–42. https://doi.org/10.1111/j.1467-7652.2011.00631.x
Whalen M, McMahan C, Shintani D (2013) Development of crops to produce industrially useful natural rubber. In: Rohmer M, Bach TJ (eds) Isoprenoid synthesis in plants and microorganisms: new concepts and experimental approaches. Springer, New York, pp 329–345
Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci 10:88–94. https://doi.org/10.1016/j.tplants.2004.12.012
Yang Y, Li R, Qi M (2000) In vivo analysis of plant promoters and transcription factors by agroinfiltration of tobacco leaves. Plant J 22:543–551
Zhang J, Zhang X, Wang Y, Hou H, Qian Y (2012) Characterization of sequence elements from Malvastrum yellow vein beta satellite regulating promoter activity and DNA replication. Virol J 9:234. https://doi.org/10.1186/1743-422X-9-234
Zhu Q, Song B, Zhang C, Ou Y, Xie C, Liu J (2008) Construction and functional charzcteristics of tuber-specific and cold-inducible chimeric promoters in potato. Plant Cell Rep 27:47–55. https://doi.org/10.1007/s00299-007-0399-3
Acknowledgements
This work was funded by the National Natural Science Foundation of China (No. 31560573), the Postgraduate Innovation Project of Crop Science of Tropical Agriculture and Forestry Institute, Hainan University (ZWCX2018030), and the Talents Training Project for Outstanding Undergraduate of Crop Science in Hainan University (ZWCX2018046).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Gong, XX., Yan, BY., Tan, YR. et al. Identification of cis-regulatory regions responsible for developmental and hormonal regulation of HbHMGS1 in transgenic Arabidopsis thaliana. Biotechnol Lett 41, 1077–1091 (2019). https://doi.org/10.1007/s10529-019-02703-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10529-019-02703-4