Skip to main content
Log in

Pineapple translation factor SUI1 and ribosomal protein L36 promoters drive constitutive transgene expression patterns in Arabidopsis thaliana

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The availability of a variety of promoter sequences is necessary for the genetic engineering of plants, in basic research studies and for the development of transgenic crops. In this study, the promoter and 5′ untranslated regions of the evolutionally conserved protein translation factor SUI1 gene and ribosomal protein L36 gene were isolated from pineapple and sequenced. Each promoter was translationally fused to the GUS reporter gene and transformed into the heterologous plant system Arabidopsis thaliana. Both the pineapple SUI1 and L36 promoters drove GUS expression in all tissues of Arabidopsis at levels comparable to the CaMV35S promoter. Transient assays determined that the pineapple SUI1 promoter also drove GUS expression in a variety of climacteric and non-climacteric fruit species. Thus the pineapple SUI1 and L36 promoters demonstrate the potential for using translation factor and ribosomal protein genes as a source of promoter sequences that can drive constitutive transgene expression patterns.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • An Y, McDowell J, Huang S, McKinney E, Chambliss S, Meagher R (1996) Strong, constitutive expression of the Arabidopsis ACT2/ACT8 actin subclass in vegetative tissues. Plant J 10:107–121

    Article  PubMed  CAS  Google Scholar 

  • Benfey PN, Chua NH (1990) The cauliflower mosaic virus-35 s promoter—combinatorial regulation of transcription in plants. Science 250(4983):959–966

    Article  PubMed  CAS  Google Scholar 

  • Benfey PN, Ren L, Chua NH (1990) Combinatorial and synergistic properties of CaMV 35S enhancer subdomains. EMBO J 9:1685–1696

    PubMed  CAS  Google Scholar 

  • Brander KA, Kuhlemeie C (1995) A pollen-specific DEAD-box protein related to translation initiation factor eIF-4A from tobacco. Plant Mol Biol 27:637–649

    Article  PubMed  CAS  Google Scholar 

  • Callis J, Raasch J, Vierstra R (1990) Ubiquitin extension proteins of Arabidopsis thaliana. J Biol Chem 265:12486–12493

    PubMed  CAS  Google Scholar 

  • Cazzonelli CI, Cavallaro AS, Botella JR (1998) Cloning and characterization of ripening-induced ethylene biosynthetic genes from non-climacteric pineapple (Ananas comosus) fruits. Australian J Plant Physiol 25:513–518

    Article  CAS  Google Scholar 

  • Christensen AH, Sharrock RA, Quail PH (1992) Maize polyubiquitin genes: structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation. Plant Mol Biol 18(4):675–689

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743

    Article  PubMed  CAS  Google Scholar 

  • Curie C, Liboz T, Bardet C, Gander E, Medale C, Axelos M, Lescure B (1991) Cis and trans-acting elements involved in the activation of Arabidopsis thaliana Al gene encoding the translation elongation factor EF-1a. Nucleic Acids Res 19:1305–1310

    Article  PubMed  CAS  Google Scholar 

  • Curie C, Axelos M, Bardet C, Atanassova R, Chanbet N, Lescure B (1993) Modular organization and developmental activity of an Arabidopsis thaliana EF-10 gene promoter. Mol Gen Genet 238:428–436

    Article  PubMed  CAS  Google Scholar 

  • Datta SK, Datta K, Soltanifar N, Donn G, Potrykus I (1992) Herbicide-resistant Indica rice plants from IRRI breeding line IR72 after PEG-mediated transformation of protoplasts. Plant Mol Biol 20(4):619–629

    Article  PubMed  CAS  Google Scholar 

  • Dey N, Maiti IB (1999) Structure and promoter/leader deletion analysis of mirabilis mosaic virus (MMV) full-length transcript promoter in transgenic plants. Plant Mol Biol 40(5):771–782

    Article  PubMed  CAS  Google Scholar 

  • Donald R, Cashmore A (1990) Mutation of either G box or I box sequences profoundly affects expression from the Arabidopsis rbcs-1A promoter. EMBO J 9:1717–1726

    PubMed  CAS  Google Scholar 

  • Duguay J, Jamal S, Liu Z, Wang T, Thompson J (2007) Leaf-specific suppression of deoxyhypusine synthase in Arabidopsis thaliana enhances growth without negative pleiotropic effects. J Plant Physiol 164(4):408–420. doi:10.1016/j.jplph.2006.02.001

    Article  PubMed  CAS  Google Scholar 

  • Eason JR, Ryan DJ, Watson LM, Hedderley D, Christey MC, Braun RH, Coupe SA (2005) Suppression of the cysteine protease, aleurain, delays floret senescence in Brassica oleracea. Plant Mol Biol 57(5):645–657. doi:10.1007/s11103-005-0999-7

    Article  PubMed  CAS  Google Scholar 

  • Elmayan T, Vaucheret H (1996) Expression of single copies of a strongly expressed 35S transgene can be silenced post-transcriptionally. Plant J 9(6):787–797

    Article  CAS  Google Scholar 

  • Fang RX, Nagy F, Sivasubramaniam S, Chua NH (1989) Multiple cis regulatory elements for maximal expression of the cauliflower mosaic virus 35S promoter in transgenic plants. Plant Cell 1:141–150

    PubMed  CAS  Google Scholar 

  • Gapper NE, Coupe SA, McKenzie MJ, Scott RW, Christey MC, Lill RE, McManus MT, Jameson PE (2005) Senescence-associated down-regulation of 1-aminocyclopropane-1-carboxylate (ACC) oxidase delays harvest-induced senescence in broccoli. Funct Plant Biol 32(10):891–901. doi:10.1071/Fp05076

    Article  CAS  Google Scholar 

  • Gidoni D, Brosio P, Bond-Nutter D, Bedbrook J, Dunsmuir P (1989) Novel cis-acting elements in Petunia Cab gene promoters. Mol Gen Genet 215(2):337–344

    Article  PubMed  CAS  Google Scholar 

  • Gilmartin PM, Sarokin L, Memelink J, Chua NH (1990) Molecular light switches for plant genes. Plant Cell 2(5):369–378

    PubMed  CAS  Google Scholar 

  • Green P, Kay S, Chua N-H (1987) Sequence-specific interactions of a pea nuclear factor with light-responsive elements upstream of the rbcs3A gene. EMBO J 6:2543–2549

    PubMed  CAS  Google Scholar 

  • Gupta P, Raghuvanshi S, Tyagi AK (2001) Assessment of the efficiency of various gene promoters via biolistics in leaf and regenerating seed callus of millets, Eleusine coracana and Echinochloa crusgalli. Plant Biotech 18(4):275–282

    Article  CAS  Google Scholar 

  • Hamilton D, Schwarz Y, Mascarenhas J (1998) A monocot pollen-specific promoter contains separable pollen-specific and quantitative elements. Plant Mol Biol 38:663–669

    Article  PubMed  CAS  Google Scholar 

  • Haralampidis K, Milioni D, Rigas S, Hatzopoulos P (2002) Combinatorial interaction of cis elements specifies the expression of the Arabidopsis AtHsp90-1 gene. Plant Physiol 129(3):1138–1149. doi:10.1104/Pp.004044

    Article  PubMed  CAS  Google Scholar 

  • Hensgens LAM, Debakker EPHM, Vanosruygrok EP, Rueb S, Vandemark F, Vandermaas HM, Vanderveen S, Koomangersmann M, Thart L, Schilperoort RA (1993) Transient and stable expression of gusA fusions with rice genes in rice, barley and perennial ryegrass. Plant Mol Biol 22(6):1101–1127

    Article  PubMed  CAS  Google Scholar 

  • Hernandez-Garcia CM, Martinelli AP, Bouchard RA, Finer JJ (2009) A soybean (Glycine max) polyubiquitin promoter gives strong constitutive expression in transgenic soybean. Plant Cell Rep 28(5):837–849

    Article  PubMed  CAS  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (place) database. Nucleic Acids Res 27(1):297–300

    Article  PubMed  CAS  Google Scholar 

  • Hofig KP, Moyle RL, Putterill J, Walter C (2003) Expression analysis of four pinus radiata male cone promoters in the heterologous host Arabidopsis. Planta 217(6):858–867. doi:10.1007/s00425-003-1057-9

    Article  PubMed  Google Scholar 

  • Hofig KP, Moller R, Donaldson L, Putterill J, Walter C (2006) Towards male sterility in Pinus radiata-a stilbene synthase approach to genetically engineer nuclear male sterility. Plant Biotechnol J 4(3):333–343. doi:10.1111/j.1467-7652.2006.00185.x

    Article  PubMed  CAS  Google Scholar 

  • Jefferson R, Kavanagh T, Bevan M (1987) GUS fusions:B-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    PubMed  CAS  Google Scholar 

  • Kosugi S, Ohashi Y (2002) E2F sites that can interact with E2F proteins cloned from rice are required for meristematic tissue-specific expression of rice and tobacco proliferating cell nuclear antigen promoters. Plant J 29(1):45–59

    Article  PubMed  CAS  Google Scholar 

  • Lam E, Chua NH (1989) ASF-2: a factor that binds to the cauliflower mosaic virus 35S promoter and a conserved GATA motif in Cab promoters. Plant Cell 1(12):1147–1156. doi:10.1105/tpc.1.12.1147

    PubMed  CAS  Google Scholar 

  • Liu Z, Duguay J, Ma F, Wang TW, Tshin R, Hopkins MT, McNamara L, Thompson JE (2008) Modulation of eIF5A1 expression alters xylem abundance in Arabidopsis thaliana. J Exp Bot 59(4):939–950. doi:10.1093/jxb/ern017

    Article  PubMed  CAS  Google Scholar 

  • Maas C, Laufs J, Grant S, Korfhage C, Werr W (1991) The combination of a novel stimulatory element in the 1st exon of the Maize Shrunken-1 gene with the following intron-1 enhances reporter gene-expression up to 1000-fold. Plant Mol Biol 16(2):199–207

    Article  PubMed  CAS  Google Scholar 

  • Maiti IB, Gowda S, Kiernan J, Ghosh SK, Shepherd RJ (1997) Promoter/leader deletion analysis and plant expression vectors with the figwort mosaic virus (FMV) full length transcript (FLt) promoter containing single or double enhancer domains. Transgenic Res 6(2):143–156

    Article  PubMed  CAS  Google Scholar 

  • Mandel T, Fleming AJ, Krahenbuhl R, Kuhlemeier C (1995) Definition of constitutive gene expression in plants: the translation initiation factor 4A gene as a model. Plant Mol Biol 29:995–1004

    Article  PubMed  CAS  Google Scholar 

  • Mann DG, King ZR, Liu W, Joyce BL, Percifield RJ, Hawkins JS, LaFayette PR, Artelt BJ, Burris JN, Mazarei M, Bennetzen JL, Parrott WA, Stewart CN Jr (2011) Switchgrass (Panicum virgatum L.) polyubiquitin gene (PvUbi1 and PvUbi2) promoters for use in plant transformation. BMC Biotechnol 11:74. doi:10.1186/1472-6750-11-74

    Article  PubMed  CAS  Google Scholar 

  • Mascarenhas D, Mettler IJ, Pierce DA, Lowe HW (1990) Intron-mediated enhancement of heterologous gene-expression in maize. Plant Mol Biol 15(6):913–920

    Article  PubMed  CAS  Google Scholar 

  • Matzke MA, Matzke AJ (1995) Homology-dependent gene silencing in transgenic plants: what does it really tell us? Trends Genet 11:1–3

    Article  PubMed  CAS  Google Scholar 

  • Moyle R, Moody J, Phillips L, Walter C, Wagner A (2002) Isolation and characterization of a Pinus radiata lignin biosynthesis-related O-methyltransferase promoter. Plant Cell Rep 20(11):1052–1060. doi:10.1007/s00299-002-0457-9

    Article  CAS  Google Scholar 

  • Moyle RL, Crowe ML, Ripi-Koia J, Fairbairn DJ, Botella JR (2005) PineappleDB: an online pineapple bioinformatics resource. BMC Plant Biol 5:21. doi:10.1186/1471-2229-5-21

    Article  PubMed  Google Scholar 

  • Mylne J, Botella JR (1998) Binary vectors for sense and antisense expression of Arabidopsis ESTs. Plant Mol Biol Report 16(3):257–262

    Article  CAS  Google Scholar 

  • Odell JT, Nagy F, Chua NH (1985) Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. Nature 313:810–812

    Article  PubMed  CAS  Google Scholar 

  • Petsch KA, Mylne J, Botella JR (2005) Cosuppression of eukaryotic release factor 1–1 in Arabidopsis affects cell elongation and radial cell division. Plant Physiol 139(1):115–126. doi:10.1104/pp.105.062695

    Article  PubMed  CAS  Google Scholar 

  • Potenza C, Aleman L, Sengupta-Gopalan C (2004) Targeting transgene expression in research, agricultural, and environmental applications: promoters used in plant transformation. In Vitro Cell Dev-Pl 40(1):1–22. doi:10.1079/Ivp2003477

    Article  CAS  Google Scholar 

  • Prestridge DS (1991) Signal scan—a computer-program that scans DNA-sequences for eukaryotic transcriptional elements. Comput Appl Biosci 7(2):203–206

    PubMed  CAS  Google Scholar 

  • Remans T, Sagi L, Elliott AR, Dietzgen RG, Swennen RL, Ebert PR, Grof CP, Manners JM, Schenk PMP (2001) Banana streak virus promoters are highly active in banana and other monocot and dicot plants. Infomusa 10:10–11

    Google Scholar 

  • Rey P, Diaz C, Schilperoort RA, Hensgens LAM (1993) Cell-type-specific expression of 3 rice genes Gos2, Gos5 and Gos9. Plant Mol Biol 23(4):889–894

    Article  PubMed  CAS  Google Scholar 

  • Rieping M, Schoffl F (1992) Synergistic effect of upstream sequences, Ccaat box elements, and Hse sequences for enhanced expression of chimeric heat-shock genes in transgenic tobacco. Mol Gen Genet 231(2):226–232

    PubMed  CAS  Google Scholar 

  • Rose A, Beliakoff J (2000) Intron-mediated enhancement of gene expression independent of unique intron sequences and splicing. Plant Physiol 122:535–542

    Article  PubMed  CAS  Google Scholar 

  • Sanger M, Daubert S, Goodman RM (1990) Characteristics of a strong promoter from figwort mosaic virus: comparison with the analogous 35S promoter from cauliflower mosaic virus and the regulated mannopine synthase promoter. Plant Mol Biol 14:433–443

    Article  PubMed  CAS  Google Scholar 

  • Terzaghi WB, Cashmore AR (1995) Light-regulated transcription. Ann Rev Plant Phys 46:445–474

    CAS  Google Scholar 

  • Urao T, Yamaguchishinozaki K, Urao S, Shinozaki K (1993) An Arabidopsis Myb homolog is induced by dehydration stress and its gene-product binds to the conserved Myb recognition sequence. Plant Cell 5(11):1529–1539

    PubMed  CAS  Google Scholar 

  • Verdaguer B, de Kochko A, Beachy RN, Fauquet C (1996) Isolation and expression in transgenic tobacco and rice plants, of the cassava vein mosaic virus (CVMV) promoter. Plant Mol Biol 31(6):1129–1139

    Article  PubMed  CAS  Google Scholar 

  • Weiher H, Konig M, Gruss P (1983) Multiple point mutations affecting the simian virus-40 enhancer. Science 219(4585):626–631

    Article  PubMed  CAS  Google Scholar 

  • Winichayakul S, Moyle RL, Coupe SA, Davies KM, Farnden KJF (2004) Analysis of the asparagus (Asparagus officinalis) asparagine synthetase gene promoter identifies evolutionarily conserved cis-regulatory elements that mediate Suc-repression. Funct Plant Biol 31(1):63–72. doi:10.1071/Fp03179

    Article  CAS  Google Scholar 

  • Zhou DX (1999) Regulatory mechanism of plant gene transcription by GT-elements and GT-factors. Trends Plant Sci 4(6):210–214

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to José Ramón Botella.

Additional information

Jonni Koia, Richard Moyle contributed equally to the work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 23 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Koia, J., Moyle, R., Hendry, C. et al. Pineapple translation factor SUI1 and ribosomal protein L36 promoters drive constitutive transgene expression patterns in Arabidopsis thaliana . Plant Mol Biol 81, 327–336 (2013). https://doi.org/10.1007/s11103-012-0002-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-012-0002-3

Navigation