Skip to main content
SpringerLink
Log in

Light-regulated expression of the Arabidopsis thaliana ferredoxin gene requires sequences upstream and downstream of the transcription initiation site

  • Research Article
  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The effect of light on the expression of the Arabidopsis thaliana ferredoxin gene (fedA) was studied in mature tobacco plants. In light-treated leaves of tobacco plants transformed with a full-length ferredoxin gene, fedA-specific mRNA levels were more than twenty fold higher than in dark-treated controls. This indicates that all components for regulation of the Arabidopsis ferredoxin gene are present in tobacco. To identify light-regulatory elements in the fedA gene, we have tested a set of chimeric genes containing various parts of the fedA gene for light-dependent expression in mature tobacco plants. A fedA promoter-GUS fusion gene was not light-responsive, indicating that the 5′-upstream promoter region is not sufficient for light regulation. Fusion genes in which different transcribed regions of the fedA gene were expressed from the CaMV 35S promoter showed only limited light regulation, if any at all. This indicates that, like the fedA upstream region, the region downstream of the transcription start site is also not sufficient for full light regulation. The combined results suggest that for full light-regulated expression of the fedA gene, both the promoter region and sequences downstream of the transcription start site are required.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Bruschi M, Guerlesquin F: Structure, function and evolution of bacterial ferredoxins. FEMS Microbiol Rev 54: 155–176 (1988).

    Google Scholar 

  2. Thomson AJ: Does ferredoxin I Azotobacter represent a novel class of DNA binding proteins that regulate gene expression in response to cellular iron-II. FEBS Lett 285: 230–236 (1991).

    Google Scholar 

  3. Matsubara H, Hase T, Wakabayashi S, Wada K: Structure and evolution of chloroplast- and bacterial-type ferredoxins. In: Sigman DS, Brazier MAB (eds) The Evolution of Protein Structure and Function, pp. 245–266. Academic Press, New York (1980).

    Google Scholar 

  4. Hall DO, Rao KK: Ferredoxin. In: Trebst A, Avron M (eds) Photosynthesis. Encyclopedia of Plant Physiology vol. 5, pp. 206–216. Springer-Verlag, Berlin (1977).

    Google Scholar 

  5. Ho KK, Krogmann DW: Photosynthesis. In: Carr NG, Whitton BA (eds) The Biology of Cyanobacteria, pp. 204–207. Blackwell Scientific Press, Oxford (1982).

    Google Scholar 

  6. Buchanan BB: The ferredoxin/thioredoxin system: a key element in the regulatory function of light in photosynthesis. BioScience 34: 378–383 (1984).

    Google Scholar 

  7. Smeekens S, van Binsbergen J, Weisbeek P: The plant ferredoxin precursor: nucleotide sequence of a full-length cDNA clone. Nucl Acids Res 13: 3179–3194 (1985).

    Google Scholar 

  8. Smeekens S, Bauerle C, Hageman J, Keegstra K, Weisbeck P: The role of the transit peptide in the routing of precursors toward different chloroplast compartments. Cell 46: 365–375 (1986).

    Google Scholar 

  9. Smeekens S, van Steeg H, Bauerle C, Bettenbroek H, Keegstra K, Weisbeek P: Import into chloroplasts of a yeast mitochondrial protein directed by ferredoxin and plastocyanin transit peptides. Plant Mol Biol 9: 377–388 (1987).

    Google Scholar 

  10. Vorst O, van Dam F, Oosterhoff-Teertstra R, Smeekens S, Weisbeek P: Tissue-specific expression directed by an Arabidopsis thaliana pre-ferredoxin promoter in transgenic tobacco plants. Plant Mol Biol 14: 491–499 (1990).

    Google Scholar 

  11. Vorst O, van Dam F, Weisbeek P, Smeekens S: Light-regulated expression of the Arabidopsis thaliana ferredoxin A gene involves both transcriptional and post-transcriptional processes. Plant J 3: 793–803 (1993).

    Google Scholar 

  12. Caspar T, Quail PH: Promoter and leader regions involved in the expression of the Arabidopsis ferredoxin-A gene. Plant J 3: 161–174 (1993).

    Google Scholar 

  13. Gallo-Meagher M, Sowinski DA, Elliott RC, Thompson WF: Both internal and external regulatory elements control expression of the pea fed-1 gene in transgenic tobacco seedlings. Plant Cell 4: 389–395 (1992).

    Google Scholar 

  14. Elliott RC, Dickey LF, White MJ, Thompson WF: cis-acting elements for light regulation of pea ferredoxin I gene expression are located within transcribed sequences. Plant Cell 1: 691–698 (1989).

    Google Scholar 

  15. Dickey LF, Gallo-Meagher M, Thompson WF: Light regulatory sequences are located within the 5′ portion of the Fed-1 message sequence. EMBO J 11: 2311–2317 (1992).

    Google Scholar 

  16. Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning. A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).

    Google Scholar 

  17. Jefferson RA, Kavanagh TA, Bevan MW: GUS-fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901–3907 (1987).

    Google Scholar 

  18. Dente L, Cesarini G, Cortese R: pEMBL: a new class of single stranded plasmids. Nucl Acids Res 11: 1645–1655 (1983).

    Google Scholar 

  19. Erlich HA: PCR Technology: Principles and Applications for DNA Amplification. Stockton Press, New York (1990).

    Google Scholar 

  20. Hoekema A, van Haaren M, Fellinger A, Hooykaas P, Schilperoort R: Non-oncogenic plant vectors for use in the Agrobacterium binary system. Plant Mol Biol 5: 85–89 (1985).

    Google Scholar 

  21. Horsch R, Fry F, Hoffman N, Eichholtz D, Rogers S, Fraley R: A simple and general method for transferring genes into plants. Science 227: 1229–1231 (1985).

    Google Scholar 

  22. Murashige T, Skoog F: A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15: 473–497 (1962).

    Google Scholar 

  23. Dobres MS, Elliott RC, Watson JC, Thompson WF: A phytochrome regulated pea transcript encodes ferredoxin I. Plant Mol Biol 8: 53–59 (1987).

    Google Scholar 

  24. Feinberg AP, Vogelstein B: A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132: 6–13 (1983).

    Google Scholar 

  25. Meinkoth J, Wahl G: Hybridization of nucleic acids immobilized on solid supports. Anal Biochem 138: 267–284 (1984).

    Google Scholar 

  26. Dickey LF, Nguyen TT, Allen GC, Thompson WF: Light modulation of ferredoxin mRNA abundance requires an open reading frame. Plant Cell 6: 1171–1176 (1994).

    Google Scholar 

  27. Antoniou M, de Boer E, Habets G, Grosveld F: The human β-globin gene contains multiple regulatory regions: identification of one promoter and two downstream enhancers. EMBO J 7: 377–384 (1988).

    Google Scholar 

  28. Kollias G, Hurst J, de Boer E, Grosveld F: The human β-globin gene contains a downstream developmental specific enhancer. Nucl Acids Res 15: 5739–5747 (1987).

    Google Scholar 

  29. Rossi P, de Crombrugghe B: Identification of a cell-specific transcriptional enhancer in the first intron of the mouse a2 (type I) collagen gene. Proc Natl Acad Sci USA 84: 5590–5594 (1987).

    Google Scholar 

  30. Evans MJ, Scarpulla RC: Both upstream and intron sequence elements are required for elevated expression of the rat somatic cytochrome c gene in COS-1 cells. Mol Cell Biol 8: 35–41 (1988).

    Google Scholar 

  31. Osborne TF, Arvidson DN, Tyau ES, Dunsworth-Browne M, Berk AJ: Transcription control region within the protein-coding portion of adenovirus E1A genes. Mol Cell Biol 4: 1293–1305 (1984).

    Google Scholar 

  32. Fantino E, Marguet D, Lauquin GJM: Downstream activating sequence within the coding region of a yeast gene: specific binding in vitro of RAP1 protein. Mol Gen Genet 236: 65–75 (1992).

    Google Scholar 

  33. Eccles S, Sarner N, Vidal M, Cox A, Grosveld F: Enhancer sequences located 3′ of the mouse immunoglobulin lambda locus specify high-level expression of an immunoglobulin lambda gene in B cells of transgenic mice. New Biol 2: 801–811 (1990).

    Google Scholar 

  34. Rosenthal N, Kornhauser JM, Donoghue M, Rosen KM, Merlie JP: Myosin light chain enhancer activates muscle-specific, developmentally regulated gene expression in transgenic mice. Proc Natl Acad Sci USA 86: 7780–7784 (1989).

    Google Scholar 

  35. Muller HP, Schaffner W: Transcriptional enhancers can act in trans. Trends Genet 6: 300–304 (1990).

    Google Scholar 

  36. Kuhlemeier C: Transcriptional and post-transcriptional regulation of gene expression in plants. Plant Mol Biol 19: 1–14 (1992).

    Google Scholar 

  37. Chappell J, Hahlbrock K: Transcription of plant defence genes in response to UV light or fungal elicitor. Nature 311: 76–78 (1984).

    Google Scholar 

  38. Douglas C, Hoffmann H, Schulz W, Hahlbrock K: Structure and elicitor or u.v.light-stimulated expression of two 4-coumarate: CoA ligase genes in parsley. EMBO J 6: 1189–1195 (1987).

    Google Scholar 

  39. Lois R, Dietrich A, Hahlbrock K: A phenylalanine ammonia-lyase gene from parsley: structure, regulation and identification of elicitor and light responsive cis-acting elements. EMBO J 8: 1641–1648 (1989).

    Google Scholar 

  40. Douglas CJ, Hauffe KD, Ites-Morales ME, Ellard M, Paszkowski U, Hahlbrock K, Dangl JL: Exonic sequences are required for elicitor and light activation of a plant defense gene, but promoter sequences are sufficient for tissue specific expression. EMBO J 10: 1767–1775 (1991).

    Google Scholar 

  41. Hentze MW: Determinants and regulation of cytoplasmic mRNA stability in eukaryotic cells. Biochim Biophys Acta 1090: 281–292 (1990).

    Google Scholar 

  42. Sachs AB: Messenger RNA degradation in eukaryotes. Cell 74: 413–421 (1993).

    Google Scholar 

  43. Gay DA, Sisodia SS, Cleveland DW: Autoregulatory control of β-tubulin mRNA stability is linked to translation elongation. Proc Natl Acad Sci USA 86: 5763–5767 (1989).

    Google Scholar 

  44. Klausner RD, Rouault TA, Harford JB: Regulating the fate of messenger RNA: the control of cellular iron metabolism. Cell 72: 19–28 (1993).

    Google Scholar 

  45. Shirley BW, Meagher RB: A potential role for RNA turnover in the light regulation of plant gene expression: ribulose—1,5-bisphosphate carboxylase small subunit in soybean. Nucl Acids Res 18: 3377–3385 (1990).

    Google Scholar 

  46. Thompson DM, Meagher RB: Transcriptional and post-transcriptional processes regulate expression of RNA encoding the small subunit of ribulose1,5-biphosphate carboxylase differently in petunia and soybean. Nucl Acids Res 18: 3621–3629 (1990).

    Google Scholar 

  47. Thompson DM, Tanzer MM, Meagher RB: Degradation products of the mRNA encoding the small subunit of ribulose1,5-bisphosphate carboxylase in soybean and transgenic petunia. Plant Cell 4: 47–58 (1992).

    Google Scholar 

  48. Klug G: The role of mRNA degradation in the regulated expression of bacterial photosynthesis genes. Mol Microbiol 9: 1–7 (1993).

    Google Scholar 

  49. Neuberger MS, Williams GT: The intron requirement for immunoglobulin gene expression is dependent upon the promoter. Nucl Acids Res 16: 6713–6724 (1988).

    Google Scholar 

  50. Enssle J, Kugler W, Hentze MW, Kulozik AE: Determination of mRNA fate by different RNA polymerase II promoters. Proc Natl Acad Sci USA 90: 10091–10095 (1993).

    Google Scholar 

  51. Braddock M, Thorburn AM, Chambers A, Elliott GD, Anderson GJ, Kingsman AJ, Kingsman SM: A nuclear translational block imposed by the HIV-1 U3 region is relieved by the Tat-TAR interaction. Cell 62: 1123–1133 (1990).

    Google Scholar 

  52. Bovy A, de Vrieze G, Lugones L, van Horssen P, van den Berg C, Borrias M, Weisbeek P: Iron-dependent stability of the ferredoxin I transcripts from the cyanobacterial strains Synechococcus species PCC 7942 and Anabaena species PCC 7937. Mol Microbiol 7: 429–439 (1993).

    Google Scholar 

  53. Bovy A, de Kruif J, de Vrieze G, Borrias M, Weisbeek P: Iron-dependent protection of the Synechococcus ferredoxin I transcript against nucleolytic degradation requires cis-regulatory sequences in the 5′ part of the messenger RNA. Plant Mol Biol 22: 1047–1065 (1993).

    Google Scholar 

Download references

Author information

Author notes

  1. Arnaud Bovy

    Present address: Department of Developmental Biology, DLO-Center for Plant Breeding and Reproduction Research (CPRO-DLO), Droevendaalsesteeg 1, P.O.Box 16, 6700 AA, Wageningen, The Netherlands

Authors and Affiliations

  1. Department of Molecular Cell Biology, University of Utrecht, Padualaan 8, 3584 CH, Utrecht, Netherlands

    Arnaud Bovy, Claudia Van Den Berg, Geert De Vrieze, Peter Weisbeek & Sjef Smeekens

  2. Department of Botany and Genetics, North Carolina State University, 27695-7612, Raleigh, NC, USA

    William F. Thompson

Authors
  1. Arnaud Bovy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Claudia Van Den Berg
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Geert De Vrieze
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. William F. Thompson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Peter Weisbeek
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sjef Smeekens
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bovy, A., Van Den Berg, C., De Vrieze, G. et al. Light-regulated expression of the Arabidopsis thaliana ferredoxin gene requires sequences upstream and downstream of the transcription initiation site. Plant Mol Biol 27, 27–39 (1995). https://doi.org/10.1007/BF00019176

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00019176

Key words

Search

Navigation