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Plant Molecular Biology

, Volume 17, Issue 1, pp 73–82 | Cite as

Post-transcriptional regulation by light of the biosynthesis ofEuglena ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit

  • Mario Keller
  • Raquel Lia Chan
  • Luc-Henri Tessier
  • Jacques-Henry Weil
  • Patrice Imbault
Article

Abstract

InEuglena gracilis, the amounts of the mature small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) increase during cell greening, while an analysis of the transcripts, performed at different stages of chloroplast development, shows no difference in the amounts of the corresponding mRNA. Pulse-chase experiments followed by immunoprecipitation show a significant increase in the rate of synthesis of the large molecular weight precursor (which consists of a transit peptide followed by eight small subunits) beginning after 12 h of illumination. Nevertheless, its half life does not change significantly during the chloroplast development. The results presented strongly suggest that the regulation of the expression of the Rubisco small subunit occurs at the translational level.

Key words

Euglena gracilis light regulation small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase post-transcriptional regulation 

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References

  1. 1.
    Berry JO, Nikolau BJ, Can JP, Klessig DF: Translational regulation of light-induced ribulose-1,5-bisphosphate carboxylase gene expression in amaranth. Mol Cell Biol 6: 2347–2353 (1986).Google Scholar
  2. 2.
    Bouet C, Schantz R, Dubertret G, Pineau B, Ledoigt G: Translational regulation of protein synthesis during light induced chloroplast development inEuglend. Planta 167: 511–520 (1986).Google Scholar
  3. 3.
    Chan RL, Keller M, Canaday J, Weil JH, Imbault P: Eight small subunits ofEuglena ribulose-1,5-bisphosphate carboxylase/oxygenase are translated from a large mRNA as a polyprotein. EMBO J 9: 333–338 (1990).Google Scholar
  4. 4.
    Coruzzi G, Broglie R, Edwards C, Chua N-H: Tissue specific and light regulated expression of a pea nuclear gene encoding the small subunit of ribulose-1,5-bisphosphate carboxylase. EMBO J 3: 1671–1679 (1984).Google Scholar
  5. 5.
    Ellis RJ: In: Roodyn PB (ed) Subcellular Biochemistry, pp. 237–261. Plenum, New York (1983).Google Scholar
  6. 6.
    Freyssinet G, Eicholz RL, Buetow D: Kinetics of accumulation of ribulose-1,5-bisphosphate carboxylase during greening inEuglena gracilis. Photoregulation. Plant Physiol 75: 850–857 (1984).Google Scholar
  7. 7.
    Freyssinet G, Freyssinet M, Buetow D: Kinetics of accumulation of ribulose-1,5-bisphosphate carboxylase during greening inEuglena gracilis. Nutritional regulation. Plant Physiol 75: 858–861 (1984).Google Scholar
  8. 8.
    Hallick RB, Greenberg BM, Gruissem W, Hollingsworth MJ, Karabin GD, Narita JO, Nickoloff JA, Passavant CW, Stiegler GL: Organization and expression of the chloroplast genome ofEuglena gracilis. In: Ciferri O, Dure L (eds) Structure and Function of Plant Genomes, pp. 155–156. Plenum, New York (1983).Google Scholar
  9. 9.
    Krauspe RS, Lerbs S, Parthier B, Wollghien R: Light induction of translatable mRNA for chloroplastic leucyl and valyl-tRNA synthetases ofEuglena gracilis. J Plant Physiol 130: 327–342 (1987).Google Scholar
  10. 10.
    Laemmli UK: Cleavage of structural proteins during the assembly of the head bacteriophage T4. Nature 227: 680–685 (1970).Google Scholar
  11. 11.
    Locker J: Analytical and preparative electrophoresis of RNA in agarose-urea. Anal Biochem 98: 358–369 (1979).Google Scholar
  12. 12.
    Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1982).Google Scholar
  13. 13.
    Manzara T, Gruissem W: Organization and expression of the genes encoding ribulose-1,5-bisphosphate carboxylase in higher plants. Photosynthesis Res 16: 117–139 (1988).Google Scholar
  14. 14.
    Miller ME, Jurgenson JE, Reardon EM, Price CA: Plastid translationin organello andin vitro during light-induced development inEuglena. J Biol Chem 258: 14478–14484 (1983).Google Scholar
  15. 15.
    Miziorko HM, Lorimer GH: Ribulose-1,5-bisphosphate carboxylase/oxygenase. Annu Rev Biochem 52: 507–535 (1983).Google Scholar
  16. 16.
    Monroy A, McCarthy SA, Schwartzbach SD: Evidence for translational regulation of chloroplast and mitochondrial biogenesis inEuglena. Plant Sci 51: 61–76 (1987).Google Scholar
  17. 17.
    Ortiz W, Reardon EM, Price CA: Preparation of chloroplasts fromEuglena highly active in protein synthesis. Plant Physiol 66: 291–294 (1980).Google Scholar
  18. 18.
    Peterson GL: A simplification of the protein assay method for Lowryet al. which is more generally applicable. Anal Biochem 83: 544–552 (1977).Google Scholar
  19. 19.
    Pineau B: Biosynthesis of ribulose-1,5-bisphosphate carboxylase in greening cells ofEuglena gracilis. Planta 156: 117–128 (1982).Google Scholar
  20. 20.
    Rawson JRY, Boerma CL, Andrews WH, Wilkerson CG: Complexity and abundance of ribonucleic acid transcribed from restriction endonuclease fragments ofEuglena chloroplast deoxyribonucleic acid during chloroplast development. Biochemistry 20: 2639–2644 (1981).Google Scholar
  21. 21.
    Reisfeld A, Edelman M: Translation of chloroplast polyA- mRNA in the wheat germ system. In: Edelman M, Hallick RB, Chua NH (eds) Methods in Chloroplast Molecular Biology, pp. 605–614. Elsevier, Amsterdam/New York/Oxford (1982).Google Scholar
  22. 22.
    Rikin A, Schwartzbach SD: Extremely large and slowly processed precursors to theEuglena light harvesting chlorophylla/b binding proteins of photosystem. II. Proc Natl Acad Sci U.S.A. 85: 5117–5121 (1988).Google Scholar
  23. 23.
    Schiff JA: Photocontrol of chloroplast development inEuglena. In: Akoyunoglou G, Argyroudi-Akoyunoglou IH (eds), Chloroplast Development, pp. 747–767. Elsevier/North Holland Biomedical Press, Amsterdam (1978).Google Scholar
  24. 24.
    Shashidhara LS, Smith AG: Expression and subcellular location of the tetrapyrrole synthesis enzyme prophobilinogen deaminase in light grownEuglena gracilis and three nonchlorophyllous cell lines. Proc Natl Acad Sci USA 88: 63–67 (1991).Google Scholar
  25. 25.
    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
  26. 26.
    Simpson J, Herrera-Estrella L: Light regulated gene expression. Plant Sci 95–109 (1990).Google Scholar
  27. 27.
    Smith SM, Ellis RJ: Light stimulated accumulation of transcripts of nuclear and chloroplast genes for ribulose-1,5-bisphosphate carboxylase. J Mol Appl Genet 1: 127–137 (1981).Google Scholar
  28. 28.
    Tobin EM, Silverthorne J: Light regulation of gene expression in higher plants. Ann Rev Plant Physiol 36: 569–593 (1985).Google Scholar
  29. 29.
    Tobin EM, Suttie JL: Light effects on the synthesis of ribulose-1,5-bisphosphate carboxylase inLemna gibba. Plant Physiol 65: 641 (1980).Google Scholar
  30. 30.
    Towbin H, Staehelin T, Gordon J: Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76: 4350–4354 (1979).Google Scholar
  31. 31.
    Tumer NE, Clark WG, Tabor GJ, Hironaka CM, Fraley RT, Shah DM: The genes encoding the small subunit of ribulose-1,5-bisphosphate carboxylase are expressed differentially in petunia leaves. Nucl Acids Res 8: 3325–3342 (1986).Google Scholar
  32. 32.
    Wallace RB, Miyada CG: Oligonucleotide probes for the screening of recombinant DNA libraries. In: Berger SL, Kimmel AR (eds) Methods in Enzymology 152: 432–442. Academic Press, London (1987).Google Scholar
  33. 33.
    Weiss C, Houlne G, Schantz ML, Schantz R: Photoregulation of the synthesis of chloroplast membrane proteins inEuglena gracilis. J Plant Physiol 133: 521–528 (1988).Google Scholar
  34. 34.
    Whatley FR, Arnon DI: Photosynthetic phosphorylation in plants. Meth Enzymol 6: 308–313 (1963).Google Scholar

Copyright information

© Kluwer Academic Publishers 1991

Authors and Affiliations

  • Mario Keller
    • 1
  • Raquel Lia Chan
    • 1
  • Luc-Henri Tessier
    • 1
  • Jacques-Henry Weil
    • 1
  • Patrice Imbault
    • 1
  1. 1.Institut de Biologie Moléculaire des Plantes du C.N.R.SUniversité Louis PasteurStrasbourg CedexFrance

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