Skip to main content
NCBI home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1986 Jul;6(7):2347–2353. doi: 10.1128/mcb.6.7.2347

Translational regulation of light-induced ribulose 1,5-bisphosphate carboxylase gene expression in amaranth.

J O Berry, B J Nikolau, J P Carr, D F Klessig
PMCID: PMC367787  PMID: 3785198

Abstract

The regulation of the genes encoding the large and small subunits of ribulose 1,5-bisphosphate carboxylase was examined in amaranth cotyledons in response to changes in illumination. When dark-grown cotyledons were transferred into light, synthesis of the large- and small-subunit polypeptides was initiated very rapidly, before any increase in the levels of their corresponding mRNAs. Similarly, when light-grown cotyledons were transferred to total darkness, synthesis of the large- and small-subunit proteins was rapidly depressed without changes in mRNA levels for either subunit. In vitro translation or in vivo pulse-chase experiments indicated that these apparent changes in protein synthesis were not due to alterations in the functionality of the mRNAs or to protein turnover, respectively. These results, in combination with our previous studies, suggest that the expression of ribulose 1,5-bisphosphate carboxylase genes can be adjusted rapidly at the translational level and over a longer period through changes in mRNA accumulation.

Full text

PDF
2347

Images in this article

2348Image
on p.2348
2348Image
on p.2348
2349Image
on p.2349
2349Image
on p.2349
2349Image
on p.2349
2350Image
on p.2350
2350Image
on p.2350
2351Image
on p.2351

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Barraclough R., Ellis R. J. The biosynthesis of ribulose bisphosphate carboxylase. Uncoupling of the synthesis of the large and small subunits in isolated soybean leaf cells. Eur J Biochem. 1979 Feb 15;94(1):165–177. doi: 10.1111/j.1432-1033.1979.tb12883.x. [DOI] [PubMed] [Google Scholar]
  2. Bennett J. Biosynthesis of the light-harvesting chlorophyll a/b protein. Polypeptide turnover in darkness. Eur J Biochem. 1981 Aug;118(1):61–70. doi: 10.1111/j.1432-1033.1981.tb05486.x. [DOI] [PubMed] [Google Scholar]
  3. Bennett J., Jenkins G. I., Hartley M. R. Differential regulation of the accumulation of the light-harvesting chlorophyll a/b complex and ribulose bisphosphate carboxylase/oxygenase in greening pea leaves. J Cell Biochem. 1984;25(1):1–13. doi: 10.1002/jcb.240250102. [DOI] [PubMed] [Google Scholar]
  4. Berry-Lowe S. L., Mc Knight T. D., Shah D. M., Meagher R. B. The nucleotide sequence, expression, and evolution of one member of a multigene family encoding the small subunit of ribulose-1,5-bisphosphate carboxylase in soybean. J Mol Appl Genet. 1982;1(6):483–498. [PubMed] [Google Scholar]
  5. Berry J. O., Nikolau B. J., Carr J. P., Klessig D. F. Transcriptional and post-transcriptional regulation of ribulose 1,5-bisphosphate carboxylase gene expression in light- and dark-grown amaranth cotyledons. Mol Cell Biol. 1985 Sep;5(9):2238–2246. doi: 10.1128/mcb.5.9.2238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cashmore A. R., Broadhurst M. K., Gray R. E. Cell-free synthesis of leaf protein: Identification of an apparent precursor of the small subunit of ribulose-1,5-bisphosphate carboxylase. Proc Natl Acad Sci U S A. 1978 Feb;75(2):655–659. doi: 10.1073/pnas.75.2.655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chua N. H., Schmidt G. W. Post-translational transport into intact chloroplasts of a precursor to the small subunit of ribulose-1,5-bisphosphate carboxylase. Proc Natl Acad Sci U S A. 1978 Dec;75(12):6110–6114. doi: 10.1073/pnas.75.12.6110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Coen D. M., Bedbrook J. R., Bogorad L., Rich A. Maize chloroplast DNA fragment encoding the large subunit of ribulosebisphosphate carboxylase. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5487–5491. doi: 10.1073/pnas.74.12.5487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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. 1984 Aug;3(8):1671–1679. doi: 10.1002/j.1460-2075.1984.tb02031.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dobberstein B., Blobel G., Chua N. H. In vitro synthesis and processing of a putative precursor for the small subunit of ribulose-1,5-bisphosphate carboxylase of Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A. 1977 Mar;74(3):1082–1085. doi: 10.1073/pnas.74.3.1082. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fromm H., Devic M., Fluhr R., Edelman M. Control of psbA gene expression: in mature Spirodela chloroplasts light regulation of 32-kd protein synthesis is independent of transcript level. EMBO J. 1985 Feb;4(2):291–295. doi: 10.1002/j.1460-2075.1985.tb03628.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gallagher T. F., Ellis R. J. Light-stimulated transcription of genes for two chloroplast polypeptides in isolated pea leaf nuclei. EMBO J. 1982;1(12):1493–1498. doi: 10.1002/j.1460-2075.1982.tb01345.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Geetha V., Mohamed A. H., Gnanam A. Cell-free synthesis of active ribulose-1,5-bisphosphate carboxylase in the mesophyll chloroplasts of Sorghum vulgare. Biochim Biophys Acta. 1980;606(1):83–94. doi: 10.1016/0005-2787(80)90100-8. [DOI] [PubMed] [Google Scholar]
  14. Grebanier A. E., Steinback K. E., Bogorad L. Comparison of the Molecular Weights of Proteins Synthesized by Isolated Chloroplasts with Those Which Appear during Greening in Zea mays. Plant Physiol. 1979 Mar;63(3):436–439. doi: 10.1104/pp.63.3.436. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hunt T. False starts in translational control of gene expression. Nature. 1985 Aug 15;316(6029):580–581. doi: 10.1038/316580a0. [DOI] [PubMed] [Google Scholar]
  16. Iwanij V., Chua N. H., Siekevitz P. Synthesis and turnover of ribulose biphosphate carboxylase and of its subunits during the cell cycle of Chlamydomonas reinhardtii. J Cell Biol. 1975 Mar;64(3):572–585. doi: 10.1083/jcb.64.3.572. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kaveh D., Harel E. Light-induced Changes in the Pattern of Protein Synthesis during the Early Stages of Greening of Etiolated Maize Leaves. Plant Physiol. 1973 Apr;51(4):671–676. doi: 10.1104/pp.51.4.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kirk M. M., Kirk D. L. Translational regulation of protein synthesis, in response to light, at a critical stage of Volvox development. Cell. 1985 Jun;41(2):419–428. doi: 10.1016/s0092-8674(85)80015-5. [DOI] [PubMed] [Google Scholar]
  19. Lorimer G. H., Miziorko H. M. Carbamate formation on the epsilon-amino group of a lysyl residue as the basis for the activation of ribulosebisphosphate carboxylase by CO2 and Mg2+. Biochemistry. 1980 Nov 11;19(23):5321–5328. doi: 10.1021/bi00564a027. [DOI] [PubMed] [Google Scholar]
  20. Lorimer G. H. Ribulosebisphosphate carboxylase: amino acid sequence of a peptide bearing the activator carbon dioxide. Biochemistry. 1981 Mar 3;20(5):1236–1240. doi: 10.1021/bi00508a028. [DOI] [PubMed] [Google Scholar]
  21. Miller M. E., Jurgenson J. E., Reardon E. M., Price C. A. Plastid translation in organello and in vitro during light-induced development in Euglena. J Biol Chem. 1983 Dec 10;258(23):14478–14484. [PubMed] [Google Scholar]
  22. Mishkind M. L., Schmidt G. W. Posttranscriptional Regulation of Ribulose 1,5-bisphosphate Carboxylase Small Subunit Accumulation in Chlamydomonas reinhardtii. Plant Physiol. 1983 Jul;72(3):847–854. doi: 10.1104/pp.72.3.847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Miziorko H. M., Lorimer G. H. Ribulose-1,5-bisphosphate carboxylase-oxygenase. Annu Rev Biochem. 1983;52:507–535. doi: 10.1146/annurev.bi.52.070183.002451. [DOI] [PubMed] [Google Scholar]
  24. Nelson T., Harpster M. H., Mayfield S. P., Taylor W. C. Light-regulated gene expression during maize leaf development. J Cell Biol. 1984 Feb;98(2):558–564. doi: 10.1083/jcb.98.2.558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Roberts B. E., Paterson B. M. Efficient translation of tobacco mosaic virus RNA and rabbit globin 9S RNA in a cell-free system from commercial wheat germ. Proc Natl Acad Sci U S A. 1973 Aug;70(8):2330–2334. doi: 10.1073/pnas.70.8.2330. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Santel H. J., Apel K. The protochlorophyllide holochrome of barley (Hordeum vulgare L.). The effect of light on the NADPH:protochlorophyllide oxidoreductase. Eur J Biochem. 1981 Nov;120(1):95–103. doi: 10.1111/j.1432-1033.1981.tb05674.x. [DOI] [PubMed] [Google Scholar]
  27. Schröder J., Kreuzaler F., Schäfer E., Hahlbrock K. Concomitant induction of phenylalanine ammonia-lyase and flavanone synthase mRNAs in irradiated plant cells. J Biol Chem. 1979 Jan 10;254(1):57–65. [PubMed] [Google Scholar]
  28. Silverthorne J., Tobin E. M. Demonstration of transcriptional regulation of specific genes by phytochrome action. Proc Natl Acad Sci U S A. 1984 Feb;81(4):1112–1116. doi: 10.1073/pnas.81.4.1112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sims T. L., Hague D. R. Light-stimulated increase of translatable mRNA for phosphoenolpyruvate carboxylase in leaves of maize. J Biol Chem. 1981 Aug 25;256(16):8252–8255. [PubMed] [Google Scholar]
  30. Smith S. M., Ellis R. J. Light-stimulated accumulation of transcripts of nuclear and chloroplast genes for ribulosebisphosphate carboxylase. J Mol Appl Genet. 1981;1(2):127–137. [PubMed] [Google Scholar]
  31. Stiekema W. J., Wimpee C. F., Silverthorne J., Tobin E. M. Phytochrome Control of the Expression of Two Nuclear Genes Encoding Chloroplast Proteins in Lemna gibba L. G-3. Plant Physiol. 1983 Jul;72(3):717–724. doi: 10.1104/pp.72.3.717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Stitt M., Lilley R. M., Heldt H. W. Adenine nucleotide levels in the cytosol, chloroplasts, and mitochondria of wheat leaf protoplasts. Plant Physiol. 1982 Oct;70(4):971–977. doi: 10.1104/pp.70.4.971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Tobin E. M. Light regulation of specific mRNA species in Lemna gibba L. G-3. Proc Natl Acad Sci U S A. 1978 Oct;75(10):4749–4753. doi: 10.1073/pnas.75.10.4749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Tobin E. M., Suttie J. L. Light Effects on the Synthesis of Ribulose-1,5-Bisphosphate Carboxylase in Lemna gibba L. G-3. Plant Physiol. 1980 Apr;65(4):641–647. doi: 10.1104/pp.65.4.641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Tobin E. M. White Light Effects on the mRNA for the Light-Harvesting Chlorophyll a/b-Protein in Lemna gibba L. G-3. Plant Physiol. 1981 Jun;67(6):1078–1083. doi: 10.1104/pp.67.6.1078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Walden R., Leaver C. J. Synthesis of Chloroplast Proteins during Germination and Early Development of Cucumber. Plant Physiol. 1981 Jun;67(6):1090–1096. doi: 10.1104/pp.67.6.1090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Zubay G. In vitro synthesis of protein in microbial systems. Annu Rev Genet. 1973;7:267–287. doi: 10.1146/annurev.ge.07.120173.001411. [DOI] [PubMed] [Google Scholar]
  38. de Heij H. T., Jochemsen A. G., Willemsen P. T., Groot G. S. Protein synthesis during chloroplast development in Spirodela oligorhiza. Coordinated synthesis of chloroplast-encoded and nuclear-encoded subunits of ATPase and ribulose-1,5-bisphosphate carboxylase. Eur J Biochem. 1984 Jan 2;138(1):161–168. doi: 10.1111/j.1432-1033.1984.tb07895.x. [DOI] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES