Abstract
Post-transcriptional regulation of the genes encoding the small subunit (rbcS) of ribulose-1,5-bisphosphate carboxylase was examined in soybean seedlings. Substantial discrepancies were detected between relative in vitro transcription rates and steady-state RNA levels in light- and dark-grown seedling leaves, indicating that rbcS RNA may be degraded more rapidly in light than in darkness. Additional data imply that the turnover mechanism is rapidly induced by light, maintained for some time in darkness, and that it may be negatively controlled by far-red light. The proposed RNA turnover system does not affect all RNAs equally since a soybean actin gene showed equivalent in vitro transcription rates and RNA levels in light and darkness. Soybean rbcS genes may be subject to a novel mode of control in which light-induced expression is accompanied by an increased rate of RNA degradation. Models for the specific regulation of rbcS RNA stability in response to light are presented.
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- Baker E. J., Keller L. R., Schloss J. A., Rosenbaum J. L. Protein synthesis is required for rapid degradation of tubulin mRNA and other deflagellation-induced RNAs in Chlamydomonas reinhardi. Mol Cell Biol. 1986 Jan;6(1):54–61. doi: 10.1128/mcb.6.1.54. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Baker E. J., Schloss J. A., Rosenbaum J. L. Rapid changes in tubulin RNA synthesis and stability induced by deflagellation in Chlamydomonas. J Cell Biol. 1984 Dec;99(6):2074–2081. doi: 10.1083/jcb.99.6.2074. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Berry-Lowe S. L., Meagher R. B. Transcriptional regulation of a gene encoding the small subunit of ribulose-1,5-bisphosphate carboxylase in soybean tissue is linked to the phytochrome response. Mol Cell Biol. 1985 Aug;5(8):1910–1917. doi: 10.1128/mcb.5.8.1910. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berry J. O., Carr J. P., Klessig D. F. mRNAs encoding ribulose-1,5-bisphosphate carboxylase remain bound to polysomes but are not translated in amaranth seedlings transferred to darkness. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4190–4194. doi: 10.1073/pnas.85.12.4190. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Berry J. O., Nikolau B. J., Carr J. P., Klessig D. F. Translational regulation of light-induced ribulose 1,5-bisphosphate carboxylase gene expression in amaranth. Mol Cell Biol. 1986 Jul;6(7):2347–2353. doi: 10.1128/mcb.6.7.2347. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Blanchard J. M., Piechaczyk M., Dani C., Chambard J. C., Franchi A., Pouyssegur J., Jeanteur P. c-myc gene is transcribed at high rate in G0-arrested fibroblasts and is post-transcriptionally regulated in response to growth factors. Nature. 1985 Oct 3;317(6036):443–445. doi: 10.1038/317443a0. [DOI] [PubMed] [Google Scholar]
- Carneiro M., Schibler U. Accumulation of rare and moderately abundant mRNAs in mouse L-cells is mainly post-transcriptionally regulated. J Mol Biol. 1984 Oct 5;178(4):869–880. doi: 10.1016/0022-2836(84)90316-4. [DOI] [PubMed] [Google Scholar]
- 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]
- Dretzen G., Bellard M., Sassone-Corsi P., Chambon P. A reliable method for the recovery of DNA fragments from agarose and acrylamide gels. Anal Biochem. 1981 Apr;112(2):295–298. doi: 10.1016/0003-2697(81)90296-7. [DOI] [PubMed] [Google Scholar]
- Eckenrode V. K., Arnold J., Meagher R. B. Comparison of the nucleotide sequence of soybean 18S rRNA with the sequences of other small-subunit rRNAs. J Mol Evol. 1984;21(3):259–269. doi: 10.1007/BF02102358. [DOI] [PubMed] [Google Scholar]
- Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
- Fitzwater T., Zhang X. Y., Elble R., Polisky B. Conditional high copy number ColE1 mutants: resistance to RNA1 inhibition in vivo and in vitro. EMBO J. 1988 Oct;7(10):3289–3297. doi: 10.1002/j.1460-2075.1988.tb03196.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fyrberg E. A., Mahaffey J. W., Bond B. J., Davidson N. Transcripts of the six Drosophila actin genes accumulate in a stage- and tissue-specific manner. Cell. 1983 May;33(1):115–123. doi: 10.1016/0092-8674(83)90340-9. [DOI] [PubMed] [Google Scholar]
- 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]
- Gilmour D. S., Lis J. T. RNA polymerase II interacts with the promoter region of the noninduced hsp70 gene in Drosophila melanogaster cells. Mol Cell Biol. 1986 Nov;6(11):3984–3989. doi: 10.1128/mcb.6.11.3984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goldschmidt-Clermont M., Rahire M. Sequence, evolution and differential expression of the two genes encoding variant small subunits of ribulose bisphosphate carboxylase/oxygenase in Chlamydomonas reinhardtii. J Mol Biol. 1986 Oct 5;191(3):421–432. doi: 10.1016/0022-2836(86)90137-3. [DOI] [PubMed] [Google Scholar]
- Gong Z. Y., Brandhorst B. P. Stabilization of tubulin mRNA by inhibition of protein synthesis in sea urchin embryos. Mol Cell Biol. 1988 Aug;8(8):3518–3525. doi: 10.1128/mcb.8.8.3518. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Graves R. A., Pandey N. B., Chodchoy N., Marzluff W. F. Translation is required for regulation of histone mRNA degradation. Cell. 1987 Feb 27;48(4):615–626. doi: 10.1016/0092-8674(87)90240-6. [DOI] [PubMed] [Google Scholar]
- Hall T. C., Ma Y., Buchbinder B. U., Pyne J. W., Sun S. M., Bliss F. A. Messenger RNA for G1 protein of French bean seeds: Cell-free translation and product characterization. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3196–3200. doi: 10.1073/pnas.75.7.3196. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hightower R. C., Meagher R. B. Divergence and differential expression of soybean actin genes. EMBO J. 1985 Jan;4(1):1–8. doi: 10.1002/j.1460-2075.1985.tb02309.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kimura S., Gonzalez F. J., Nebert D. W. Tissue-specific expression of the mouse dioxin-inducible P(1)450 and P(3)450 genes: differential transcriptional activation and mRNA stability in liver and extrahepatic tissues. Mol Cell Biol. 1986 May;6(5):1471–1477. doi: 10.1128/mcb.6.5.1471. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Mangiarotti G., Giorda R., Ceccarelli A., Perlo C. mRNA stabilization controls the expression of a class of developmentally regulated genes in Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1985 Sep;82(17):5786–5790. doi: 10.1073/pnas.82.17.5786. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Meagher R. B., Berry-Lowe S., Rice K. Molecular evolution of the small subunit of ribulose bisphosphate carboxylase: nucleotide substitution and gene conversion. Genetics. 1989 Dec;123(4):845–863. doi: 10.1093/genetics/123.4.845. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- O'Farrell P. H. High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975 May 25;250(10):4007–4021. [PMC free article] [PubMed] [Google Scholar]
- Plumley F. G., Kirchman D. L., Hodson R. E., Schmidt G. W. Ribulose Bisphosphate Carboxylase from Three Chlorophyll c-Containing Algae : Physical and Immunological Characterizations. Plant Physiol. 1986 Mar;80(3):685–691. doi: 10.1104/pp.80.3.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rao T. R., Slobin L. I. The stability of mRNA for eucaryotic elongation factor Tu in Friend erythroleukemia cells varies with growth rate. Mol Cell Biol. 1988 Mar;8(3):1085–1092. doi: 10.1128/mcb.8.3.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ross J., Kobs G., Brewer G., Peltz S. W. Properties of the exonuclease activity that degrades H4 histone mRNA. J Biol Chem. 1987 Jul 5;262(19):9374–9381. [PubMed] [Google Scholar]
- Rowland L. J., Strommer J. N. Anaerobic treatment of maize roots affects transcription of Adh1 and transcript stability. Mol Cell Biol. 1986 Oct;6(10):3368–3372. doi: 10.1128/mcb.6.10.3368. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schmidt G. W., Mishkind M. L. Rapid degradation of unassembled ribulose 1,5-bisphosphate carboxylase small subunits in chloroplasts. Proc Natl Acad Sci U S A. 1983 May;80(9):2632–2636. doi: 10.1073/pnas.80.9.2632. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shaw C. H., Sanders D. M., Bates M. R., Shaw C. H. Light regulation of a SSRubisco-nos chimaeric gene: photoregulatory control sequences from a C3 plant function in cells of a CAM plant. Nucleic Acids Res. 1986 Aug 26;14(16):6603–6612. doi: 10.1093/nar/14.16.6603. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shaw G., Kamen R. A conserved AU sequence from the 3' untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell. 1986 Aug 29;46(5):659–667. doi: 10.1016/0092-8674(86)90341-7. [DOI] [PubMed] [Google Scholar]
- Shirley B. W., Berry-Lowe S. L., Rogers S. G., Flick J. S., Horsch R., Fraley R. T., Meagher R. B. 5' proximal sequences of a soybean ribulose-1,5-bisphosphate carboxylase small subunit gene direct light and phytochrome controlled transcription. Nucleic Acids Res. 1987 Aug 25;15(16):6501–6514. doi: 10.1093/nar/15.16.6501. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Timko M. P., Kausch A. P., Castresana C., Fassler J., Herrera-Estrella L., Van den Broeck G., Van Montagu M., Schell J., Cashmore A. R. Light regulation of plant gene expression by an upstream enhancer-like element. Nature. 1985 Dec 12;318(6046):579–582. doi: 10.1038/318579a0. [DOI] [PubMed] [Google Scholar]
- 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]
- Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tumer N. E., Clark W. G., Tabor G. J., Hironaka C. M., Fraley R. T., Shah D. M. The genes encoding the small subunit of ribulose-1,5-bisphosphate carboxylase are expressed differentially in petunia leaves. Nucleic Acids Res. 1986 Apr 25;14(8):3325–3342. doi: 10.1093/nar/14.8.3325. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Walling L., Drews G. N., Goldberg R. B. Transcriptional and post-transcriptional regulation of soybean seed protein mRNA levels. Proc Natl Acad Sci U S A. 1986 Apr;83(7):2123–2127. doi: 10.1073/pnas.83.7.2123. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Watson G., Paigen K. mRNA synthesis rates in vivo for androgen-inducible sequences in mouse kidney. Mol Cell Biol. 1988 May;8(5):2117–2124. doi: 10.1128/mcb.8.5.2117. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wilson T., Treisman R. Removal of poly(A) and consequent degradation of c-fos mRNA facilitated by 3' AU-rich sequences. Nature. 1988 Nov 24;336(6197):396–399. doi: 10.1038/336396a0. [DOI] [PubMed] [Google Scholar]
- Yen T. J., Gay D. A., Pachter J. S., Cleveland D. W. Autoregulated changes in stability of polyribosome-bound beta-tubulin mRNAs are specified by the first 13 translated nucleotides. Mol Cell Biol. 1988 Mar;8(3):1224–1235. doi: 10.1128/mcb.8.3.1224. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhu Y. S., Kung S. D., Bogorad L. Phytochrome control of levels of mRNA complementary to plastid and nuclear genes of maize. Plant Physiol. 1985 Oct;79(2):371–376. doi: 10.1104/pp.79.2.371. [DOI] [PMC free article] [PubMed] [Google Scholar]