Abstract
We investigated the basis for quantitative differences in leaf expression of the petunia genes (rbcS) encoding the small subunit of ribulose bisphosphate carboxylase. The most abundantly, SSU301, and the most weakly, SSU911, expressed petunia rbcS genes maintained their differential expression when transferred to tobacco, indicating that the determinants of quantitative expression are intrinsic to these rbcS genes. Analysis of chimeric genes in which the sequences of SSU301 and SSU911 had been exchanged at the translation start showed that sequences both 5' and 3' to the start codon contribute to differences in steady-state mRNA levels. The sequences 3' to the translation initiation codon were investigated by preparing chimeric genes in which sequences of the SSU301 and SSU911 were exchanged between each intron and at the translation termination codon. The results showed that sequences downstream of the coding region contribute to quantitative differences in expression of SSU301 and SSU911, and nuclear run-on transcription experiments indicated that the 3' sequences affect transcription rates of the rbcS genes.
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- Bodine D. M., Ley T. J. An enhancer element lies 3' to the human A gamma globin gene. EMBO J. 1987 Oct;6(10):2997–3004. doi: 10.1002/j.1460-2075.1987.tb02605.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brinster R. L., Allen J. M., Behringer R. R., Gelinas R. E., Palmiter R. D. Introns increase transcriptional efficiency in transgenic mice. Proc Natl Acad Sci U S A. 1988 Feb;85(3):836–840. doi: 10.1073/pnas.85.3.836. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Callis J., Fromm M., Walbot V. Introns increase gene expression in cultured maize cells. Genes Dev. 1987 Dec;1(10):1183–1200. doi: 10.1101/gad.1.10.1183. [DOI] [PubMed] [Google Scholar]
- Choi O. R., Engel J. D. A 3' enhancer is required for temporal and tissue-specific transcriptional activation of the chicken adult beta-globin gene. Nature. 1986 Oct 23;323(6090):731–734. doi: 10.1038/323731a0. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Dean C., Elzen P., Tamaki S., Dunsmuir P., Bedbrook J. Differential expression of the eight genes of the petunia ribulose bisphosphate carboxylase small subunit multi-gene family. EMBO J. 1985 Dec 1;4(12):3055–3061. doi: 10.1002/j.1460-2075.1985.tb04045.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dean C., Favreau M., Bedbrook J., Dunsmuir P. Sequences 5' to translation start regulate expression of petunia rbcS genes. Plant Cell. 1989 Feb;1(2):209–215. doi: 10.1105/tpc.1.2.209. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dean C., Favreau M., Dunsmuir P., Bedbrook J. Confirmation of the relative expression levels of the Petunia (Mitchell) rbcS genes. Nucleic Acids Res. 1987 Jun 11;15(11):4655–4668. doi: 10.1093/nar/15.11.4655. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dean C., Favreau M., Tamaki S., Bond-Nutter D., Dunsmuir P., Bedbrook J. Expression of tandem gene fusions in transgenic tobacco plants. Nucleic Acids Res. 1988 Aug 11;16(15):7601–7617. doi: 10.1093/nar/16.15.7601. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dean C., Jones J., Favreau M., Dunsmuir P., Bedbrook J. Influence of flanking sequences on variability in expression levels of an introduced gene in transgenic tobacco plants. Nucleic Acids Res. 1988 Oct 11;16(19):9267–9283. doi: 10.1093/nar/16.19.9267. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dean C., van den Elzen P., Tamaki S., Dunsmuir P., Bedbrook J. Linkage and homology analysis divides the eight genes for the small subunit of petunia ribulose 1,5-bisphosphate carboxylase into three gene families. Proc Natl Acad Sci U S A. 1985 Aug;82(15):4964–4968. doi: 10.1073/pnas.82.15.4964. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dunsmuir P., Smith S., Bedbrook J. A number of different nuclear genes for the small subunit of RuBPCase are transcribed in petunia. Nucleic Acids Res. 1983 Jun 25;11(12):4177–4183. doi: 10.1093/nar/11.12.4177. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Figurski D. H., Helinski D. R. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1648–1652. doi: 10.1073/pnas.76.4.1648. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Firtel R. A. Multigene families encoding actin and tubulin. Cell. 1981 Apr;24(1):6–7. doi: 10.1016/0092-8674(81)90494-3. [DOI] [PubMed] [Google Scholar]
- Fischer J. A., Maniatis T. Regulatory elements involved in Drosophila Adh gene expression are conserved in divergent species and separate elements mediate expression in different tissues. EMBO J. 1986 Jun;5(6):1275–1289. doi: 10.1002/j.1460-2075.1986.tb04357.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]
- 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]
- Kawashima N., Wildman S. G. Studies on fraction I protein. IV. Mode of inheritance of primary structure in relation to whether chloroplast or nuclear DNA contains the code for a chloroplast protein. Biochim Biophys Acta. 1972 Feb 23;262(1):42–49. doi: 10.1016/0005-2787(72)90217-1. [DOI] [PubMed] [Google Scholar]
- Kim K. H., Rheinwald J. G., Fuchs E. V. Tissue specificity of epithelial keratins: differential expression of mRNAs from two multigene families. Mol Cell Biol. 1983 Apr;3(4):495–502. doi: 10.1128/mcb.3.4.495. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kunkel T. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc Natl Acad Sci U S A. 1985 Jan;82(2):488–492. doi: 10.1073/pnas.82.2.488. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leys E. J., Crouse G. F., Kellems R. E. Dihydrofolate reductase gene expression in cultured mouse cells is regulated by transcript stabilization in the nucleus. J Cell Biol. 1984 Jul;99(1 Pt 1):180–187. doi: 10.1083/jcb.99.1.180. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Luthe D. S., Quatrano R. S. Transcription in Isolated Wheat Nuclei: I. ISOLATION OF NUCLEI AND ELIMINATION OF ENDOGENOUS RIBONUCLEASE ACTIVITY. Plant Physiol. 1980 Feb;65(2):305–308. doi: 10.1104/pp.65.2.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Owen D., Kühn L. C. Noncoding 3' sequences of the transferrin receptor gene are required for mRNA regulation by iron. EMBO J. 1987 May;6(5):1287–1293. doi: 10.1002/j.1460-2075.1987.tb02366.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sugita M., Gruissem W. Developmental, organ-specific, and light-dependent expression of the tomato ribulose-1,5-bisphosphate carboxylase small subunit gene family. Proc Natl Acad Sci U S A. 1987 Oct;84(20):7104–7108. doi: 10.1073/pnas.84.20.7104. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thornburg R. W., An G., Cleveland T. E., Johnson R., Ryan C. A. Wound-inducible expression of a potato inhibitor II-chloramphenicol acetyltransferase gene fusion in transgenic tobacco plants. Proc Natl Acad Sci U S A. 1987 Feb;84(3):744–748. doi: 10.1073/pnas.84.3.744. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Trainor C. D., Stamler S. J., Engel J. D. Erythroid-specific transcription of the chicken histone H5 gene is directed by a 3' enhancer. 1987 Aug 27-Sep 2Nature. 328(6133):827–830. doi: 10.1038/328827a0. [DOI] [PubMed] [Google Scholar]
- Vieira J., Messing J. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene. 1982 Oct;19(3):259–268. doi: 10.1016/0378-1119(82)90015-4. [DOI] [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]