Abstract
The rRNA genes in most eucaryotic organisms are present in a tandem array. There is substantial evidence that transcription of one of these genes may not be independent of transcription of others. In particular, in the yeast Saccharomyces cerevisiae, the enhancer of rRNA transcription that lies 2.2 kilobases 5' of the transcription initiation site is at least partly within the upstream transcription unit. To ask more directly about the relationship of the tandemness of these genes to their transcription, we have constructed a minirepeat containing two identifiable test genes, with or without enhancer(s). On integration into the URA3 locus, these genes were transcribed by RNA polymerase I. A single enhancer effectively stimulated transcription of both genes by 10- to 30-fold, even when it was located upstream of both or downstream of both. Two enhancers had roughly additive effects. These results suggest a model of enhancer function in tandemly repeated genes.
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- Bateman E., Paule M. R. Promoter occlusion during ribosomal RNA transcription. Cell. 1988 Sep 23;54(7):985–992. doi: 10.1016/0092-8674(88)90113-4. [DOI] [PubMed] [Google Scholar]
- Brill S. J., DiNardo S., Voelkel-Meiman K., Sternglanz R. Need for DNA topoisomerase activity as a swivel for DNA replication for transcription of ribosomal RNA. 1987 Mar 26-Apr 1Nature. 326(6111):414–416. doi: 10.1038/326414a0. [DOI] [PubMed] [Google Scholar]
- Callan H. G. The Croonian Lecture, 1981. Lampbrush chromosomes. Proc R Soc Lond B Biol Sci. 1982 Mar 22;214(1197):417–448. doi: 10.1098/rspb.1982.0020. [DOI] [PubMed] [Google Scholar]
- Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dabeva M. D., Warner J. R. The yeast ribosomal protein L32 and its gene. J Biol Chem. 1987 Nov 25;262(33):16055–16059. [PubMed] [Google Scholar]
- De Winter R. F., Moss T. A complex array of sequences enhances ribosomal transcription in Xenopus laevis. J Mol Biol. 1987 Aug 20;196(4):813–827. doi: 10.1016/0022-2836(87)90407-4. [DOI] [PubMed] [Google Scholar]
- De Winter R. F., Moss T. Spacer promoters are essential for efficient enhancement of X. laevis ribosomal transcription. Cell. 1986 Jan 31;44(2):313–318. doi: 10.1016/0092-8674(86)90765-8. [DOI] [PubMed] [Google Scholar]
- Dixit A., Garg L. C., Chao W., Jacob S. T. An enhancer element in the far upstream spacer region of rat ribosomal RNA gene. J Biol Chem. 1987 Aug 25;262(24):11616–11622. [PubMed] [Google Scholar]
- Elion E. A., Warner J. R. An RNA polymerase I enhancer in Saccharomyces cerevisiae. Mol Cell Biol. 1986 Jun;6(6):2089–2097. doi: 10.1128/mcb.6.6.2089. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Elion E. A., Warner J. R. The major promoter element of rRNA transcription in yeast lies 2 kb upstream. Cell. 1984 Dec;39(3 Pt 2):663–673. doi: 10.1016/0092-8674(84)90473-2. [DOI] [PubMed] [Google Scholar]
- Grummt I., Kuhn A., Bartsch I., Rosenbauer H. A transcription terminator located upstream of the mouse rDNA initiation site affects rRNA synthesis. Cell. 1986 Dec 26;47(6):901–911. doi: 10.1016/0092-8674(86)90805-6. [DOI] [PubMed] [Google Scholar]
- Grummt I., Maier U., Ohrlein A., Hassouna N., Bachellerie J. P. Transcription of mouse rDNA terminates downstream of the 3' end of 28S RNA and involves interaction of factors with repeated sequences in the 3' spacer. Cell. 1985 Dec;43(3 Pt 2):801–810. doi: 10.1016/0092-8674(85)90253-3. [DOI] [PubMed] [Google Scholar]
- Guarente L., Hoar E. Upstream activation sites of the CYC1 gene of Saccharomyces cerevisiae are active when inverted but not when placed downstream of the "TATA box". Proc Natl Acad Sci U S A. 1984 Dec;81(24):7860–7864. doi: 10.1073/pnas.81.24.7860. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Henderson S., Sollner-Webb B. A transcriptional terminator is a novel element of the promoter of the mouse ribosomal RNA gene. Cell. 1986 Dec 26;47(6):891–900. doi: 10.1016/0092-8674(86)90804-4. [DOI] [PubMed] [Google Scholar]
- Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. doi: 10.1128/jb.153.1.163-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kempers-Veenstra A. E., Oliemans J., Offenberg H., Dekker A. F., Piper P. W., Planta R. J., Klootwijk J. 3'-End formation of transcripts from the yeast rRNA operon. EMBO J. 1986 Oct;5(10):2703–2710. doi: 10.1002/j.1460-2075.1986.tb04554.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Klemenz R., Geiduschek E. P. The 5' terminus of the precursor ribosomal RNA of Saccharomyces cerevisiae. Nucleic Acids Res. 1980 Jun 25;8(12):2679–2689. doi: 10.1093/nar/8.12.2679. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kohorn B. D., Rae P. M. Nontranscribed spacer sequences promote in vitro transcription of Drosophila ribosomal DNA. Nucleic Acids Res. 1982 Nov 11;10(21):6879–6886. doi: 10.1093/nar/10.21.6879. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kuhn A., Grummt I. A novel promoter in the mouse rDNA spacer is active in vivo and in vitro. EMBO J. 1987 Nov;6(11):3487–3492. doi: 10.1002/j.1460-2075.1987.tb02673.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Labhart P., Reeder R. H. Characterization of three sites of RNA 3' end formation in the Xenopus ribosomal gene spacer. Cell. 1986 May 9;45(3):431–443. doi: 10.1016/0092-8674(86)90329-6. [DOI] [PubMed] [Google Scholar]
- Labhart P., Reeder R. H. Enhancer-like properties of the 60/81 bp elements in the ribosomal gene spacer of Xenopus laevis. Cell. 1984 May;37(1):285–289. doi: 10.1016/0092-8674(84)90324-6. [DOI] [PubMed] [Google Scholar]
- Labhart P., Reeder R. H. Xenopus ribosomal gene enhancers function when inserted inside the gene they enhance. Nucleic Acids Res. 1985 Dec 20;13(24):8999–9009. doi: 10.1093/nar/13.24.8999. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lucchini R., Reeder R. H. A test of 'polymerase handover' as a mechanism for stimulating initiation by RNA polymerase I. Nucleic Acids Res. 1989 Jan 11;17(1):373–387. doi: 10.1093/nar/17.1.373. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McStay B., Reeder R. H. A termination site for Xenopus RNA polymerase I also acts as an element of an adjacent promoter. Cell. 1986 Dec 26;47(6):913–920. doi: 10.1016/0092-8674(86)90806-8. [DOI] [PubMed] [Google Scholar]
- Mestel R., Yip M., Holland J. P., Wang E., Kang J., Holland M. J. Sequences within the spacer region of yeast rRNA cistrons that stimulate 35S rRNA synthesis in vivo mediate RNA polymerase I-dependent promoter and terminator activities. Mol Cell Biol. 1989 Mar;9(3):1243–1254. doi: 10.1128/mcb.9.3.1243. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mitchelson K., Moss T. The enhancement of ribosomal transcription by the recycling of RNA polymerase I. Nucleic Acids Res. 1987 Nov 25;15(22):9577–9596. doi: 10.1093/nar/15.22.9577. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morrow B. E., Johnson S. P., Warner J. R. Proteins that bind to the yeast rDNA enhancer. J Biol Chem. 1989 May 25;264(15):9061–9068. [PubMed] [Google Scholar]
- Moss T. A transcriptional function for the repetitive ribosomal spacer in Xenopus laevis. Nature. 1983 Mar 17;302(5905):223–228. doi: 10.1038/302223a0. [DOI] [PubMed] [Google Scholar]
- Murtif V. L., Rae P. M. In vivo transcription of rDNA spacers in Drosophila. Nucleic Acids Res. 1985 May 10;13(9):3221–3239. doi: 10.1093/nar/13.9.3221. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Müller M. M., Gerster T., Schaffner W. Enhancer sequences and the regulation of gene transcription. Eur J Biochem. 1988 Oct 1;176(3):485–495. doi: 10.1111/j.1432-1033.1988.tb14306.x. [DOI] [PubMed] [Google Scholar]
- Philippsen P., Thomas M., Kramer R. A., Davis R. W. Unique arrangement of coding sequences for 5 S, 5.8 S, 18 S and 25 S ribosomal RNA in Saccharomyces cerevisiae as determined by R-loop and hybridization analysis. J Mol Biol. 1978 Aug 15;123(3):387–404. doi: 10.1016/0022-2836(78)90086-4. [DOI] [PubMed] [Google Scholar]
- Pikaard C. S., Reeder R. H. Sequence elements essential for function of the Xenopus laevis ribosomal DNA enhancers. Mol Cell Biol. 1988 Oct;8(10):4282–4288. doi: 10.1128/mcb.8.10.4282. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rose M., Grisafi P., Botstein D. Structure and function of the yeast URA3 gene: expression in Escherichia coli. Gene. 1984 Jul-Aug;29(1-2):113–124. doi: 10.1016/0378-1119(84)90172-0. [DOI] [PubMed] [Google Scholar]
- Schultz L. D., Friesen J. D. Nucleotide sequence of the tcml gene (ribosomal protein L3) of Saccharomyces cerevisiae. J Bacteriol. 1983 Jul;155(1):8–14. doi: 10.1128/jb.155.1.8-14.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Skryabin K. G., Eldarov M. A., Larionov V. L., Bayev A. A., Klootwijk J., de Regt V. C., Veldman G. M., Planta R. J., Georgiev O. I., Hadjiolov A. A. Structure and function of the nontranscribed spacer regions of yeast rDNA. Nucleic Acids Res. 1984 Mar 26;12(6):2955–2968. doi: 10.1093/nar/12.6.2955. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sollner-Webb B., Tower J. Transcription of cloned eukaryotic ribosomal RNA genes. Annu Rev Biochem. 1986;55:801–830. doi: 10.1146/annurev.bi.55.070186.004101. [DOI] [PubMed] [Google Scholar]
- Swanson M. E., Holland M. J. RNA polymerase I-dependent selective transcription of yeast ribosomal DNA. Identification of a new cellular ribosomal RNA precursor. J Biol Chem. 1983 Mar 10;258(5):3242–3250. [PubMed] [Google Scholar]
- Swanson M. E., Yip M., Holland M. J. Characterization of an RNA polymerase I-dependent promoter within the spacer region of yeast ribosomal cistrons. J Biol Chem. 1985 Aug 15;260(17):9905–9915. [PubMed] [Google Scholar]
- Tautz D., Dover G. A. Transcription of the tandem array of ribosomal DNA in Drosophila melanogaster does not terminate at any fixed point. EMBO J. 1986 Jun;5(6):1267–1273. doi: 10.1002/j.1460-2075.1986.tb04356.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tollervey D. A yeast small nuclear RNA is required for normal processing of pre-ribosomal RNA. EMBO J. 1987 Dec 20;6(13):4169–4175. doi: 10.1002/j.1460-2075.1987.tb02763.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tower J., Henderson S. L., Dougherty K. M., Wejksnora P. J., Sollner-Webb B. An RNA polymerase I promoter located in the CHO and mouse ribosomal DNA spacers: functional analysis and factor and sequence requirements. Mol Cell Biol. 1989 Apr;9(4):1513–1525. doi: 10.1128/mcb.9.4.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Warner J. R. The assembly of ribosomes in yeast. J Biol Chem. 1971 Jan 25;246(2):447–454. [PubMed] [Google Scholar]