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. 1984 Jan 25;12(2):1137–1148. doi: 10.1093/nar/12.2.1137

A conserved sequence element is present around the transcription initiation site for RNA polymerase A in Saccharomycetoideae.

M P Verbeet, J Klootwijk, H van Heerikhuizen, R D Fontijn, E Vreugdenhil, R J Planta
PMCID: PMC318561  PMID: 6364043

Abstract

To identify DNA elements involved in the initiation of rRNA transcription in yeast we located the start site of the rRNA operon of Kluyveromyces lactis and Hansenula wingei, both members of the Saccharomycetoideae, by S1 nuclease analysis and determined the surrounding nucleotide sequences. Comparison of these sequences with those of Saccharomyces carlsbergensis, S. cerevisiae and S. rosei (all belonging to the same yeast subfamily) reveals an identical sequence at the site of transcription initiation from position +1 to +7 which is part of a larger conserved region extending from position -9 to +23; the conserved heptanucleotide sequence is supposed to constitute an important part of the promoter for yeast RNA polymerase A. The non-transcribed spacers (NTS) upstream of position -9 have diverged strongly with the exception of two short elements around positions -75 and -135. The external transcribed spacer (ETS) downstream of position +23 is largely conserved between K. lactis, S. rosei and S. carlsbergensis except for a divergent region around position +75. On the other hand, the ETS of H. wingei has diverged significantly.

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Selected References

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  1. Bach R., Allet B., Crippa M. Sequence organization of the spacer in the ribosomal genes of Xenopus clivii and Xenopus borealis. Nucleic Acids Res. 1981 Oct 24;9(20):5311–5330. doi: 10.1093/nar/9.20.5311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bayev A. A., Georgiev O. I., Hadjiolov A. A., Kermekchiev M. B., Nikolaev N., Skryabin K. G., Zakharyev V. M. The structure of the yeast ribosomal RNA genes. 2. The nucleotide sequence of the initiation site for ribosomal RNA transcription. Nucleic Acids Res. 1980 Nov 11;8(21):4919–4926. doi: 10.1093/nar/8.21.4919. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boseley P., Moss T., Mächler M., Portmann R., Birnstiel M. Sequence organization of the spacer DNA in a ribosomal gene unit of Xenopus laevis. Cell. 1979 May;17(1):19–31. doi: 10.1016/0092-8674(79)90291-5. [DOI] [PubMed] [Google Scholar]
  4. Brand R. C., Klootwijk J., Van Steenbergen T. J., De Kok A. J., Planta R. J. Secondary methylation of yeast ribosomal precursor RNA. Eur J Biochem. 1977 May 2;75(1):311–318. doi: 10.1111/j.1432-1033.1977.tb11531.x. [DOI] [PubMed] [Google Scholar]
  5. Breathnach R., Chambon P. Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem. 1981;50:349–383. doi: 10.1146/annurev.bi.50.070181.002025. [DOI] [PubMed] [Google Scholar]
  6. Clewell D. B., Helinski D. R. Properties of a supercoiled deoxyribonucleic acid-protein relaxation complex and strand specificity of the relaxation event. Biochemistry. 1970 Oct 27;9(22):4428–4440. doi: 10.1021/bi00824a026. [DOI] [PubMed] [Google Scholar]
  7. Coen E., Strachan T., Dover G. Dynamics of concerted evolution of ribosomal DNA and histone gene families in the melanogaster species subgroup of Drosophila. J Mol Biol. 1982 Jun 15;158(1):17–35. doi: 10.1016/0022-2836(82)90448-x. [DOI] [PubMed] [Google Scholar]
  8. Financsek I., Mizumoto K., Mishima Y., Muramatsu M. Human ribosomal RNA gene: nucleotide sequence of the transcription initiation region and comparison of three mammalian genes. Proc Natl Acad Sci U S A. 1982 May;79(10):3092–3096. doi: 10.1073/pnas.79.10.3092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Financsek I., Mizumoto K., Muramatsu M. Nucleotide sequence of the transcription initiation region of a rat ribosomal RNA gene. Gene. 1982 May;18(2):115–122. doi: 10.1016/0378-1119(82)90109-3. [DOI] [PubMed] [Google Scholar]
  10. Grosschedl R., Birnstiel M. L. Identification of regulatory sequences in the prelude sequences of an H2A histone gene by the study of specific deletion mutants in vivo. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1432–1436. doi: 10.1073/pnas.77.3.1432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Grosveld G. C., de Boer E., Shewmaker C. K., Flavell R. A. DNA sequences necessary for transcription of the rabbit beta-globin gene in vivo. Nature. 1982 Jan 14;295(5845):120–126. doi: 10.1038/295120a0. [DOI] [PubMed] [Google Scholar]
  12. Grummt I. Mapping of a mouse ribosomal DNA promoter by in vitro transcription. Nucleic Acids Res. 1981 Nov 25;9(22):6093–6102. doi: 10.1093/nar/9.22.6093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Grummt I. Nucleotide sequence requirements for specific initiation of transcription by RNA polymerase I. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6908–6911. doi: 10.1073/pnas.79.22.6908. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Grummt I., Roth E., Paule M. R. Ribosomal RNA transcription in vitro is species specific. Nature. 1982 Mar 11;296(5853):173–174. doi: 10.1038/296173a0. [DOI] [PubMed] [Google Scholar]
  15. Hall B. D., Clarkson S. G., Tocchini-Valentini G. Transcription initiation of eucaryotic transfer RNA genes. Cell. 1982 May;29(1):3–5. doi: 10.1016/0092-8674(82)90083-6. [DOI] [PubMed] [Google Scholar]
  16. Hoshikawa Y., Iida Y., Iwabuchi M. Nucleotide sequence of the transcriptional initiation region of Dictyostelium discoideum rRNA gene and comparison of the initiation regions of three lower eukaryotes' genes. Nucleic Acids Res. 1983 Mar 25;11(6):1725–1734. doi: 10.1093/nar/11.6.1725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Klootwijk J., de Jonge P., Planta R. J. The primary transcript of the ribosomal repeating unit in yeast. Nucleic Acids Res. 1979 Jan;6(1):27–39. doi: 10.1093/nar/6.1.27. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kohorn B. D., Rae P. M. Localization of DNA sequences promoting RNA polymerase I activity in Drosophila. Proc Natl Acad Sci U S A. 1983 Jun;80(11):3265–3268. doi: 10.1073/pnas.80.11.3265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Korn L. J. Transcription of Xenopus 5S ribosomal RNA genes. Nature. 1982 Jan 14;295(5845):101–105. doi: 10.1038/295101a0. [DOI] [PubMed] [Google Scholar]
  21. Learned R. M., Smale S. T., Haltiner M. M., Tjian R. Regulation of human ribosomal RNA transcription. Proc Natl Acad Sci U S A. 1983 Jun;80(12):3558–3562. doi: 10.1073/pnas.80.12.3558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Long E. O., Rebbert M. L., Dawid I. B. Nucleotide sequence of the initiation site for ribosomal RNA transcription in Drosophila melanogaster: comparison of genes with and without insertions. Proc Natl Acad Sci U S A. 1981 Mar;78(3):1513–1517. doi: 10.1073/pnas.78.3.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Maxam A. M., Gilbert W. A new method for sequencing DNA. Proc Natl Acad Sci U S A. 1977 Feb;74(2):560–564. doi: 10.1073/pnas.74.2.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Miesfeld R., Arnheim N. Identification of the in vivo and in vitro origin of transcription in human rDNA. Nucleic Acids Res. 1982 Jul 10;10(13):3933–3949. doi: 10.1093/nar/10.13.3933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Miller K. G., Sollner-Webb B. Transcription of mouse rRNA genes by RNA polymerase I: in vitro and in vivo initiation and processing sites. Cell. 1981 Nov;27(1 Pt 2):165–174. doi: 10.1016/0092-8674(81)90370-6. [DOI] [PubMed] [Google Scholar]
  26. Mishima Y., Yamamoto O., Kominami R., Muramatsu M. In vitro transcription of a cloned mouse ribosomal RNA gene. Nucleic Acids Res. 1981 Dec 21;9(24):6773–6785. doi: 10.1093/nar/9.24.6773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Moss T. Transcription of cloned Xenopus laevis ribosomal DNA microinjected into Xenopus oocytes, and the identification of an RNA polymerase I promoter. Cell. 1982 Oct;30(3):835–842. doi: 10.1016/0092-8674(82)90288-4. [DOI] [PubMed] [Google Scholar]
  28. Niles E. G., Sutiphong J., Haque S. Structure of the Tetrahymena pyriformis rRNA gene. Nucleotide sequence of the transcription initiation region. J Biol Chem. 1981 Dec 25;256(24):12849–12856. [PubMed] [Google Scholar]
  29. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  30. Rubtsov P. M., Musakhanov M. M., Zakharyev V. M., Krayev A. S., Skryabin K. G., Bayev A. A. The structure of the yeast ribosomal RNA genes. I. The complete nucleotide sequence of the 18S ribosomal RNA gene from Saccharomyces cerevisiae. Nucleic Acids Res. 1980 Dec 11;8(23):5779–5794. doi: 10.1093/nar/8.23.5779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Saiga H., Mizumoto K., Matsui T., Higashinakagawa T. Determination of the transcription initiation site of Tetrahymena pyriformis rDNA using in vitro capping of 35S pre-rRNA. Nucleic Acids Res. 1982 Jul 24;10(14):4223–4236. doi: 10.1093/nar/10.14.4223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sollner-Webb B., Reeder R. H. The nucleotide sequence of the initiation and termination sites for ribosomal RNA transcription in X. laevis. Cell. 1979 Oct;18(2):485–499. doi: 10.1016/0092-8674(79)90066-7. [DOI] [PubMed] [Google Scholar]
  33. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  34. Verbeet M. P., Klootwijk J., van Heerikhuizen H., Fontijn R., Vreugdenhil E., Planta R. J. Molecular cloning of the rDNA of Saccharomyces rosei and comparison of its transcription initiation region with that of Saccharomyces carlsbergensis. Gene. 1983 Jul;23(1):53–63. doi: 10.1016/0378-1119(83)90216-0. [DOI] [PubMed] [Google Scholar]

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