Abstract
We have determined the complete nucleotide sequence (4712 nucleotides) of the mouse 28S rRNA gene. Comparison with all other homologs indicates that the potential for major variations in size during the evolution has been restricted to a unique set of a few sites within a largely conserved secondary structure core. The D (divergent) domains, responsible for the large increase in size of the molecule from procaryotes to higher eukaryotes, represent half the mouse 28S rRNA length. They show a clear potential to form self-contained secondary structures. Their high GC content in vertebrates is correlated with the folding of very long stable stems. Their comparison with the two other vertebrates, xenopus and rat, reveals an history of repeated insertions and deletions. During the evolution of vertebrates, insertion or deletion of new sequence tracts preferentially takes place in the subareas of D domains where the more recently fixed insertions/deletions were located in the ancestor sequence. These D domains appear closely related to the transcribed spacers of rRNA precursor but a sizable fraction displays a much slower rate of sequence variation.
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- Branlant C., Krol A., Machatt M. A., Pouyet J., Ebel J. P., Edwards K., Kössel H. Primary and secondary structures of Escherichia coli MRE 600 23S ribosomal RNA. Comparison with models of secondary structure for maize chloroplast 23S rRNA and for large portions of mouse and human 16S mitochondrial rRNAs. Nucleic Acids Res. 1981 Sep 11;9(17):4303–4324. doi: 10.1093/nar/9.17.4303. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brosius J., Dull T. J., Noller H. F. Complete nucleotide sequence of a 23S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci U S A. 1980 Jan;77(1):201–204. doi: 10.1073/pnas.77.1.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chan Y. L., Olvera J., Wool I. G. The structure of rat 28S ribosomal ribonucleic acid inferred from the sequence of nucleotides in a gene. Nucleic Acids Res. 1983 Nov 25;11(22):7819–7831. doi: 10.1093/nar/11.22.7819. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Edwards K., Kössel H. The rRNA operon from Zea mays chloroplasts: nucleotide sequence of 23S rDNA and its homology with E.coli 23S rDNA. Nucleic Acids Res. 1981 Jun 25;9(12):2853–2869. doi: 10.1093/nar/9.12.2853. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Efstratiadis A., Posakony J. W., Maniatis T., Lawn R. M., O'Connell C., Spritz R. A., DeRiel J. K., Forget B. G., Weissman S. M., Slightom J. L. The structure and evolution of the human beta-globin gene family. Cell. 1980 Oct;21(3):653–668. doi: 10.1016/0092-8674(80)90429-8. [DOI] [PubMed] [Google Scholar]
- Furlong J. C., Forbes J., Robertson M., Maden B. E. The external transcribed spacer and preceding region of Xenopus borealis rDNA: comparison with the corresponding region of Xenopus laevis rDNA. Nucleic Acids Res. 1983 Dec 10;11(23):8183–8196. doi: 10.1093/nar/11.23.8183. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Furlong J. C., Maden B. E. Patterns of major divergence between the internal transcribed spacers of ribosomal DNA in Xenopus borealis and Xenopus laevis, and of minimal divergence within ribosomal coding regions. EMBO J. 1983;2(3):443–448. doi: 10.1002/j.1460-2075.1983.tb01442.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Georgiev O. I., Nikolaev N., Hadjiolov A. A., Skryabin K. G., Zakharyev V. M., Bayev A. A. The structure of the yeast ribosomal RNA genes. 4. Complete sequence of the 25 S rRNA gene from Saccharomyces cerevisae. Nucleic Acids Res. 1981 Dec 21;9(24):6953–6958. doi: 10.1093/nar/9.24.6953. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Glotz C., Zwieb C., Brimacombe R., Edwards K., Kössel H. Secondary structure of the large subunit ribosomal RNA from Escherichia coli, Zea mays chloroplast, and human and mouse mitochondrial ribosomes. Nucleic Acids Res. 1981 Jul 24;9(14):3287–3306. doi: 10.1093/nar/9.14.3287. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goebel W., Bonewald R. Class of small multicopy plasmids originating from the mutant antibiotic resistance factor R1 drd-19B2. J Bacteriol. 1975 Aug;123(2):658–665. doi: 10.1128/jb.123.2.658-665.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gourse R. L., Thurlow D. L., Gerbi S. A., Zimmermann R. A. Specific binding of a prokaryotic ribosomal protein to a eukaryotic ribosomal RNA: implications for evolution and autoregulation. Proc Natl Acad Sci U S A. 1981 May;78(5):2722–2726. doi: 10.1073/pnas.78.5.2722. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hall L. M., Maden B. E. Nucleotide sequence through the 18S-28S intergene region of a vertebrate ribosomal transcription unit. Nucleic Acids Res. 1980 Dec 20;8(24):5993–6005. doi: 10.1093/nar/8.24.5993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kominami R., Mishima Y., Urano Y., Sakai M., Muramatsu M. Cloning and determination of the transcription termination site of ribosomal RNA gene of the mouse. Nucleic Acids Res. 1982 Mar 25;10(6):1963–1979. doi: 10.1093/nar/10.6.1963. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kumano M., Tomioka N., Sugiura M. The complete nucleotide sequence of a 23S rRNA gene from a blue-green alga, Anacystis nidulans. Gene. 1983 Oct;24(2-3):219–225. doi: 10.1016/0378-1119(83)90082-3. [DOI] [PubMed] [Google Scholar]
- Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
- Michel F., Jacquier A., Dujon B. Comparison of fungal mitochondrial introns reveals extensive homologies in RNA secondary structure. Biochimie. 1982 Oct;64(10):867–881. doi: 10.1016/s0300-9084(82)80349-0. [DOI] [PubMed] [Google Scholar]
- Michot B., Bachellerie J. P., Raynal F. Sequence and secondary structure of mouse 28S rRNA 5'terminal domain. Organisation of the 5.8S-28S rRNA complex. Nucleic Acids Res. 1982 Sep 11;10(17):5273–5283. doi: 10.1093/nar/10.17.5273. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Michot B., Bachellerie J. P., Raynal F. Structure of mouse rRNA precursors. Complete sequence and potential folding of the spacer regions between 18S and 28S rRNA. Nucleic Acids Res. 1983 May 25;11(10):3375–3391. doi: 10.1093/nar/11.10.3375. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Noller H. F., Kop J., Wheaton V., Brosius J., Gutell R. R., Kopylov A. M., Dohme F., Herr W., Stahl D. A., Gupta R. Secondary structure model for 23S ribosomal RNA. Nucleic Acids Res. 1981 Nov 25;9(22):6167–6189. doi: 10.1093/nar/9.22.6167. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Otsuka T., Nomiyama H., Yoshida H., Kukita T., Kuhara S., Sakaki Y. Complete nucleotide sequence of the 26S rRNA gene of Physarum polycephalum: its significance in gene evolution. Proc Natl Acad Sci U S A. 1983 Jun;80(11):3163–3167. doi: 10.1073/pnas.80.11.3163. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rae P. M., Kohorn B. D., Wade R. P. The 10 kb Drosophila virilis 28S rDNA intervening sequence is flanked by a direct repeat of 14 base pairs of coding sequence. Nucleic Acids Res. 1980 Aug 25;8(16):3491–3504. doi: 10.1093/nar/8.16.3491. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roiha H., Glover D. M. Duplicated rDNA sequences of variable lengths flanking the short type I insertions in the rDNA of Drosophila melanogaster. Nucleic Acids Res. 1981 Nov 11;9(21):5521–5532. doi: 10.1093/nar/9.21.5521. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schibler U., Wyler T., Hagenbüchle O. Changes in size and secondary structure of the ribosomal transcription unit during vertebrate evolution. J Mol Biol. 1975 May 25;94(3):503–517. doi: 10.1016/0022-2836(75)90217-x. [DOI] [PubMed] [Google Scholar]
- Skriabin K. G., Kraev A. S., Rubtsov P. M., Baev A. A. Polnaia posledovatel'nost' nukleotidov speisernoi oblasti, raspolozhennoi mezhdu genami 18S i 5.8S RNK drozhzhei. Dokl Akad Nauk SSSR. 1979;247(3):761–765. [PubMed] [Google Scholar]
- Subrahmanyam C. S., Cassidy B., Busch H., Rothblum L. I. Nucleotide sequence of the region between the 18S rRNA sequence and the 28S rRNA sequence of rat ribosomal DNA. Nucleic Acids Res. 1982 Jun 25;10(12):3667–3680. doi: 10.1093/nar/10.12.3667. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Veldman G. M., Brand R. C., Klootwijk J., Planta R. Some characteristics of processing sites in ribosomal precursor RNA of yeast. Nucleic Acids Res. 1980 Jul 11;8(13):2907–2920. doi: 10.1093/nar/8.13.2907. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Veldman G. M., Klootwijk J., de Regt V. C., Planta R. J., Branlant C., Krol A., Ebel J. P. The primary and secondary structure of yeast 26S rRNA. Nucleic Acids Res. 1981 Dec 21;9(24):6935–6952. doi: 10.1093/nar/9.24.6935. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Veldman G. M., Klootwijk J., van Heerikhuizen H., Planta R. J. The nucleotide sequence of the intergenic region between the 5.8S and 26S rRNA genes of the yeast ribosomal RNA operon. Possible implications for the interaction between 5.8S and 26S rRNA and the processing of the primary transcript. Nucleic Acids Res. 1981 Oct 10;9(19):4847–4862. doi: 10.1093/nar/9.19.4847. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ware V. C., Tague B. W., Clark C. G., Gourse R. L., Brand R. C., Gerbi S. A. Sequence analysis of 28S ribosomal DNA from the amphibian Xenopus laevis. Nucleic Acids Res. 1983 Nov 25;11(22):7795–7817. doi: 10.1093/nar/11.22.7795. [DOI] [PMC free article] [PubMed] [Google Scholar]