Skip to main content
PMC home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1986 Mar 11;14(5):2345–2364. doi: 10.1093/nar/14.5.2345

The rDNA of C. elegans: sequence and structure.

R E Ellis, J E Sulston, A R Coulson
PMCID: PMC339662  PMID: 3960722

Abstract

We have sequenced one complete rDNA tandem repeat from the nematode C. elegans. By comparative analysis we derive secondary structures for the 18s, 5.8s, and 26s rRNA molecules, and comment on other important features of the sequence. We also present the sequence of a junction between the rDNA and non-ribosomal DNA. Finally, we use our data to quantify the evolutionary relationships among several organisms currently studied in developmental biology.

Full text

PDF
2345

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Albertson D. G. Localization of the ribosomal genes in Caenorhabditis elegans chromosomes by in situ hybridization using biotin-labeled probes. EMBO J. 1984 Jun;3(6):1227–1234. doi: 10.1002/j.1460-2075.1984.tb01957.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anderson P., Brenner S. A selection for myosin heavy chain mutants in the nematode Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4470–4474. doi: 10.1073/pnas.81.14.4470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Atmadja J., Brimacombe R., Maden B. E. Xenopus laevis 18S ribosomal RNA: experimental determination of secondary structural elements, and locations of methyl groups in the secondary structure model. Nucleic Acids Res. 1984 Mar 26;12(6):2649–2667. doi: 10.1093/nar/12.6.2649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Bach R., Grummt I., Allet B. The nucleotide sequence of the initiation region of the ribosomal transcription unit from mouse. Nucleic Acids Res. 1981 Apr 10;9(7):1559–1569. doi: 10.1093/nar/9.7.1559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Biggin M. D., Gibson T. J., Hong G. F. Buffer gradient gels and 35S label as an aid to rapid DNA sequence determination. Proc Natl Acad Sci U S A. 1983 Jul;80(13):3963–3965. doi: 10.1073/pnas.80.13.3963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Blum B., Seebeck T., Braun R., Ferris P., Vogt V. Localization and DNA sequence around the initiation site of ribosomal RNA transcription in Physarum polycephalum. Nucleic Acids Res. 1983 Dec 10;11(23):8519–8533. doi: 10.1093/nar/11.23.8519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Clark C. G., Tague B. W., Ware V. C., Gerbi S. A. Xenopus laevis 28S ribosomal RNA: a secondary structure model and its evolutionary and functional implications. Nucleic Acids Res. 1984 Aug 10;12(15):6197–6220. doi: 10.1093/nar/12.15.6197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Deininger P. L. Random subcloning of sonicated DNA: application to shotgun DNA sequence analysis. Anal Biochem. 1983 Feb 15;129(1):216–223. doi: 10.1016/0003-2697(83)90072-6. [DOI] [PubMed] [Google Scholar]
  11. Engberg J., Din N., Saiga H., Higashinakagawa T. Nucleotide sequence of the 5'-terminal coding region for pre-rRNA and mature 17S rRNA in Tetrahymena thermophila rDNA. Nucleic Acids Res. 1984 Jan 25;12(2):959–972. doi: 10.1093/nar/12.2.959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Files J. G., Hirsh D. Ribosomal DNA of Caenorhabditis elegans. J Mol Biol. 1981 Jun 25;149(2):223–240. doi: 10.1016/0022-2836(81)90299-0. [DOI] [PubMed] [Google Scholar]
  13. Hadjiolov A. A., Georgiev O. I., Nosikov V. V., Yavachev L. P. Primary and secondary structure of rat 28 S ribosomal RNA. Nucleic Acids Res. 1984 Apr 25;12(8):3677–3693. doi: 10.1093/nar/12.8.3677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Harrington C. A., Chikaraishi D. M. Identification and sequence of the initiation site for rat 45S ribosomal RNA synthesis. Nucleic Acids Res. 1983 May 25;11(10):3317–3332. doi: 10.1093/nar/11.10.3317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hassouna N., Michot B., Bachellerie J. P. The complete nucleotide sequence of mouse 28S rRNA gene. Implications for the process of size increase of the large subunit rRNA in higher eukaryotes. Nucleic Acids Res. 1984 Apr 25;12(8):3563–3583. doi: 10.1093/nar/12.8.3563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Helms C., Graham M. Y., Dutchik J. E., Olson M. V. A new method for purifying lambda DNA from phage lysates. DNA. 1985 Feb;4(1):39–49. doi: 10.1089/dna.1985.4.39. [DOI] [PubMed] [Google Scholar]
  17. Hindenach B. R., Stafford D. W. Nucleotide sequence of the 18S-26S rRNA intergene region of the sea urchin. Nucleic Acids Res. 1984 Feb 10;12(3):1737–1747. doi: 10.1093/nar/12.3.1737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hogan J. J., Gutell R. R., Noller H. F. Probing the conformation of 18S rRNA in yeast 40S ribosomal subunits with kethoxal. Biochemistry. 1984 Jul 3;23(14):3322–3330. doi: 10.1021/bi00309a032. [DOI] [PubMed] [Google Scholar]
  19. Hong G. F. A method for sequencing single-stranded cloned DNA in both directions. Biosci Rep. 1981 Mar;1(3):243–252. doi: 10.1007/BF01114911. [DOI] [PubMed] [Google Scholar]
  20. Karn J., Brenner S., Barnett L., Cesareni G. Novel bacteriophage lambda cloning vector. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5172–5176. doi: 10.1073/pnas.77.9.5172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Karn J., Brenner S., Barnett L. New bacteriophage lambda vectors with positive selection for cloned inserts. Methods Enzymol. 1983;101:3–19. doi: 10.1016/0076-6879(83)01004-6. [DOI] [PubMed] [Google Scholar]
  22. Karn J., Matthes H. W., Gait M. J., Brenner S. A new selective phage cloning vector, lambda 2001, with sites for XbaI, BamHI, HindIII, EcoRI, SstI and XhoI. Gene. 1984 Dec;32(1-2):217–224. doi: 10.1016/0378-1119(84)90049-0. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Kunkel G. R., Martinson H. G. Nucleosomes will not form on double-stranded RNa or over poly(dA).poly(dT) tracts in recombinant DNA. Nucleic Acids Res. 1981 Dec 21;9(24):6869–6888. doi: 10.1093/nar/9.24.6869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Mankin A. S., Kopylov A. M., Bogdanov A. A. Modification of 18 S rRNA in the 40 S ribosomal subunit of yeast with dimethyl sulfate. FEBS Lett. 1981 Nov 2;134(1):11–14. doi: 10.1016/0014-5793(81)80539-x. [DOI] [PubMed] [Google Scholar]
  27. Messing J. New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. doi: 10.1016/0076-6879(83)01005-8. [DOI] [PubMed] [Google Scholar]
  28. Messing J., Vieira J. A new pair of M13 vectors for selecting either DNA strand of double-digest restriction fragments. Gene. 1982 Oct;19(3):269–276. doi: 10.1016/0378-1119(82)90016-6. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. 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]
  31. Michot B., Hassouna N., Bachellerie J. P. Secondary structure of mouse 28S rRNA and general model for the folding of the large rRNA in eukaryotes. Nucleic Acids Res. 1984 May 25;12(10):4259–4279. doi: 10.1093/nar/12.10.4259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. Nelles L., Fang B. L., Volckaert G., Vandenberghe A., De Wachter R. Nucleotide sequence of a crustacean 18S ribosomal RNA gene and secondary structure of eukaryotic small subunit ribosomal RNAs. Nucleic Acids Res. 1984 Dec 11;12(23):8749–8768. doi: 10.1093/nar/12.23.8749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Olsen G. J., McCarroll R., Sogin M. L. Secondary structure of the Dictyostelium discoideum small subunit ribosomal RNA. Nucleic Acids Res. 1983 Nov 25;11(22):8037–8049. doi: 10.1093/nar/11.22.8037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. 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]
  36. Petes T. D. Unequal meiotic recombination within tandem arrays of yeast ribosomal DNA genes. Cell. 1980 Mar;19(3):765–774. doi: 10.1016/s0092-8674(80)80052-3. [DOI] [PubMed] [Google Scholar]
  37. Prunell A. Nucleosome reconstitution on plasmid-inserted poly(dA) . poly(dT). EMBO J. 1982;1(2):173–179. doi: 10.1002/j.1460-2075.1982.tb01143.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Reddy R., Rothblum L. I., Subrahmanyam C. S., Liu M. H., Henning D., Cassidy B., Busch H. The nucleotide sequence of 8 S RNA bound to preribosomal RNA of Novikoff hepatoma. The 5'-end of 8 S RNA is 5.8 S RNA. J Biol Chem. 1983 Jan 10;258(1):584–589. [PubMed] [Google Scholar]
  39. Sanger F., Coulson A. R., Barrell B. G., Smith A. J., Roe B. A. Cloning in single-stranded bacteriophage as an aid to rapid DNA sequencing. J Mol Biol. 1980 Oct 25;143(2):161–178. doi: 10.1016/0022-2836(80)90196-5. [DOI] [PubMed] [Google Scholar]
  40. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. 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]
  42. Smith G. P. Evolution of repeated DNA sequences by unequal crossover. Science. 1976 Feb 13;191(4227):528–535. doi: 10.1126/science.1251186. [DOI] [PubMed] [Google Scholar]
  43. 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]
  44. Staden R. Automation of the computer handling of gel reading data produced by the shotgun method of DNA sequencing. Nucleic Acids Res. 1982 Aug 11;10(15):4731–4751. doi: 10.1093/nar/10.15.4731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Staden R. Graphic methods to determine the function of nucleic acid sequences. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 2):521–538. doi: 10.1093/nar/12.1part2.521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Sulston J. E., Brenner S. The DNA of Caenorhabditis elegans. Genetics. 1974 May;77(1):95–104. doi: 10.1093/genetics/77.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Szostak J. W., Wu R. Insertion of a genetic marker into the ribosomal DNA of yeast. Plasmid. 1979 Oct;2(4):536–554. doi: 10.1016/0147-619x(79)90053-2. [DOI] [PubMed] [Google Scholar]
  48. Szostak J. W., Wu R. Unequal crossing over in the ribosomal DNA of Saccharomyces cerevisiae. Nature. 1980 Apr 3;284(5755):426–430. doi: 10.1038/284426a0. [DOI] [PubMed] [Google Scholar]
  49. Ursi D., Vandenberghe A., De Wachter R. Nucleotide sequences of the 5.8S rRNAs of a mollusc and a porifer, and considerations regarding the secondary structure of 5.8S rRNA and its interaction with 28S rRNA. Nucleic Acids Res. 1983 Nov 25;11(22):8111–8120. doi: 10.1093/nar/11.22.8111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Ursi D., Vandenberghe A., De Wachter R. The sequence of the 5.8 S ribosomal RNA of the crustacean Artemia salina. With a proposal for a general secondary structure model for 5.8 S ribosomal RNA. Nucleic Acids Res. 1982 Jun 11;10(11):3517–3530. doi: 10.1093/nar/10.11.3517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Vaughn J. C., Sperbeck S. J., Ramsey W. J., Lawrence C. B. A universal model for the secondary structure of 5.8S ribosomal RNA molecules, their contact sites with 28S ribosomal RNAs, and their prokaryotic equivalent. Nucleic Acids Res. 1984 Oct 11;12(19):7479–7502. doi: 10.1093/nar/12.19.7479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. 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]
  53. 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]
  54. Walker T. A., Johnson K. D., Olsen G. J., Peters M. A., Pace N. R. Enzymatic and chemical structure mapping of mouse 28S ribosomal ribonucleic acid contacts in 5.8S ribosomal ribonucleic acid. Biochemistry. 1982 May 11;21(10):2320–2329. doi: 10.1021/bi00539a008. [DOI] [PubMed] [Google Scholar]
  55. 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]
  56. Winter G., Fields S. Cloning of influenza cDNA ino M13: the sequence of the RNA segment encoding the A/PR/8/34 matrix protein. Nucleic Acids Res. 1980 May 10;8(9):1965–1974. doi: 10.1093/nar/8.9.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES