Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1981 Jul 24;9(14):3531–3543. doi: 10.1093/nar/9.14.3531

Replication of the extrachromosomal ribosomal RNA genes of Tetrahymena thermophilia.

T R Cech, S L Brehm
PMCID: PMC327369  PMID: 7279667

Abstract

Cultures of Tetrahymena thermophila were deprived of nutrients and later refed with enriched medium to obtain partial synchrony of DNA replication. Preferential replication of the extrachromosomal, macronuclear ribosomal RNA genes (rDNA) was found to occur at 40-80 min after refeeding. The rDNA accounted for one half of the label incorporated into cellular DNA during this period. Electron microscopy of the purified rDNA showed 1% replicative intermediates. Their structure was that expected for bidirectional replication of the linear rDNA from an origin or origins located in the central nontranscribed region of the palindromic molecule. Similar forms had previously been observed for the rDNA of a related species, Tetrahymena pyriformis. The electron microscopic data was consistent with an origin of replication located approximatley 600 base pairs from the center of the rDNA of T. thermophila, in contrast to a more central location in the rDNA of T. pyriformis. One implication of an off-center origin of replication is that there are two such sequences per palindromic molecule.

Full text

PDF
3533

Images in this article

Selected References

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

  1. Blackburn E. H., Chiou S. S. Non-nucleosomal packaging of a tandemly repeated DNA sequence at termini of extrachromosomal DNA coding for rRNA in Tetrahymena. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2263–2267. doi: 10.1073/pnas.78.4.2263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Blackburn E. H., Gall J. G. A tandemly repeated sequence at the termini of the extrachromosomal ribosomal RNA genes in Tetrahymena. J Mol Biol. 1978 Mar 25;120(1):33–53. doi: 10.1016/0022-2836(78)90294-2. [DOI] [PubMed] [Google Scholar]
  3. Blumenthal A. B., Kriegstein H. J., Hogness D. S. The units of DNA replication in Drosophila melanogaster chromosomes. Cold Spring Harb Symp Quant Biol. 1974;38:205–223. doi: 10.1101/sqb.1974.038.01.024. [DOI] [PubMed] [Google Scholar]
  4. Cech T. R., Rio D. C. Localization of transcribed regions on extrachromosomal ribosomal RNA genes of Tetrahymena thermophila by R-loop mapping. Proc Natl Acad Sci U S A. 1979 Oct;76(10):5051–5055. doi: 10.1073/pnas.76.10.5051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Charret R. L'ADN nucléolaire chez Tetrahymena pyriformis: chronoloe de sa réplication. Exp Cell Res. 1969 Mar;54(3):353–361. doi: 10.1016/0014-4827(69)90214-6. [DOI] [PubMed] [Google Scholar]
  6. Crawford L. V., Robbins A. K., Nicklin P. M. Location of the origin and terminus of replication in polyoma virus DNA. J Gen Virol. 1974 Oct;25(1):133–142. doi: 10.1099/0022-1317-25-1-133. [DOI] [PubMed] [Google Scholar]
  7. Din N., Engberg J. Extrachromosomal ribosomal RNA genes in Tetrahymena: structure and evolution. J Mol Biol. 1979 Nov 5;134(3):555–574. doi: 10.1016/0022-2836(79)90367-x. [DOI] [PubMed] [Google Scholar]
  8. Eckert W. A., Kaffenberger W., Krohne G., Franke W. W. Introduction of hidden breaks during rRNA maturation and ageing in Tetrahymena pyriformis. Eur J Biochem. 1978 Jul 3;87(3):607–616. doi: 10.1111/j.1432-1033.1978.tb12413.x. [DOI] [PubMed] [Google Scholar]
  9. Engberg J., Andersson P., Leick V., Collins J. Free ribosomal DNA molecules from Tetrahymena pyriformis GL are giant palindromes. J Mol Biol. 1976 Jun 25;104(2):455–470. doi: 10.1016/0022-2836(76)90281-3. [DOI] [PubMed] [Google Scholar]
  10. Engberg J., Nasir-ud-Din, Eckert W. A., Kaffenberger W., Pearlman R. E. Detailed transcription map of the extrachromosomal ribosomal RNA genes in Tetrahymena thermophila. J Mol Biol. 1980 Sep 25;142(3):289–313. doi: 10.1016/0022-2836(80)90274-0. [DOI] [PubMed] [Google Scholar]
  11. Fareed G. C., Garon G. F., Salzman N. P. Origin and direction of simian virus 40 deoxyribonucleic acid replication. J Virol. 1972 Sep;10(3):484–491. doi: 10.1128/jvi.10.3.484-491.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gocke E., Leer J. C., Nielsen O. F., Westergaard O. Transcriptional properties of nucleoli isolated from Tetrahymena. Nucleic Acids Res. 1978 Nov;5(11):3993–4006. doi: 10.1093/nar/5.11.3993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Grabowski P. J., Zaug A. J., Cech T. R. The intervening sequence of the ribosomal RNA precursor is converted to a circular RNA in isolated nuclei of Tetrahymena. Cell. 1981 Feb;23(2):467–476. doi: 10.1016/0092-8674(81)90142-2. [DOI] [PubMed] [Google Scholar]
  14. Hallberg R. L., Bruns P. J. Ribosome biosynthesis in Tetrahymena pyriformis. Regulation in response to nutritional changes. J Cell Biol. 1976 Nov;71(2):383–394. doi: 10.1083/jcb.71.2.383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kaffenberger W., Eckert W. A. Regulation of rRNA metabolism in Tetrahymena pyriformis. II. Nutritional shift-up. Eur J Cell Biol. 1980 Jun;21(2):200–207. [PubMed] [Google Scholar]
  16. Karrer K. M., Gall J. G. The macronuclear ribosomal DNA of Tetrahymena pyriformis is a palindrome. J Mol Biol. 1976 Jun 25;104(2):421–453. doi: 10.1016/0022-2836(76)90280-1. [DOI] [PubMed] [Google Scholar]
  17. Mathis D. J., Gorovsky M. A. Subunit structure of rDNA-containing chromatin. Biochemistry. 1976 Feb 24;15(4):750–755. doi: 10.1021/bi00649a005. [DOI] [PubMed] [Google Scholar]
  18. Niles E. G., Jain R. K. Physical map of the ribosomal ribonucleic acid gene from Tetrahymena pyriformis. Biochemistry. 1981 Feb 17;20(4):905–909. doi: 10.1021/bi00507a039. [DOI] [PubMed] [Google Scholar]
  19. Pan W. C., Blackburn E. H. Single extrachromosomal ribosomal RNA gene copies are synthesized during amplification of the rDNA in Tetrahymena. Cell. 1981 Feb;23(2):459–466. doi: 10.1016/0092-8674(81)90141-0. [DOI] [PubMed] [Google Scholar]
  20. Schnös M., Inman R. B. Position of branch points in replicating lambda DNA. J Mol Biol. 1970 Jul 14;51(1):61–73. doi: 10.1016/0022-2836(70)90270-6. [DOI] [PubMed] [Google Scholar]
  21. Sutton C. A., Hallberg R. L. Ribosome biosynthesis in Tetrahymena thermophila. III. Regulation of ribosomal RNA degradation in growing and growth arrested cells. J Cell Physiol. 1979 Nov;101(2):349–358. doi: 10.1002/jcp.1041010214. [DOI] [PubMed] [Google Scholar]
  22. Sutton C. A., Sylvan P., Hallberg R. L. Ribosome biosynthesis in Tetrahymena thermophila. IV. Regulation of ribosomal RNA synthesis in growing and growth arrested cells. J Cell Physiol. 1979 Dec;101(3):503–513. doi: 10.1002/jcp.1041010316. [DOI] [PubMed] [Google Scholar]
  23. Truett M. A., Gall J. G. The replication of ribosomal DNA in the macronucleus of Tetrahymena. Chromosoma. 1977 Dec 6;64(4):295–303. doi: 10.1007/BF00294937. [DOI] [PubMed] [Google Scholar]
  24. Vogt V. M., Braun R. The replication of ribosomal DNA in Physarum polycephalum. Eur J Biochem. 1977 Nov 1;80(2):557–566. doi: 10.1111/j.1432-1033.1977.tb11912.x. [DOI] [PubMed] [Google Scholar]
  25. Wild M. A., Gall J. G. An intervening sequence in the gene coding for 25S ribosomal RNA of Tetrahymena pigmentosa. Cell. 1979 Mar;16(3):565–573. doi: 10.1016/0092-8674(79)90030-8. [DOI] [PubMed] [Google Scholar]
  26. Yao M. C., Blackburn E., Gall J. G. Amplification of the rRNA genes in Tetrahymena. Cold Spring Harb Symp Quant Biol. 1979;43(Pt 2):1293–1296. doi: 10.1101/sqb.1979.043.01.147. [DOI] [PubMed] [Google Scholar]

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

RESOURCES