Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1988 Jan;8(1):251–258. doi: 10.1128/mcb.8.1.251

Developmentally controlled telomere addition in wild-type and mutant paramecia.

J D Forney 1, E H Blackburn 1
PMCID: PMC363111  PMID: 3336360

Abstract

We analyzed sites of macronuclear telomere addition at a single genetic locus in Paramecium tetraurelia. We showed that in homozygous wild-type cells, differential genomic processing during macronuclear development resulted in the A surface antigen gene being located 8, 13, or 26 kilobases upstream from a macronuclear telomere. We describe variable rearrangements that occurred at the telomere 8 kilobases from the A gene. A mutant (d48) that forms a telomere near the 5' end of the A gene was also analyzed. This mutant was shown to create simple terminal deletions; telomeric repeats were added directly to the truncated wild-type A gene sequence. In both the mutant and wild-type cells, the telomeric sequences (a mixture of C4A2 and C3A3 repeats) were added to various sequences within a specific 200- to 500-base-pair region rather than to a single site. No similarities were found in the primary sequences surrounding the telomere addition sites. The mutation in d48 changed the region of telomere addition at the A gene locus; this is the first example in ciliates of a mutation that affects the site of telomere addition.

Full text

PDF
257

Images in this article

Selected References

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

  1. Altschuler M. I., Yao M. C. Macronuclear DNA of Tetrahymena thermophila exists as defined subchromosomal-sized molecules. Nucleic Acids Res. 1985 Aug 26;13(16):5817–5831. doi: 10.1093/nar/13.16.5817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Austerberry C. F., Yao M. C. Nucleotide sequence structure and consistency of a developmentally regulated DNA deletion in Tetrahymena thermophila. Mol Cell Biol. 1987 Jan;7(1):435–443. doi: 10.1128/mcb.7.1.435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baroin A., Prat A., Caron F. Telomeric site position heterogeneity in macronuclear DNA of Paramecium primaurelia. Nucleic Acids Res. 1987 Feb 25;15(4):1717–1728. doi: 10.1093/nar/15.4.1717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Blackburn E. H., Karrer K. M. Genomic reorganization in ciliated protozoans. Annu Rev Genet. 1986;20:501–521. doi: 10.1146/annurev.ge.20.120186.002441. [DOI] [PubMed] [Google Scholar]
  6. Borst P. Discontinuous transcription and antigenic variation in trypanosomes. Annu Rev Biochem. 1986;55:701–732. doi: 10.1146/annurev.bi.55.070186.003413. [DOI] [PubMed] [Google Scholar]
  7. Conover R. K., Brunk C. F. Macronuclear DNA molecules of Tetrahymena thermophila. Mol Cell Biol. 1986 Mar;6(3):900–905. doi: 10.1128/mcb.6.3.900. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Epstein L. M., Forney J. D. Mendelian and non-mendelian mutations affecting surface antigen expression in Paramecium tetraurelia. Mol Cell Biol. 1984 Aug;4(8):1583–1590. doi: 10.1128/mcb.4.8.1583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Forney J. D., Epstein L. M., Preer L. B., Rudman B. M., Widmayer D. J., Klein W. H., Preer J. R., Jr Structure and expression of genes for surface proteins in Paramecium. Mol Cell Biol. 1983 Mar;3(3):466–474. doi: 10.1128/mcb.3.3.466. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Godiska R. Structure and sequence of the H surface protein gene of Paramecium and comparison with related genes. Mol Gen Genet. 1987 Jul;208(3):529–536. doi: 10.1007/BF00328151. [DOI] [PubMed] [Google Scholar]
  11. Greider C. W., Blackburn E. H. Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell. 1985 Dec;43(2 Pt 1):405–413. doi: 10.1016/0092-8674(85)90170-9. [DOI] [PubMed] [Google Scholar]
  12. Harumoto T. Induced change in a non-mendelian determinant by transplantation of macronucleoplasm in Paramecium tetraurelia. Mol Cell Biol. 1986 Oct;6(10):3498–3501. doi: 10.1128/mcb.6.10.3498. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Herrick G., Hunter D., Williams K., Kotter K. Alternative processing during development of a macronuclear chromosome family in Oxytricha fallax. Genes Dev. 1987 Dec;1(10):1047–1058. doi: 10.1101/gad.1.10.1047. [DOI] [PubMed] [Google Scholar]
  14. Howard E. A., Blackburn E. H. Reproducible and variable genomic rearrangements occur in the developing somatic nucleus of the ciliate Tetrahymena thermophila. Mol Cell Biol. 1985 Aug;5(8):2039–2050. doi: 10.1128/mcb.5.8.2039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Katzen A. L., Cann G. M., Blackburn E. H. Sequence-specific fragmentation of macronuclear DNA in a holotrichous ciliate. Cell. 1981 May;24(2):313–320. doi: 10.1016/0092-8674(81)90321-4. [DOI] [PubMed] [Google Scholar]
  16. Klobutcher L. A., Jahn C. L., Prescott D. M. Internal sequences are eliminated from genes during macronuclear development in the ciliated protozoan Oxytricha nova. Cell. 1984 Apr;36(4):1045–1055. doi: 10.1016/0092-8674(84)90054-0. [DOI] [PubMed] [Google Scholar]
  17. Klobutcher L. A., Swanton M. T., Donini P., Prescott D. M. All gene-sized DNA molecules in four species of hypotrichs have the same terminal sequence and an unusual 3' terminus. Proc Natl Acad Sci U S A. 1981 May;78(5):3015–3019. doi: 10.1073/pnas.78.5.3015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Maniatis T., Jeffrey A., Kleid D. G. Nucleotide sequence of the rightward operator of phage lambda. Proc Natl Acad Sci U S A. 1975 Mar;72(3):1184–1188. doi: 10.1073/pnas.72.3.1184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Meyer E., Caron F., Baroin A. Macronuclear structure of the G surface antigen gene of Paramecium primaurelia and direct expression of its repeated epitopes in Escherichia coli. Mol Cell Biol. 1985 Sep;5(9):2414–2422. doi: 10.1128/mcb.5.9.2414. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Preer J. R., Jr, Preer L. B., Rudman B. M., Barnett A. J. Deviation from the universal code shown by the gene for surface protein 51A in Paramecium. Nature. 1985 Mar 14;314(6007):188–190. doi: 10.1038/314188a0. [DOI] [PubMed] [Google Scholar]
  21. Ribas-Aparicio R. M., Sparkowski J. J., Proulx A. E., Mitchell J. D., Klobutcher L. A. Nucleic acid splicing events occur frequently during macronuclear development in the protozoan Oxytricha nova and involve the elimination of unique DNA. Genes Dev. 1987 Jun;1(4):323–336. doi: 10.1101/gad.1.4.323. [DOI] [PubMed] [Google Scholar]
  22. Soldo A. T., Godoy G. A. The kinetic complexity of Paramecium macronuclear deoxyribonucleic acid. J Protozool. 1972 Nov;19(4):673–678. doi: 10.1111/j.1550-7408.1972.tb03558.x. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Yao M. C., Choi J., Yokoyama S., Austerberry C. F., Yao C. H. DNA elimination in Tetrahymena: a developmental process involving extensive breakage and rejoining of DNA at defined sites. Cell. 1984 Feb;36(2):433–440. doi: 10.1016/0092-8674(84)90236-8. [DOI] [PubMed] [Google Scholar]
  25. Yao M. C., Yao C. H. Repeated hexanucleotide C-C-C-C-A-A is present near free ends of macronuclear DNA of Tetrahymena. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7436–7439. doi: 10.1073/pnas.78.12.7436. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Yao M. C., Zheng K., Yao C. H. A conserved nucleotide sequence at the sites of developmentally regulated chromosomal breakage in Tetrahymena. Cell. 1987 Mar 13;48(5):779–788. doi: 10.1016/0092-8674(87)90075-4. [DOI] [PubMed] [Google Scholar]
  27. Yao M. C., Zhu S. G., Yao C. H. Gene amplification in Tetrahymena thermophila: formation of extrachromosomal palindromic genes coding for rRNA. Mol Cell Biol. 1985 Jun;5(6):1260–1267. doi: 10.1128/mcb.5.6.1260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Yokoyama R., Yao M. C. Sequence characterization of Tetrahymena macronuclear DNA ends. Nucleic Acids Res. 1986 Mar 11;14(5):2109–2122. doi: 10.1093/nar/14.5.2109. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES