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. 1997 Jun 15;25(12):2448–2454. doi: 10.1093/nar/25.12.2448

Deletion endpoint allele-specificity in the developmentally regulated elimination of an internal sequence (IES) in Paramecium.

K Dubrana 1, A Le Mouël 1, L Amar 1
PMCID: PMC146731  PMID: 9171098

Abstract

Ciliated protozoa undergo thousands of site-specific DNA deletion events during the programmed development of micronuclear genomes to macronuclear genomes. Two deletion elements, W1 and W2, were identified in the Paramecium primaurelia wild-type 156 strain. Here, we report the characterization of both elements in wild-type strain 168 and show that they display variant deletion patterns when compared with those of strain 156. The W1 ( 168 ) element is defective for deletion. The W2 ( 168 ) element is excised utilizing two alternative boundaries on one side, both are different from the boundary utilized to excise the W2156 element. By crossing the 156 and 168 strains, we demonstrate that the definition of all deletion endpoints are each controlled by cis -acting determinant(s) rather than by strain-specific trans-acting factor(s). Sequence comparison of all deleted DNA segments indicates that the 5'-TA-3'terminal sequence is strictly required at their ends. Furthermore the identity of the first eight base pairs of these ends to a previously established consensus sequence correlates with the frequency of the corresponding deletion events. Our data implies the existence of an adaptive convergent evolution of these Paramecium deleted DNA segment end sequences.

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Selected References

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

  1. Amar L. Chromosome End Formation and Internal Sequence Elimination as Alternative Genomic Rearrangements in the Ciliate Paramecium. J Mol Biol. 1997 Jan 31;265(4):465–465. doi: 10.1006/jmbi.1996.0792. [DOI] [PubMed] [Google Scholar]
  2. Amar L. Chromosome end formation and internal sequence elimination as alternative genomic rearrangements in the ciliate Paramecium. J Mol Biol. 1994 Feb 18;236(2):421–426. doi: 10.1006/jmbi.1994.1154. [DOI] [PubMed] [Google Scholar]
  3. Caron F. A high degree of macronuclear chromosome polymorphism is generated by variable DNA rearrangements in Paramecium primaurelia during macronuclear differentiation. J Mol Biol. 1992 Jun 5;225(3):661–678. doi: 10.1016/0022-2836(92)90393-x. [DOI] [PubMed] [Google Scholar]
  4. Chalker D. L., Yao M. C. Non-Mendelian, heritable blocks to DNA rearrangement are induced by loading the somatic nucleus of Tetrahymena thermophila with germ line-limited DNA. Mol Cell Biol. 1996 Jul;16(7):3658–3667. doi: 10.1128/mcb.16.7.3658. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chalmers R. M., Kleckner N. IS10/Tn10 transposition efficiently accommodates diverse transposon end configurations. EMBO J. 1996 Sep 16;15(18):5112–5122. [PMC free article] [PubMed] [Google Scholar]
  6. Duharcourt S., Butler A., Meyer E. Epigenetic self-regulation of developmental excision of an internal eliminated sequence on Paramecium tetraurelia. Genes Dev. 1995 Aug 15;9(16):2065–2077. doi: 10.1101/gad.9.16.2065. [DOI] [PubMed] [Google Scholar]
  7. Godiska R., James C., Yao M. C. A distant 10-bp sequence specifies the boundaries of a programmed DNA deletion in Tetrahymena. Genes Dev. 1993 Dec;7(12A):2357–2365. doi: 10.1101/gad.7.12a.2357. [DOI] [PubMed] [Google Scholar]
  8. Godiska R., Yao M. C. A programmed site-specific DNA rearrangement in Tetrahymena thermophila requires flanking polypurine tracts. Cell. 1990 Jun 29;61(7):1237–1246. doi: 10.1016/0092-8674(90)90688-b. [DOI] [PubMed] [Google Scholar]
  9. Keller A. M., Le Mouël A., Caron F., Katinka M., Meyer E. The differential expression of the G surface antigen alleles in Paramecium primaurelia heterozygous cells correlates to macronuclear DNA rearrangement. Dev Genet. 1992;13(4):306–317. doi: 10.1002/dvg.1020130408. [DOI] [PubMed] [Google Scholar]
  10. Klobutcher L. A., Herrick G. Consensus inverted terminal repeat sequence of Paramecium IESs: resemblance to termini of Tc1-related and Euplotes Tec transposons. Nucleic Acids Res. 1995 Jun 11;23(11):2006–2013. doi: 10.1093/nar/23.11.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Klobutcher L. A., Jahn C. L. Developmentally controlled genomic rearrangements in ciliated protozoa. Curr Opin Genet Dev. 1991 Oct;1(3):397–403. doi: 10.1016/s0959-437x(05)80306-5. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Meyer E. Induction of specific macronuclear developmental mutations by microinjection of a cloned telomeric gene in Paramecium primaurelia. Genes Dev. 1992 Feb;6(2):211–222. doi: 10.1101/gad.6.2.211. [DOI] [PubMed] [Google Scholar]
  14. Meyer E., Keller A. M. A Mendelian mutation affecting mating-type determination also affects developmental genomic rearrangements in Paramecium tetraurelia. Genetics. 1996 May;143(1):191–202. doi: 10.1093/genetics/143.1.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Prescott D. M. The DNA of ciliated protozoa. Microbiol Rev. 1994 Jun;58(2):233–267. doi: 10.1128/mr.58.2.233-267.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Saveliev S. V., Cox M. M. Developmentally programmed DNA deletion in Tetrahymena thermophila by a transposition-like reaction pathway. EMBO J. 1996 Jun 3;15(11):2858–2869. [PMC free article] [PubMed] [Google Scholar]
  17. Saveliev S. V., Cox M. M. The fate of deleted DNA produced during programmed genomic deletion events in Tetrahymena thermophila. Nucleic Acids Res. 1994 Dec 25;22(25):5695–5701. doi: 10.1093/nar/22.25.5695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Saveliev S. V., Cox M. M. Transient DNA breaks associated with programmed genomic deletion events in conjugating cells of Tetrahymena thermophila. Genes Dev. 1995 Jan 15;9(2):248–255. doi: 10.1101/gad.9.2.248. [DOI] [PubMed] [Google Scholar]
  19. Scott J., Leeck C., Forney J. Analysis of the micronuclear B type surface protein gene in Paramecium tetraurelia. Nucleic Acids Res. 1994 Nov 25;22(23):5079–5084. doi: 10.1093/nar/22.23.5079. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Steele C. J., Barkocy-Gallagher G. A., Preer L. B., Preer J. R., Jr Developmentally excised sequences in micronuclear DNA of Paramecium. Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2255–2259. doi: 10.1073/pnas.91.6.2255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Tsubota S. I., Huong D. V. Capture of flanking DNA by a P element in Drosophila melanogaster: creation of a transposable element. Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):693–697. doi: 10.1073/pnas.88.3.693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Vayssié L., Sperling L., Madeddu L. Characterization of multigene families in the micronuclear genome of Paramecium tetraurelia reveals a germline specific sequence in an intron of a centrin gene. Nucleic Acids Res. 1997 Mar 1;25(5):1036–1041. doi: 10.1093/nar/25.5.1036. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Wen J., Maercker C., Lipps H. J. Sequential excision of internal eliminated DNA sequences in the differentiating macronucleus of the hypotrichous ciliate Stylonychia lemnae. Nucleic Acids Res. 1996 Nov 15;24(22):4415–4419. doi: 10.1093/nar/24.22.4415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Yao M. C. Programmed DNA deletions in Tetrahymena: mechanisms and implications. Trends Genet. 1996 Jan;12(1):26–30. doi: 10.1016/0168-9525(96)81385-0. [DOI] [PubMed] [Google Scholar]
  26. Yao M. C., Yao C. H. Detection of circular excised DNA deletion elements in Tetrahymena thermophila during development. Nucleic Acids Res. 1994 Dec 25;22(25):5702–5708. doi: 10.1093/nar/22.25.5702. [DOI] [PMC free article] [PubMed] [Google Scholar]

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