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. 1998 Jan;148(1):233–242. doi: 10.1093/genetics/148.1.233

Conserved subfamilies of the Drosophila HeT-A telomere-specific retrotransposon.

O N Danilevskaya 1, K Lowenhaupt 1, M L Pardue 1
PMCID: PMC1459768  PMID: 9475735

Abstract

HeT-A, a major component of Drosophila telomeres, is the first retrotransposon proposed to have a vital cellular function. Unlike most retrotransposons, more than half of its genome is noncoding. The 3' end contains > 2.5 kb of noncoding sequence. Copies of HeT-A differ by insertions or deletions and multiple nucleotide changes, which initially led us to conclude that HeT-A noncoding sequences are very fluid. However, we can now report, on the basis of new sequences and further analyses, that most of these differences are due to the existence of a small number of conserved sequence subfamilies, not to extensive sequence change during each transposition event. The high level of sequence conservation within subfamilies suggests that they arise from a small number of replicatively active elements. All HeT-A subfamilies show preservation of two intriguing features. First, segments of extremely A-rich sequence form a distinctive pattern within the 3' noncoding region. Second, there is a strong strand bias of nucleotide composition: The DNA strand running 5' to 3' toward the middle of the chromosome is unusually rich in adenine and unusually poor in guanine. Although not faced with the constraints of coding sequences, the HeT-A 3' noncoding sequence appears to be under other evolutionary constraints, possibly reflecting its roles in the telomeres.

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Selected References

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  1. Adey N. B., Schichman S. A., Graham D. K., Peterson S. N., Edgell M. H., Hutchison C. A., 3rd Rodent L1 evolution has been driven by a single dominant lineage that has repeatedly acquired new transcriptional regulatory sequences. Mol Biol Evol. 1994 Sep;11(5):778–789. doi: 10.1093/oxfordjournals.molbev.a040158. [DOI] [PubMed] [Google Scholar]
  2. Bebenek K., Abbotts J., Roberts J. D., Wilson S. H., Kunkel T. A. Specificity and mechanism of error-prone replication by human immunodeficiency virus-1 reverse transcriptase. J Biol Chem. 1989 Oct 5;264(28):16948–16956. [PubMed] [Google Scholar]
  3. Biessmann H., Kasravi B., Bui T., Fujiwara G., Champion L. E., Mason J. M. Comparison of two active HeT-A retroposons of Drosophila melanogaster. Chromosoma. 1994 Apr;103(2):90–98. doi: 10.1007/BF00352317. [DOI] [PubMed] [Google Scholar]
  4. Biessmann H., Mason J. M., Ferry K., d'Hulst M., Valgeirsdottir K., Traverse K. L., Pardue M. L. Addition of telomere-associated HeT DNA sequences "heals" broken chromosome ends in Drosophila. Cell. 1990 May 18;61(4):663–673. doi: 10.1016/0092-8674(90)90478-w. [DOI] [PubMed] [Google Scholar]
  5. Biessmann H., Valgeirsdottir K., Lofsky A., Chin C., Ginther B., Levis R. W., Pardue M. L. HeT-A, a transposable element specifically involved in "healing" broken chromosome ends in Drosophila melanogaster. Mol Cell Biol. 1992 Sep;12(9):3910–3918. doi: 10.1128/mcb.12.9.3910. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Blackburn E. H. Telomerases. Annu Rev Biochem. 1992;61:113–129. doi: 10.1146/annurev.bi.61.070192.000553. [DOI] [PubMed] [Google Scholar]
  7. Casacuberta J. M., Vernhettes S., Grandbastien M. A. Sequence variability within the tobacco retrotransposon Tnt1 population. EMBO J. 1995 Jun 1;14(11):2670–2678. doi: 10.1002/j.1460-2075.1995.tb07265.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Corpet F. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 1988 Nov 25;16(22):10881–10890. doi: 10.1093/nar/16.22.10881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Danilevskaya O. N., Petrov D. A., Pavlova M. N., Koga A., Kurenova E. V., Hartl D. L. A repetitive DNA element, associated with telomeric sequences in Drosophila melanogaster, contains open reading frames. Chromosoma. 1992 Dec;102(1):32–40. doi: 10.1007/BF00352288. [DOI] [PubMed] [Google Scholar]
  10. Danilevskaya O., Lofsky A., Kurenova E. V., Pardue M. L. The Y chromosome of Drosophila melanogaster contains a distinctive subclass of Het-A-related repeats. Genetics. 1993 Jun;134(2):531–543. doi: 10.1093/genetics/134.2.531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Danilevskaya O., Slot F., Pavlova M., Pardue M. L. Structure of the Drosophila HeT-A transposon: a retrotransposon-like element forming telomeres. Chromosoma. 1994 Jun;103(3):215–224. doi: 10.1007/BF00368015. [DOI] [PubMed] [Google Scholar]
  12. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Drake J. W. Rates of spontaneous mutation among RNA viruses. Proc Natl Acad Sci U S A. 1993 May 1;90(9):4171–4175. doi: 10.1073/pnas.90.9.4171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Furano A. V., Usdin K. DNA "fossils" and phylogenetic analysis. Using L1 (LINE-1, long interspersed repeated) DNA to determine the evolutionary history of mammals. J Biol Chem. 1995 Oct 27;270(43):25301–25304. doi: 10.1074/jbc.270.43.25301. [DOI] [PubMed] [Google Scholar]
  15. Gabriel A., Willems M., Mules E. H., Boeke J. D. Replication infidelity during a single cycle of Ty1 retrotransposition. Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7767–7771. doi: 10.1073/pnas.93.15.7767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hardies S. C., Martin S. L., Voliva C. F., Hutchison C. A., 3rd, Edgell M. H. An analysis of replacement and synonymous changes in the rodent L1 repeat family. Mol Biol Evol. 1986 Mar;3(2):109–125. doi: 10.1093/oxfordjournals.molbev.a040386. [DOI] [PubMed] [Google Scholar]
  17. Karpen G. H., Spradling A. C. Analysis of subtelomeric heterochromatin in the Drosophila minichromosome Dp1187 by single P element insertional mutagenesis. Genetics. 1992 Nov;132(3):737–753. doi: 10.1093/genetics/132.3.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Koo H. S., Wu H. M., Crothers D. M. DNA bending at adenine . thymine tracts. Nature. 1986 Apr 10;320(6062):501–506. doi: 10.1038/320501a0. [DOI] [PubMed] [Google Scholar]
  19. Levis R. W., Ganesan R., Houtchens K., Tolar L. A., Sheen F. M. Transposons in place of telomeric repeats at a Drosophila telomere. Cell. 1993 Dec 17;75(6):1083–1093. doi: 10.1016/0092-8674(93)90318-k. [DOI] [PubMed] [Google Scholar]
  20. Mason J. M., Strobel E., Green M. M. mu-2: mutator gene in Drosophila that potentiates the induction of terminal deficiencies. Proc Natl Acad Sci U S A. 1984 Oct;81(19):6090–6094. doi: 10.1073/pnas.81.19.6090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Pardue M. L., Danilevskaya O. N., Lowenhaupt K., Slot F., Traverse K. L. Drosophila telomeres: new views on chromosome evolution. Trends Genet. 1996 Feb;12(2):48–52. doi: 10.1016/0168-9525(96)81399-0. [DOI] [PubMed] [Google Scholar]
  22. Pardue M. L., Danilevskaya O. N., Lowenhaupt K., Wong J., Erby K. The gag coding region of the Drosophila telomeric retrotransposon, HeT-A, has an internal frame shift and a length polymorphic region. J Mol Evol. 1996 Dec;43(6):572–583. doi: 10.1007/BF02202105. [DOI] [PubMed] [Google Scholar]
  23. Parthasarathi S., Varela-Echavarría A., Ron Y., Preston B. D., Dougherty J. P. Genetic rearrangements occurring during a single cycle of murine leukemia virus vector replication: characterization and implications. J Virol. 1995 Dec;69(12):7991–8000. doi: 10.1128/jvi.69.12.7991-8000.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Preston B. D., Dougherty J. P. Mechanisms of retroviral mutation. Trends Microbiol. 1996 Jan;4(1):16–21. doi: 10.1016/0966-842x(96)81500-9. [DOI] [PubMed] [Google Scholar]
  25. Preston B. D. Error-prone retrotransposition: rime of the ancient mutators. Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7427–7431. doi: 10.1073/pnas.93.15.7427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]

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