Abstract
We characterized TRAS1, a retrotransposable element which was inserted into the telomeric repetitive sequence (CCTAA)n of the silkworm, Bombyx mori. The complete sequence of TRAS1, a stretch of 7.8 kb with a poly(A) tract at the 3' end, was determined. No long terminal repeat (LTR) was found at the termini of the element. TRAS1 contains gag- and pol-like open reading frames (ORFs) which are similar to those of non-LTR retrotransposons. The two ORFs overlap but are one nucleotide out of frame (+1 frameshift). Most of the approximately 250 copies of TRAS1 elements in the genome were highly conserved in the structure. Chromosomal in situ hybridization showed that TRAS1 elements are clustered at the telomeres of Bombyx chromosomes. A phylogenetic analysis using the amino acid sequence of the reverse transcriptase domain within the pol-like ORF revealed that TRAS1 falls into one lineage with R1, which is a family of non-LTR retrotransposons inserted into the same site within the 28S ribosomal DNA unit in most insects. TRAS1 may have been derived from R1 and changed the target specificity so that TRAS1 inserts into the telomeric repetitive sequence (CCTAA)n. Southern hybridization and Bal 31 exonuclease analyses showed that TRAS1 elements are clustered proximal to the terminal long tract of (CCTAA)n. TRAS1 is a novel family of non-LTR retrotransposons which are inserted into the telomeric repetitive sequences as target sites.
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- Ajioka J. W., Eanes W. F. The accumulation of P-elements on the tip of the X chromosome in populations of Drosophila melanogaster. Genet Res. 1989 Feb;53(1):1–6. doi: 10.1017/s0016672300027798. [DOI] [PubMed] [Google Scholar]
- Aksoy S., Williams S., Chang S., Richards F. F. SLACS retrotransposon from Trypanosoma brucei gambiense is similar to mammalian LINEs. Nucleic Acids Res. 1990 Feb 25;18(4):785–792. doi: 10.1093/nar/18.4.785. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Biessmann H., Champion L. E., O'Hair M., Ikenaga K., Kasravi B., Mason J. M. Frequent transpositions of Drosophila melanogaster HeT-A transposable elements to receding chromosome ends. EMBO J. 1992 Dec;11(12):4459–4469. doi: 10.1002/j.1460-2075.1992.tb05547.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Biessmann H., Kasravi B., Jakes K., Bui T., Ikenaga K., Mason J. M. The genomic organization of HeT-A retroposons in Drosophila melanogaster. Chromosoma. 1993 May;102(5):297–305. doi: 10.1007/BF00661272. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Blackburn E. H. The molecular structure of centromeres and telomeres. Annu Rev Biochem. 1984;53:163–194. doi: 10.1146/annurev.bi.53.070184.001115. [DOI] [PubMed] [Google Scholar]
- Brierley I., Digard P., Inglis S. C. Characterization of an efficient coronavirus ribosomal frameshifting signal: requirement for an RNA pseudoknot. Cell. 1989 May 19;57(4):537–547. doi: 10.1016/0092-8674(89)90124-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Burke W. D., Calalang C. C., Eickbush T. H. The site-specific ribosomal insertion element type II of Bombyx mori (R2Bm) contains the coding sequence for a reverse transcriptase-like enzyme. Mol Cell Biol. 1987 Jun;7(6):2221–2230. doi: 10.1128/mcb.7.6.2221. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clare J. J., Belcourt M., Farabaugh P. J. Efficient translational frameshifting occurs within a conserved sequence of the overlap between the two genes of a yeast Ty1 transposon. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6816–6820. doi: 10.1073/pnas.85.18.6816. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Eickbush T. H., Robins B. Bombyx mori 28S ribosomal genes contain insertion elements similar to the Type I and II elements of Drosophila melanogaster. EMBO J. 1985 Sep;4(9):2281–2285. doi: 10.1002/j.1460-2075.1985.tb03927.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fujiwara H., Ogura T., Takada N., Miyajima N., Ishikawa H., Maekawa H. Introns and their flanking sequences of Bombyx mori rDNA. Nucleic Acids Res. 1984 Sep 11;12(17):6861–6869. doi: 10.1093/nar/12.17.6861. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gabriel A., Yen T. J., Schwartz D. C., Smith C. L., Boeke J. D., Sollner-Webb B., Cleveland D. W. A rapidly rearranging retrotransposon within the miniexon gene locus of Crithidia fasciculata. Mol Cell Biol. 1990 Feb;10(2):615–624. doi: 10.1128/mcb.10.2.615. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gottschling D. E. Telomere-proximal DNA in Saccharomyces cerevisiae is refractory to methyltransferase activity in vivo. Proc Natl Acad Sci U S A. 1992 May 1;89(9):4062–4065. doi: 10.1073/pnas.89.9.4062. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Higgins D. G., Bleasby A. J., Fuchs R. CLUSTAL V: improved software for multiple sequence alignment. Comput Appl Biosci. 1992 Apr;8(2):189–191. doi: 10.1093/bioinformatics/8.2.189. [DOI] [PubMed] [Google Scholar]
- Jacks T., Madhani H. D., Masiarz F. R., Varmus H. E. Signals for ribosomal frameshifting in the Rous sarcoma virus gag-pol region. Cell. 1988 Nov 4;55(3):447–458. doi: 10.1016/0092-8674(88)90031-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jacks T., Power M. D., Masiarz F. R., Luciw P. A., Barr P. J., Varmus H. E. Characterization of ribosomal frameshifting in HIV-1 gag-pol expression. Nature. 1988 Jan 21;331(6153):280–283. doi: 10.1038/331280a0. [DOI] [PubMed] [Google Scholar]
- Jacks T., Townsley K., Varmus H. E., Majors J. Two efficient ribosomal frameshifting events are required for synthesis of mouse mammary tumor virus gag-related polyproteins. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4298–4302. doi: 10.1073/pnas.84.12.4298. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jacks T., Varmus H. E. Expression of the Rous sarcoma virus pol gene by ribosomal frameshifting. Science. 1985 Dec 13;230(4731):1237–1242. doi: 10.1126/science.2416054. [DOI] [PubMed] [Google Scholar]
- Jakubczak J. L., Burke W. D., Eickbush T. H. Retrotransposable elements R1 and R2 interrupt the rRNA genes of most insects. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3295–3299. doi: 10.1073/pnas.88.8.3295. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jakubczak J. L., Xiong Y., Eickbush T. H. Type I (R1) and type II (R2) ribosomal DNA insertions of Drosophila melanogaster are retrotransposable elements closely related to those of Bombyx mori. J Mol Biol. 1990 Mar 5;212(1):37–52. doi: 10.1016/0022-2836(90)90303-4. [DOI] [PubMed] [Google Scholar]
- 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]
- Levis R. W. Drosophila melanogaster does not share the telomeric repeat sequence of another invertebrate, Ascaris lumbricoides. Mol Gen Genet. 1993 Jan;236(2-3):440–442. doi: 10.1007/BF00277145. [DOI] [PubMed] [Google Scholar]
- 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]
- Louis E. J., Haber J. E. Mitotic recombination among subtelomeric Y' repeats in Saccharomyces cerevisiae. Genetics. 1990 Mar;124(3):547–559. doi: 10.1093/genetics/124.3.547. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Louis E. J., Haber J. E. The structure and evolution of subtelomeric Y' repeats in Saccharomyces cerevisiae. Genetics. 1992 Jul;131(3):559–574. doi: 10.1093/genetics/131.3.559. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Louis E. J., Haber J. E. The subtelomeric Y' repeat family in Saccharomyces cerevisiae: an experimental system for repeated sequence evolution. Genetics. 1990 Mar;124(3):533–545. doi: 10.1093/genetics/124.3.533. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Luan D. D., Korman M. H., Jakubczak J. L., Eickbush T. H. Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell. 1993 Feb 26;72(4):595–605. doi: 10.1016/0092-8674(93)90078-5. [DOI] [PubMed] [Google Scholar]
- Lundblad V., Blackburn E. H. An alternative pathway for yeast telomere maintenance rescues est1- senescence. Cell. 1993 Apr 23;73(2):347–360. doi: 10.1016/0092-8674(93)90234-h. [DOI] [PubMed] [Google Scholar]
- Lundblad V., Szostak J. W. A mutant with a defect in telomere elongation leads to senescence in yeast. Cell. 1989 May 19;57(4):633–643. doi: 10.1016/0092-8674(89)90132-3. [DOI] [PubMed] [Google Scholar]
- Makarov V. L., Lejnine S., Bedoyan J., Langmore J. P. Nucleosomal organization of telomere-specific chromatin in rat. Cell. 1993 May 21;73(4):775–787. doi: 10.1016/0092-8674(93)90256-p. [DOI] [PubMed] [Google Scholar]
- Marlor R. L., Parkhurst S. M., Corces V. G. The Drosophila melanogaster gypsy transposable element encodes putative gene products homologous to retroviral proteins. Mol Cell Biol. 1986 Apr;6(4):1129–1134. doi: 10.1128/mcb.6.4.1129. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mellor J., Fulton S. M., Dobson M. J., Wilson W., Kingsman S. M., Kingsman A. J. A retrovirus-like strategy for expression of a fusion protein encoded by yeast transposon Ty1. Nature. 1985 Jan 17;313(5999):243–246. doi: 10.1038/313243a0. [DOI] [PubMed] [Google Scholar]
- Okazaki S., Tsuchida K., Maekawa H., Ishikawa H., Fujiwara H. Identification of a pentanucleotide telomeric sequence, (TTAGG)n, in the silkworm Bombyx mori and in other insects. Mol Cell Biol. 1993 Mar;13(3):1424–1432. doi: 10.1128/mcb.13.3.1424. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Poch O., Sauvaget I., Delarue M., Tordo N. Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO J. 1989 Dec 1;8(12):3867–3874. doi: 10.1002/j.1460-2075.1989.tb08565.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saigo K., Kugimiya W., Matsuo Y., Inouye S., Yoshioka K., Yuki S. Identification of the coding sequence for a reverse transcriptase-like enzyme in a transposable genetic element in Drosophila melanogaster. Nature. 1984 Dec 13;312(5995):659–661. doi: 10.1038/312659a0. [DOI] [PubMed] [Google Scholar]
- Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
- 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]
- Sheen F. M., Levis R. W. Transposition of the LINE-like retrotransposon TART to Drosophila chromosome termini. Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12510–12514. doi: 10.1073/pnas.91.26.12510. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Tommerup H., Dousmanis A., de Lange T. Unusual chromatin in human telomeres. Mol Cell Biol. 1994 Sep;14(9):5777–5785. doi: 10.1128/mcb.14.9.5777. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Traverse K. L., Pardue M. L. A spontaneously opened ring chromosome of Drosophila melanogaster has acquired He-T DNA sequences at both new telomeres. Proc Natl Acad Sci U S A. 1988 Nov;85(21):8116–8120. doi: 10.1073/pnas.85.21.8116. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Villanueva M. S., Williams S. P., Beard C. B., Richards F. F., Aksoy S. A new member of a family of site-specific retrotransposons is present in the spliced leader RNA genes of Trypanosoma cruzi. Mol Cell Biol. 1991 Dec;11(12):6139–6148. doi: 10.1128/mcb.11.12.6139. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Voytas D. F., Boeke J. D. Yeast retrotransposons and tRNAs. Trends Genet. 1993 Dec;9(12):421–427. doi: 10.1016/0168-9525(93)90105-q. [DOI] [PubMed] [Google Scholar]
- Wright J. H., Gottschling D. E., Zakian V. A. Saccharomyces telomeres assume a non-nucleosomal chromatin structure. Genes Dev. 1992 Feb;6(2):197–210. doi: 10.1101/gad.6.2.197. [DOI] [PubMed] [Google Scholar]
- Xiong Y. E., Eickbush T. H. Functional expression of a sequence-specific endonuclease encoded by the retrotransposon R2Bm. Cell. 1988 Oct 21;55(2):235–246. doi: 10.1016/0092-8674(88)90046-3. [DOI] [PubMed] [Google Scholar]
- Xiong Y., Eickbush T. H. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 1990 Oct;9(10):3353–3362. doi: 10.1002/j.1460-2075.1990.tb07536.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Xiong Y., Eickbush T. H. Similarity of reverse transcriptase-like sequences of viruses, transposable elements, and mitochondrial introns. Mol Biol Evol. 1988 Nov;5(6):675–690. doi: 10.1093/oxfordjournals.molbev.a040521. [DOI] [PubMed] [Google Scholar]
- Xiong Y., Eickbush T. H. The site-specific ribosomal DNA insertion element R1Bm belongs to a class of non-long-terminal-repeat retrotransposons. Mol Cell Biol. 1988 Jan;8(1):114–123. doi: 10.1128/mcb.8.1.114. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Young B. S., Pession A., Traverse K. L., French C., Pardue M. L. Telomere regions in Drosophila share complex DNA sequences with pericentric heterochromatin. Cell. 1983 Aug;34(1):85–94. doi: 10.1016/0092-8674(83)90138-1. [DOI] [PubMed] [Google Scholar]
- Zakian V. A. Structure and function of telomeres. Annu Rev Genet. 1989;23:579–604. doi: 10.1146/annurev.ge.23.120189.003051. [DOI] [PubMed] [Google Scholar]
- de Lange T. Human telomeres are attached to the nuclear matrix. EMBO J. 1992 Feb;11(2):717–724. doi: 10.1002/j.1460-2075.1992.tb05104.x. [DOI] [PMC free article] [PubMed] [Google Scholar]