Abstract
Earlier related to parasitic elements, retrotransposons of eukaryotes have been demonstrated to participate in general cell processes such as chromosome repair and evolution of gene expression (Teng et al., 1996; McDonald, 1993). Here, we report the existence of two class of genomic copies of retrotransposon 1731 with different expression strategies, one of which might be driven by natural selection. The first class uses conventional translation frameshifting known to ensure expression of revere transcriptase (RT) open reading frame (ORF), depending on the efficiency of frameshifting. The bulk of genomic copies are related to the second class where the frameshift is prevented as a result of the substitution of a rare codon recoginsing rare tRNA by a codon preferred by host genome, whereas the RT ORF is restored by downstream single nuclotide deletion. We suggest that natural selection has driven the switching of 1731 expression strategy from retrovirus-like to the fussion-ORF expression. This observation is in accordance with the detection in testes of fused Gag-RT polypetide encoded by 1731. The abundance of RT in testes may serve for normal development of host tissue.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aquadro, S.F., 1992. Why is genome variable? Insights from Drosophila. Trends Genet. 8: 355–362.
Ashburner, M., 1989. Drosophila: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
Atwood, A., J.H. Lin & H.L. Levin, 1996. The retrotransposon Tf1 assembles virus-like particles that contain exess Gag relative to integrase because of a regulated degradation process. Mol. Cell Biol. 16: 338–346.
Blumenthal, T., 1998. Gene clusters and polycistronic transcription in eukaryotes. Bioessays 20: 480–487.
Brierley, C. & A.J. Flavell, 1990. The retrotransposon copia controls the relative levels of its gene products post-transcriptionally by differential expression from its two major mRNAs. Nucleic Acids Res. 18: 2947–2951.
Champion, S., C. Maisonhaute, M-H. Kim & M. Best-Belpomme, 1992. Characterization of the reverse transcriptase of 1731, a Drosophila melanogaster retrotransposon. Eur. J. Biochem. 209: 523–531.
Farabaugh, P.J., 1995. Post-transcriptional regulation of transposition by Ty retrotransposons of Saccharomyces cerevisiae. J. Biol. Chem. 270: 10361–10364.
Farabaugh, P.J., 1996. Programmed translational frameshifting. Microbiol. Rev. 60: 103–134.
Fourcade-Peronnet, F., L. d'Auriol, J. Becker, F. Galibert & M. Best-Belpomme, 1988. Primary structure and functional organization of Drosophila 1731 retrotransposon. Nucl. Acids Res. 16: 6113–6125.
Haoudi, A., M.-H. Kim, S. Champion, M. Best-Belpomme & C. Maisonhaute, 1995. The Gag polypeptides of the Drosophila 1731 retrotransposon are associated to virus-like particles and to nuclei. FEBS Lett. 377: 67–72.
Haoudi, A., M. Rachidi, M.H. Kim, S. Champion & M. Best-Belpomme et al., 1997. Developmental expression analysis of the 1731 retrotransposon reveals an enhancement of Gag-Pol frameshifting in males of Drosophila melanogaster. Gene 196: 83–93.
Kawakami, K., S. Pande, B. Faiola, D.P. Moore & J.D. Boeke et al., 1993. A rare tRNA-Arg(CCU) that regulates Ty1 element ribosomal frameshifting is essential for Ty1 retrotransposition in Saccharomyces cerevisiae. Genetics 135: 309–320.
Kirchner, J., S.B. Sandmeyer & D.B. Forrest, 1992. Transposition of a Ty3 Gag3-Pol3 fusion mutant is limited by availability of capsid protein. J. Virol. 66: 6081–6092.
Levin, H.L., D.C. Weaver & J.D., Boeke, 1993. Novel gene expression mechanism in a fission yeast retroelement: Tf1 proteins are derived from a single primary translation product. EMBO J. 12: 4885–4895.
McDonald, J.F., 1993. Evolution and consequences of transposable elements. Current Opin. Genet. Devel. 3: 855–864.
Menninger, J.R., 1983. Computer simulation of ribosome editing. J. Mol. Biol. 171: 383–399.
Pardue, M.L., 1995. Drosophila telomeres: another way to end it all, pp. 339–370 in Telomeres, edited by E.H. Blackburh and C.W. Greider. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
Powell, J.R. & J.U. Gleason, 1996. Codon usage and the origin of P elements. Mol. Biol. Evol. 13: 278–279.
Schields, D.C., P.M. Sharp, D.G. Higgins & F. Wright, 1988. 'silent' sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol. Biol. Evol. 5: 704–716.
Teng, S.C., B. Kim & A. Gabriel, 1996. Retrotransposon reverse-transcriptase-mediated repair of chromosomal breaks. Nature 383: 641–644.
Voytas, D.E. & J.D. Boeke, 1993. Yeast retrotransposons and tRNAs. Trends in Genet. 9: 421–427.
Xu, H. & J.D. Boeke, 1990. Host genes that influence transposition in yeast: the abundance of a rare tRNA regulates Ty1 transposition frequency. Proc. Natl. Acad. Sci. USA 87: 8360–8364.
Youngren, S.D., J.D. Boeke, N.J. Sanders & D.J. Garfinkel, 1988. Functional organization of the retrotransposon Ty from Saccharomyces cerevisiae: Ty protease is required for transposition. Mol. Cell. Biol. 8: 1421–1431.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Kalmykova, A., Maisonhaute, C. & Gvozdev, V. Retrotransposon 1731 in Drosophila melanogaster changes retrovirus-like expression strategy in host genome. Genetica 107, 73–77 (1999). https://doi.org/10.1023/A:1003969625694
Issue Date:
DOI: https://doi.org/10.1023/A:1003969625694