Skip to main content

Advertisement

SpringerLink
Log in

Ltr retrotransposons and the evolution of eukaryotic enhancers

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Since LTR retrotransposons and retroviruses are especially prone to regional duplications and recombination events, these viral-like systems may be especially conducive to the evolution of closely spaced combinatorial regulatory motifs. Using the Drosophila copia LTR retrotransposon as a model, we show that a regulatory region contained within the element's untranslated leader region (ULR) consists of multiple copies of an 8 bp motif (TTGTGAAA) with similarity to the core sequence of the SV40 enhancer. Naturally occurring variation in the number of these motifs is correlated with the enhancer strength of the ULR. Our results indicate that inter-element selection may favor the evolution of more active enhancers within permissive genetic backgrounds. We propose that LTR retroelements and perhaps other retrotransposons constitute drive mechanisms for the evolution of eukaryotic enhancers which can be subsequently distributed throughout host genomes to play a role in regulatory evolution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Atchison, M.L., 1988. Enhancers: mechanism of action and cell specificity. Annu. Rev. Cell Biol. 4: 127–153.

    Article  PubMed  Google Scholar 

  • Berg, D.E. & M.M. Howe (editors), 1989. Mobile DNA. American Society for Microbiology, Washington, D.C.

    Google Scholar 

  • Brosius, J. & H. Tiedge, 1996. Reverse transcriptase:mediator of genomic plasticity. Virus Genes 11: 163–179.

    Article  Google Scholar 

  • Burns, D.P. & H.M. Temin, 1994. High rates of frameshift mutations within homo-oligomeric runs during a single cycle of retroviral replication. J. Virol. 68: 4196–4203.

    PubMed  Google Scholar 

  • Casacuberta, J., S. Vernhettes & M-A. Grandbastien, 1995. Sequence variability within the tobacco retrotransposon Tnt 1 population. EMBO J. 14: 2670–2678.

    PubMed  Google Scholar 

  • Csink, A.K. & J.F. McDonald, 1990. Copia expression is variable among natural populations of Drosophila. Genetics 126: 375–385.

    PubMed  Google Scholar 

  • Csink, A.K. & J.F. McDonald, 1995. Analysis of copia sequence variation within and between Drosophila species. Mol. Biol. Evol. 12: 83–93.

    PubMed  Google Scholar 

  • Devlin, R.H., B. Bingham & B.T. Wakimoto, 1990. The organiza-tion and expression of the light gene, a heterochromatic gene of Drosophila melanogaster. Genetics 127: 553–565.

    Google Scholar 

  • Graves, B.J., P.F. Johnson & S.L. McKnight, 1986. Homologous recognition of a promoter domain common to the MSV LTR and the HSV tk gene. Cell 44: 565–576.

    Article  PubMed  Google Scholar 

  • Gerasimova, T.I., D.A. Gdula, D.V. Gerasimova, O. Simonova & V.G. Corces, 1995. A Drosophila protein that imparts directionality on a chromatin insulator is an enhancer of position-effect variegation. Cell 82: 587–597.

    Article  PubMed  Google Scholar 

  • Jordan, I.K. & J.F. McDonald, 1997. Evolution of the copia retro-transposon in the Drosophila melanogaster species subgroup.Mol. Biol. Evol. (submitted).

  • Koken, S.E., J.L. van Wamel, J. Goudsmit, B. Berkhout & J.L. Geelen, 1992. Natural variants of the HIV-1 long terminal repeat: analysis of promoters with duplicated DNA regulatory motifs. Virology 191: 968–972.

    Article  PubMed  Google Scholar 

  • Lohe, A.R. & A.J. Hilliker, 1995. Return of the H-word (heterochro-matin). Curr. Biol. 5: 746–755.

    Google Scholar 

  • Makalowski, W., 1995. SINES as agenomic scrap yard: an essay on genomic evolution, pp. 81–104 in The Impact of Short Inter-spersed Elements (SINES) on the Host Genome, edited by R.J. Maraia, R.G. Landes Co., Austin, TX.

    Google Scholar 

  • Maniatis, T., S. Goodbourn & J.A. Fisher, 1987. Regulation of inducible and tissue-specific gene expression. Science 236: 1237–1244.

    PubMed  Google Scholar 

  • Matyunina, L.V., I.K. Jordan & J.F. McDonald, 1996. Naturally occurring variation in copia expression is due to both element (cis) and host (trans) regulatory variation. Proc. Natl. Acad. Sci. (USA) 93: 7097–7102.

    Article  PubMed  Google Scholar 

  • McClintock, B., 1951. Chromosome organization and genic expres-sion.Cold Spr. Harb. Symp. Quant. Biol. 16: 13–47.

    Google Scholar 

  • McClintock, B., 1956. Controlling elements and the gene. Cold Spr. Harb. Symp. Quant. Biol. 21: 197–216.

    Google Scholar 

  • McDonald, J.F., 1995. Transposable elements: possible catalysts of organismic evolution. Trends Ecol. Evol. 10: 123–126.

    Article  Google Scholar 

  • McDonald, J.F., 1993. Evolution and consequences of transposable elements. Curr. Opin. Gen. Dev. 3: 855–864.

    Article  Google Scholar 

  • Mitchelson, A.M., M. Simonelig, C. Williams & K. O'Hare, 1993.Homology with Saccharomyces cerevisiae RNA14 suggests that phenotypic suppression in Drosophila melanogaster by suppres-sor of forked occurs at the level of RNA stability. Genes Dev. 7: 241–249.

    PubMed  Google Scholar 

  • Miller, W.J., N. Paricio, S. Hagemann, M.J. Martinez-Sebastian, W. Pinsker & R. de Frutos, 1995. Structure and expression of clustered P element homologues in Drosophila subobscura and Drosophila guanche. Gene 156: 167–174.

    Article  PubMed  Google Scholar 

  • Moon, A.M. & T.J. Ley, 1990. Conservation of the primary structure, organization, and function of the human and mouse _-globin locus-activating regions. Proc. Natl. Acad. Sci. (USA) 87: 7693–7697.

    Article  Google Scholar 

  • Montell, D.J., P. Rorth & A.C. Spradling, 1992. Slow border cells, a locus required for a developmentally regulated cell migration during oogenesis, encodes Drosophila C/EBP. Cell 71: 51–62.

    Article  PubMed  Google Scholar 

  • Nilsson, M. & S. Bohm, 1994. Inducible and cell type-specific expression of VL30 U3 subgroups correlate with their enhancer design. J. Virol. 68: 276–288.

    PubMed  Google Scholar 

  • Olson, P. & H.M. Temin, 1992. Unusually high frequency of recon-stitution of long terminal repeats in U3-minus retrovirus vectors by DNA recombination or gene conversion. J. Virol. 66: 1336–1343.

    PubMed  Google Scholar 

  • Parthasarathi, S., A. Varela-Echavarria, Y. Ron, B.D. Preston & J.P. Dougherty, 1995. Genetic rearrangements occurring during a single cycle of murine leukemia virus vector replication: charac-terization and implications. J. Virol. 69: 7991–8000.

    PubMed  Google Scholar 

  • Pasyukova, E., S. Nuzhdin, L. Wei & A. Flavell, 1997. Germline transposition of the copia retrotransposon in Drosophila melanogaster is restricted to males by tissue-specific control of copia RNA levels. Mol. Gen. Genet. (in press).

  • Preston, B.D. & J.P. Dougherty, 1996. Mechanisms of retroviral mutation. Trends Microb. 4: 16–21.

    Article  Google Scholar 

  • Robins, D.M. & L.C. Samuelson, 1992. Retrotransposons and the evolution of mammalian gene expression. Genetica 86: 191–202.

    Article  PubMed  Google Scholar 

  • Rorth, P. & D.J. Montell, 1993. Drosophila C/EBP: a tissue-specific DNA-binding protein required for embryonic develop-ment. Genes Dev. 6: 2299–2311.

    Google Scholar 

  • Ruocco, M.R., X. Chen, C. Ambrosino, E. Dragonetti, W. Liu, M. Mallardo, G. De Falco, C. Palmieri, G. Franzoso, I. Quinto, S. Ventura & G. Scala, 1996. Regulation of HIV-1 long terminal repeats by interaction of C/EBP (NF-IL6) and NfkappaB/Rel transcription factors. J. Biol. Chem. 271: 22479–22486.

    Article  PubMed  Google Scholar 

  • Serfling, E., M. Jasin & W. Schaffner, 1985. Enhancers and eukaryotic gene transcription. Trends Genet. 1: 224–230.

    Article  Google Scholar 

  • Skalka, A.M. & S.P. Groff (editors), 1993. Reverse Transcriptase.Cold Spr. Harb. Press, Plainview, N.Y.

    Google Scholar 

  • Smith, P.A. & V.G. Corces, 1995. The suppressor-of-hairy-wing protein regulates the tissue-specific expression of the Drosophila gypsy retrotransposon. Genetics 139: 215–228.

    PubMed  Google Scholar 

  • Spana, C., D.A. Harrison & V.C. Corces, 1988. The Drosophila melanogaster suppressor-of-hairy-wing protein binds to specific sequences of the gypsy retrotransposon. Genes Dev. 2: 1414–1423.

    PubMed  Google Scholar 

  • Tijan, R. & T. Maniatis, 1994. Transcriptional activation: a complex puzzle with few easy pieces. Cell 77: 5–8.

    Article  Google Scholar 

  • Walters, M.C., W. Magis, S. Fiering, J. Eidemiller, D. Scalzo, M. Groudine & D.I.K. Martin, 1996. Transcriptional enhancers act in cis to suppress position-effect variegation. Genes Dev. 10: 185–195.

    PubMed  Google Scholar 

  • White, S.E., L. Habera & S.R. Wessler, 1994. Retrotransposons in the flanking regions of normal plant genes: a role of copia-like elements in the evolution of gene structure and expression. Proc. Natl. Acad. Sci. (USA) 91: 11792–11796.

    Article  Google Scholar 

  • Wessler, S.R., T.E. Bureau & S.E. White, 1995. LTR-retrotransposons and LITES: important players in the evolution of plant genomes. Curr. Opin. Genet. Dev. 5: 814–821.

    Article  PubMed  Google Scholar 

  • Wilson, S., L. Matyunina & J.F. McDonald, 1997. An enhancer-like region with the copia untranslated leader which is variable in nat-ural populations contains binding sites for Drosophila regulatory proteins. Nucl. Acids Res. (submitted).

  • Zang, P. & A.C. Spradling, 1995. The Drosophila salivary gland chromocenter contains highly polytenized subdomains of mitotic heterochromatin. Genetics 139: 659–670.

    Google Scholar 

  • Zang, J. & H.M. Temin, 1994. Retrovirus recombination depends on the length of sequence identity and is not error prone. J. Virol. 68: 2409–2414.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Genetics, University of Georgia, Athens, GA, 30602, USA

    John F. McDonald, Lilya V. Matyunina, Susanne Wilson, I. King Jordan, Nathan J. Bowen & Wolfgang J. Miller

Authors
  1. John F. McDonald
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lilya V. Matyunina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Susanne Wilson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. I. King Jordan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nathan J. Bowen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wolfgang J. Miller
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

McDonald, J.F., Matyunina, L.V., Wilson, S. et al. Ltr retrotransposons and the evolution of eukaryotic enhancers. Genetica 100, 3–13 (1997). https://doi.org/10.1023/A:1018392117410

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1018392117410

Search

Navigation