Genetica

, Volume 100, Issue 1–3, pp 3–13 | Cite as

Ltr retrotransposons and the evolution of eukaryotic enhancers

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

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.

long terminal repeat retrotransposon transposable element enhancer gene expression copia/Drosophila 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Atchison, M.L., 1988. Enhancers: mechanism of action and cell specificity. Annu. Rev. Cell Biol. 4: 127–153.PubMedCrossRefGoogle Scholar
  2. Berg, D.E. & M.M. Howe (editors), 1989. Mobile DNA. American Society for Microbiology, Washington, D.C.Google Scholar
  3. Brosius, J. & H. Tiedge, 1996. Reverse transcriptase:mediator of genomic plasticity. Virus Genes 11: 163–179.CrossRefGoogle Scholar
  4. 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.PubMedGoogle Scholar
  5. Casacuberta, J., S. Vernhettes & M-A. Grandbastien, 1995. Sequence variability within the tobacco retrotransposon Tnt 1 population. EMBO J. 14: 2670–2678.PubMedGoogle Scholar
  6. Csink, A.K. & J.F. McDonald, 1990. Copia expression is variable among natural populations of Drosophila. Genetics 126: 375–385.PubMedGoogle Scholar
  7. Csink, A.K. & J.F. McDonald, 1995. Analysis of copia sequence variation within and between Drosophila species. Mol. Biol. Evol. 12: 83–93.PubMedGoogle Scholar
  8. 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
  9. 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.PubMedCrossRefGoogle Scholar
  10. 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.PubMedCrossRefGoogle Scholar
  11. Jordan, I.K. & J.F. McDonald, 1997. Evolution of the copia retro-transposon in the Drosophila melanogaster species subgroup.Mol. Biol. Evol. (submitted).Google Scholar
  12. 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.PubMedCrossRefGoogle Scholar
  13. Lohe, A.R. & A.J. Hilliker, 1995. Return of the H-word (heterochro-matin). Curr. Biol. 5: 746–755.Google Scholar
  14. 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
  15. Maniatis, T., S. Goodbourn & J.A. Fisher, 1987. Regulation of inducible and tissue-specific gene expression. Science 236: 1237–1244.PubMedGoogle Scholar
  16. 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.PubMedCrossRefGoogle Scholar
  17. McClintock, B., 1951. Chromosome organization and genic expres-sion.Cold Spr. Harb. Symp. Quant. Biol. 16: 13–47.Google Scholar
  18. McClintock, B., 1956. Controlling elements and the gene. Cold Spr. Harb. Symp. Quant. Biol. 21: 197–216.Google Scholar
  19. McDonald, J.F., 1995. Transposable elements: possible catalysts of organismic evolution. Trends Ecol. Evol. 10: 123–126.CrossRefGoogle Scholar
  20. McDonald, J.F., 1993. Evolution and consequences of transposable elements. Curr. Opin. Gen. Dev. 3: 855–864.CrossRefGoogle Scholar
  21. 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.PubMedGoogle Scholar
  22. 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.PubMedCrossRefGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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.PubMedCrossRefGoogle Scholar
  25. 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.PubMedGoogle Scholar
  26. 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.PubMedGoogle Scholar
  27. 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.PubMedGoogle Scholar
  28. 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).Google Scholar
  29. Preston, B.D. & J.P. Dougherty, 1996. Mechanisms of retroviral mutation. Trends Microb. 4: 16–21.CrossRefGoogle Scholar
  30. Robins, D.M. & L.C. Samuelson, 1992. Retrotransposons and the evolution of mammalian gene expression. Genetica 86: 191–202.PubMedCrossRefGoogle Scholar
  31. 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
  32. 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.PubMedCrossRefGoogle Scholar
  33. Serfling, E., M. Jasin & W. Schaffner, 1985. Enhancers and eukaryotic gene transcription. Trends Genet. 1: 224–230.CrossRefGoogle Scholar
  34. Skalka, A.M. & S.P. Groff (editors), 1993. Reverse Transcriptase.Cold Spr. Harb. Press, Plainview, N.Y.Google Scholar
  35. 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.PubMedGoogle Scholar
  36. 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.PubMedGoogle Scholar
  37. Tijan, R. & T. Maniatis, 1994. Transcriptional activation: a complex puzzle with few easy pieces. Cell 77: 5–8.CrossRefGoogle Scholar
  38. 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.PubMedGoogle Scholar
  39. 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.CrossRefGoogle Scholar
  40. 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.PubMedCrossRefGoogle Scholar
  41. 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).Google Scholar
  42. Zang, P. & A.C. Spradling, 1995. The Drosophila salivary gland chromocenter contains highly polytenized subdomains of mitotic heterochromatin. Genetics 139: 659–670.Google Scholar
  43. 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

Copyright information

© Kluwer Academic Publishers 1997

Authors and Affiliations

  • John F. McDonald
    • 1
  • Lilya V. Matyunina
    • 1
  • Susanne Wilson
    • 1
  • I. King Jordan
    • 1
  • Nathan J. Bowen
    • 1
  • Wolfgang J. Miller
    • 1
  1. 1.Department of GeneticsUniversity of GeorgiaAthensUSA

Personalised recommendations