Transposable Element Orientation Bias in the Drosophila melanogaster Genome

  • Asher D. Cutter
  • Jeffrey M. Good
  • Christopher T. Pappas
  • Matthew A. Saunders
  • Dean M. Starrett
  • Travis J. Wheeler
Article

Abstract

Nonrandom distributions of transposable elements can be generated by a variety of genomic features. Using the full D. melanogaster genome as a model, we characterize the orientations of different classes of transposable elements in relation to the directionality of genes. DNA-mediated transposable elements are more likely to be in the same orientation as neighboring genes when they occur in the nontranscribed region’s that flank genes. However, RNA-mediated transposable elements located in an intron are more often oriented in the direction opposite to that of the host gene. These orientation biases are strongest for genes with highly biased codon usage, probably reflecting the ability of such loci to respond to weak positive or negative selection. The leading hypothesis for selection against transposable elements in the coding orientation proposes that transcription termination poly(A) signal motifs within retroelements interfere with normal gene transcription. However, after accounting for differences in base composition between the strands, we find no evidence for global selection against spurious transcription termination signals in introns. We therefore conclude that premature termination of host gene transcription due to the presence of poly(A) signal motifs in retroelements might only partially explain strand-specific detrimental effects in the D. melanogaster genome.

Keywords

Transposable elements Drosophila melanogaster Polyadenylation Codon usage bias 

Supplementary material

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Supplementary material

References

  1. Akashi H (1994) Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy. Genetics 136:927–935PubMedGoogle Scholar
  2. Bartolome C, Maside X, Charlesworth B (2002) On the abundance and distribution of transposable elements in the genome of Drosophila melanogaster. Mol Biol Evol 19:926–937PubMedGoogle Scholar
  3. Biemont C, Tsitrone A, Vieira C, Hoogland C (1997) Transposable element distribution in Drosophila. Genetics 147:1997–1999PubMedGoogle Scholar
  4. Burge C, Campbell AM, Karlin S (1992) Over-representation and under-representation of short oligonucleotides in DNA-sequences. Proc Natl Acad Sci USA 89:1358–1362PubMedGoogle Scholar
  5. Carr M, Soloway JR, Robinson TE, Brookfield JFY (2002) Mechanisms regulating the copy numbers of six LTR retrotransposons in the genome of Drosophila melanogaster. Chromosoma 110:511–518PubMedGoogle Scholar
  6. Charlesworth B, Charlesworth D (1983) The population-dynamics of transposable elements. Genet Res 42:1–27Google Scholar
  7. Charlesworth B, Langley CH (1989) The population-genetics of Drosophila transposable elements. Annu Rev Genet 23:251–287PubMedCrossRefGoogle Scholar
  8. Charlesworth B, Morgan MT, Charlesworth D (1993) The effect of deleterious mutations on neutral molecular variation. Genetics 134:1289–1303PubMedGoogle Scholar
  9. Daborn PJ, Yen JL, Bogwitz MR et al (2002) A single P450 allele associated with insecticide resistance in Drosophila. Science 297:2253–2256PubMedCrossRefGoogle Scholar
  10. Dieringer D, Schlotterer C (2003) Two distinct modes of microsatellite mutation processes: Evidence from the complete genomic sequences of nine species. Genome Res 13:2242–2251PubMedCrossRefGoogle Scholar
  11. Duret L, Marais G, Biemont C (2000) Transposons but not retrotransposons are located preferentially in regions of high recombination rate in Caenorhabditis elegans. Genetics 156:1661–1669PubMedGoogle Scholar
  12. Duret L, Mouchiroud D (1999) Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, Arabidopsis. Proc Natl Acad Sci USA 96:4482–4487PubMedCrossRefGoogle Scholar
  13. Errede B, Company M, Hutchison CA (1987) Ty1 sequence with enhancer and mating–type–dependent regulatory activities. Mol Cell Biol 7:258–265PubMedGoogle Scholar
  14. Franchini LF, Ganko EW, McDonald JF (2004) Retrotransposon-gene associations are widespread among D. melanogaster populations. Mol Biol Evol 21:1323–1331PubMedGoogle Scholar
  15. Girard L, Freeling M (1999) Regulatory changes as a consequence of transposon insertion. Dev Genet 25:291–296PubMedCrossRefGoogle Scholar
  16. Hey J, Kliman RM (2002) Interactions between natural selection, recombination and gene density in the genes of Drosophila. Genetics 160:595–608PubMedGoogle Scholar
  17. Hill WG, Robertson A (1966) Effect of linkage on limits to artificial selection. Genet Res 8:269–294PubMedGoogle Scholar
  18. Ikemura T (1985) Codon usage and transfer-RNA content in unicellular and multicellular organisms. Mol Biol Evol 2:13–34PubMedGoogle Scholar
  19. Jakubczak JL, Burke WD, Eickbush TH (1991) Retrotransposable elements R1 and R2 interrupt the ribosomal-RNA genes of most insects. Proc Natl Acad Sci USA 88:3295–3299PubMedGoogle Scholar
  20. Jiang YW (2002) Transcriptional cosuppression of yeast Ty1 retrotransposons. Genes & Development 16:467–478PubMedGoogle Scholar
  21. Kaminker J, Bergman C, Kronmiller B, et al. (2002) The transposable elements of the Drosophila melanogaster euchromatin: a genomics perspective. Genome Biol 3:research0084.1–20PubMedCrossRefGoogle Scholar
  22. Kidwell MG, Lisch DR (2001) Perspective: Transposable elements, parasitic DNA, and genome evolution. Evolution 55:1–24PubMedGoogle Scholar
  23. Kliman RM, Hey J (2003) Hill–Robertson interference in Drosophila melanogaster: reply to Marais, Mouchiroud and Duret. Genet Res 81:89–90PubMedCrossRefGoogle Scholar
  24. Kreitman M (1983) Nucleotide polymorphism at the alcohol-dehydrogenase locus of Drosophila melanogaster. Nature 304:412–417PubMedCrossRefGoogle Scholar
  25. Langley CH, Montgomery E, Hudson R, Kaplan N, Charlesworth B (1988) On the role of unequal exchange in the containment of transposable element copy number. Genet Res 52:223–235PubMedCrossRefGoogle Scholar
  26. Lerat E, Rizzon C, Biemont C (2003) Sequence divergence within transposable element families in the Drosophila melanogaster genome. Genome Res 13:1889–1896PubMedGoogle Scholar
  27. Lerman DN, Michalak P, Helin AB, Bettencourt BR, Feder ME (2003) Modification of heat-shock gene expression in Drosophila melanogaster populations via transposable elements. Mol Biol Evol 20:135–144PubMedGoogle Scholar
  28. Li W–H (1997) Molecular evolution. Sinauer, Sunderland, MAGoogle Scholar
  29. Lynch M, Walsh JB (1997) Genetics and analysis of quantitative traits. Sinauer Associates, Sunderland, MAGoogle Scholar
  30. Marais G, Mouchiroud D, Duret L (2001) Does recombination improve selection on codon usage? Lessons from nematode and fly complete genomes. Proc Natl Acad Sci USA 98:5688–5692PubMedCrossRefGoogle Scholar
  31. Marais G, Mouchiroud D, Duret L (2003) Neutral effect of recombination on base composition in Drosophila. Genet Res 81:79–87PubMedCrossRefGoogle Scholar
  32. Martin E, Laloux H, Couette G, Alvarez T, Bessou C, Hauser O, Sookhareea S, Labouesse M, Segalat L (2002) Identification of 1088 new transposon insertions of Caenorhabditis elegans: A pilot study toward large-scale screens. Genetics 162:521–524PubMedGoogle Scholar
  33. McDonald JF, Matyunina LV, Wilson S, Jordan IK, Bowen NJ, Miller WJ (1997) LTR retrotransposons and the evolution of eukaryotic enhancers. Genetica 100:3–13PubMedCrossRefGoogle Scholar
  34. Medstrand P, van de Lagemaat LN, Mager DL (2002) Retroelement distributions in the human genome: Variations associated with age and proximity to genes. Genome Res 12:1483–1495PubMedCrossRefGoogle Scholar
  35. Montgomery E, Charlesworth B, Langley CH (1987) A test for the role of natural selection in the stabilization of transposable element copy number in a population of Drosophila melanogaster. Genet Res 49:31–41PubMedGoogle Scholar
  36. Pardue ML, DeBaryshe PG (1999) Drosophila telomeres: two transposable elements with important roles in chromosomes. Genetica 107:189–196PubMedCrossRefGoogle Scholar
  37. Petrov DA, Lozovskaya ER, Hartl DL (1996) High intrinsic: Rate of DNA loss in Drosophila. Nature 384:346–349PubMedCrossRefGoogle Scholar
  38. Petrov DA, Hartl DL (1998) High rate of DNA loss in the Drosophila melanogaster and Drosophila virilis species groups. Mol Biol Evol 15:293–302PubMedGoogle Scholar
  39. Petrov DA, Aminetzach YT, Davis JC, Bensasson D, Hirsh AE (2003) Size matters: Non-LTR retrotransposable elements and ectopic recombination in Drosophila. Mol Biol Evol 20:880–892PubMedGoogle Scholar
  40. Rizzon C, Marais G, Gouy M, Biemont C (2002) Recombination rate and the distribution of transposable elements in the Drosophila melanogaster genome. Genome Res 12:400–407PubMedCrossRefGoogle Scholar
  41. Rizzon C, Martin E, Marais G, Duret L, Segalat L, Biemont C (2003) Patterns of selection against transposons, inferred from the distribution of Tc1, Tc3 and Tc5 insertions in the mut-7 line of the nematode Caenorhabditis elegans. Genetics 165:1127–1135PubMedGoogle Scholar
  42. Schlenke TA, Begun DJ (2004) Strong selective sweep associated with a transposon insertion in Drosophila simulans. Proc Natl Acad Sci USA 101:1626–1631PubMedCrossRefGoogle Scholar
  43. Semon M, Duret L (2004) Evidence that functional transcription units cover at least half of the human genome. Trends Genet 20:229–232PubMedCrossRefGoogle Scholar
  44. Smit AFA (1999) Interspersed repeats and other mementos of transposable elements in mammalian genomes. Curr Opin Genet Dev 9:657–663PubMedCrossRefGoogle Scholar
  45. Sokal RR, Rohlf FJ (1995) Biometry. W.H. Freeman and Company, New YorkGoogle Scholar
  46. Spradling AC, Stern DM, Kiss I, Roote J, Laverty T, Rubin GM (1995) Gene disruptions using P transposable elements: An integral component of the Drosophila genome project. Proc Natl Acad Sci USA 92:10824–10830PubMedGoogle Scholar
  47. Stolc V, Gauhar Z, Mason C, et al. (2004) A gene expression map for the euchromatic genome of Drosophila melanogaster. Science 306:655–660PubMedCrossRefGoogle Scholar
  48. van de Lagemaat LN, Landry JR, Mager DL, Medstrand P (2003) Transposable elements in mammals promote regulatory variation and diversification of genes with specialized functions. Trends Genet 19:530–536PubMedGoogle Scholar
  49. Waterston RH, Lindblad-Toh K, Birney E, et al. (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420:520–562PubMedGoogle Scholar
  50. Wright SI, Agrawal N, Bureau TE (2003) Effects of recombination rate and gene density on transposable element distributions in Arabidopsis thaliana. Genome Res 13:1897–1903PubMedGoogle Scholar
  51. Yu N, Jensen–Seaman MI, Chemnick L, Ryder O, Li W–H (2004) Nucleotide diversity in gorillas. Genetics 166:1375–1383PubMedGoogle Scholar
  52. Zhao J, Hyman L, Moore C (1999) Formation of mRNA 3′ ends in eukaryotes: Mechanism, regulation, and interrelationships with other steps in mRNA synthesis. Microbiol Mol Biol Rev 63:405–445PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • Asher D. Cutter
    • 1
  • Jeffrey M. Good
    • 1
  • Christopher T. Pappas
    • 2
  • Matthew A. Saunders
    • 1
  • Dean M. Starrett
    • 3
  • Travis J. Wheeler
    • 3
  1. 1.Department of Ecology & Evolutionary BiologyUniversity of ArizonaTucsonUSA
  2. 2.Department of Molecular and Cellular BiologyUniversity of ArizonaTucsonUSA
  3. 3.Department of Computer ScienceUniversity of ArizonaTucsonUSA

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