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Transposable Element Orientation Bias in the Drosophila melanogaster Genome

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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.

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Acknowledgments

We are grateful to H. Ochman for his critical advising and steadfast encouragement and to L. Duret for introducing us to the issue of TE orientation bias. We also thank the discussion and comments of the University of Arizona IGERT fellows, C. Bartolomé, B. Charlesworth, E. Lerat, D. Petrov, R. Reed, and several anonymous reviewers. This research was conducted as part of the University of Arizona NSF Integrative Graduate Education Research Training (IGERT) grant Genomics Initiative (DGE-0114420).

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Authors and Affiliations

  1. Department of Ecology & Evolutionary Biology, University of Arizona, Tucson, AZ, 85721, USA

    Asher D. Cutter, Jeffrey M. Good & Matthew A. Saunders

  2. Department of Molecular and Cellular Biology, University of Arizona, Tucson, AZ, 85721, USA

    Christopher T. Pappas

  3. Department of Computer Science, University of Arizona, Tucson, AZ, 85721, USA

    Dean M. Starrett & Travis J. Wheeler

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  1. Asher D. Cutter
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  2. Jeffrey M. Good
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Correspondence to Asher D. Cutter.

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[Reviewing Editor : Dr. Dmitri Petrov]

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Cutter, A.D., Good, J.M., Pappas, C.T. et al. Transposable Element Orientation Bias in the Drosophila melanogaster Genome. J Mol Evol 61, 733–741 (2005). https://doi.org/10.1007/s00239-004-0243-0

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  • DOI: https://doi.org/10.1007/s00239-004-0243-0

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