Positive selection of yeast nonhomologous end-joining genes and a retrotransposon conflict hypothesis

  1. Sara L. Sawyer and
  2. Harmit S. Malik
  1. Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA 98109
  1. Edited by Susan R. Wessler, University of Georgia, Athens, GA, and approved September 14, 2006 (received for review June 30, 2006)

Abstract

Transposable elements have clearly played a major role in shaping both the size and organization of eukaryotic genomes. However, the evolution of essential genes in core biological processes may also have been shaped by coevolution with these elements. This would be predicted to occur in instances where host proteins are either hijacked for use by mobile elements or recruited to defend against them. To detect such cases, we have used the Saccharomyces cerevisiaeSaccharomyces paradoxus sibling species pair to identify genes that have evolved under positive selection. We identify 72 such genes, which participate in a variety of biological processes but are enriched for genes involved in meiosis and DNA repair by nonhomologous end-joining (NHEJ). We confirm the signature of positive selection acting on NHEJ genes using orthologous sequences from all seven Saccharomyces sensu stricto species. Previous studies have found altered rates of Ty retrotransposition when these NHEJ genes are disrupted. We propose that the evolution of these repair proteins is likely to have been shaped by their interactions with Ty elements. Antagonistic pleiotropy, where critical genes like those involved in DNA repair are also subject to selective pressures imposed by mobile elements, could favor alleles that might be otherwise deleterious for their normal roles related to genome stability.

Footnotes

  • To whom correspondence should be addressed at:
    1100 Fairview Avenue North, A1-162, Seattle, WA 98109.
    E-mail: hsmalik{at}fhcrc.org
  • Author contributions: S.L.S. and H.S.M. designed research; S.L.S. performed research; S.L.S. and H.S.M. analyzed data; and S.L.S. and H.S.M. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS direct submission.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. DQ889943DQ889967).

  • Abbreviations:
    GO,
    gene ontology;
    NHEJ,
    nonhomologous end-joining;
    PIC,
    preintegration complex;
    DSB,
    double-strand break.
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