Retrotransposons and Their Recognition of pol II Promoters: A Comprehensive Survey of the Transposable Elements From the Complete Genome Sequence of Schizosaccharomyces pombe

  1. Nathan J. Bowen1,5,
  2. I. King Jordan2,
  3. Jonathan A. Epstein3,
  4. Valerie Wood4, and
  5. Henry L. Levin1,6
  1. 1 Section on Eukaryotic Transposable Elements, Laboratory of Gene Regulation and Development, National Institute of Child Health and Human Development (NICHD), National Institutes of Health (NIH), Bethesda, Maryland 20892, USA
  2. 2 National Center for Biotechnology Information, National Library of Medicine, NIH, Bethesda, Maryland 20894, USA
  3. 3 Unit on Biologic Computation, NICHD/OSD, NIH, Bethesda, Maryland 20892, USA
  4. 4 The Wellcome Trust Sanger Institute, The Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK

Abstract

The complete DNA sequence of the genome of Schizosaccharomyces pombe provides the opportunity to investigate the entire complement of transposable elements (TEs), their association with specific sequences, their chromosomal distribution, and their evolution. Using homology-based sequence identification, we found that the sequenced strain of S. pombe contained only one family of full-length transposons. This family, Tf2, consisted of 13 full-length copies of a long terminal repeat (LTR) retrotransposon. We found that LTR-LTR recombination of previously existing transposons had resulted in extensive populations of solo LTRs. These included 35 solo LTRs of Tf2, as well as 139 solo LTRs from other Tf families. Phylogenetic analysis of solo Tf LTRs reveals that Tf1 and Tf2 were the most recently active elements within the genome. The solo LTRs also served as footprints for previous insertion events by the Tf retrotransposons. Analysis of 186 genomic insertion events revealed a close association with RNA polymerase II promoters. These insertions clustered in the promoter-proximal regions of genes, upstream of protein coding regions by 100 to 400 nucleotides. The association of Tf insertions with pol II promoters was very similar to the preference previously observed for Tf1 integration. We found that the recently active Tf elements were absent from centromeres and pericentromeric regions of the genome containing tandem tRNA gene clusters. In addition, our analysis revealed that chromosome III has twice the density of insertion events compared to the other two chromosomes. Finally we describe a novel repetitive sequence, wtf, which was also preferentially located on chromosome III, and was often located near solo LTRs of Tf elements.

Footnotes

  • Article and publication are at http://www.genome.org/cgi/doi/10.1101/gr.1191603.

  • [Supplemental material is available at www.genome.org.]

  • 5 Present address: Department of Genetics, University of Georgia, Athens, GA 30602, USA.

  • 6 Corresponding author. E-MAIL henry_levin{at}nih.gov; FAX (301) 496-4491.

    • Accepted July 10, 2003.
    • Received January 17, 2003.
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