Coordination of transposon expression with DNA replication in the targeting of telomeric retrotransposons in Drosophila

EMBO J. 2014 May 16;33(10):1148-58. doi: 10.1002/embj.201386940. Epub 2014 Apr 14.

Abstract

In Drosophila, a group of retrotransposons is mobilized exclusively to telomeres in a sequence-independent manner. How they target chromosome ends is not understood. Here, we focused on the telomeric element HeT-A and characterized the cell cycle expression and cytological distribution of its protein and RNA products. We determined the timing of telomere replication by creating a single lacO-marked telomere and provide evidence suggesting that transposon expression and recruitment to telomeres is linked to telomere replication. The HeT-A-encoded ORF1p protein is expressed predominantly in S phase, particularly in early S phase. Orf1p binds HeT-A transcripts and forms spherical structures at telomeres undergoing DNA replication. HeT-A sphere formation requires Verrocchio, a putative homolog of the conserved Stn1 telomeric protein. Our results suggest that coupling of telomere elongation and telomere replication is a universal feature, and raise the possibility that transposon recruitment to Drosophila telomeres is mechanistically related to telomerase recruitment in other organisms. Our study also supports a co-adaptive relationship between the Drosophila host and HeT-A mobile elements.

Keywords: CST complex; Drosophila telomere; telomere replication; telomeric transposon.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Animals
  • DNA Replication / genetics
  • DNA Replication / physiology*
  • DNA Transposable Elements / genetics*
  • Drosophila / genetics
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Gene Expression Regulation*
  • Gene Products, gag / genetics
  • Gene Products, gag / metabolism
  • Retroelements / genetics*
  • Telomere / genetics*

Substances

  • DNA Transposable Elements
  • Drosophila Proteins
  • Gene Products, gag
  • HeT-A-gag protein, Drosophila
  • I-element-gag protein, Drosophila
  • Retroelements