Expression of the Retrotransposon Helena Reveals a Complex Pattern of TE Deregulation in Drosophila Hybrids

PLoS One. 2016 Jan 26;11(1):e0147903. doi: 10.1371/journal.pone.0147903. eCollection 2016.

Abstract

Transposable elements (TEs), repeated mobile sequences, are ubiquitous in the eukaryotic kingdom. Their mobilizing capacity confers on them a high mutagenic potential, which must be strongly regulated to guarantee genome stability. In the Drosophila germline, a small RNA-mediated silencing system, the piRNA (Piwi-interacting RNA) pathway, is the main responsible TE regulating mechanism, but some stressful conditions can destabilize it. For instance, during interspecific hybridization, genomic stress caused by the shock of two different genomes can lead, in both animals and plants, to higher transposition rates. A recent study in D. buzatii-D. koepferae hybrids detected mobilization of 28 TEs, yet little is known about the molecular mechanisms explaining this transposition release. We have characterized one of the mobilized TEs, the retrotransposon Helena, and used quantitative expression to assess whether its high transposition rates in hybrids are preceded by increased expression. We have also localized Helena expression in the gonads to see if cellular expression patterns have changed in the hybrids. To give more insight into changes in TE regulation in hybrids, we analysed Helena-specific piRNA populations of hybrids and parental species. Helena expression is not globally altered in somatic tissues, but male and female gonads have different patterns of deregulation. In testes, Helena is repressed in F1, increasing then its expression up to parental values. This is linked with a mislocation of Helena transcripts along with an increase of their specific piRNA levels. Ovaries have additive levels of Helena expression, but the ping-pong cycle efficiency seems to be reduced in F1 hybrids. This could be at the origin of new Helena insertions in hybrids, which would be transmitted to F1 hybrid female progeny.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Base Sequence
  • Chimera / genetics
  • DNA Transposable Elements / genetics*
  • Drosophila / classification
  • Drosophila / genetics*
  • Female
  • Gene Expression Regulation*
  • In Situ Hybridization, Fluorescence
  • Male
  • Molecular Sequence Data
  • Ovary / metabolism
  • Phylogeny
  • RNA, Small Interfering / metabolism
  • Real-Time Polymerase Chain Reaction
  • Retroelements / genetics*
  • Testis / metabolism

Substances

  • DNA Transposable Elements
  • RNA, Small Interfering
  • Retroelements

Grants and funding

This work was supported by research grant CGL2013-42432-P from the Ministerio de Economía y Competitividad (Spain) and grant 2014 SGR 1346 from Generalitat de Catalunya to the Grup de Genòmica, Bioinformàtica i Biologia Evolutiva (GGBE). VRS was supported by a PIF PhD fellowship from the Universitat Autònoma de Barcelona (Spain). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.