Achilles, a New Family of Transcriptionally Active Retrotransposons from the Olive Fruit Fly, with Y Chromosome Preferential Distribution

PLoS One. 2015 Sep 23;10(9):e0137050. doi: 10.1371/journal.pone.0137050. eCollection 2015.

Abstract

Sex chromosomes have many unusual features relative to autosomes. The in depth exploration of their structure will improve our understanding of their origin and divergence (degeneration) as well as the evolution of genetic sex determination pathways which, most often are attributed to them. In Tephritids, the structure of Y chromosome, where the male-determining factor M is localized, is largely unexplored and limited data concerning its sequence content and evolution are available. In order to get insight into the structure and organization of the Y chromosome of the major olive insect pest, the olive fly Bactrocera oleae, we characterized sequences from a Pulse Field Gel Electrophoresis (PFGE)-isolated Y chromosome. Here, we report the discovery of the first olive fly LTR retrotransposon with increased presence on the Y chromosome. The element belongs to the BEL-Pao superfamily, however, its sequence comparison with the other members of the superfamily suggests that it constitutes a new family that we termed Achilles. Its ~7.5 kb sequence consists of the 5'LTR, the 5'non-coding sequence and the open reading frame (ORF), which encodes the polyprotein Gag-Pol. In situ hybridization to the B. oleae polytene chromosomes showed that Achilles is distributed in discrete bands dispersed on all five autosomes, in all centromeric regions and in the granular heterochromatic network corresponding to the mitotic sex chromosomes. The between sexes comparison revealed a variation in Achilles copy number, with male flies possessing 5-10 copies more than female (CI range: 18-38 and 12-33 copies respectively per genome). The examination of its transcriptional activity demonstrated the presence of at least one intact active copy in the genome, showing a differential level of expression between sexes as well as during embryonic development. The higher expression was detected in male germline tissues (testes). Moreover, the presence of Achilles-like elements in different species of the Tephritidae family suggests an ancient origin of this element.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Aspartic Acid Proteases / chemistry
  • Aspartic Acid Proteases / genetics
  • Aspartic Acid Proteases / metabolism
  • Gene Dosage
  • Genome, Insect
  • Insect Proteins / chemistry
  • Insect Proteins / genetics*
  • Insect Proteins / metabolism
  • Molecular Sequence Data
  • Phylogeny
  • Retroelements*
  • Tephritidae / genetics*
  • Tephritidae / metabolism
  • Transcription, Genetic*
  • Transcriptional Activation
  • Y Chromosome / genetics*

Substances

  • Insect Proteins
  • Retroelements
  • Aspartic Acid Proteases

Grants and funding

This work was partially supported by a grant from the Hellenic General Secretariat of Research and Technology (99 ED529), the Pythagoras II grant from the Greek Ministry of National Education and Religious Affairs and the two Graduate Programs of the Biochemistry and Biotechnology Department of the University of Thessaly (‘Biotechnology - Nutrition and Environment’ and ‘Molecular Biology and Genetics applications’). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.