Har-P, a short P-element variant, weaponizes P-transposase to severely impair Drosophila development

Elife. 2019 Dec 17;8:e49948. doi: 10.7554/eLife.49948.

Abstract

Without transposon-silencing Piwi-interacting RNAs (piRNAs), transposition causes an ovarian atrophy syndrome in Drosophila called gonadal dysgenesis (GD). Harwich (Har) strains with P-elements cause severe GD in F1 daughters when Har fathers mate with mothers lacking P-element-piRNAs (i.e. ISO1 strain). To address the mystery of why Har induces severe GD, we bred hybrid Drosophila with Har genomic fragments into the ISO1 background to create HISR-D or HISR-N lines that still cause Dysgenesis or are Non-dysgenic, respectively. In these lines, we discovered a highly truncated P-element variant we named 'Har-P' as the most frequent de novo insertion. Although HISR-D lines still contain full-length P-elements, HISR-N lines lost functional P-transposase but retained Har-P's that when crossed back to P-transposase restores GD induction. Finally, we uncovered P-element-piRNA-directed repression on Har-P's transmitted paternally to suppress somatic transposition. The Drosophila short Har-P's and full-length P-elements relationship parallels the MITEs/DNA-transposase in plants and SINEs/LINEs in mammals.

Keywords: D. melanogaster; P-element; chromosomes; gene expression; genetics; genomics; gonadal dysgenesis; piRNA; transposon silencing.

Publication types

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

MeSH terms

  • Animals
  • DNA Transposable Elements / genetics*
  • Drosophila melanogaster / genetics*
  • Drosophila melanogaster / growth & development*
  • Female
  • Gene Dosage
  • Gene Silencing
  • Germ Cells / metabolism
  • Ovary / metabolism
  • Pupa / genetics
  • RNA, Small Interfering / genetics
  • Transposases / metabolism*

Substances

  • DNA Transposable Elements
  • RNA, Small Interfering
  • Transposases