Piwi Is Required during Drosophila Embryogenesis to License Dual-Strand piRNA Clusters for Transposon Repression in Adult Ovaries

Mol Cell. 2017 May 4;66(3):411-419.e4. doi: 10.1016/j.molcel.2017.03.017. Epub 2017 Apr 27.


Most piRNAs in the Drosophila female germline are transcribed from heterochromatic regions called dual-strand piRNA clusters. Histone 3 lysine 9 trimethylation (H3K9me3) is required for licensing piRNA production by these clusters. However, it is unclear when and how they acquire this permissive heterochromatic state. Here, we show that transient Piwi depletion in Drosophila embryos results in H3K9me3 decrease at piRNA clusters in ovaries. This is accompanied by impaired biogenesis of ovarian piRNAs, accumulation of transposable element transcripts, and female sterility. Conversely, Piwi depletion at later developmental stages does not disturb piRNA cluster licensing. These results indicate that the identity of piRNA clusters is epigenetically acquired in a Piwi-dependent manner during embryonic development, which is reminiscent of the widespread genome reprogramming occurring during early mammalian zygotic development.

Keywords: Drosophila embryo; H3K9me3; Piwi; epigenetics; heterochromatin; piRNA; reprogramming; transposable elements.

MeSH terms

  • Age Factors
  • Animals
  • Argonaute Proteins / genetics
  • Argonaute Proteins / metabolism*
  • Chromosomal Proteins, Non-Histone / genetics
  • Chromosomal Proteins, Non-Histone / metabolism
  • DNA Methylation*
  • DNA Transposable Elements*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / embryology
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / metabolism*
  • Epigenetic Repression*
  • Female
  • Fertility
  • Gene Expression Regulation, Developmental
  • Heterochromatin / genetics
  • Heterochromatin / metabolism*
  • Histones / metabolism
  • Infertility, Female / genetics
  • Infertility, Female / metabolism
  • Infertility, Female / physiopathology
  • Methylation
  • Morphogenesis
  • Ovary / embryology
  • Ovary / metabolism*
  • Protein Binding
  • RNA Interference*
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism*


  • Argonaute Proteins
  • Chromosomal Proteins, Non-Histone
  • DNA Transposable Elements
  • Drosophila Proteins
  • Heterochromatin
  • Histones
  • RNA, Small Interfering
  • piwi protein, Drosophila
  • rhi protein, Drosophila