Maelstrom Represses Canonical Polymerase II Transcription within Bi-directional piRNA Clusters in Drosophila melanogaster

Mol Cell. 2019 Jan 17;73(2):291-303.e6. doi: 10.1016/j.molcel.2018.10.038. Epub 2018 Dec 6.

Abstract

In Drosophila, 23-30 nt long PIWI-interacting RNAs (piRNAs) direct the protein Piwi to silence germline transposon transcription. Most germline piRNAs derive from dual-strand piRNA clusters, heterochromatic transposon graveyards that are transcribed from both genomic strands. These piRNA sources are marked by the heterochromatin protein 1 homolog Rhino (Rhi), which facilitates their promoter-independent transcription, suppresses splicing, and inhibits transcriptional termination. Here, we report that the protein Maelstrom (Mael) represses canonical, promoter-dependent transcription in dual-strand clusters, allowing Rhi to initiate piRNA precursor transcription. Mael also represses promoter-dependent transcription at sites outside clusters. At some loci, Mael repression requires the piRNA pathway, while at others, piRNAs play no role. We propose that by repressing canonical transcription of individual transposon mRNAs, Mael helps Rhi drive non-canonical transcription of piRNA precursors without generating mRNAs encoding transposon proteins.

Keywords: Argonaute; Armitage; Maelstrom; PIWI-interacting RNA; Piwi; Rhino; piRNA; small silencing RNA; transcription; transposon.

Publication types

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

MeSH terms

  • Animals
  • Argonaute Proteins / genetics
  • Argonaute Proteins / metabolism
  • Binding Sites
  • Chromosomal Proteins, Non-Histone / genetics
  • Chromosomal Proteins, Non-Histone / metabolism
  • DNA Transposable Elements*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / enzymology*
  • Drosophila melanogaster / genetics
  • Gene Expression Regulation
  • Promoter Regions, Genetic
  • Protein Binding
  • RNA Helicases / genetics
  • RNA Helicases / metabolism
  • RNA Polymerase II / genetics
  • RNA Polymerase II / metabolism*
  • RNA, Guide, CRISPR-Cas Systems
  • RNA, Messenger / biosynthesis*
  • RNA, Messenger / genetics
  • RNA, Small Interfering / biosynthesis*
  • RNA, Small Interfering / genetics
  • Transcription, Genetic*

Substances

  • Argonaute Proteins
  • Chromosomal Proteins, Non-Histone
  • DNA Transposable Elements
  • Drosophila Proteins
  • RNA, Messenger
  • RNA, Small Interfering
  • mael protein, Drosophila
  • piwi protein, Drosophila
  • rhi protein, Drosophila
  • RNA Polymerase II
  • armi protein, Drosophila
  • RNA Helicases