The RNA polymerase II subunit RPB-9 recruits the integrator complex to terminate Caenorhabditis elegans piRNA transcription

EMBO J. 2021 Mar 1;40(5):e105565. doi: 10.15252/embj.2020105565. Epub 2021 Feb 3.

Abstract

PIWI-interacting RNAs (piRNAs) are genome-encoded small RNAs that regulate germ cell development and maintain germline integrity in many animals. Mature piRNAs engage Piwi Argonaute proteins to silence complementary transcripts, including transposable elements and endogenous genes. piRNA biogenesis mechanisms are diverse and remain poorly understood. Here, we identify the RNA polymerase II (RNA Pol II) core subunit RPB-9 as required for piRNA-mediated silencing in the nematode Caenorhabditis elegans. We show that rpb-9 initiates heritable piRNA-mediated gene silencing at two DNA transposon families and at a subset of somatic genes in the germline. We provide genetic and biochemical evidence that RPB-9 is required for piRNA biogenesis by recruiting the Integrator complex at piRNA genes, hence promoting transcriptional termination. We conclude that, as a part of its rapid evolution, the piRNA pathway has co-opted an ancient machinery for high-fidelity transcription.

Keywords: rpb-9; RNA polymerase II; integrator; piRNAs; transcription termination.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism*
  • Gene Expression Regulation*
  • Gene Silencing*
  • Germ Cells
  • Promoter Regions, Genetic
  • Protein Subunits
  • RNA Polymerase II / genetics
  • RNA Polymerase II / metabolism*
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism*
  • Transcription, Genetic*

Substances

  • Caenorhabditis elegans Proteins
  • Protein Subunits
  • RNA, Small Interfering
  • RNA Polymerase II