The absence of core piRNA biogenesis factors does not impact efficient transposon silencing in Drosophila

PLoS Biol. 2023 Jun 6;21(6):e3002099. doi: 10.1371/journal.pbio.3002099. eCollection 2023 Jun.

Abstract

Organisms require mechanisms to distinguish self and non-self-RNA. This distinction is crucial to initiate the biogenesis of Piwi-interacting RNAs (piRNAs). In Drosophila ovaries, PIWI-guided slicing and the recognition of piRNA precursor transcripts by the DEAD-box RNA helicase Yb are the 2 known mechanisms to licence an RNA for piRNA biogenesis in the germline and the soma, respectively. Both the PIWI proteins and Yb are highly conserved across most Drosophila species and are thought to be essential to the piRNA pathway and for silencing transposons. However, we find that species closely related to Drosophila melanogaster have lost the yb gene, as well as the PIWI gene Ago3. We show that the precursor RNA is still selected in the absence of Yb to abundantly generate transposon antisense piRNAs in the soma. We further demonstrate that Drosophila eugracilis, which lacks Ago3, is completely devoid of ping-pong piRNAs and exclusively produces phased piRNAs in the absence of slicing. Thus, core piRNA pathway genes can be lost in evolution while still maintaining efficient transposon silencing.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Argonaute Proteins / genetics
  • Argonaute Proteins / metabolism
  • DNA Transposable Elements / genetics
  • Drosophila Proteins* / genetics
  • Drosophila Proteins* / metabolism
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / metabolism
  • Drosophila* / metabolism
  • Piwi-Interacting RNA
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism

Substances

  • Piwi-Interacting RNA
  • Drosophila Proteins
  • RNA, Small Interfering
  • Argonaute Proteins
  • DNA Transposable Elements

Grants and funding

This work was supported by Australian Research Council (https://www.arc.gov.au/, DP210102385) to RH, Australian National University start-up (https://www.anu.edu.au/) to RH, and Australian National University Vice-Chancellor's travel fellowship (https://www.anu.edu.au/study/scholarships/find-a-scholarship/vice-chancellors-hdr-travel-grants) to SC. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.