An essential role for the piRNA pathway in regulating the ribosomal RNA pool in C. elegans

Dev Cell. 2021 Aug 23;56(16):2295-2312.e6. doi: 10.1016/j.devcel.2021.07.014. Epub 2021 Aug 12.

Abstract

Piwi-interacting RNAs (piRNAs) are RNA effectors with key roles in maintaining genome integrity and promoting fertility in metazoans. In Caenorhabditis elegans loss of piRNAs leads to a transgenerational sterility phenotype. The plethora of piRNAs and their ability to silence transcripts with imperfect complementarity have raised several (non-exclusive) models for the underlying drivers of sterility. Here, we report the extranuclear and transferable nature of the sterility driver, its suppression via mutations disrupting the endogenous RNAi and poly-uridylation machinery, and copy-number amplification at the ribosomal DNA locus. In piRNA-deficient animals, several small interfering RNA (siRNA) populations become increasingly overabundant in the generations preceding loss of germline function, including ribosomal siRNAs (risiRNAs). A concomitant increase in uridylated sense rRNA fragments suggests that poly-uridylation may potentiate RNAi-mediated gene silencing of rRNAs. We conclude that loss of the piRNA machinery allows for unchecked amplification of siRNA populations, originating from abundant highly structured RNAs, to deleterious levels.

Keywords: endo-siRNAs; piRNAs; poly-uridylation; rDNA copy number maintenance; small RNA pathways; transgenerational inheritance.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caenorhabditis elegans
  • Epigenesis, Genetic
  • Female
  • Fertility / genetics
  • Oogonial Stem Cells / cytology
  • Oogonial Stem Cells / metabolism
  • RNA Processing, Post-Transcriptional
  • RNA, Ribosomal / genetics*
  • RNA, Ribosomal / metabolism
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism*

Substances

  • RNA, Ribosomal
  • RNA, Small Interfering