A Small RNA-Catalytic Argonaute Pathway Tunes Germline Transcript Levels to Ensure Embryonic Divisions

Cell. 2016 Apr 7;165(2):396-409. doi: 10.1016/j.cell.2016.02.040. Epub 2016 Mar 24.

Abstract

Multiple division cycles without growth are a characteristic feature of early embryogenesis. The female germline loads proteins and RNAs into oocytes to support these divisions, which lack many quality control mechanisms operating in somatic cells undergoing growth. Here, we describe a small RNA-Argonaute pathway that ensures early embryonic divisions in C. elegans by employing catalytic slicing activity to broadly tune, instead of silence, germline gene expression. Misregulation of one target, a kinesin-13 microtubule depolymerase, underlies a major phenotype associated with pathway loss. Tuning of target transcript levels is guided by the density of homologous small RNAs, whose generation must ultimately be related to target sequence. Thus, the tuning action of a small RNA-catalytic Argonaute pathway generates oocytes capable of supporting embryogenesis. We speculate that the specialized nature of germline chromatin led to the emergence of small RNA-catalytic Argonaute pathways in the female germline as a post-transcriptional control layer to optimize oocyte composition.

Keywords: 22G RNA; Argonaute; C. elegans; CSR-1; centromere; chromosome; embryogenesis; fertility; germline; maternal load; oogenesis; small RNA.

Publication types

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

MeSH terms

  • Animals
  • Argonaute Proteins / metabolism
  • Base Sequence
  • Caenorhabditis elegans / cytology
  • Caenorhabditis elegans / embryology*
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans Proteins / metabolism
  • Cell Division
  • Embryo, Nonmammalian / cytology
  • Embryo, Nonmammalian / metabolism*
  • Embryonic Development
  • Female
  • Kinesins / metabolism
  • Metabolic Networks and Pathways*
  • Microtubules / metabolism
  • Molecular Sequence Data
  • Oocytes / metabolism*
  • RNA Processing, Post-Transcriptional

Substances

  • Argonaute Proteins
  • CSR-1 protein, C elegans
  • Caenorhabditis elegans Proteins
  • klp-7 protein, C elegans
  • Kinesins