Argonautes promote male fertility and provide a paternal memory of germline gene expression in C. elegans

Cell. 2013 Dec 19;155(7):1532-44. doi: 10.1016/j.cell.2013.11.032.


During each life cycle, germ cells preserve and pass on both genetic and epigenetic information. In C. elegans, the ALG-3/4 Argonaute proteins are expressed during male gametogenesis and promote male fertility. Here, we show that the CSR-1 Argonaute functions with ALG-3/4 to positively regulate target genes required for spermiogenesis. Our findings suggest that ALG-3/4 functions during spermatogenesis to amplify a small RNA signal that represents an epigenetic memory of male-specific gene expression. CSR-1, which is abundant in mature sperm, appears to transmit this memory to offspring. Surprisingly, in addition to small RNAs targeting male-specific genes, we show that males also harbor an extensive repertoire of CSR-1 small RNAs targeting oogenesis-specific mRNAs. Together, these findings suggest that C. elegans sperm transmit not only the genome but also epigenetic binary signals in the form of Argonaute/small RNA complexes that constitute a memory of gene expression in preceding generations.

Publication types

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

MeSH terms

  • Animals
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans Proteins / metabolism*
  • Epigenesis, Genetic*
  • Female
  • Male
  • RNA, Small Untranslated / metabolism
  • RNA-Binding Proteins / metabolism*
  • Signal Transduction
  • Spermatogenesis*
  • Spermatozoa
  • Transcription, Genetic


  • ALG-4 protein, C elegans
  • CSR-1 protein, C elegans
  • Caenorhabditis elegans Proteins
  • RNA, Small Untranslated
  • RNA-Binding Proteins
  • T22B3.2 protein, C elegans

Associated data

  • GEO/GSE49672