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

Colin C. Conine, James J. Moresco, Weifeng Gu, Masaki Shirayama, Darryl Conte, John R. Yates, Craig C. Mello

Research output: Contribution to journalArticle

76 Scopus citations

Abstract

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.

Original languageEnglish (US)
Pages (from-to)1532-1544
Number of pages13
JournalCell
Volume155
Issue number7
DOIs
Publication statusPublished - Dec 19 2013
Externally publishedYes

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ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)

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