title: Argonautes promote male fertility and provide a paternal memory of germline gene expression in C. elegans.
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.
authors.affiliation: RNA Therapeutics Institute and Program in Molecular Medicine, University of Massachusetts Medical School, Worcester, MA 01605, USA.
authors.forename: Colin C
authors.initials: CC
authors.lastname: Conine
authors.affiliation: Department of Chemical Physiology, 10550 North Torrey Pines Road, SR11, The Scripps Research Institute, La Jolla, CA 92037, USA.
authors.forename: James J
authors.initials: JJ
authors.lastname: Moresco
authors.affiliation: RNA Therapeutics Institute and Program in Molecular Medicine, University of Massachusetts Medical School, Worcester, MA 01605, USA.
authors.forename: Weifeng
authors.initials: W
authors.lastname: Gu
authors.affiliation: RNA Therapeutics Institute and Program in Molecular Medicine, University of Massachusetts Medical School, Worcester, MA 01605, USA; Howard Hughes Medical Institute, Worcester, MA 01605, USA.
authors.forename: Masaki
authors.initials: M
authors.lastname: Shirayama
authors.affiliation: RNA Therapeutics Institute and Program in Molecular Medicine, University of Massachusetts Medical School, Worcester, MA 01605, USA.
authors.forename: Darryl
authors.initials: D
authors.lastname: Conte
authors.affiliation: Department of Chemical Physiology, 10550 North Torrey Pines Road, SR11, The Scripps Research Institute, La Jolla, CA 92037, USA.
authors.forename: John R
authors.initials: JR
authors.lastname: Yates
authors.affiliation: RNA Therapeutics Institute and Program in Molecular Medicine, University of Massachusetts Medical School, Worcester, MA 01605, USA; Howard Hughes Medical Institute, Worcester, MA 01605, USA. Electronic address: craig.mello@umassmed.edu.
authors.forename: Craig C
authors.initials: CC
authors.lastname: Mello
mesh_terms: D000818:Animals; D017173:Caenorhabditis elegans / Q000235:genetics / Q000378:metabolism*; D029742:Caenorhabditis elegans Proteins / Q000378:metabolism*; D044127:Epigenesis, Genetic; D005260:Female; D008297:Male; D058727:RNA, Small Untranslated / Q000378:metabolism; D016601:RNA-Binding Proteins / Q000378:metabolism*; D015398:Signal Transduction; D013091:Spermatogenesis; D013094:Spermatozoa; D014158:Transcription, Genetic
chemical_list: C548336:ALG-4 protein, C elegans; C544459:CSR-1 protein, C elegans; D029742:Caenorhabditis elegans Proteins; D058727:RNA, Small Untranslated; D016601:RNA-Binding Proteins; C548335:T22B3.2 protein, C elegans