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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 (AGO) proteins and their small-RNA cofactors are expressed during male gametogenesis and promote male fertility. Here we show that the CSR-1 AGO 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, while CSR-1, which is abundant in mature sperm, transmits 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 which genes were active in preceding generations.

ORGANISM(S): Caenorhabditis elegans

PROVIDER: GSE49672 | GEO | 2013/12/19

SECONDARY ACCESSION(S): PRJNA214695

REPOSITORIES: GEO

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Project description:Epigenetic inheritance is the transmission of information independently of the nucleotide sequence of the genome. A fundamental question in biology is to what extent does epigenetics contribute to trans-generational inheritance. Here we investigate the role of Argonaute-small-RNA pathways in epigenetic inheritance in the nematode C. elegans. Argonautes present their guide RNAs for base-pairing with target sequences and, upon binding, can cleave the target RNA and/or recruit cofactors that mediate post-transcriptional or transcriptional silencing 1,2. Previous studies have shown that Argonaute small-RNA pathways reinforce and maintain epigenetic silencing in C. elegans 3-5. For example, the conserved PIWI-related Argonaute PRG-1 initiates a remarkably stable mode of epigenetic silencing, termed RNA-induced epigenetic silencing (RNAe) 3. Alleles that are silenced by RNAe send trans-acting Argonaute-small-RNA signals that can act in a sequence-specific manner to induce the permanent Epigenetic inheritance is the transmission of information independently of the nucleotide sequence of the genome. A fundamental question in biology is to what extent does epigenetics contribute to trans-generational inheritance. Here we investigate the role of Argonaute-small-RNA pathways in epigenetic inheritance in the nematode C. elegans. Argonautes present their guide RNAs for base-pairing with target sequences and, upon binding, can cleave the target RNA and/or recruit cofactors that mediate post-transcriptional or transcriptional silencing 1,2. Previous studies have shown that Argonaute small-RNA pathways reinforce and maintain epigenetic silencing in C. elegans 3-5. For example, the conserved PIWI-related Argonaute PRG-1 initiates a remarkably stable mode of epigenetic silencing, termed RNA-induced epigenetic silencing (RNAe) 3. Alleles that are silenced by RNAe send trans-acting Argonaute-small-RNA signals that can act in a sequence-specific manner to induce the permanent silencing of homologous genes 3. Here we explore an opposite phenomenon, RNA-induced gene activation (RNAa), in which an expressed gene provides a sequence-specific signal that can activate a silent homologous gene. We provide evidence that the CSR-1 Argonaute is required for this trans-activating signal. CSR-1 engages antisense small RNAs complementary to most, if not all, germline-expressed mRNAs 6,7. Moreover, we show that the ability of a foreign sequence to mediate RNAa is correlated with acquisition of CSR-1-associated small RNAs targeting the foreign sequence. Thus CSR-1 small RNAs constitute a memory of previous germline-gene expression that protects endogenous genes from epigenetic silencing. These findings reveal a remarkably sophisticated epigenetic surveillance mechanism that monitors the flow of transgenerational information ensuring that progeny express only those genes also expressed in their parents. Examine small RNA population changes in different transgene lines

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

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