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The C. elegans CSR-1 argonaute pathway counteracts epigenetic silencing to promote germline gene expression

ABSTRACT: Organisms can develop adaptive sequence-specific immunity by reexpressing pathogen-specific small RNAs that guide gene silencing. For example, the C. elegans PIWI-Argonaute/piwi-interacting RNA (piRNA) pathway recruits RNA-dependent RNA polymerase (RdRP) to foreign sequences to amplify a transgenerational small-RNA-induced epigenetic silencing signal (termed RNAe). Here, we provide evidence that, in addition to an adaptive memory of silenced sequences, C. elegans can also develop an opposing adaptive memory of expressed/self-mRNAs. We refer to this mechanism, which can prevent or reverse RNAe, as RNA-induced epigenetic gene activation (RNAa). We show that CSR-1, which engages RdRP-amplified small RNAs complementary to germline-expressed mRNAs, is required for RNAa. We show that a transgene with RNAa activity also exhibits accumulation of cognate CSR-1 small RNAs. Our findings suggest that C. elegans adaptively acquires and maintains a transgenerational CSR-1 memory that recognizes and protects self-mRNAs, allowing piRNAs to recognize foreign sequences innately, without the need for prior exposure.

ORGANISM(S): Caenorhabditis elegans

PROVIDER: GSE49532 | GEO | 2013/12/23

SECONDARY ACCESSION(S): PRJNA214176

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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The C. elegans CSR-1 argonaute pathway counteracts epigenetic silencing to promote germline gene expression

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