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A Small RNA-Catalytic Argonaute Pathway Tunes Germline Transcript Levels to Ensure Embryonic Divisions

ABSTRACT: Multiple division cycles without growth are a characteristic feature of early embryogenesis. The female germline deposits proteins and RNAs into oocytes to support these divisions, which lack many of the quality control mechanisms operating in somatic cells undergoing growth. How the composition of the oocyte maternal load is regulated to ensure its ability to support early embryogenesis is not known. Here we describe a small RNA-Argonaute pathway, operating in the C. elegans germline, that ensures early embryonic divisions by employing catalytic slicing activity to broadly tune, instead of silence, germline gene expression. Misregulation of one target, a kinesin-13 microtubule depolymerase, underlies a major embryonic phenotype associated with pathway loss. Tuning of target expression is guided by small RNA density, which must ultimately be related to target sequence. Thus, C. elegans employs a single catalytic Argonaute for small RNA-mediated tuning of the mRNA levels of germline-expressed genes that support early embryogenesis.

ORGANISM(S): Caenorhabditis elegans

PROVIDER: GSE75128 | GEO | 2016/03/24

SECONDARY ACCESSION(S): PRJNA302596

REPOSITORIES: GEO

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A Small RNA-Catalytic Argonaute Pathway Tunes Germline Transcript Levels to Ensure Embryonic Divisions

Project description:Multiple division cycles without growth are a characteristic feature of early embryogenesis. The female germline deposits proteins and RNAs into oocytes to support these divisions, which lack many of the quality control mechanisms operating in somatic cells undergoing growth. How the composition of the oocyte maternal load is regulated to ensure its ability to support early embryogenesis is not known. Here we describe a small RNA-Argonaute pathway, operating in the C. elegans germline, that ensures early embryonic divisions by employing catalytic slicing activity to broadly tune, instead of silence, germline gene expression. Misregulation of one target, a kinesin-13 microtubule depolymerase, underlies a major embryonic phenotype associated with pathway loss. Tuning of target expression is guided by small RNA density, which must ultimately be related to target sequence. Thus, C. elegans employs a single catalytic Argonaute for small RNA-mediated tuning of the mRNA levels of germline-expressed genes that support early embryogenesis. mRNA profiling of 2 replicates each for 3 genotypes of adult-stage C. elegans worms

2016-03-24 | E-GEOD-75128 | biostudies-arrayexpress

Caenorhabditis elegans

Project description:A Small RNA-Catalytic Argonaute Pathway Tunes Germline Transcript Levels to Ensure Embryonic Divisions

| PRJNA302596 | ENA

CSR-1A post-translational modification

Project description:CSR-1 is an essential Argonaute protein that binds to a subclass of 22G-RNAs targeting most germline-expressed genes. Here we show that the two isoforms of CSR-1 have distinct expression patterns; CSR-1B is ubiquitously expressed throughout the germline and during all stages of development while CSR-1A expression is restricted to germ cells undergoing spermatogenesis. Furthermore, CSR-1A associates preferentially with 22G-RNAs mapping to spermatogenesis-specific genes whereas CSR-1B-bound small RNAs map predominantly to oogenesis-specific genes. Interestingly, the exon unique to CSR-1A contains multiple dimethylarginine modifications, which are necessary for the preferential binding of CSR-1A to spermatogenesis-specific 22G-RNAs. Thus, we have discovered a regulatory mechanism for C. elegans Argonaute proteins that allows for specificity of small RNA binding between similar Argonaute proteins with overlapping temporal and spatial localization.

2021-06-17 | PXD021227 | Pride

A cytoplasmic Argonaute protein promotes the inheritance of RNAi

Project description:RNAi-elicited gene silencing is heritable and can persist for multiple generations after its initial induction in C. elegans. However, the mechanism by which parental-acquired trait-specific information from RNAi is inherited by the progenies is not fully understood. Here, we identified a cytoplasmic Argonaute protein, WAGO-4, necessary for the inheritance of RNAi. WAGO-4 exhibits asymmetrical translocation to the germline during early embryogenesis, accumulates at the perinuclear foci in the germline, and is required for the inheritance of exogenous RNAi targeting both germline- and soma-expressed genes. WAGO-4 binds to 22G-RNA and its mRNA targets. Interestingly, WAGO-4-associated endogenous 22G-RNA targets the same cohort of germline genes as CSR-1 and similarly contains untemplated addition of uracil at the 3' ends. The poly(U) polymerase CDE-1 is required for the untemplated polyuridylation of WAGO-4-associated 22G-RNAs and inheritance of RNAi. Therefore, we conclude that the cytoplasmic Argonaute protein WAGO-4 also promotes the inheritance of RNAi in addition to the nuclear RNAi pathway.

2018-04-28 | GSE112475 | GEO

A family of C. elegans VASA homologs control Argonaute pathway specificity and promote transgenerational silencing

Project description:Germline Argonautes direct transcriptome surveillance within peri-nuclear membraneless organelles called nuage. In C. elegans, a family of Vasa-related Germ Line Helicase (GLH) proteins localize in, and promote the formation of nuage called P granules. Previous studies have implicated GLH proteins in inherited silencing but direct roles in amplification of small RNAs, or in target mRNA or Argonatue binding have not been identified. Here we show that GLH proteins compete with each other to control Argonaute pathway specificity, bind directly to Argonaute-target mRNAs and act to promote the amplification of small RNAs required for transgenerational inheritance. We show that the ATPase cycle of GLH-1 regulates its direct binding to the Argonaute WAGO-1 which engages amplified small RNAs. Our findings support a dynamic and direct role for GLH proteins in inherited silencing beyond their role as structural components of nuage.

2022-01-30 | GSE195536 | GEO

A family of C. elegans VASA homologs control Argonaute pathway specificity and promote transgenerational silencing [IP small-RNA seq]

2022-03-10 | GSE198101 | GEO

Translation and codon usage regulate Argonaute slicer activity to trigger small RNA biogenesis

Project description:In the Caenorhabditis elegans germline, thousands of mRNAs are concomitantly expressed with antisense 22G-RNAs, which are loaded into the Argonaute CSR-1. Despite their essential functions for animal fertility and embryonic development, how CSR-1 22G-RNAs are produced remains unknown. Here, we show that CSR-1 slicer activity is primarily involved in triggering the synthesis of small RNAs on the coding sequences of germline mRNAs and post-transcriptionally regulates a fraction of targets. CSR-1-cleaved mRNAs prime the RNA-dependent RNA polymerase, EGO-1, to synthesize 22G-RNAs in phase with ribosome translation in the cytoplasm, in contrast to other 22G-RNAs mostly synthesized in germ granules. Moreover, codon optimality and efficient translation antagonize CSR-1 slicing and 22G-RNAs biogenesis. We propose that codon usage differences encoded into mRNA sequences might be a conserved strategy in eukaryotes to regulate small RNA biogenesis and Argonaute targeting

2021-04-23 | PXD020293 | Pride

Cues from mRNA splicing prevent default Argonaute silencing in C. elegans

Project description:In animals Argonaute small-RNA pathways scan germline transcripts to silence self-replicating genetic elements. Little is known however about how endogenous gene expression is recognized and licensed. Here we show that the presence of introns and by inference the process of mRNA splicing prevents default Argonaute-mediated silencing in the C. elegans germline. Silencing of intronless genes is initiated independently of the piRNA pathway but nevertheless engages multiple components of the downstream amplification and maintenance mechanisms that mediate transgenerational silencing including both nuclear and cytoplasmic members of the worm-specific Argonaute gene family (WAGOs). Small RNAs amplified from intronless mRNAs can trans-silence cognate intron-containing genes. Interestingly, a second small RNA-independent cis-acting mode of silencing also acts on intronless mRNAs. Our findings suggest that cues put in place during mRNA splicing license germline gene expression and provide evidence for a splicing-dependent and dsRNA- and piRNA-independent mechanism that can program Argonaute silencing.

2021-06-28 | GSE178985 | GEO

C. elegans piRNAs mediate the genome-wide surveillance of germline transcripts

Project description:Piwi Argonautes and Piwi-interacting RNAs (piRNAs) mediate genome defense by targeting transposons. However, many piRNA species lack obvious sequence complementarity to transposons or other loci. For example, only one C. elegans transposon is a known piRNA target. Here we show that, in mutants lacking the Piwi Argonaute PRG-1 and associated piRNAs (21U-RNAs), many silent loci in the germline exhibit increased levels of mRNA expression and depletion of an amplified RNAdependent RNA polymerase (RdRP)-derived species of small RNA termed 22G-RNAs. Sequences depleted of 22G-RNAs are enriched nearby potential target sites that base pair imperfectly but extensively to 21U-RNAs. We show that PRG-1 is required to initiate, but not to maintain, silencing of transgenes engineered to contain complementarity to endogenous 21U-RNAs. Our findings support a model in which C. elegans piRNAs utilize their enormous repertoire of targeting capacity to scan the germline transcriptome for foreign sequences, while endogenous germline-expressed genes are actively protected from piRNA-induced silencing. Examine small RNA population changes in prg-1 and rescued strains

2012-09-01 | E-GEOD-38723 | biostudies-arrayexpress

The activity of the Caenorhabditis elegans Aquarius helicase EMB-4 enables the nuclear RNAi machinery to engage nascent RNA

Project description:Germline small RNA pathways initiate silencing of repetitive elements in animals and an interplay of nuclear small RNAs and chromatin modifications maintain this silencing, protecting the germline from spreading of transposable elements. In C. elegans germline, nuclear argonaute protein HRDE-1 initiates the transcriptional silencing pathway that is crucial for long term and heritable silencing of genes and repetitive regions. Here, we show that HRDE-1 interacts with components of the splicing machinery and the exon-junction complex. One such factor is the conserved RNA helicase EMB-4/AQR that binds introns and recruits the exon-junction proteins to newly spliced RNA. Our data shows that EMB-4/AQR is required for the transcriptional silencing pathway initiated by HRDE-1 and it functions by removing the intronic barriers to silencing thorugh its helicase function.

2017-06-30 | PXD004416 | Pride

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