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CSR-1 and P granules suppress sperm-specific transcription in the C. elegans germline

ABSTRACT: P granules in C. elegans are required for fertility and function to maintain germ cell identity and pluripotency. Sterility in the absence of P granules is often accompanied by the mis-expression of soma-specific proteins and the initiation of somatic differentiation in germ cells. To investigate whether this is caused by the accumulation of somatic transcripts, we performed mRNA-seq on dissected germlines with and without P granules. Strikingly, we found that somatic transcripts do not increase in the young adult germline when P granules are impaired. Instead, we found that impairing P granules causes sperm-specific mRNAs to become highly overexpressed. This includes the accumulation of major sperm protein (MSP) transcripts in germ cells, a phenotype that is suppressed by feminization of the germline. A core component of P granules, the endo-siRNA-binding Argonaute protein CSR-1, has recently been ascribed with the ability to license transcripts for germline expression. However, impairing CSR-1 has very little effect on the accumulation of its mRNA targets. Instead, we found that CSR-1 functions with P granules to prevent MSP and sperm-specific mRNAs from being transcribed in the hermaphrodite germline. These findings suggest that P granules protect germline integrity through two different mechanisms, by 1) preventing the inappropriate expression of somatic proteins at the level of translational regulation, and by 2) functioning with CSR-1 to limit the domain of sperm-specific expression at the level of transcription.

ORGANISM(S): Caenorhabditis elegans

PROVIDER: GSE67954 | GEO | 2015/05/20

SECONDARY ACCESSION(S): PRJNA281372

REPOSITORIES: GEO

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CSR-1 and P granules suppress sperm-specific transcription in the C. elegans germline

Project description:P granules in C. elegans are required for fertility and function to maintain germ cell identity and pluripotency. Sterility in the absence of P granules is often accompanied by the mis-expression of soma-specific proteins and the initiation of somatic differentiation in germ cells. To investigate whether this is caused by the accumulation of somatic transcripts, we performed mRNA-seq on dissected germlines with and without P granules. Strikingly, we found that somatic transcripts do not increase in the young adult germline when P granules are impaired. Instead, we found that impairing P granules causes sperm-specific mRNAs to become highly overexpressed. This includes the accumulation of major sperm protein (MSP) transcripts in germ cells, a phenotype that is suppressed by feminization of the germline. A core component of P granules, the endo-siRNA-binding Argonaute protein CSR-1, has recently been ascribed with the ability to license transcripts for germline expression. However, impairing CSR-1 has very little effect on the accumulation of its mRNA targets. Instead, we found that CSR-1 functions with P granules to prevent MSP and sperm-specific mRNAs from being transcribed in the hermaphrodite germline. These findings suggest that P granules protect germline integrity through two different mechanisms, by 1) preventing the inappropriate expression of somatic proteins at the level of translational regulation, and by 2) functioning with CSR-1 to limit the domain of sperm-specific expression at the level of transcription. Four biological replicates of each condition (empty vector control, P granule RNAi, and CSR-1 RNAi germlines) were collected for total RNA.

2015-05-20 | E-GEOD-67954 | biostudies-arrayexpress

elli-1 gene expression array

Project description:Germ cells contain non-membrane bound cytoplasmic organelles that help maintain germline integrity. In C. elegans they are called P granules; without them, the germline undergoes partial masculinization or aberrant differentiation. One key P-granule component is the Argonaute CSR-1, a small-RNA binding protein that antagonizes accumulation of sperm-specific transcripts in developing oocytes. Loss of CSR-1 or components of its pathway results in a very specific, enlarged P-granule phenotype. In a forward screen to identify mutants with abnormal P granules, ten alleles were recovered with csr-1 P-granule phenotypes, eight of which contain mutations in known CSR-1 pathway components (csr-1, ego-1, ekl-1, and drh-3). The remaining two alleles are in a novel gene now called elli-1 (enlarged germline granules). ELLI-1 is first expressed in primordial germ cells during mid-embryogenesis and continues to be expressed in the adult germline. While ELLI-1 forms cytoplasmic aggregates, they occasionally dock, but do not co-localize with P granules. Instead, the majority of ELLI-1 aggregates accumulate in the shared germline cytoplasm. In elli-1 mutants, several genes that promote RNAi and P-granule accumulation are upregulated, and embryonic lethality, sterility, and RNAi resistance in a hypomorphic drh-3 allele is enhanced. Like mutations in other CSR-1 pathway components, elli-1 is an enhancer of glp-1 sterility, suggesting that ELLI-1 functions with the CSR-1 pathway to modulate RNAi activity, P-granule accumulation, and post-transcriptional expression in the germline.

2016-06-08 | GSE82322 | GEO

Protein interactors of MEG-1 in C. elegans embryos

Project description:In animals with germ plasm, specification of the germline involves “germ granules”, cytoplasmic condensates that enrich maternal transcripts in the germline founder cells. In C. elegans embryos, P granules enrich maternal transcripts, but surprisingly P granules are not essential for germ cell fate specification. Here we have described a second condensate in the C. elegans germ plasm. Like canonical P-bodies found in somatic cells, “germline P-bodies” contain regulators of mRNA decapping and deadenylation and, in addition, the intrinsically-disordered proteins MEG-1 and MEG-2 and the TIS11-family RNA-binding protein POS-1. Embryos lacking meg-1 and meg-2 do not stabilize P-body components, miss-regulate POS-1 targets, miss-specify the germline founder cell, and do not develop a germline. Our findings suggest that specification of the germ line involves at least two distinct condensates that independently enrich and regulate maternal mRNAs in the germline founder cells.

2022-10-05 | PXD036610 | Pride

Specialized germline P-bodies are required to specify germ cell fate in C. elegans embryos

Project description:In animals with germ plasm, specification of the germline involves “germ granules”, cytoplasmic condensates that enrich maternal transcripts in the germline founder cells. In C. elegans embryos, P granules enrich maternal transcripts, but surprisingly P granules are not essential for germ cell fate specification. Here we describe a second condensate in the C. elegans germ plasm. Like canonical P-bodies found in somatic cells, “germline P-bodies” contain regulators of mRNA decapping and deadenylation and, in addition, the intrinsically-disordered proteins MEG-1 and MEG-2 and the TIS11-family RNA-binding protein POS-1. Embryos lacking meg-1 and meg-2 do not stabilize P-body components, miss-regulate POS-1 targets, miss-specify the germline founder cell, and do not develop a germline. Our findings suggest that specification of the germ line involves at least two distinct condensates that independently enrich and regulate maternal mRNAs in the germline founder cells.

2022-10-04 | GSE211555 | 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

Germ granule association drives small RNA specificity for a nuclear Argonaute protein

Project description:RNA interference (RNAi) is a conserved gene silencing process that exists in diverse organisms to protect genome integrity and regulate gene expression. In C. elegans, the majority of RNAi pathway proteins localize to perinuclear, phase-separated germ granules, which are comprised of sub-domains referred to as P granules, Mutator foci, Z granules, and SIMR foci. However, the protein components and function of the newly discovered SIMR foci are unknown. Here we demonstrate that HRDE-2 localizes to SIMR foci and interacts with the germline nuclear RNAi Argonaute HRDE-1. Furthermore, HRDE-1 also localizes to SIMR foci, dependent on HRDE-2, but only in its small RNA unbound state. This germ granule localization is critical to promote the small RNA binding specificity of HRDE-1 and, in the absence of HRDE-2, HRDE-1 exclusively loads CSR-class 22G-RNAs rather than WAGO-class 22G-RNAs, resulting in H3K9me3 deposition on CSR-target genes. Thus, our study demonstrates that HRDE-2 is critical to ensure that the correct small RNAs are used to guide nuclear RNA silencing in the C. elegans germline.

2023-07-27 | MSV000092546 | MassIVE

Transcriptome profiling of sterile daf-2; mes-1 double vs. mes-1 single mutants

Project description:The germ lineage is considered to be immortal. In the quest to extend lifespan, a possible strategy is to drive germline traits in somatic cells, to try to confer some of the germ lineage’s immortality on the somatic body. Notably, a study in C. elegans suggested that expression of germline genes in the somatic cells of long-lived daf-2 mutants confers some of daf-2’s longevity. Specifically, mRNAs encoding components of C. elegans germ granules (P granules) were up-regulated in daf-2 mutant worms, and knock-down of individual P-granule and other germline genes in daf-2 young adults modestly reduced their lifespan. We investigated the contribution of a germline program to daf-2’s long lifespan, and also tested if other mutants known to express germline genes in their somatic cells are long-lived. Our key findings are: 1) We could not detect P-granule proteins in the somatic cells of daf-2 mutants by immunostaining or by expression of a P-granule transgene. 2) Whole-genome transcript profiling of animals lacking a germline revealed that germline transcripts are not up-regulated in the soma of daf-2 worms compared to the soma of control worms. 3) Simultaneous removal of multiple P-granule proteins or the entire germline program from daf-2 worms did not reduce their lifespan. 4) Several mutants that robustly express a broad spectrum of germline genes in their somatic cells are not long-lived. Taken together, our findings argue against the hypothesis that acquisition of a germ cell program in somatic cells increases lifespan and contributes to daf-2’s longevity.

2016-01-20 | GSE76946 | GEO

C. elegans germ granules regulate both germline and somatic RNAome [RNA-Seq]

Project description:Germ granules are membrane-less organelles essential for small RNA biogenesis and germline development. Among the conserved properties of germ granules is their association with the nuclear membrane. Recent studies demonstrated that LOTUS domain proteins, EGGD-1 and EGGD-2 (also known as MIP-1 and MIP-2 respectively), promote the formation of perinuclear germ granules in C. elegans. This finding presents a unique opportunity to evaluate the significance of perinuclear localization of germ granules. Here we show that loss of eggd-1 causes the coalescence of germ granules and formation of abnormal cytoplasmic aggregates. Impairment of perinuclear granules affects certain germline classes of small RNAs including Piwi-interacting RNAs. Transcriptome profiling reveals overexpression of spermatogenic and cuticle-related genes in eggd-1 hermaphrodites. We further demonstrate that disruption of germ granules activates HLH-30-mediated transcriptional program in somatic tissues. Collectively, our findings underscore the essential role of EGGD-1 in germ granule organization and reveal an unexpected germ granule-to-soma communication.

2023-07-20 | GSE228858 | GEO

C. elegans germ granules regulate both germline and somatic RNAome [miRNA-Seq]

2023-07-20 | GSE228857 | GEO

Transcriptome profiling of P-granule-depleted or P-granule mutant gonads versus control gonads over time

Project description:The germ cells of multicellular organisms protect their developmental potential through specialized mechanisms. A shared feature of germ cells from worms to humans is the presence of non-membrane-bound ribonucleoprotein organelles called germ granules. Depletion of germ granules in Caenorhabditis elegans (i.e., P granules) leads to sterility and in some germlines expression of the neuronal transgene unc-119::gfp and the muscle myosin MYO-3. Thus, P granules are hypothesized to maintain germ cell totipotency by preventing somatic development, although the mechanism by which P granules carry out this function is unknown. In this study, we performed transcriptome and single molecule RNA-FISH analyses of dissected P-granule-depleted gonads at different developmental stages. Our results demonstrate that P granules are necessary for adult germ cells to down-regulate spermatogenesis RNAs and to prevent the accumulation of numerous soma-specific RNAs. P-granule-depleted gonads that express the unc-119::gfp transgene also express many other genes involved in neuronal development and concomitantly lose expression of germ cell fate markers. Finally, we show that removal of either of two critical P-granule components, PGL-1 or GLH-1, is sufficient to cause germ cells to express UNC-119::GFP and MYO-3 and to display RNA accumulation defects similar to those observed after depletion of P granules. Our data identify P granules as critical modulators of the germline transcriptome and guardians of germ cell fate.

2016-12-22 | GSE92690 | GEO

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