Unknown,Transcriptomics,Genomics,Proteomics

Dataset Information

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. Four biological replicates of each condition (empty vector control, P granule RNAi, and CSR-1 RNAi germlines) were collected for total RNA.

ORGANISM(S): Caenorhabditis elegans

SUBMITTER: Dustin Updike

PROVIDER: E-GEOD-67954 | biostudies-arrayexpress |

REPOSITORIES: biostudies-arrayexpress

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Publications

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

Campbell Anne C AC Updike Dustin L DL

Development (Cambridge, England) 20150501 10

Germ granules (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 misexpression 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 ...[more]

PMID: 25968310

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Project description:RNA-seq transcriptome analysis of C. elegans germlines that inherited only paternal chromosomes (non-Mendelian inheritance, 'red-head worms') and the germlines of their offspring ('offspring of red-head worms') vs. germlines that inherited both maternal and paternal chromosomes (Mendelian inheritance, HBR1280 control). Given that epigenetic marking of sperm chromosomes is faithfully transmitted through embryo cell divisions, and that sperm epigenetic marking is important in offspring, we tested if sperm epigenetic marking alone is sufficient for proper development of the germline in offspring. We utilized a mutant that, during the first embryonic division, delivers the sperm genome to the daughter cell that generates the germline and the oocyte genome to the other daughter cell (Besseling & Bringmann, 2016). This mutant over-expresses GPR-1, a protein involved in regulation of kinetochore pulling forces. GPR-1 over-expression results in excessive pulling forces, causing the paternal and maternal pronuclei to inappropriately move to opposite poles of the 1-cell embryo instead of merging in the center of the embryo. In this mutant background, ~60% of offspring undergo atypical chromosome segregation, generating mosaic embryos whose germlines are derived entirely from sperm chromosomes (Besseling & Bringmann, 2016). To track the parental genomes, differentially tagged histone transgenes were used: a GFP-tagged histone H2B encoded in the sperm genome, and a TdTomato-tagged histone H2B encoded in the oocyte genome. The mosaic embryos whose germline inherited only sperm chromosomes (‘red-head' worms) develop into fertile adults with a normal brood size, similar to control worms, in which the germline inherited both sperm and oocyte chromosomes. RNA-seq analysis demonstrated that the germline transcriptome of ‘red-head’ worms and their offspring show few (<80 genes) and minor changes compared to control worms. These findings demonstrate that epigenetic information provided by sperm can guide proper germ cell development.

Dataset Information

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

Publications

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

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