Paternal RNA contributions in the C. elegans zygote
Ontology highlight
ABSTRACT:
ORGANISM(S): Caenorhabditis elegans
PROVIDER: GSE57351 | GEO | 2014/06/04
SECONDARY ACCESSION(S): PRJNA246316
REPOSITORIES: GEO
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Project description:Development of the early embryo is thought to be mainly driven by maternal gene products and post-transcriptional gene regulation. Here, we used metabolic labeling to show that RNA can be transferred by sperm into the embryo. To identify genes with paternal expression in the embryo, we performed crosses of males and females from divergent C. elegans strains. RNA sequencing of mRNAs and small RNAs in the 1-cell hybrid embryo revealed that about two hundred paternal mRNAs are reproducibly expressed in the embryo, and that about half of assayed endogenous siRNAs and piRNAs are also of paternal origin. Together, our results suggest an unexplored paternal contribution to early development. To reveal the identity of paternal RNA molecules, we performed a cross of males and females from two divergent C. elegans strains because we reasoned that sequencing of embryonic RNA and SNP analysis should then identify and quantify maternal and paternal transcripts. These sequencing experiments were carried out in purified hybrid 1-cell embryos and comprised small RNAs and mRNAs. For comparison we sequenced mRNAs and small RNAs from the parental strains: paternal (Hawaiian males, CB4856) and maternal (fem-1(hc17ts)/TX189(OMA-1::GFP). For the annotation of strain specific mutations (SNPs) we sequenced mRNA and small RNAs extracted from whole worms. All experiments were performed in at least two independent biological replicates.
2014-06-04 | E-GEOD-57351 | biostudies-arrayexpress
Project description:Development of the early embryo is thought to be mainly driven by maternal gene products and post-transcriptional gene regulation. Here, we used metabolic labeling to show that RNA can be transferred by sperm into the oocyte upon fertilization. To identify genes with paternal expression in the embryo, we performed crosses of males and females from divergent Caenorhabditis elegans strains. RNA sequencing of mRNAs and small RNAs in the 1-cell hybrid embryo revealed that about one hundred sixty paternal mRNAs are reproducibly expressed in the embryo and that about half of all assayed endogenous siRNAs and piRNAs are also of paternal origin. Together, our results suggest an unexplored paternal contribution to early development.
| S-EPMC4195758 | biostudies-literature
Project description:Polyploidy, the presence of more than two sets of chromosomes within the nucleus, is a common phenomenon among plants that has shaped genome organization and is thought to be a major driver of speciation. The triploid block acts as a reproductive barrier that prevents successful backcrosses of newly formed polyploids with their progenitors. It is established in the endosperm, an ephemeral tissue that nurtures the developing embryo. Here we show that paternal 21/22 nucleotide epigenetically activated small interfering RNAs (easiRNAs) in Arabidopis thaliana are responsible for the establishment of the triploid block associated seed abortion. This dramatic phenotype is overcome when crosses are performed with a paternal mutant in the plant specific RNA polymerase IV (Pol IV). Loss of Pol IV reduces both easiRNAs and hetsiRNAs in the pollen grain. Seeds derived from crosses between wild type tetraploid fathers and diploid mothers have reduced levels of hetsiRNAs and cytosine methylation at transposable elements (TEs), indicating that they have suffered an excess of epigenetic reprogramming due to an excess of paternally derived easiRNAs. Paternal Pol IV mutants are able to buffer that easiRNA excess and rescue the abortion phenotype by rescuing both the cytosine methylation level at TEs and the 24 nt hetsiRNA accumulation levels. This mechanism highlights the elegant and important TE regulation mechanism controlled by the plant specific Pol IV that takes place pre-fertilization and regulates paternal easiRNAs and maternal hetsiRNAs, and determines the post-fertilization epigenetic stability and seed viability.
2017-12-14 | GSE84122 | GEO
Project description:Pachytene piRNAs are PIWI-interacting small RNAs abundantly expressed in pachytene spermatocytes and spermatids in adult mouse testes. Both MIWI and MILI-bound pachytene piRNAs have been found enriched in round spermatids. Miwi-null male mice are sterile due to spermiogenic arrest. In C. elegans, sperm-borne piRNAs appear to have an epigenetic role during fertilization and development because progeny of offspring derived from piRNA-deficient sperm display a progressive fertility loss after several generations. In mice, it remains unknown whether MIWI-bound pachytene piRNA-deficient round spermatids can produce offspring, and whether the progeny of offspring derived from MIWI-bound pachytene piRNA-deficient round spermatids also exhibit transgenerational loss of fertility. Here, we report that Miwi KO round spermatids could fertilize both wild type (WT) and Miwi KO oocytes through round spermatid microinjection (ROSI), and produce healthy and fertile offspring despite the aberrant pachytene piRNA profiles in those Miwi KO spermatids. Progeny of ROSI-derived heterozygotes, both male and female, displayed normal fertility for at least three generations when bred with either WT or Miwi KO females. Our data indicate that aberrant MIWI-bound pachytene piRNAs profiles in spermatids do not affect fertilization, early embryonic development, or fertility of the offspring, suggesting a normal pachytene piRNAs profile is not required for paternal transgenerational epigenetic inheritance in mice. Method: Round spermatids were purified from WT and Miwi KO adult testes using a mini-STA-PUT method[Methods Enzymol 1993; 225:84-113.]，the purity of round spermatids was >90% based on our previous report[ J Biol Chem 2012; 287:25173-25190.]. Small RNA was isolated from round spermatids using the mirVana RNA isolation kit (Ambion) according to the manufacturer’s instructions. RNA quality and quantity were assessed using the Agilent 2100 Bioanalyzer. Small RNA-Seq was performed on an Ion Proton sequencer (Life Technologies). Libraries were prepared using the Ion Total RNA-Seq Kit v2 (Invitrogen) with biological triplicates for WT and Miwi KO samples. Resutls:Our data indicate that aberrant MIWI-bound pachytene piRNAs profiles in spermatids do not affect fertilization, early embryonic development, or fertility of the offspring, suggesting a normal pachytene piRNAs profile is not required for paternal transgenerational epigenetic inheritance in mice.
2016-09-01 | GSE86319 | GEO
Project description:The Piwi-interacting RNA (piRNA) pathway plays an essential role in the repression of transposons in the germline. Other functions of piRNAs such as post-transcriptional regulation of mRNAs are now emerging. Here, we perform iCLIP with the PIWI protein Aubergine (Aub) and identify hundreds of maternal mRNAs interacting with Aub in the early Drosophila embryo. Gene expression profiling reveals that a proportion of these mRNAs undergoes Aub-dependent destabilization during the maternal-to-zygotic transition. Strikingly, Aub-dependent unstable mRNAs encode germ cell determinants. iCLIP with an Aub mutant that is unable to bind piRNAs confirms that binding of Aub to mRNAs is piRNA dependent. Base-pairing between piRNAs and mRNAs can induce mRNA cleavage and decay that are essential for embryonic development. These results reveal a general regulation of maternal mRNAs by Aub and piRNAs, which plays a key developmental role in the embryo, by mediating decay and localization of mRNAs encoding germ cell determinants.
2015-08-19 | GSE70777 | GEO
Project description:In animals, maternal gene products deposited into eggs regulate embryonic development before activation of the zygotic genome. In plants, an analogous period of prolonged maternal control over embryogenesis is thought to occur based on gene-expression studies. However, other gene-expression studies and genetic analyses show that some transcripts must derive from the early zygotic genome, implying that the prevailing model does not fully explain the nature of zygotic genome activation in plants. To determine the maternal, paternal and zygotic contributions to the early embryonic transcriptome, we sequenced the transcripts of hybrid embryos from crosses between two polymorphic inbred lines of Arabidopsis thaliana and used single-nucleotide polymorphisms (SNPs) diagnostic of each parental line to quantify parental contributions. Although some transcripts appeared to be either inherited from primarily one parent or transcribed from imprinted embryonic loci, the vast majority of transcripts were produced in near-equal amounts from both maternal and paternal alleles, even during the initial stages of embryogenesis. Results of reporter experiments and analyses of transcripts from genes that are not expressed in sperm and egg indicate early and widespread zygotic transcription. Thus, in contrast to early animal embryogenesis, early plant embryogenesis is mostly under zygotic control.
2012-01-12 | GSE33713 | GEO
Project description:PRC2 8 cell embryo paternal epigenetic inheritance
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Project description:This dataset provide deep-profiling of the embryonic transcriptome of total RNA at an early developmental stage (2-to-4 cells stage) and at the globular stage in Arabidopsis. Embryos were derived from either a cross between a Landsberg erecta (Ler) maternal parent and a Columbia (Col0) paternal parent or a cross between a kyp-2 Ler maternal parent and a Columbia paternal parent. Embryos were manually dissected ensuring no contamination with maternal seed coat or endosperm. 6 samples: crosses between Ler and Col, or kyp-2 (Ler) and Col; Ler seed coat at 2-4cells embryo stage # SC_2.
2011-06-01 | E-GEOD-24198 | biostudies-arrayexpress
Project description:There is increasing evidence that epigenetic information can be inherited across generations in mammals, despite extensive reprogramming both in the gametes and the early developing embryo. One corollary to this is that disruption of the establishment of epigenetic state in the gametes of a parent, as a result of heterozygosity for mutations in genes involved in reprogramming, could affect the phenotype of offspring that do not inherit the mutant allele. Here we show that such effects do occur following paternal inheritance in the mouse. We detect changes to transcription and chromosome ploidy in adult animals. Paternal effects of this type have not been reported previously in mammals and suggest that the untransmitted genotype of male parents can influence the phenotype of their offspring. Keywords: Offspring of Dnmt3L+/- sires compared to offspring of Dnmt3L+/+ sires
2007-03-29 | GSE7384 | GEO
Project description:Seed development is sensitive to parental dosage, with excess maternal or paternal genomes creating reciprocal phenotypes. Paternal genomic excess results in extensive endosperm proliferation without cellularization and eventual seed abortion. We previously showed that loss of the RNA POL IV gene nrpd1 in tetraploid fathers represses seed abortion in paternal excess crosses. Here we show genetically that RNA-directed DNA methylation (RdDM) pathway activity in the paternal parent is sufficient to determine the viability of paternal excess seeds. The status of the RdDM pathway in paternal excess endosperm does not impact seed viability. Comparison of endosperm transcriptomes, DNA methylation, and small RNAs from balanced and paternal excess endosperm demonstrates that paternal excess seed abortion is unlikely to be dependent on either transposable element or imprinted gene mis-regulation. We suggest instead that loss of paternal RdDM modulates expression at a small subset of genes and desensitizes endosperm to paternal excess. Finally, using allele-specific transcription data, we present evidence of a transcriptional buffering system that up37 regulates maternal alleles and represses paternal alleles in response to excess paternal genomic dosage. These findings prompt reconsideration of models for dosage sensitivity in endosperm.
2019-05-01 | GSE126929 | GEO