Transcriptome analysis of wild-type and maternal ybx1 mutant zebrafish embryos during early development
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ABSTRACT:
ORGANISM(S): Danio rerio
PROVIDER: GSE108924 | GEO | 2018/09/01
REPOSITORIES: GEO
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Project description:In mammals, maternal gene products decay and zygotic genome activation (ZGA) onsets during maternal to zygotic transition (MZT). Y-box binding protein YBX1 plays vital roles in RNA stabilization and transcriptional regulation, but its roles in pre-implantation development remain to be elucidated. In the present study, we aim to investigate the role of YBX1 during goat MZT and further explore the molecular mechanisms. The expression of YBX1 was increased during MZT in goat, bovine, human, and mice. We successfully knocked down YBX1 by microinjection of siRNA against YBX1, and the embryo development was impaired when YBX1 was knocked down. Using RNA-seq, we identified 1623 up-regulated and 3531 down-regulated genes in the 8-cell stage YBX1 knockdown embryos. GO/KEGG/GSEA enrichment analysis revealed that the down-regulated genes were enriched in regulation of RNA/mRNA stability and spliceosome, suggesting that YBX1 might medicate pre-implantation development by alternative splicing and maternal mRNA decay. To this end, we identified 3284 differential alternative splicing events and 1322 differentially expressed maternal mRNAs at the 8-cell stage YBX1 knockdown embryos compared to the controls. Moreover, the splicing factors and mRNA decay related genes were aberrantly expressed. Lastly, knockdown of YBX1 impaired transcriptional activity during ZGA in goat and mice as revealed by 5-EU staining. Our results identify that YBX1 serves an important role in maternal mRNA decay, alternative splicing, and the transcriptional activity required for early embryogenesis, which will broaden the current understanding of YBX1 functions during the stochastic reprogramming events.
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Project description:The maternal-to-zygotic transition (MZT) is a conserved and fundamental process during which the embryo undergoes dramatic reprogramming to convert maternal environment to embryonic-driven programing. However, how the maternally supplied transcripts are dynamically regulated during MZT remains largely unknown. Herein, through genome-wide profiling of RNA 5-methylcytosine (m5C) in zebrafish early embryos, we show that m5C methylated maternal mRNAs display higher stability during MZT. We identify that the Y box-binding protein 1 (Ybx1) prefers to recognizing m5C-modified mRNAs through p-p interaction with a key residue Trp45 in its cold shock domain (CSD), which plays essential roles in maternal mRNA stability and early embryogenesis of zebrafish. Cooperated with an mRNA stabilizer Pabpc1a, Ybx1 promotes the stability of its target mRNAs in an m5C-dependent manner. Our study demonstrates a novel mechanism of RNA m5C methylation-regulated maternal mRNA stability during zebrafish MZT, highlighting the critical role of m5C mRNA methylation in early development.
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Project description:Embryogenesis entails dramatic shifts in mRNA translation and turnover to account for gene expression differences during proliferation and cellular differentiation. Codon identity modulates mRNA stability during early vertebrate embryogenesis, but how the composition of tRNA pools adapts to the embryo s translational demand is unknown. By quantitatively profiling the tRNA repertoires of zebrafish embryos during the maternal-to-zygotic transition, here we find that maternal and zygotic tRNA pools are distinct. We show that translational activation during embryogenesis and tRNA gene derepression are temporally coordinated by TORC1 activity, which increases at gastrulation and inactivates the RNA polymerase III repressor Maf1a/b in vivo. Reshaping of tRNA pools results in differential tRNA anticodon supply, but these changes do not alter decoding rates in zebrafish embryos. Instead, our data indicate that tRNA repertoires reflect the inherent codon bias of the zebrafish mRNA transcriptome, and tRNA levels are boosted at gastrulation to ensure efficient translation as embryos enter differentiation.
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Project description:The maternal-to-zygotic transition (MZT) is a conserved and fundamental process during which the embryo undergoes dramatic reprogramming to convert maternal environment to embryonic-driven programing. However, how the maternally supplied transcripts are dynamically regulated during MZT remains largely unknown. Herein, through genome-wide profiling of RNA 5-methylcytosine (m5C) in zebrafish early embryos, we show that m5C methylated maternal mRNAs display higher stability during MZT. We identify that the Y box-binding protein 1 (Ybx1) prefers to recognizing m5C-modified mRNAs through p-p interaction with a key residue Trp45 in its cold shock domain (CSD), which plays essential roles in maternal mRNA stability and early embryogenesis of zebrafish. Cooperated with an mRNA stabilizer Pabpc1a, Ybx1 promotes the stability of its target mRNAs in an m5C-dependent manner. Our study demonstrates a novel mechanism of RNA m5C methylation-regulated maternal mRNA stability during zebrafish MZT, highlighting the critical role of m5C mRNA methylation in early development.
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Project description:Upon fertilization, the embryonic genome remains transcriptionally inactive until the mid-blastula transition. Zygotic genome activation (ZGA) of vertebrate embryos has been extensively studied using nucleic acid-based strategies, but proteomics data are still scarce, impeding the full mechanistic understanding of how ZGA is executed during the maternal-to-zygotic transition (MZT). Here, we performed quantitative proteomics to decipher the proteome landscape of zebrafish embryos during the MZT, quantifying nearly 5,000 proteins across four embryonic stages. The stage-specific clustering based on protein expression pattern revealed that helicases (i.e., eif4a2 and ruvbl1) facilitate pluripotency factors (i.e., nanog, pou5f3, ctcf, and hmga1) triggering ZGA in zebrafish, accompanied by the maternal product decay with P-bodies and ubiquitin dependent proteolytic pathway. Dozens of transcription factors show wave-like expression patterns during MZT, implying their diverse functions in triggering the ZGA and modulating differentiation for organ development. The combination of morpholino knockdown and quantitative proteomics demonstrated that maternal Nanog is required for proper embryogenesis by regulating 1) interactions with other pluripotency factors, 2) F-actin band formation, 3) cell cycle checkpoints and 4) maternal product degradation. This study represents the most systematic proteomics survey of developmentally regulated proteins and their expression profiles accompanying MZT in zebrafish, which is a valuable proteome resource for understanding ZGA.
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