Global characterization of the oocyte-to-embryo transition in Caenorhabditis elegans uncovers a novel mRNA clearance mechanism

Marlon Stoeckius, Dominic Grün, Marieluise Kirchner, Salah Ayoub, Francesca Torti, Fabio Piano, Margareta Herzog, Matthias Selbach, Nikolaus Rajewsky

Research output: Contribution to journalArticle

Abstract

The oocyte-to-embryo transition (OET) is thought to be mainly driven by post-transcriptional gene regulation. However, expression of both RNAs and proteins during the OET has not been comprehensively assayed. Furthermore, specific molecular mechanisms that regulate gene expression during OET are largely unknown. Here, we quantify and analyze transcriptome-wide, expression of mRNAs and thousands of proteins in Caenorhabditis elegans oocytes, 1-cell, and 2-cell embryos. This represents a first comprehensive gene expression atlas during the OET in animals. We discovered a first wave of degradation in which thousands of mRNAs are cleared shortly after fertilization. Sequence analysis revealed a statistically highly significant presence of a polyC motif in the 3′ untranslated regions of most of these degraded mRNAs. Transgenic reporter assays demonstrated that this polyC motif is required and sufficient for mRNA degradation after fertilization. We show that orthologs of human polyC-binding protein specifically bind this motif. Our data suggest a mechanism in which the polyC motif and binding partners direct degradation of maternal mRNAs. Our data also indicate that endogenous siRNAs but not miRNAs promote mRNA clearance during the OET. Synopsis The first molecular quantification of transcriptome and proteome changes during the oocyte-to-embryo transition reveals coordinated degradation of thousands of mRNAs shortly after fertilization. First quantification of transcriptome and proteome changes between the Caenorhabditis elegans oocyte and fertilized, totipotent 1-cell embryo in any organism Discovered a wave of destruction where thousands of mRNAs are cleared right after fertilization A novel polyC motif in 3′ untranslated regions (3′ UTRs) explains the targeted degradation of mRNAs Conserved RNA-binding proteins bind the polyC motif in vitro, offering a mechanism for mRNA clearance. The first molecular quantification of transcriptome and proteome changes during the oocyte-to-embryo transition reveals coordinated degradation of thousands of mRNAs shortly after fertilization.

Original languageEnglish (US)
Pages (from-to)1751-1766
Number of pages16
JournalEMBO Journal
Volume33
Issue number16
DOIs
StatePublished - Aug 18 2014

Keywords

  • Caenorhabditis elegans
  • embryogenesis
  • maternal mRNA
  • oocyte-to-embryo transition
  • posttranscriptional gene regulation

ASJC Scopus subject areas

  • Neuroscience(all)
  • Molecular Biology
  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)

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  • Cite this

    Stoeckius, M., Grün, D., Kirchner, M., Ayoub, S., Torti, F., Piano, F., Herzog, M., Selbach, M., & Rajewsky, N. (2014). Global characterization of the oocyte-to-embryo transition in Caenorhabditis elegans uncovers a novel mRNA clearance mechanism. EMBO Journal, 33(16), 1751-1766. https://doi.org/10.15252/embj.201488769