title: Global characterization of the oocyte-to-embryo transition in Caenorhabditis elegans uncovers a novel mRNA clearance mechanism.
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.
authors: Systems Biology of Gene Regulatory Elements, Max Delbrück Center Berlin, Berlin, Germany.
authors: Marlon
authors: M
authors: Stoeckius
authors: Systems Biology of Gene Regulatory Elements, Max Delbrück Center Berlin, Berlin, Germany.
authors: Dominic
authors: D
authors: Grün
authors: Cell Signalling and Mass Spectrometry, Max Delbrück Center Berlin, Berlin, Germany.
authors: Marieluise
authors: M
authors: Kirchner
authors: Systems Biology of Gene Regulatory Elements, Max Delbrück Center Berlin, Berlin, Germany.
authors: Salah
authors: S
authors: Ayoub
authors: Systems Biology of Gene Regulatory Elements, Max Delbrück Center Berlin, Berlin, Germany.
authors: Francesca
authors: F
authors: Torti
authors: Center for Genomics and Systems Biology, Department of Biology New York University, New York, NY, USA Division of Science, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates.
authors: Fabio
authors: F
authors: Piano
authors: Systems Biology of Gene Regulatory Elements, Max Delbrück Center Berlin, Berlin, Germany.
authors: Margareta
authors: M
authors: Herzog
authors: Cell Signalling and Mass Spectrometry, Max Delbrück Center Berlin, Berlin, Germany.
authors: Matthias
authors: M
authors: Selbach
authors: Systems Biology of Gene Regulatory Elements, Max Delbrück Center Berlin, Berlin, Germany rajewsky@mdc-berlin.de.
authors: Nikolaus
authors: N
authors: Rajewsky
mesh_terms: D020413:3' Untranslated Regions; D000818:Animals; D030801:Animals, Genetically Modified; D017173:Caenorhabditis elegans / Q000196:embryology* / Q000235:genetics*; D029742:Caenorhabditis elegans Proteins / Q000235:genetics / Q000378:metabolism; D004625:Embryo, Nonmammalian / Q000166:cytology / Q000502:physiology; D005260:Female; D005306:Fertilization / Q000235:genetics; D020869:Gene Expression Profiling; D018507:Gene Expression Regulation, Developmental; D035683:MicroRNAs; D009865:Oocytes / Q000502:physiology*; D011066:Poly C; D020543:Proteome / Q000378:metabolism; D020871:RNA Stability; D023121:RNA, Messenger, Stored / Q000378:metabolism; D034741:RNA, Small Interfering; D016601:RNA-Binding Proteins / Q000235:genetics / Q000378:metabolism
chemical_list: D020413:3' Untranslated Regions; D029742:Caenorhabditis elegans Proteins; D035683:MicroRNAs; D020543:Proteome; D023121:RNA, Messenger, Stored; D034741:RNA, Small Interfering; D016601:RNA-Binding Proteins; D011066:Poly C
keywords: Caenorhabditis elegans; embryogenesis; maternal mRNA; oocyte‐to‐embryo transition; posttranscriptional gene regulation