Global characterization of the oocyte-to-embryo transition in C. elegans uncovers a novel mRNA turnover mechanism

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, small RNAs and thousands of proteins in C. 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 turned over shortly after fertilization. Sequence analysis revealed a statistically highly significant presence of a novel polyC motif in the 3' untranslated regions (3' UTRs) of most of these degraded mRNAs. Transgenic reporter assays showed that this polyC motif is indeed required and sufficient for mRNA degradation after fertilization. We show that orthologs of human poly-C binding-protein specifically bind this motif. Together, 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. To study the OET in C.elegans we isolated large quantities of oocytes, 1-cell embryos, 2-cell embryos and sperm. We then sequenced polyA RNA.