Genome-wide analysis identifies cis-acting elements regulating mRNA polyadenylation and translation during vertebrate oocyte maturation

Abstract

Changes in gene expression are required to orchestrate changes in cell state during development. Most cells change patterns of gene expression through transcriptional regulation. In contrast, oocytes are transcriptionally silent and use changes in mRNA poly-A tail length to control protein production. Poly-A tail length is positively correlated with translation activation during early development. However, it is not clear how poly-A tail changes affect mRNA translation at a during vertebrate oocyte maturation. We used Tail-seq and polyribosome analysis to measure poly-A tail and translational changes during oocyte maturation in Xenopus laevis. We identified large-scale poly-A and translational changes during oocyte maturation and found that poly-A tail changes precede translation changes. Additionally, we identified a family of U-rich sequence elements that are enriched near the polyadenylation signal of polyadenylated and translationally activated mRNAs. A modest density of U-rich elements was correlated with polyadenylation while a high density of U-rich elements was required to activate translation, showing that polyadenylation and translation activation can be uncoupled. Collectively, our data show that changes in mRNA polyadenylation are a key mechanism regulating protein expression during vertebrate oocyte maturation and that these changes are controlled by a spatial code of cis-acting sequence elements. Our results provide insight into mechanisms of translational control in oocytes and identify novel proteins important for the completion of meiosis.