A meiotic midbody structure in mouse oocytes acts as a barrier for nascent translation to ensure developmental competence

Successful embryo development is dependent upon maternally deposited components. During egg formation, developmental competence is acquired through regulated translation of maternal mRNA stores. In addition, egg precursors undergo two rounds of chromosome segregation, each coupled to an asymmetric cytokinesis that produces two non-functional polar bodies. In somatic cells, cytokinesis produces two daughter cells and one midbody remnant (MBR), a signaling organelle assembled from the midbody (MB), which first appears in Telophase. MBs contain transcription and translation factors, and epigenetic modifiers. Once MBs mature to MBRs by abscission, they can be subsequently phagocytosed by another cell and influence cellular function or fate. Although the significance of MBs is elucidated in several cell types like neurons, cancer cells and stem cells, the presence and function of MBs in gametes and their roles in reproductive fitness are unknown. Here, we examined the formation and regulation of meiotic midbodies (mMB) in mouse oocytes. We find that although mouse oocyte mMBs contain analogous structures to somatic MBs, they also have a unique cap-like structure composed of the centralspindlin complex, and that cap formation depends upon an asymmetric microtubule abundance in the egg compared to the polar body. Furthermore, our results show that mMBs are translationally active ribonucleoprotein granules, supported by detection of ribosomes, polyadenylated mRNAs and nascent translation. Finally, by pharmacological and laser ablation-based approaches, we demonstrate that the mMB cap is a barrier to prevent translated products from leaving the egg and escaping into the polar body. Crucially, this barrier is critical for successful early embryonic development. Here, we document an evolutionary adaptation to the highly conserved process of cytokinesis in mouse oocytes and describe a new structure and new mechanism by which egg quality and embryonic developmental competence are regulated.