Bojorquez, D.; Moghareh, S.; Elsayed, M.; Kizhedathu, A.; Jison, G.; Bardwell, L.; Lara-Gonzalez, P.

During early embryogenesis, gene expression relies on maternally loaded mRNAs whose translation is controlled by RNA binding proteins. Here, we identify a critical role for the cyclin B3-CDK1 complex, known for its function in mitosis, in driving early embryonic gene expression in C. elegans. The cyclin B3-CDK1 complex works by marking the RNA binding OMA proteins (OMA-1 and OMA-2) for degradation, which ensures the de-repression and translation of their target mRNAs. OMA protein degradation relies on cyclin B3's conserved phosphate-binding pocket, which promotes multi-site OMA phosphorylation and the generation of phospho-degrons. Notably, the phosphate-binding pocket of cyclin B3 does not substantially contribute to its mitotic roles, indicating that the mitotic and translational functions of the cyclin B3-CDK1 complex are separable. These findings establish that embryonic activation of the cyclin B3-CDK1 complex drives both mitotic divisions and mRNA de-repression, which ensures that cell division is coupled to the early gene expression program in development.