Maternal Ybx1 safeguards zebrafish oocyte maturation and maternal-to-zygotic transition by repressing global translation

Abstract

Maternal mRNAs and proteins dictate early embryonic development before zygotic genome activation. In the absence of transcription, elaborate control of maternal mRNA translation is of particular importance for oocyte maturation and early embryogenesis. By analyzing zebrafish ybx1 mutants with a null allele, we demonstrate an essential role of maternal ybx1 in repressing global translation in oocytes and embryos. Loss of maternal Ybx1 leads to impaired oocyte maturation and egg activation. Maternal ybx1 (Mybx1) mutant embryos fail to undergo normal cleavage and the maternal-to-zygotic transition (MZT). Morpholino knockdown of ybx1 also results in MZT loss and epiboly failure, suggesting the post-fertilization requirement of Ybx1. Additionally, elevated global translation level and the unfolded protein response were found in Ybx1-depleted embryos. Supplementing translational repression by eIF4E inhibition markedly rescues the Mybx1 phenotype. Mechanistically, Ybx1 in embryos may associate with processing body (P-body) components and represses translation when tethered to target mRNAs. Collectively, our results identify maternal Ybx1 as a global translational repressor required for oocyte maturation and early embryogenesis.