Maternal mRNA deadenylation and allocation via Rbm14 condensates facilitate vertebrate blastula development

Abstract

Early embryonic development depends on proper utilization and clearance of maternal transcriptomes. How these processes are spatiotemporally regulated remains unclear. Here we show that nuclear RNA‐binding protein Rbm14 and maternal mRNAs co‐phase separate into cytoplasmic condensates to facilitate vertebrate blastula‐to‐gastrula development. In zebrafish, Rbm14 condensates were highly abundant in blastomeres and markedly reduced after prominent activation of zygotic transcription. They concentrated at spindle poles by associating with centrosomal γ‐tubulin puncta and displayed mainly asymmetric divisions with a global symmetry across embryonic midline in 8‐ and 16‐cell embryos. Their formation was dose‐dependently stimulated by m 6 A, but repressed by m 5 C modification of the maternal mRNA. Furthermore, deadenylase Parn co‐phase separated with these condensates, and this was required for deadenylation of the mRNAs in early blastomeres. Depletion of Rbm14 impaired embryonic cell differentiations and full activations of the zygotic genome in both zebrafish and mouse and resulted in developmental arrest at the blastula stage. Our results suggest that cytoplasmic Rbm14 condensate formation regulates early embryogenesis by facilitating deadenylation, protection, and mitotic allocation of m 6 A‐modified maternal mRNAs, and by releasing the poly(A)‐less transcripts upon regulated disassembly to allow their re‐polyadenylation and translation or clearance. image The mechanisms mediating the spatiotemporal control of maternal mRNA translational competence and decay remain largely unclear. In this study, maternal mRNAs in zebrafish and mouse embryos are shown to form condensates with the RNA binding protein Rbm14 for their deadenylation, sequestration, mitotic allocation, and timely release during early embryogenesis. Rbm14 co‐phase‐separates with deadenylase Parn and maternal m 6 A‐modified mRNAs into cytoplasmic condensates in early embryos. The condensates are segregated into daughter blastomeres through associations with centrosomal γ‐tubulin‐positive puncta. Rbm14 is required for correct maternal mRNA deadenylation, sequestration, and release from the condensates during embryonic development for timely re‐activation or clearance. Depletion of Rbm14 represses maternal‐to‐zygotic transition and blastula‐to‐gastrula development in both zebrafish and mouse.