High-resolution Ribosome Profiling Reveals Translational Selectivity in Bovine Preimplantation Embryo Development

High resolution polysome fractionation and low-input ribosome profiling of bovine oocytes and preimplantation embryos has enabled us to define the translational landscape of early embryo development at an unprecedented level. We systematically and comparatively analyzed the transcriptome, polysome- and nonpolysome-bound RNA profiles of bovine oocytes and early embryos at 2-, 8-cell, morula, and blastocyst stage, and defined four modes of translational selectivity in bovine preimplantation embryo development: i. selective translation of non-abundant mRNAs, ii. active translating highly expressed mRNAs, iii. Translationally suppressed abundant mRNAs, and iv. Monosomaly occupied mRNAs. A strong selection towards genes involved in mitochondrial function and metabolic pathways was found throughout bovine preimplantation development. We found translatome largely follows transcriptome at oocytes, followed by a marked translational control at 8-cell embryos, which is gradually synchronized at the morula and blastocyst stage. We identified important novel cellular/embryonic functional regulators that being utilized and prioritized for translation at each developmental stage, that accompanies little-known bovine embryonic developmental programming. Together, these data reveal a unique spatiotemporal translational regulation that accompanies bovine preimplantation development. Overall design: First, 10 ribosome fractionations were collected from each of 200 bovine oocytes (GV and MII stage oocyte) or preimplantation embryos at 2-, 8-cell, morula, and blastocyst stages, followed by RNA-sequencing analysis. This experiment was performed in biological duplicates. In addition, the oocytes or embryos collected from the same batch in each developmental stage were used to profile their transcriptomes by mRNA-seq. This experiment was performed in biological triplicates.