High-resolution ribosome fractionation and low-input ribosome profiling of bovine oocytes and preimplantation embryos has enabled us to define the translational landscapes of early embryo development at an unprecedented level. We analyzed the transcriptome and the polysome- and non-polysome-bound RNA profiles of bovine oocytes (germinal vesicle and metaphase II stages) and early embryos at the two-cell, eight-cell, morula and blastocyst stages, and revealed four modes of translational selectivity: (1) selective translation of non-abundant mRNAs; (2) active, but modest translation of a selection of highly expressed mRNAs; (3) translationally suppressed abundant to moderately abundant mRNAs; and (4) mRNAs associated specifically with monosomes. A strong translational selection of low-abundance transcripts involved in metabolic pathways and lysosomes was found throughout bovine embryonic development. Notably, genes involved in mitochondrial function were prioritized for translation. We found that translation largely reflected transcription in oocytes and two-cell embryos, but observed a marked shift in the translational control in eight-cell embryos that was associated with the main phase of embryonic genome activation. Subsequently, transcription and translation become more synchronized in morulae and blastocysts. Taken together, these data reveal a unique spatiotemporal translational regulation that accompanies bovine preimplantation development.

Department of Animal Sciences Bond Life Sciences Center University of Missouri Columbia MO 65211 7310 USA

Department of Physiology and Cell Biology University of Nevada Reno School of Medicine Reno NV 89557 0352 USA

Division of Biomedical Sciences School of Medicine University of California Riverside CA 92521 USA

Laboratory of Biochemistry and Molecular Biology of Germ Cells Institute of Animal Physiology and Genetics CAS 277 21 Liběchov Czech Republic

School of Animal Sciences AgCenter Louisiana State University Baton Rouge LA 70803 USA

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Spatiotemporal dynamics and selectivity of mRNA translation during mouse pre-implantation development

The translational oscillation in oocyte and early embryo development