Translation is critical for development as transcription in the oocyte and early embryo is silenced. To illustrate the translational changes during meiosis and consecutive two mitoses of the oocyte and early embryo, we performed a genome-wide translatome analysis. Acquired data showed significant and uniform activation of key translational initiation and elongation axes specific to M-phases. Although global protein synthesis decreases in M-phases, translation initiation and elongation activity increases in a uniformly fluctuating manner, leading to qualitative changes in translation regulation via the mTOR1/4F/eEF2 axis. Overall, we have uncovered a highly dynamic and oscillatory pattern of translational reprogramming that contributes to the translational regulation of specific mRNAs with different modes of polysomal occupancy/translation that are important for oocyte and embryo developmental competence. Our results provide new insights into the regulation of gene expression during oocyte meiosis as well as the first two embryonic mitoses and show how temporal translation can be optimized. This study is the first step towards a comprehensive analysis of the molecular mechanisms that not only control translation during early development, but also regulate translation-related networks employed in the oocyte-to-embryo transition and embryonic genome activation.

Bioinformatics Group Division of Molecular Biology Department of Biology Faculty of Science University of Zagreb 10000 Zagreb Croatia

Department of Animal Sciences University of Florida Gainesville FL 32610 USA

Laboratory of Biochemistry and Molecular Biology of Germ Cells Institute of Animal Physiology and Genetics of the Czech Academy of Sciences Rumburska 89 277 21 Libechov Czech Republic

Laboratory of Early Mammalian Developmental Biology Department of Molecular Biology and Genetics Faculty of Science University of South Bohemia in České Budějovice Branisovšká 31a České Budějovice Czech Republic

Laboratory of Epigenetic Regulations Institute of Molecular Genetics of the Czech Academy of Sciences Videnska 1083 142 20 Prague 4 Czech Republic

Laboratory of RNA Biochemistry Department of Genetics and Microbiology Faculty of Science Charles University Viničná 5 128 44 Prague 2 Czech Republic

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