Widespread Changes in the Posttranscriptional Landscape at the Drosophila Oocyte-to-Embryo Transition

•The translatome is extensively altered at egg activation•PNG kinase is a major regulator of translational status of mRNAs at egg activation•A subset of proteins is “reset” at the Drosophila oocyte-to-embryo transition•A catalog of candidate new regulators of early embryogenesis (e.g., Lid) is provided

SummaryThe oocyte-to-embryo transition marks the onset of development. The initial phase of this profound change from the differentiated oocyte to the totipotent embryo occurs in the absence of both transcription and mRNA degradation. Here we combine global polysome profiling, ribosome-footprint profiling, and quantitative mass spectrometry in a comprehensive approach to delineate the translational and proteomic changes that occur during this important transition in Drosophila. Our results show that PNG kinase is a critical regulator of the extensive changes in the translatome, acting uniquely at this developmental window. Analysis of the proteome in png mutants provided insights into the contributions of translation to changes in protein levels, revealing a compensatory dynamic between translation and protein turnover during proteome remodeling at the return to totipotency. The proteome changes additionally suggested regulators of meiosis and early embryogenesis, including the conserved H3K4 demethylase LID, which we demonstrated is required during this period despite transcriptional inactivity.

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