Cytoplasmic polyadenylation-mediated translational control of maternal mRNAs directs maternal to zygotic transition [RESEARCH ARTICLE]

Cecilia Lanny Winata, Maciej Łapinski, Leszek Pryszcz, Candida Vaz, Muhammad Hisyam bin Ismail, Srikanth Nama, Hajira Shreen Hajan, Serene Gek Ping Lee, Vladimir Korzh, Prabha Sampath, Vivek Tanavde, and Sinnakaruppan Mathavan

In the earliest stages of animal development following fertilization, maternally deposited mRNAs direct biological processes to the point of zygotic genome activation (ZGA). These maternal mRNAs undergo cytoplasmic polyadenylation (CPA), suggesting translational control of their activation. To elucidate the biological role of CPA during embryogenesis, we performed genome-wide polysome profiling at several stages of zebrafish development. Our analysis revealed a correlation between CPA and polysome association dynamics, demonstrating a coupling of translation to the CPA of maternal mRNAs. Pan-embryonic CPA inhibition disrupted the maternal to zygotic transition (MZT), causing a failure of developmental progression past the MBT and changes in global gene expression that indicated a failure of ZGA and maternal mRNA clearance. Among the genes that were differentially expressed were those encoding chromatin modifiers and key transcription factors involved in ZGA, including nanog, pou5f3, and sox19b, which present distinct CPA dynamics. Our results establish the necessity of CPA to ensure progression of the MZT. The RNA-seq data generated in this study represents a valuable zebrafish resource for the discovery of novel elements of the early embryonic transcriptome.

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