Cytoplasmic polyadenylation-mediated translational control of maternal mRNAs directs maternal-to-zygotic transition

• Published in: Development (Cambridge) Vol. 145; no. 1; p. dev159566
• Main Authors: Winata, Cecilia Lanny, Łapiński, Maciej, Pryszcz, Leszek, Vaz, Candida, Bin Ismail, Muhammad Hisyam, Nama, Srikanth, Hajan, Hajira Shreen, Lee, Serene Gek Ping, Korzh, Vladimir, Sampath, Prabha, Tanavde, Vivek, Mathavan, Sinnakaruppan
• Format: Journal Article
• Language: English
• Published: England The Company of Biologists Ltd 01.01.2018
• Subjects: Animals; Blastula; Chromatin; Cytoplasm - metabolism; Danio rerio; Developmental stages; Embryogenesis; Female; Fertilization; Gene expression; Genomes; Polyadenylation; Polyadenylation - physiology; Protein Biosynthesis - physiology; RNA, Messenger - genetics; RNA, Messenger - metabolism; Transcription factors; Translation; Zebrafish - embryology; Zebrafish - genetics; Zebrafish Proteins - biosynthesis; Zebrafish Proteins - genetics; Zygote - cytology; Zygote - metabolism; Zebrafish; Polysome profiling; Cytoplasmic polyadenylation; Translational regulation; Maternal-to-zygotic transition; Maternal mRNA
• ISSN: 0950-1991; 1477-9129
• DOI: 10.1242/dev.159566

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 beyond the mid-blastula transition 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 , and , which have distinct CPA dynamics. Our results establish the necessity of CPA for ensuring progression of the MZT. The RNA-seq data generated in this study represent a valuable zebrafish resource for the discovery of novel elements of the early embryonic transcriptome.