A cell cycle-coordinated Polymerase II transcription compartment encompasses gene expression before global genome activation

• Published in: Nature communications Vol. 10; no. 1; p. 691
• Main Authors: Hadzhiev, Yavor, Qureshi, Haseeb K., Wheatley, Lucy, Cooper, Ledean, Jasiulewicz, Aleksandra, Van Nguyen, Huy, Wragg, Joseph W., Poovathumkadavil, Divyasree, Conic, Sascha, Bajan, Sarah, Sik, Attila, Hutvàgner, György, Tora, Làszlò, Gambus, Agnieszka, Fossey, John S., Müller, Ferenc
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 11-02-2019; Nature Publishing Group; Nature Portfolio
• Subjects: 14; 14/34; 14/35; 14/63; 38; 631/136; 631/1647/245; 631/337/572; 631/80/386; Animals; Blastocyst - physiology; Blastula; Blastula - diagnostic imaging; Blastula - physiology; Cell activation; Cell cycle; Cell Cycle - genetics; Cell Cycle - physiology; Cell Division; Cell Nucleus - physiology; Chromatin; Chromosomes; Compartments; Development Biology; Embryos; Four-Dimensional Computed Tomography; Gene expression; Gene Expression Regulation, Developmental - genetics; Gene Expression Regulation, Developmental - physiology; Gene silencing; Genome - genetics; Genome - physiology; Genomes; Homology; Humanities and Social Sciences; Life Sciences; MicroRNAs; Models, Animal; multidisciplinary; S Phase - physiology; Science; Science (multidisciplinary); Spatio-Temporal Analysis; Transcription; Transcription, Genetic - genetics; Transcription, Genetic - physiology; Transcriptome - genetics; Zebrafish; Zebrafish - genetics; Zinc; Zinc finger proteins; Zygote - physiology
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-019-08487-5

Most metazoan embryos commence development with rapid, transcriptionally silent cell divisions, with genome activation delayed until the mid-blastula transition (MBT). However, a set of genes escapes global repression and gets activated before MBT. Here we describe the formation and the spatio-temporal dynamics of a pair of distinct transcription compartments, which encompasses the earliest gene expression in zebrafish. 4D imaging of pri-
miR430
and zinc-finger-gene activities by a novel, native transcription imaging approach reveals transcriptional sharing of nuclear compartments, which are regulated by homologous chromosome organisation. These compartments carry the majority of nascent-RNAs and active Polymerase II, are chromatin-depleted and represent the main sites of detectable transcription before MBT. Transcription occurs during the S-phase of increasingly permissive cleavage cycles. It is proposed, that the transcription compartment is part of the regulatory architecture of embryonic nuclei and offers a transcriptionally competent environment to facilitate early escape from repression before global genome activation.
Transcription is globally repressed in early stage of embryo development, but a set of genes including pri-miR-430 and zinc finger genes is known to escape the repression. Here the authors image the very first transcriptional activities in the living zebra fish embryo, demonstrating a cell cycle-coordinated polymerase II transcription compartment.