Spatiotemporal Patterning of Zygotic Genome Activation in a Model Vertebrate Embryo

• Published in: Developmental cell Vol. 49; no. 6; pp. 852 - 866.e7
• Main Authors: Chen, Hui, Einstein, Lily C., Little, Shawn C., Good, Matthew C.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 17-06-2019
• Subjects: Animals; cell size; counter; early embryogenesis; Embryo, Nonmammalian - cytology; Embryo, Nonmammalian - metabolism; Embryonic Development; Female; Gene Expression Regulation, Developmental; Genome; Male; miniature embryo; nascent transcription; single cell; Single-Cell Analysis; sizer; Spatio-Temporal Analysis; spatiotemporal pattern; timer; Transcriptome; Xenopus laevis - embryology; Xenopus Proteins - genetics; Xenopus Proteins - metabolism; Zygote - cytology; Zygote - metabolism; zygotic genome activation; timer; single cell; spatiotemporal pattern; nascent transcription; miniature embryo; sizer; early embryogenesis; counter; cell size; zygotic genome activation
• ISSN: 1534-5807; 1878-1551
• DOI: 10.1016/j.devcel.2019.05.036

A defining feature of early embryogenesis is the transition from maternal to zygotic control. This transition requires embryo-wide zygotic genome activation (ZGA), but the extent of spatiotemporal coordination of ZGA between individual cells is unknown. Multiple interrelated parameters, including elapsed time, completed cycles of cell division, and cell size may impact ZGA onset; however, the principal determinant of ZGA during vertebrate embryogenesis is debated. Here, we perform single-cell imaging of large-scale ZGA in whole-mount Xenopus embryos. We find a striking new spatiotemporal pattern of ZGA whose onset tightly correlates with cell size but not with elapsed time or number of cell divisions. Further, reducing cell size induces premature ZGA, dose dependently. We conclude that large-scale ZGA is not spatially uniform and that its onset is determined at the single-cell level, primarily by cell size. Our study suggests that spatial patterns of ZGA onset may be a common feature of embryonic systems.
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•Quantitative, single-cell imaging of nascent transcription during early embryogenesis•Large-scale ZGA onset is not globally uniform; it follows a stereotypic spatial pattern•Patterned ZGA onset is explained by a cell sizer, not a simple timer or cycle counter•Reducing cell size is sufficient to trigger precocious ZGA in Xenopus embryos
Zygotic genome activation (ZGA) is a hallmark of early embryonic development. Chen et al. imaged nascent transcripts at the single-cell level in Xenopus whole-mount embryos, discovering a stereotypic spatiotemporal pattern of large-scale ZGA. This patterned ZGA onset is dependent on cells reaching a threshold size, not time or cell-cycle count.