A single-cell time-lapse of mouse prenatal development from gastrula to birth

Chengxiang Qiu (), Beth K. Martin, Ian C. Welsh, Riza M. Daza, Truc-Mai Le, Xingfan Huang, Eva K. Nichols, Megan L. Taylor, Olivia Fulton, Diana R. O’Day, Anne Roshella Gomes, Saskia Ilcisin, Sanjay Srivatsan, Xinxian Deng, Christine M. Disteche, William Stafford Noble, Nobuhiko Hamazaki, Cecilia B. Moens, David Kimelman, Junyue Cao, Alexander F. Schier, Malte Spielmann, Stephen A. Murray, Cole Trapnell and Jay Shendure ()
Additional contact information
Chengxiang Qiu: University of Washington
Beth K. Martin: University of Washington
Ian C. Welsh: The Jackson Laboratory
Riza M. Daza: University of Washington
Truc-Mai Le: Brotman Baty Institute for Precision Medicine
Xingfan Huang: University of Washington
Eva K. Nichols: University of Washington
Megan L. Taylor: University of Washington
Olivia Fulton: University of Washington
Diana R. O’Day: Brotman Baty Institute for Precision Medicine
Anne Roshella Gomes: Brotman Baty Institute for Precision Medicine
Saskia Ilcisin: Brotman Baty Institute for Precision Medicine
Sanjay Srivatsan: University of Washington
Xinxian Deng: University of Washington
Christine M. Disteche: University of Washington
William Stafford Noble: University of Washington
Nobuhiko Hamazaki: University of Washington
Cecilia B. Moens: Fred Hutchinson Cancer Center
David Kimelman: University of Washington
Junyue Cao: The Rockefeller University
Alexander F. Schier: University of Basel
Malte Spielmann: Max Planck Institute for Molecular Genetics
Stephen A. Murray: The Jackson Laboratory
Cole Trapnell: University of Washington
Jay Shendure: University of Washington

Nature, 2024, vol. 626, issue 8001, 1084-1093

Abstract: Abstract The house mouse (Mus musculus) is an exceptional model system, combining genetic tractability with close evolutionary affinity to humans1,2. Mouse gestation lasts only 3 weeks, during which the genome orchestrates the astonishing transformation of a single-cell zygote into a free-living pup composed of more than 500 million cells. Here, to establish a global framework for exploring mammalian development, we applied optimized single-cell combinatorial indexing3 to profile the transcriptional states of 12.4 million nuclei from 83 embryos, precisely staged at 2- to 6-hour intervals spanning late gastrulation (embryonic day 8) to birth (postnatal day 0). From these data, we annotate hundreds of cell types and explore the ontogenesis of the posterior embryo during somitogenesis and of kidney, mesenchyme, retina and early neurons. We leverage the temporal resolution and sampling depth of these whole-embryo snapshots, together with published data4–8 from earlier timepoints, to construct a rooted tree of cell-type relationships that spans the entirety of prenatal development, from zygote to birth. Throughout this tree, we systematically nominate genes encoding transcription factors and other proteins as candidate drivers of the in vivo differentiation of hundreds of cell types. Remarkably, the most marked temporal shifts in cell states are observed within one hour of birth and presumably underlie the massive physiological adaptations that must accompany the successful transition of a mammalian fetus to life outside the womb.

Date: 2024
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DOI: 10.1038/s41586-024-07069-w

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