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In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript. Tissue stem cells are generated from a population of embryonic progenitors through organ-specific morphogenetic events 1 , 2. Although tissue stem cells are central to organ homeostasis and regeneration, it remains unclear how they are induced during development, mainly because of the lack of markers that exclusively label prospective stem cells.

Here we combine marker-independent long-term 3D live imaging and single-cell transcriptomics to capture a dynamic lineage progression and transcriptome changes in the entire epithelium of the mouse hair follicle as it develops. We found that the precursors of different epithelial lineages were aligned in a 2D concentric manner in the basal layer of the hair placode. Each concentric ring acquired unique transcriptomes and extended to form longitudinally aligned, 3D cylindrical compartments.

Prospective bulge stem cells were derived from the peripheral ring of the placode basal layer, but not from suprabasal cells as was previously suggested 3. The fate of placode cells is determined by the cell position, rather than by the orientation of cell division.

We also identified 13 gene clusters: the ensemble expression dynamics of these clusters drew the entire transcriptional landscape of epithelial lineage diversification, consistent with cell lineage data. Your institute does not have access to this article. Cell Research Open Access 12 July Any other relevant data are available from the corresponding author upon reasonable request.

Source data are provided with this paper. Xin, T. Hardwiring stem cell communication through tissue structure. Cell , — Guiu, J. Tracing the origin of adult intestinal stem cells. Nature , — Ouspenskaia, T. Article Google Scholar. Lecuit, T. Proximal—distal axis formation in the Drosophila leg. Ruiz-Losada, M. Specification and patterning of Drosophila appendages.

Pispa, J. Mechanisms of ectodermal organogenesis. Fujiwara, H. Multi-tasking epidermal stem cells: beyond epidermal maintenance. Growth Differ. Solanas, G. Regenerating the skin: a task for the heterogeneous stem cell pool and surrounding niche.

Cell Biol. Nowak, J. Hair follicle stem cells are specified and function in early skin morphogenesis. Cell Stem Cell 3 , 33—43 Liu, Y. Keratin 15 promoter targets putative epithelial stem cells in the hair follicle bulge.

Rhee, H. Lhx2 maintains stem cell character in hair follicles. Science , — Horsley, V. NFATc1 balances quiescence and proliferation of skin stem cells. Xu, Z. Morita, R. Coordination of cellular dynamics contributes to tooth epithelium deformations. Tsutsui, H. Semi-rational engineering of a coral fluorescent protein into an efficient highlighter. EMBO Rep. Hayashi, T. Qiu, X. Single-cell mRNA quantification and differential analysis with Census.

Methods 14 , — Reversed graph embedding resolves complex single-cell trajectories. Huelsken, J. Sostdc1 defines the size and number of skin appendage placodes.

Kandyba, E. Natl Acad. USA , — Genander, M. Cell Stem Cell 15 , — Joost, S. Single-cell transcriptomics reveals that differentiation and spatial signatures shape epidermal and hair follicle heterogeneity. Cell Syst. Smad1 and 5 but not Smad8 establish stem cell quiescence which is critical to transform the premature hair follicle during morphogenesis toward the postnatal state. Stem Cells 32 , — Saxena, N. An updated classification of hair follicle morphogenesis. Maini, P.

The Turing model comes of molecular age. Ahtiainen, L. Directional cell migration, but not proliferation, drives hair placode morphogenesis. Cell 28 , — Glover, J. Hierarchical patterning modes orchestrate hair follicle morphogenesis. PLoS Biol. Abe, T. Establishment of conditional reporter mouse lines at ROSA26 locus for live cell imaging. Genesis 49 , — Vassar, R. Tissue-specific and differentiation-specific expression of a human K14 keratin gene in transgenic mice.

USA 86 , — Sakaue-Sawano, A. Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Biggs, L. Hair follicle dermal condensation forms via Fgf20 primed cell cycle exit, cell motility, and aggregation. Stuart, T. Comprehensive integration of single-cell data. La Manno, G. RNA velocity of single cells. Angerer, P. Bioinformatics 32 , — Street, K. Slingshot: cell lineage and pseudotime inference for single-cell transcriptomics. BMC Genomics 19 , Yu, G.