How dermis maintains tissue homeostasis in cyclic growth and wounding is a fundamental un-solved question. Here we study how dermal components of feather follicles undergo physiological (molting) and plucking injury-induced regeneration. Proliferation analyses reveal quiescent, transient-amplifying, and long-term label-retaining dermal cell (LRDC) states. In Growth phase, LRDCs are activated to make new dermal components with distinct cellular flows. Dermal transient amplifying (TA) cells, enriched in the proximal follicle, generate (i) peripheral pulp which extends distally to expand the epithelial-mesenchymal interactive interface for barb patterning, and (ii) central pulp which provides nutrition. Entering Resting phase, LRDCs, accompanying collar bulge epidermal LRC cells, descend to the apical dermal papilla. In the next cycle, these apical derma papilla LRDCs are re-activated to become new pulp progenitor TA cells. In growth phase, lower dermal sheath can generate dermal papilla and pulp. Transcriptome analyses identify marker genes and highlight molecular signaling associated with dermal specification. We compare cyclic topological changes with that of hair follicle, a convergently evolved follicle configuration. The work presents a model for analyzing homeostasis and tissue remodeling of mesenchymal progenitors.

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