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Tissue homeostasis and regeneration rely on mobilisation of tissue resident progenitor cells or de-differentiation of functional cell types. We have found that a small number of mature vascular smooth muscle cell (VSMC) expand clonally in response to vascular injury. This suggested the existence of rare VSMC that are primed to respond to injury. We have delineated molecular VSMC heterogeneity by profiling individual cells from healthy arteries. We identified a small subset of cells co-expressing VSMC markers (Acta2, Tagln) with the progenitor cells marker Sca1. Our results suggest that Sca1-expression in VSMCs mark a spectrum of phenotypically distinct states ranging from quiescent, contractile to activated cells that may be more responsive to injury-induced cues. These signatures will allow future functional testing of specific cell subsets in animal models and identification of equivalent cell populations in human arteries, which can be activated to promote vascular remodelling in tissue regeneration.