BACKGROUND: Embryos are regeneration and wound healing masters. They rapidly close wounds and scarlessly remodel and regenerate injured tissue. Regeneration has been extensively studied in many animal models using new tools such as single-cell analysis. However, until now, they have been based primarily on experiments assessing from 1 day post injury. RESULTS: In this paper, we reveal that critical steps initiating regeneration occur within hours after injury. We discovered the regeneration initiating cells (RICs) using single-cell and spatial transcriptomics of the regenerating Xenopus laevis tail. RICs are formed transiently from the basal epidermal cells, and their expression signature suggests they are important for modifying the surrounding extracellular matrix thus regulating development. The absence or deregulation of RICs leads to excessive extracellular matrix deposition and defective regeneration. CONCLUSION: RICs represent a newly discovered transient cell state involved in the initiation of the regeneration process.

1st Faculty of Medicine Charles University Prague 2 Czech Republic

1st Faculty of Medicine Institute of Anatomy Charles University Prague 2 128 00 Czech Republic

Department Dermatovenereology 1st Faculty of Medicine and General University Hospital Charles University Prague Czech Republic

Faculty of Fisheries and Protection of Waters South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses University of South Bohemia in Ceske Budejovice Vodnany 389 25 Czech Republic

Faculty of Science Charles University Prague 2 Czech Republic

Laboratory of Gene Expression Institute of Biotechnology of the Czech Academy of Sciences Vestec 252 50 Czech Republic

Laboratory of Molecular Therapy Institute of Biotechnology of the Czech Academy of Sciences Vestec 252 50 Czech Republic

School of Pharmacy and Medical Science Griffith University Southport QLD Australia

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