Epidermal injury-induced derepression of key regulator ATML1 in newly exposed cells elicits epidermis regeneration

Plant cell fate determination depends on the relative positions of the cells in developing organisms. The shoot epidermis, the outermost cell layer of the above-ground organs in land plants, protects plants from environmental stresses. How the shoot epidermis is formed only from the outermost cells has remained unknown. Here we show that when inner leaf mesophyll cells are exposed to the surface, these cells show up-regulation of ATML1, a master regulator for epidermal cell identity in Arabidopsis thaliana. Epidermal cell types such as stomatal guard cells regenerate from young inner-lineage tissues that have a potential to accumulate ATML1 protein after epidermal injury. Surgical analyses indicate that application of pressure to the exposed site was sufficient to inhibit ATML1 derepression in the outermost mesophyll cells, suggesting this process requires pressure release. Furthermore, pharmacological analyses suggest that ATML1 derepression in the outermost mesophyll cells require cortical microtubule formation, MAPK signaling and proteasome activity. Our results suggest that surface-positional cues involving mechanical signaling are used to restrict ATML1 activity to the outermost cells and facilitate epidermal differentiation.