Epidermal identity is maintained by cell-cell communication via a universally active feedback-loop in Arabidopsis thaliana

The transcription factors ATML1 and PDF2 are indispensable for epidermal cell fate specification in Arabidopsis embryos. However, the regulation of these genes, and in particular their relationship with cell-cell signalling pathways, although the subject of considerable speculation, remains unclear. Here we demonstrate that the receptor kinase ACR4 positively affects the expression of ATML1 and PDF2 in seedlings. In contrast, ATML1 and PDF2 containing complexes directly and negatively affect both their own expression and that of ACR4. By modelling the resulting feedback loop we demonstrate a network structure capable of maintaining robust epidermal cell identity post germination. We show that a second seed-specific signalling pathway involving the subtilase ALE1 and the receptor kinases GSO1 and GSO2, acts parallel to the epidermal loop to control embryonic surface formation via an ATML1/PDF2 independent pathway. Genetic interactions between components of this linear pathway and of the epidermal loop suggest that an intact embryo surface is necessary for the initiation and/or stabilization of the epidermal loop specifically during early embryogenesis.