Chromatin Accessibility Dynamics and a Hierarchical Transcriptional Regulatory Network Structure for Plant Somatic Embryogenesis

Plant somatic embryogenesis refers to a phenomenon where embryos develop from somatic cells in the absence of fertilization. It provides a powerful system to produce genetically modified crops as well as to obtain artificial seeds. Previous studies have revealed that somatic embryo formation can be achieved by the treatment of somatic tissues with auxin, ectopic overexpression of a specific transcription factor, or the disruption of certain chromatin-modifying proteins. However, how auxin induces the cell totipotent state and how transcription factors trigger somatic embryogenesis are poorly understood. Here, we show that auxin rapidly rewires the cell totipotency network by altering chromatin accessibility. The analysis of chromatin accessibility dynamics further reveals a hierarchical gene regulatory network underlying somatic embryogenesis. Particularly, we find that the embryonic nature of explants is a prerequisite for somatic cell reprogramming. Upon cell reprogramming, the B3-type totipotent transcription factor LEC2 promotes somatic embryo formation by direct activation of the early embryonic patterning genes WOX2 and WOX3. Our results thus shed light on the molecular mechanism by which auxin promotes the acquisition of plant cell totipotency, and establish a direct link between cell totipotent genes and the embryonic development pathway.