Dynamic chromatin state profiling reveals regulatory roles of auxin and cytokinin in shoot regeneration

Highlights•The dynamic chromatin state landscape during shoot regeneration is revealed•Collapse of pluripotency in the absence of cytokinin signaling•Generation of a catalog of regulatory sequences during shoot regeneration•A cohort of transcription factors involved in shoot regeneration is outlinedSummaryShoot regeneration is mediated by the sequential action of two phytohormones, auxin and cytokinin. However, the chromatin regulatory landscapes underlying this dynamic response have not yet been studied. In this study, we jointly profiled chromatin accessibility, histone modifications, and transcriptomes to demonstrate that a high auxin/cytokinin ratio environment primes Arabidopsis shoot regeneration by increasing the accessibility of the gene loci associated with pluripotency and shoot fate determination. Cytokinin signaling not only triggers the commitment of the shoot progenitor at later stages but also allows chromatin to maintain shoot identity genes at the priming stage. Our analysis of transcriptional regulatory dynamics further identifies a catalog of regeneration cis-elements dedicated to cell fate transitions and uncovers important roles of BES1, MYC, IDD, and PIF transcription factors in shoot regeneration. Our results, thus, provide a comprehensive resource for studying cell reprogramming in plants and provide potential targets for improving future shoot regeneration efficiency.Graphical abstract