Histone deacetylases and cell-cycle regulators orchestrate cell-identity transitions during Arabidopsis root regeneration

The widespread regenerative capacity of plants is mediated by the ability of specialized cells to reprogram their fate, but the sequential cellular states of regenerating plant cells remain an open question. Here, we characterize the trajectory of cellular reprogramming during Arabidopsis root regeneration using single-cell RNA sequencing, ATAC sequencing, imaging, and mutant analysis. The earliest events during regeneration are dependent on repressive chromatin modification, where Multiome and genetic analysis showed that class I histone deacetylases (HDACs) HDA9 and HDA19 play a role in shutting down old identities and to prevent a runaway stress response. Cell division mediates a second step needed for the acquisition of many new identity markers, where division rates were tuned by the DOF transcription factor OBP1 that accelerates and SMR5, SMR7, and SMR10 that decelerate division rates hours later. Collectively, our study provides mechanistic insights into how plants actively mediate the loss of remnant identities within hours of injury and then tune cell-division rates to rapidly reprogram cells to new identities.