A ubiquitin carboxyl-terminal hydrolase facilitates H2A.Z removal in response to phosphate starvation

The histone variant H2A.Z plays a critical role in the modulation of environmental responses, but the mechanisms regulating H2A.Z dynamics in response to stresses remain poorly understood in plants. Here we identify the ubiquitin carboxyl-terminal hydrolase UCH2 as a Pi-responsive chromatin regulator that promotes Pi starvation-induced (PSI) gene activation. We show that PHR1 recruits UCH2 to PSI gene promoters under Pi deficiency, where UCH2 deubiquitinates H2A.Z and promotes reduction in H2A.Z occupancy at PSI gene promoters. Loss of UCH2 impairs this reduction in H2A.Z occupancy, represses PSI gene induction, and reduces Pi accumulation. A catalytically inactive UCH2 mutant fails to complement these defects, and ubiquitination-deficient H2A.Z variants render plants insensitive to UCH2 loss. Our findings establish UCH2 as a critical chromatin regulator linking Pi sensing with H2A.Z dynamics and provide insights into how plants integrate chromatin-based regulation to maintain Pi homeostasis. Under phosphate starvation, plants undergo transcriptional reprogramming. Here Meng et al. show that the PHR1 transcription factor recruits the UCH2 deubiquitinase to remove ubiquitin from the H2A.Z histone variant at target genes, promoting H2A.Z eviction and activating phosphate starvation responses.