FVE and HDA9 form a complex to promote thermomorphogenesis by reducing H2A.Z deposition through histone deacetylation

Many plants, including Arabidopsis thaliana, respond to elevated ambient temperatures by altering their growth through a process known as thermomorphogenesis. This response involves the depletion of the repressive histone variant H2A.Z from the gene bodies of certain PHYTOCHROME INTERACTING FACTOR 4 (PIF4)-regulated auxin-related genes, enabling their transcriptional activation. Intriguingly, this activation also requires HISTONE DEACETYLASE 9 (HDA9), which is generally considered a transcriptional repressor due to its role in removing permissive histone acetylation marks such as H3 acetylation. This raises the question of how a histone deacetylase can instead promote gene activation. Here, we identify FVE as a co-regulator that partners with HDA9 to activate a subset of PIF4 target genes at elevated temperatures. PIF4 directly interacts with and recruits the FVE-HDA9 complex to its target genes, where it removes acetylation from histone H4 and H2A.Z. This deacetylation coincides with reduced binding of the SWI2/SNF2-RELATED 1 (SWR1) complex responsible for H2A.Z deposition. Mutating acetylated residues on H2A.Z also diminishes SWR1 complex recruitment and H2A.Z accumulation across gene bodies, suggesting the importance of these residues, probably through their acetylation, in promoting H2A.Z deposition. Moreover, we show that, in addition to limiting H2A.Z deposition, H2A.Z depletion also results from INO80-mediated eviction. Together, these findings suggest a dual mechanism underlying H2A.Z depletion: active H2A.Z eviction and inhibition of H2A.Z deposition by deacetylation of likely H2A.Z and other histones. This mechanism underlies PIF4 target gene activation and provides a plausible explanation for the seemingly paradoxical role of histone deacetylation in transcriptional activation.