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FVE and HDA9 form a complex to promote thermomorphogenesis by reducing H2A.Z deposition through histone deacetylation [RNA-Seq]

ABSTRACT: 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 PIF4-regulated auxin-related genes, enabling their transcriptional activation. Interestingly, this activation also requires the histone deacetylase HDA9, raising the question of how histone deacetylation, typically associated with transcriptional repression, can instead promote gene activation. Here, we identify FVE as a co-regulator that partners with HDA9 to activate PIF4 target genes at elevated temperatures. PIF4 directly interacts with and recruits the FVE-HDA9 complex to its target genes to remove acetylation from histone H4 and H2A.Z. We show that H2A.Z acetylation is required for recruiting the SWR1 complex, which deposits H2A.Z. Consequently, FVE-HDA9-mediated deacetylation reduces SWR1 complex binding and limits H2A.Z deposition. Moreover, we demonstrate that in addition to limiting H2A.Z deposition, H2A.Z depletion also results from H2A.Z eviction mediated by the INO80 complex. Together, these findings uncover a dual mechanism contributing to H2A.Z depletion: INO80-mediated active eviction and histone deacetylation-mediated inhibition of H2A.Z deposition, which underlies PIF4 target gene activation and explain the paradoxical role of histone deacetylation in transcriptional activation.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE303133 | GEO | 2026/01/29

REPOSITORIES: GEO

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FVE and HDA9 form a complex to promote thermomorphogenesis by reducing H2A.Z deposition through histone deacetylation [ChIP-Seq]

Project description: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 PIF4-regulated auxin-related genes, enabling their transcriptional activation. Interestingly, this activation also requires the histone deacetylase HDA9, raising the question of how histone deacetylation, typically associated with transcriptional repression, can instead promote gene activation. Here, we identify FVE as a co-regulator that partners with HDA9 to activate PIF4 target genes at elevated temperatures. PIF4 directly interacts with and recruits the FVE-HDA9 complex to its target genes to remove acetylation from histone H4 and H2A.Z. We show that H2A.Z acetylation is required for recruiting the SWR1 complex, which deposits H2A.Z. Consequently, FVE-HDA9-mediated deacetylation reduces SWR1 complex binding and limits H2A.Z deposition. Moreover, we demonstrate that in addition to limiting H2A.Z deposition, H2A.Z depletion also results from H2A.Z eviction mediated by the INO80 complex. Together, these findings uncover a dual mechanism contributing to H2A.Z depletion: INO80-mediated active eviction and histone deacetylation-mediated inhibition of H2A.Z deposition, which underlies PIF4 target gene activation and explain the paradoxical role of histone deacetylation in transcriptional activation.

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Project description:Plants can sense temperature changes and adjust their development and morphology accordingly in a process called thermomorphogenesis. This phenotypic plasticity implies complex mechanisms regulating gene expression reprogramming in response to environmental alteration. Histone variants contribute to the chromatin dynamics and transcriptional control, yet how their deposition/eviction modulates transcriptional changes induced by environmental cues remains elusive. In Arabidopsis thaliana, temperature elevation-induced transcriptional activation at thermo-responsive genes entails the chromatin eviction of a histone variant H2A.Z by INO80, which is recruited to these loci via interacting with a key thermomorphogenesis regulator PHYTOCHROME-INTERACTING FACTOR 4 (PIF4). Here, we show that both INO80 and the deposition chaperones of another histone variant H3.3 associate with EARLY FLOWERING7 (ELF7), a critical component of the transcription elongation factor polymerase-associated factor 1 complex (PAF1c). H3.3 promotes thermomorphogenesis and the high temperature-enhanced RNA Pol II transcription at PIF4 targets, and it is broadly required for the H2A.Z removal-induced gene activation. Reciprocally, INO80 and ELF7 regulate H3.3 deposition, and are necessary for the high temperature-induced H3.3 enrichment at PIF4 targets. Our findings demonstrate close coordination between H2A.Z eviction and H3.3 deposition in gene activation induced by high temperature, and pinpoint the importance of histone variants dynamics in transcriptional regulation.

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Coordinated histone variant H2A.Z eviction and H3.3 deposition control plant thermomorphogenesis [HTR5-GFP ChIP-seq]

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Coordinated histone variant H2A.Z eviction and H3.3 deposition control plant thermomorphogenesis [RNA-seq II]

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Coordinated histone variant H2A.Z eviction and H3.3 deposition control plant thermomorphogenesis [RNA-seq III]

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The INO80 chromatin remodeling complex promotes thermomorphogenesis by connecting H2A.Z eviction and active transcription in Arabidopsis[RNA-seq]

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FVE and HDA9 form a complex to promote thermomorphogenesis by reducing H2A.Z deposition through histone deacetylation [RNA-Seq]

Project description:FVE and HDA9 form a complex to promote thermomorphogenesis by reducing H2A.Z deposition through histone deacetylation [RNA-Seq]

| PRJNA1294226 | ENA

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