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

ABSTRACT: Global warming imposes a major threat to plant growth and crop production. In some plants including Arabidopsis thaliana, elevated temperatures induce a series of morphological and developmental adjustments, termed thermomorphogenesis to facilitate plant cooling under high-temperature conditions. Plant thermal response is suppressed by histone variant H2A.Z. At warm temperatures, H2A.Z is evicted from nucleosomes at thermo-responsive genes, resulting in their activation. However, the mechanisms that regulate H2A.Z eviction and subsequent transcription activation are largely unknown. Here, we show that the ino80 chromatin-remodeling complex (ino80-C) promotes thermomorphogenesis and activates the expression of thermo-responsive and auxin-related genes. ino80-C associates with PHYTOCHROME-INTERACTING FACTOR 4 (PIF4), a potent regulator in thermomorphogenesis, and mediates temperature-induced H2A.Z eviction at PIF4 targets. Moreover, ino80-C directly interacts with COMPASS-like and transcription elongation factors to promote active histone modification Histone H3 lysine 4 trimethylation (H3K4me3) and RNA Polymerase II (RNA Pol II) elongation, leading to the thermal induction of transcription. Notably, transcription elongation factors are required for the eviction of H2A.Z at PIF4 targets, suggesting the cooperation of ino80-C and transcription elongation in H2A.Z removal. Our results demonstrate that the (PIF4)-(ino80-C)-(COMPASS-like)-(transcription elongator) module controls plant thermal response, and establish a link between H2A.Z eviction and active transcription.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE168118 | GEO | 2021/11/27

REPOSITORIES: GEO

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

Project description:Global warming imposes a major threat to plant growth and crop production. In some plants including Arabidopsis thaliana, elevated temperatures induce a series of morphological and developmental adjustments, termed thermomorphogenesis to facilitate plant cooling under high-temperature conditions. Plant thermal response is suppressed by histone variant H2A.Z. At warm temperatures, H2A.Z is evicted from nucleosomes at thermo-responsive genes, resulting in their activation. However, the mechanisms that regulate H2A.Z eviction and subsequent transcription activation are largely unknown. Here, we show that the ino80 chromatin-remodeling complex (ino80-C) promotes thermomorphogenesis and activates the expression of thermo-responsive and auxin-related genes. ino80-C associates with PHYTOCHROME-INTERACTING FACTOR 4 (PIF4), a potent regulator in thermomorphogenesis, and mediates temperature-induced H2A.Z eviction at PIF4 targets. Moreover, ino80-C directly interacts with COMPASS-like and transcription elongation factors to promote active histone modification Histone H3 lysine 4 trimethylation (H3K4me3) and RNA Polymerase II (RNA Pol II) elongation, leading to the thermal induction of transcription. Notably, transcription elongation factors are required for the eviction of H2A.Z at PIF4 targets, suggesting the cooperation of ino80-C and transcription elongation in H2A.Z removal. Our results demonstrate that the (PIF4)-(ino80-C)-(COMPASS-like)-(transcription elongator) module controls plant thermal response, and establish a link between H2A.Z eviction and active transcription.

2021-11-27 | GSE168119 | GEO

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

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 [RNA-seq III]

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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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Project description:INO80 complex promotes thermomorphogenesis by integrating H2A.Z eviction and active transcription

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The novel chemical growth regulator ‘Heatin’ stimulates thermomorphogenesis by inhibiting the Arabidopsis thaliana NIT1-subfamily of nitrilases

Project description:Temperature passively affects many biological processes. It is therefore challenging to study dedicated temperature signalling pathways orchestrating plant thermomorphogenesis, a suite of elongation growth-based adaptations that enhance leaf cooling capacity. We screened a chemical library for compounds that restored abolished hypocotyl elongation in the pif4-2 deficient mutant background in the model plant Arabidopsis thaliana to identify novel regulators of thermomorphogenesis. The small aromatic compound ‘Heatin’, with 1-aminomethyl-2-naphthol as minimal active moiety, was isolated as potent enhancer of elongation growth. Following a chemical proteomics approach, the NITRILASE1-subfamily auxin biosynthesis enzymes were identified as molecular targets of Heatin. We show that Heatin inhibits NIT1-subfamily enzymatic activity and that accumulation of its substrate indole-3-acetonitrile (IAN) is sufficient for elongation growth in a NIT1-subfamily-dependent manner. Our work assigns a role for NITRILASE1-subfamily in mediating elongation growth. Moreover, Heatin and its functional analogues present novel chemical entities for understanding auxin biology.

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MPK4 mediated phosphorylation of PIF4 controls thermosensing by regulation of H2A.Z deposition in Arabidopsis

Project description:Plants have the ability to perceive a slight upsurge in ambient temperature and respond by undergoing morphological changes, such as elongated hypocotyls and early flowering. The dynamic functioning of PHYTOCHROME INTERACTING FACTOR4 (PIF4) in thermomorphogenesis has been well established, although the regulatory pathway involved in thermosensing is not deciphered completely. In our study, we demonstrate that an increase in temperature from 22˚C to 28˚C induces the phosphorylation of PIF4 by MITOGEN-ACTIVATED PROTEIN KINASE 4 (MPK4) which shows high expression and activation at 28˚C. Phosphorylated PIF4 represses the expression of ACTIN-RELATED PROTEIN 6 (ARP6) that is required for mediating histone variant H2A.Z deposition at its target gene loci. We demonstrate that variation of ARP6 expression in PIF4 phosphor -null and phosphor-mimetic seedlings affects hypocotyl growth and flowering at 22˚C and 28˚C. Further, we show that change in ARP6 expression affects H2A.Z deposition at the loci of genes involved in hypocotyl elongation using PIF4 phosphor -null and phosphor-mimetic seedlings. Interestingly, the expression of MPK4 is also controlled by H2A.Z deposition in temperature dependent manner. Taken together, our findings highlight the cumulative molecular interplay between MPK4, PIF4, and chromatin modification by ARP6-mediated H2A.Z deposition as a regulatory mechanism of thermosensing.

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The INO80 chromatin remodeling complex promotes thermomorphogenesis by connecting H2A.Z eviction and active transcription in Arabidopsis

Project description:The INO80 chromatin remodeling complex promotes thermomorphogenesis by connecting H2A.Z eviction and active transcription in Arabidopsis

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B-box family proteins BBX18 and BBX23 control thermoresponsive hypocotyl growth in Arabidopsis

Project description:Plants coordinate their growth and developmental programs with various endogenous signals and environmental challenges such as seasonal and diurnal temperature fluctuations. The bHLH transcription factor PIF4 plays critical roles in thermoresponsive hypocotyl growth in Arabidopsis, and the evening complex component ELF3 negatively regulates PIF4's activity for downstream gene expression and hypocotyl elongation at elevated temperature. However, how warm temperature signal is transmitted to ELF3 is not known. Here, we report the identification of two B-Box protein BBX18/BBX23 as new regulators of thermomorphogenesis in Arabidopsis. Mutations of BBX18/BBX23 confer reduced thermoresponsive hypocotyl elongation. Overexpression of BBX18 enhances the sensitivity of hypocotyl growth to elevated temperature, which is dependent on the function of PIF4 and RING E3 ligase COP1, respectively. Both BBX18 and BBX23 interact with ELF3 or COP1, relegating the protein abundance of ELF3 at warm temperature. Further, the expression of multiple thermoresponsive genes is impaired in both the PIF4 single mutant and BBX18/BBX23 double mutant. In addition, both the transcription and protein levels of BBX18/BBX23 are up-regulated by elevated ambient temperature. Thus, our findings reveal the important roles of B-Box proteins in plant thermomorphogenesis, and build a new connection from warm temperature information to ELF3 and its downstream signaling components.

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