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The TRIPLE PHD FINGERS proteins are required for SWI/SNF complex-mediated +1 nucleosome positioning and transcription start site selection in Arabidopsis [RNA-seq]

ABSTRACT: In eukaryotes, DNA is associated with histones to form nucleosomes, the basic component of the chromatin. This structure presents a physical barrier for nuclear proteins to access DNA and, therefore, its plays a critical role in multiple processes such as transcription, replication and repair. Eukaryotes have evolved multiple chromatin remodelers to control nucleosome position and composition like the SWI/SNF family, which has been studied in detailed in diverse model organisms. We recently uncovered an evolutionarily conserved SWI/SNF complex in plants reminiscent of the mammalian BAF subclass, which incorporates the ATPases MINU and signature subunits TPF. In this study we characterize the impact of TPF depletion in the model plant Arabidopsis and we explore the genomic targets of the BAF complex, as well as its impact on nucleosome position and gene expression. Our results show that TPF mutants have strong developmental phenotypes, suggesting an important role in the complex function. TPF and MINU genomic targets show change in the position of the +1 nucleosome towards the promoter when the complex is mutated. While there is little correlation between this shift and changes in gene expression levels, we find a strong correlation between +1 nucleosome shift and the presence of extended 5´ regions towards the promoter in hundreds of BAF targets, suggesting a change in TSS usage. These additional 5´ UTR regions might alter RNA function and be responsible for the strong developmental phenotypes observed in the TPF and MINU mutants.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE205111 | GEO | 2022/09/16

REPOSITORIES: GEO

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The TRIPLE PHD FINGERS proteins are required for SWI/SNF complex-mediated +1 nucleosome positioning and transcription start site selection in Arabidopsis [ChIP-seq]

Project description:In eukaryotes, DNA is associated with histones to form nucleosomes, the basic component of the chromatin. This structure presents a physical barrier for nuclear proteins to access DNA and, therefore, its plays a critical role in multiple processes such as transcription, replication and repair. Eukaryotes have evolved multiple chromatin remodelers to control nucleosome position and composition like the SWI/SNF family, which has been studied in detailed in diverse model organisms. We recently uncovered an evolutionarily conserved SWI/SNF complex in plants reminiscent of the mammalian BAF subclass, which incorporates the ATPases MINU and signature subunits TPF. In this study we characterize the impact of TPF depletion in the model plant Arabidopsis and we explore the genomic targets of the BAF complex, as well as its impact on nucleosome position and gene expression. Our results show that TPF mutants have strong developmental phenotypes, suggesting an important role in the complex function. TPF and MINU genomic targets show change in the position of the +1 nucleosome towards the promoter when the complex is mutated. While there is little correlation between this shift and changes in gene expression levels, we find a strong correlation between +1 nucleosome shift and the presence of extended 5´ regions towards the promoter in hundreds of BAF targets, suggesting a change in TSS usage. These additional 5´ UTR regions might alter RNA function and be responsible for the strong developmental phenotypes observed in the TPF and MINU mutants.

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The TRIPLE PHD FINGERS proteins are required for SWI/SNF complex-mediated +1 nucleosome positioning and transcription start site selection in Arabidopsis [MNase-seq]

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The TRIPLE PHD FINGERS proteins are required for SWI/SNF complex-mediated +1 nucleosome positioning and transcription start site usage in Arabidopsis

Project description:Eukaryotes have evolved multiple ATP-dependent chromatin remodelers to shape the nucleosome landscape. We recently uncovered an evolutionarily conserved SWItch/Sucrose Non-Fermentable (SWI/SNF) chromatin remodeler complex in plants reminiscent of the mammalian BAF subclass, which specifically incorporates the MINUSCULE (MINU) catalytic subunits and the TRIPLE PHD FINGERS (TPF) signature subunits. Here we report experimental evidence that establishes the functional relevance of TPF proteins for the complex activity. Our results show that depletion of TPF triggers similar pleiotropic phenotypes and molecular defects to those found in minu mutants. Moreover, we report the genomic location of MINU2 and TPF proteins as representative members of the plant BAF-like complex and their impact on nucleosome positioning and transcription. These analyses unravel the binding of the complex to thousands of expressed genes where it modulates the position of the +1 nucleosome. These targets tend to produce 5´-shifted transcripts in the tpf and minu mutants pointing to the participation of the complex in alternative transcriptional start site (TSS) usage. Interestingly, there is a remarkable correlation between +1 nucleosome shift and upstream TSS usage suggesting their functional connection. In summary, this study unravels the function of a plant SWI/SNF complex involved in +1 nucleosome positioning and alternative TSS usage.

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Project description:BAF and PBAF are mammalian SWI/SNF family chromatin remodeling complexes that possess multiple histone/DNA-binding subunits and create nucleosome-depleted/free regions for transcription activation. Despite previous structural studies and recent advance of SWI/SNF family complexes, it remains incompletely understood how PBAF-nucleosome complex is organized. Here we determined structure of 13-subunit human PBAF in complex with acetylated nucleosome in ADP-BeF3-bound state. Four PBAF-specific subunits work together with nine BAF/PBAF-shared subunits to generate PBAF-specific modular organization, distinct from that of BAF at various regions. PBAF-nucleosome structure reveals six histone-binding domains and four DNA-binding domains/modules, the majority of which directly bind histone/DNA. This multivalent nucleosome-binding pattern, not observed in previous studies, suggests that PBAF may integrate comprehensive chromatin information to target genomic loci for function. Our study reveals molecular organization of subunits and histone/DNA-binding domains/modules in PBAF-nucleosome complex and provides structural insights into PBAF-mediated nucleosome association complimentary to the recently reported PBAF-nucleosome structure.

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A structural model of the human mSWI/SNF (BAF) complex bound to the nucleosome informs disease mechanisms

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The Swi/Snf tumor suppressor complex establishes nucleosome occupancy at target promoters [Mnase-Seq I]

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The Swi/Snf tumor suppressor complex establishes nucleosome occupancy at target promoters [Mnase-Seq II]

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ARID-DNA interactions are required for promoter occupancy by SWI/SNF

Project description:Every known SWI/SNF chromatin-remodeling complex incorporates an ARID DNA binding domain-containing subunit. Despite being a ubiquitous component of the complex, physiological roles for this domain remain undefined. Here we show that disruption of ARID1a-DNA binding in mice results in embryonic lethality, with mutant embryos manifesting prominent defects in the heart and extraembryonic vasculature. The DNA binding defective mutant ARID1a subunit is stably expressed and capable of assembling into a SWI/SNF complex with chromatin remodeling activity, but promoter occupancy by ARID1a-containing, SWI/SNF complexes (BAF-A) is impaired. Depletion of ARID domain-dependent, BAF-A associations at THROMBOSPONDIN 1 (THBS1) led to the concomitant upregulation of this anti-angiogenic protein. Using a THBS1 promoter-reporter gene, we further show that BAF-A directly regulates THBS1 promoter activity in an ARID domain-dependent manner. Our data not only demonstrate that ARID-DNA interactions are physiologically relevant in higher eukaryotes, but also indicate these interactions can facilitate SWI/SNF binding to target sites in vivo. These findings support the model wherein cooperative interactions among intrinsic subunit-chromatin interaction domains and sequence-specific transcription factors drive SWI/SNF recruitment.

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