Organization, genomic targeting and assembly of three distinct SWI/SNF chromatin remodeling complexes in<i>Arabidopsis</i>

Fu, Wei; Yu, Yaoguang; Yu, Zewang; Zhu, Tao; Zhong, Yixiong; Zhang, Zhihao; Liang, Zeyin; Cui, Yuhai; Chen, Chen; Li, Chenlong

doi:10.1101/2022.11.24.517835

Cited by 3 publications

(6 citation statements)

References 58 publications

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“…Our data is also consistent with LFR being a component of a MINU1/2 ATPase‐containing SWI/SNF complex (Diego‐Martin et al., 2022), although in this case, the interaction between LFR and MINU1/2 would be indirect. During the review of our manuscript, two recent studies reported that LFR is involved in both the SAS and MAS complex (SYD‐ and MINU1/2‐associated SWI/SNF complexes) (Fu et al., 2023; Guo et al., 2022), which serves as supports of our work. Indeed, multiple SAS or MAS components were specifically co‐purified with LFR‐3FLAG in our IP‐MS assays (Figure 1c).…”

Section: Discussionsupporting

confidence: 73%

The regulation of chromatin configuration at AGAMOUS locus by LFR‐SYD‐containing complex is critical for reproductive organ development in Arabidopsis

et al. 2023

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SUMMARYSwitch defective/sucrose non‐fermentable (SWI/SNF) chromatin remodeling complexes are evolutionarily conserved, multi‐subunit machinery that play vital roles in the regulation of gene expression by controlling nucleosome positioning and occupancy. However, little is known about the subunit composition of SPLAYED (SYD)‐containing SWI/SNF complexes in plants. Here, we show that the Arabidopsis thaliana Leaf and Flower Related (LFR) is a subunit of SYD‐containing SWI/SNF complexes. LFR interacts directly with multiple SWI/SNF subunits, including the catalytic ATPase subunit SYD, in vitro and in vivo. Phenotypic analyses of lfr‐2 mutant flowers revealed that LFR is important for proper filament and pistil development, resembling the function of SYD. Transcriptome profiling revealed that LFR and SYD shared a subset of co‐regulated genes. We further demonstrate that the LFR and SYD interdependently activate the transcription of AGAMOUS (AG), a C‐class floral organ identity gene, by regulating the occupation of nucleosome, chromatin loop, histone modification, and Pol II enrichment on the AG locus. Furthermore, the chromosome conformation capture (3C) assay revealed that the gene loop at AG locus is negatively correlated with the AG expression level, and LFR‐SYD was functional to demolish the AG chromatin loop to promote its transcription. Collectively, these results provide insight into the molecular mechanism of the Arabidopsis SYD‐SWI/SNF complex in the control of higher chromatin conformation of the floral identity gene essential to plant reproductive organ development.

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Section: Discussionsupporting

confidence: 73%

The regulation of chromatin configuration at AGAMOUS locus by LFR‐SYD‐containing complex is critical for reproductive organ development in Arabidopsis

et al. 2023

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“…4B; Supplemental Dataset 5). Previous studies have indicated that, in seedlings, BAS and SAS share the majority of their binding peaks, while most of the binding peaks of MAS are different from those of BAS and SAS (Guo et al, 2022; Fu et al, 2023). The overlapping patterns of BAS, SAS, and MAS peaks in inflorescences were similar to those in seedlings (Supplemental Fig.…”

Section: Resultsmentioning

confidence: 98%

“…SWI/SNF complexes play crucial roles in the regulation of diverse developmental processes in both metazoans and plants. Recent studies have illustrated the functional variations among the three Arabidopsis SWI/SNF complexes: BAS, SAS, and MAS (Guo et al, 2022; Fu et al, 2023). However, the precise mechanisms by which these complexes exert specific functions during different developmental stages remain largely unknown.…”

Section: Discussionmentioning

confidence: 99%

“…Recent studies utilizing affinity purification followed by mass spectrometry (AP-MS) analysis have identified three classes of SWI/SNF complexes in Arabidopsis: the BRM-associated SWI/SNF (BAS) complex, the SYD-associated SWI/SNF (SAS) complex, and the MINU1/2-associated SWI/SNF (MAS) complex. Each of these complexes is composed of 8-15 subunits, with some subunits being specific to a particular complex, while others are shared by two or three complexes (Guo et al, 2022; Fu et al, 2023). However, the precise roles of different Arabidopsis SWI/SNF complexes in specific developmental processes remain elusive.…”

Section: Introductionmentioning

confidence: 99%

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The SAS Chromatin-Remodeling Complex Mediates Inflorescence-Specific Chromatin Accessibility for Transcription Factor Binding

Guo,

Liu,

et al. 2024

Preprint

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While the role of transcription factors in flower development is well understood, the effect of chromatin remodeling on this process remains largely unclear. We conducted a comprehensive analysis to investigate the genome-wide effects of the SAS, BAS, and MAS-type SWI/SNF complexes on chromatin accessibility and gene transcription in both seedlings and inflorescences ofArabidopsis thaliana. Our results indicate that the SAS complex plays a crucial role in promoting the accessibility of genes involved in flower development. Within inflorescences, the SAS complex binds to numerous genes related to flower development and is responsible for establishing chromatin accessibility at distal promoter and upstream intergenic regions of these genes. In contrast, the BAS and MAS complexes exhibit minimal involvement in regulating the accessibility of these genes. Notably, the genomic regions bound by the SAS complex are enriched with sites occupied by multiple MADS family transcription factors associated with flower development. This study highlights the significant role of the SAS complex in modulating chromatin accessibility during flower development, providing insights into the dynamic regulation of chromatin remodeling during plant development.One-sentence summaryThe SAS-type SWI/SNF complex establishes chromatin accessibility at distal promoter and upstream intergenic regions of flower development-related genes, thereby contributing to flower development.

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“…Active regulatory DNA regions require continuous chromatin remodeling activity of SWI/SNF complexes; therefore, their activities must be tightly regulated to ensure fidelity and plasticity of genomic processes (39,40). In Arabidopsis, three subclasses of SWI/SNF chromatin remodeling complexes were identified: BRM-associated SWI/SNF complexes (BAS), SPLAYEDassociated SWI/SNF complexes (SAS), and MINUSCULE-associated SWI/SNF complexes (MAS) (41,42). However, the molecular mechanisms responsible for the precise localization of SWI/SNF chromatin remodeling complexes to specific genomic loci, therefore ensuring their proper activity during the intricate processes of growth and development, remain obscure.…”

Section: Introductionmentioning

confidence: 99%

SWI/SNF chromatin remodeling determines brassinosteroid-induced transcriptional activation

Tao

Wei

et al. 2023

Preprint

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The brassinosteroid (BR) hormone is a central modulator of plant growth, development, and responses to stresses by activating or repressing the expression of thousands of genes through the transcription factor BRASSINAZOLE-RESISTANT 1 (BZR1) and its homologues. However, the molecular mechanism that determines the transcriptional activation versus repressive activity of BZR1 remains largely unclear. Here, we show that BZR1-responsive transcriptional activation at thousands of loci requires the Switch defective/sucrose non-fermentable (SWI/SNF)-complexes-mediated chromatin accessibility regulation. BR-activated BZR1 controls the activation or repression of thousands of BZR1 target genes through reprograming genome-wide chromatin accessibility landscape in Arabidopsis thaliana. BZR1 physically interacts with the BRAHMA (BRM)-Associated SWI/SNF complexes (BAS), co-localizes with BRM on the genome, and enhances BRM occupancy at BR-increased accessibility sites. Furthermore, loss of BRM abrogates the capacity of BZR1 to increase but not decrease chromatin accessibility, blocks BR-induced hypocotyl elongation, and diminishes BZR1-mediated transcriptional activation rather than repression. Together, our work reveals that the BAS chromatin remodeling complex is a critical epigenetic regulatory partner in dictating BZR1-mediated transcriptional activation ability, thus providing a long-sought mechanistic explanation for how BR signaling activates gene transcription in shaping diverse developmental programs.

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Organization, genomic targeting and assembly of three distinct SWI/SNF chromatin remodeling complexes inArabidopsis

Cited by 3 publications

References 58 publications

The regulation of chromatin configuration at AGAMOUS locus by LFR‐SYD‐containing complex is critical for reproductive organ development in Arabidopsis

The regulation of chromatin configuration at AGAMOUS locus by LFR‐SYD‐containing complex is critical for reproductive organ development in Arabidopsis

The SAS Chromatin-Remodeling Complex Mediates Inflorescence-Specific Chromatin Accessibility for Transcription Factor Binding

SWI/SNF chromatin remodeling determines brassinosteroid-induced transcriptional activation

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