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

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

doi:10.1093/plcell/koad111

Cited by 8 publications

(14 citation statements)

References 63 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: Lfr Functions As a Syd-containing Swi/snf Crc Componentsupporting

confidence: 59%

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: Lfr Functions As a Syd-containing Swi/snf Crc Componentsupporting

confidence: 59%

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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“…Recently, we and others showed the existence of three concurrently expressed plant SWI/SNF family sub-complexes that have specific subunits and are separately assembled on a mutually exclusive catalytic subunit, BRM, SYD, or MINUs. These three plant SWI/SNF sub-complexes were termed BAS ( B RM- A ssociated S WI/SNF complex), SAS ( S YD- A ssociated S WI/SNF complex), and MAS ( M INU- A ssociated S WI/SNF complex), respectively 14 – 17 .…”

Section: Introductionmentioning

confidence: 99%

BCL7A and BCL7B potentiate SWI/SNF-complex-mediated chromatin accessibility to regulate gene expression and vegetative phase transition in plants

Lei,

Yu,

et al. 2024

Nat Commun

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Switch defective/sucrose non-fermentable (SWI/SNF) chromatin remodeling complexes are multi-subunit machineries that establish and maintain chromatin accessibility and gene expression by regulating chromatin structure. However, how the remodeling activities of SWI/SNF complexes are regulated in eukaryotes remains elusive. B-cell lymphoma/leukemia protein 7 A/B/C (BCL7A/B/C) have been reported as subunits of SWI/SNF complexes for decades in animals and recently in plants; however, the role of BCL7 subunits in SWI/SNF function remains undefined. Here, we identify a unique role for plant BCL7A and BCL7B homologous subunits in potentiating the genome-wide chromatin remodeling activities of SWI/SNF complexes in plants. BCL7A/B require the catalytic ATPase BRAHMA (BRM) to assemble with the signature subunits of the BRM-Associated SWI/SNF complexes (BAS) and for genomic binding at a subset of target genes. Loss of BCL7A and BCL7B diminishes BAS-mediated genome-wide chromatin accessibility without changing the stability and genomic targeting of the BAS complex, highlighting the specialized role of BCL7A/B in regulating remodeling activity. We further show that BCL7A/B fine-tune the remodeling activity of BAS complexes to generate accessible chromatin at the juvenility resetting region (JRR) of the microRNAs MIR156A/C for plant juvenile identity maintenance. In summary, our work uncovers the function of previously elusive SWI/SNF subunits in multicellular eukaryotes and provides insights into the mechanisms whereby plants memorize the juvenile identity through SWI/SNF-mediated control of chromatin accessibility.

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

Cited by 8 publications

References 63 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

BCL7A and BCL7B potentiate SWI/SNF-complex-mediated chromatin accessibility to regulate gene expression and vegetative phase transition in plants

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