Bromodomain-containing proteins BRD1, BRD2, and BRD13 are core subunits of SWI/SNF complexes and vital for their genomic targeting in Arabidopsis

Yu, Yaoguang; Fu, Wei; Xu, Jianqu; Lei, Yawen; Song, Xin; Liang, Zeyin; Zhu, Tao; Liang, Yuhui; Hao, Yuanhao; Yuan, Lei; Li, Chenlong

doi:10.1016/j.molp.2021.03.018

Cited by 30 publications

(61 citation statements)

References 71 publications

(130 reference statements)

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“…These core subunits are required for the assembly and activity of the SWI/SNF complex ( Sudarsanam and Winston, 2000 ; Yang et al, 2007 ; Sundaramoorthy and Owen-Hughes, 2020 ). Several core subunits of the plant Swi2/Snf2 ATPase BRAHMA (BRM)-SWI/SNF complex, such as BRAHMA-interacting proteins 1 (BRIP1) and BRIP2, and bromodomain-containing proteins BRD1, BRD2, and BRD13, have recently been discovered to co-localize and act together with BRM on chromatin to regulate gene expression ( Yu et al, 2020 , 2021 ). In the genome of the model plant, Arabidopsis thaliana , there are four Swi3 proteins, including SWI3A/3B/3C/3D ( Sarnowski et al, 2005 ).…”

Section: Introductionmentioning

confidence: 99%

LFR Physically and Genetically Interacts With SWI/SNF Component SWI3B to Regulate Leaf Blade Development in Arabidopsis

et al. 2021

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Leaves start to develop at the peripheral zone of the shoot apical meristem. Thereafter, symmetric and flattened leaf laminae are formed. These events are simultaneously regulated by auxin, transcription factors, and epigenetic regulatory factors. However, the relationships among these factors are not well known. In this study, we conducted protein-protein interaction assays to show that our previously reported Leaf and Flower Related (LFR) physically interacted with SWI3B, a component of the ATP-dependent chromatin remodeling SWI/SNF complex in Arabidopsis. The results of truncated analysis and transgenic complementation showed that the N-terminal domain (25–60 amino acids) of LFR was necessary for its interaction with SWI3B and was crucial for LFR functions in Arabidopsis leaf development. Genetic results showed that the artificial microRNA knockdown lines of SWI3B (SWI3B-amic) had a similar upward-curling leaf phenotype with that of LFR loss-of-function mutants. ChIP-qPCR assay was conducted to show that LFR and SWI3B co-targeted the promoters of YABBY1/FILAMENTOUS FLOWER (YAB1/FIL) and IAA carboxyl methyltransferase 1 (IAMT1), which were misexpressed in lfr and SWI3B-amic mutants. In addition, the association between LFR and the FIL and IAMT1 loci was partly hampered by the knockdown of SWI3B. These data suggest that LFR interacts with the chromatin-remodeling complex component, SWI3B, and influences the transcriptional expression of the important transcription factor, FIL, and the auxin metabolism enzyme, IAMT1, in flattened leaf lamina development.

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Section: Introductionmentioning

confidence: 99%

LFR Physically and Genetically Interacts With SWI/SNF Component SWI3B to Regulate Leaf Blade Development in Arabidopsis

et al. 2021

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“…Similarly, most Archaeplastida species have bromodomain proteins highly similar to BRD7/9. Importantly, the three A. thaliana BRDs predicted to be orthologs of HsBRD7/9 (i.e., BRD1, BRD2, and BRD13) have been found to co-immunoprecipitate with other SWI/SNF subunits in vivo and contribute to the proper function of the complex in plants 27 – 29 , supporting orthology with functional conservation. From these findings, we suggest SMARCI also originated in the LECA.…”

Section: Resultsmentioning

confidence: 82%

Comprehensive identification of SWI/SNF complex subunits underpins deep eukaryotic ancestry and reveals new plant components

et al. 2022

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Over millions of years, eukaryotes evolved from unicellular to multicellular organisms with increasingly complex genomes and sophisticated gene expression networks. Consequently, chromatin regulators evolved to support this increased complexity. The ATP-dependent chromatin remodelers of the SWI/SNF family are multiprotein complexes that modulate nucleosome positioning and appear under different configurations, which perform distinct functions. While the composition, architecture, and activity of these subclasses are well understood in a limited number of fungal and animal model organisms, the lack of comprehensive information in other eukaryotic organisms precludes the identification of a reliable evolutionary model of SWI/SNF complexes. Here, we performed a systematic analysis using 36 species from animal, fungal, and plant lineages to assess the conservation of known SWI/SNF subunits across eukaryotes. We identified evolutionary relationships that allowed us to propose the composition of a hypothetical ancestral SWI/SNF complex in the last eukaryotic common ancestor. This last common ancestor appears to have undergone several rounds of lineage-specific subunit gains and losses, shaping the current conformation of the known subclasses in animals and fungi. In addition, our results unravel a plant SWI/SNF complex, reminiscent of the animal BAF subclass, which incorporates a set of plant-specific subunits of still unknown function.

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“…One is reminiscent of the mammalian BAF-PBAF complexes and incorporates the MINU ATPases while the other is similar to the metazoan ncBAF complex and incorporates the BRM ATPase (35). There is abundant information about the molecular function of subunits of the plant ncBAF-like complex, like BRM (38)(39)(40)(41), as well as the bromodomain-containing proteins BRD1,2,13 (BRDs), BRAHMA-INTERACTING PROTEINS (BRIPs), and GRF-INTERACTING FACTORS (GIF) (42)(43)(44)(45) signature subunits. However, there is a significant lack of information about the components and molecular function of the plant BAF-like complex.…”

Section: Introductionmentioning

confidence: 99%

The TRIPLE PHD FINGERS proteins are required for SWI/SNF complex-mediated +1 nucleosome positioning and 5’ transcript length determination in Arabidopsis

Diego-Martin

Pérez-Alemany

Candela-Ferre

et al. 2022

Preprint

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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 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 usage. Interestingly, there is a remarkable correlation between +1 nucleosome shift and 5′ transcript length change suggesting their functional connection. In summary, this study unravels the function of a plant SWI/SNF complex involved in +1 nucleosome positioning and 5′ transcript length determination.

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Bromodomain-containing proteins BRD1, BRD2, and BRD13 are core subunits of SWI/SNF complexes and vital for their genomic targeting in Arabidopsis

Cited by 30 publications

References 71 publications

LFR Physically and Genetically Interacts With SWI/SNF Component SWI3B to Regulate Leaf Blade Development in Arabidopsis

LFR Physically and Genetically Interacts With SWI/SNF Component SWI3B to Regulate Leaf Blade Development in Arabidopsis

Comprehensive identification of SWI/SNF complex subunits underpins deep eukaryotic ancestry and reveals new plant components

The TRIPLE PHD FINGERS proteins are required for SWI/SNF complex-mediated +1 nucleosome positioning and 5’ transcript length determination in Arabidopsis

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