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

Wei Fu, Yaoguang Yu, Jie Shu, Zewang Yu, Tao Zhu, Yixiong Zhong, Zhihao Zhang, Zhenwei Liang, Yuhai Cui, Chen Chen, Chenlong Li
doi: https://doi.org/10.1101/2022.11.24.517835
Wei Fu
1State Key Laboratory of Biocontrol and Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, 510275, China
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Yaoguang Yu
1State Key Laboratory of Biocontrol and Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, 510275, China
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Jie Shu
2Key Laboratory of South China Agricultural Plant Molecular Analysis and Genetic Improvement & Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, Guangdong, 510650, China
3University of the Chinese Academy of Sciences, Beijing, 100049, China
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Zewang Yu
1State Key Laboratory of Biocontrol and Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, 510275, China
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Tao Zhu
1State Key Laboratory of Biocontrol and Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, 510275, China
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Yixiong Zhong
1State Key Laboratory of Biocontrol and Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, 510275, China
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Zhihao Zhang
1State Key Laboratory of Biocontrol and Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, 510275, China
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Zhenwei Liang
1State Key Laboratory of Biocontrol and Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, 510275, China
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Yuhai Cui
4London Research and Development Centre, Agriculture and Agri-Food Canada, London, Ontario, N5V 4T3 Canada
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Chen Chen
2Key Laboratory of South China Agricultural Plant Molecular Analysis and Genetic Improvement & Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, Guangdong, 510650, China
3University of the Chinese Academy of Sciences, Beijing, 100049, China
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Chenlong Li
1State Key Laboratory of Biocontrol and Guangdong Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, Guangzhou, 510275, China
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  • For correspondence: lichlong3@mail.sysu.edu.cn
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Abstract

Switch defective/sucrose non-fermentable (SWI/SNF) complexes are evolutionarily conserved multi-subunit machines that play vital roles in chromatin architecture regulation for modulating gene expression via sliding or ejection of nucleosomes in eukaryotes. In plants, perturbations of SWI/SNF subunits often result in severe developmental disorders. However, the subunit composition, pathways of assembly, and genomic targeting of the plant SWI/SNF complexes remain undefined. Here, we reveal the organization, genomic targeting and assembly of three distinct Arabidopsis SWI/SNF complexes: BRAHMA-Associated SWI/SNF complexes (BAS), SPLAYED-Associated SWI/SNF complexes (SAS) and MINUSCULE-Associated SWI/SNF complexes (MAS). We show that BAS complexes are equivalent to human ncBAF, whereas SAS and MAS complexes evolve in multiple subunits unique to plants, suggesting a plant-specific functional evolution of SWI/SNF complexes. We further demonstrate overlapping and specific genomic targeting of the three plant SWI/SNF complexes on chromatin and reveal that SAS complexes are necessary for the correct genomic localization of the BAS complexes. Finally, we define the role of core module subunit in the assembly of the plant SWI/SNF complexes and highlight that ATPase module subunit is required for global complex stability and the interaction of core module subunits in SAS and BAS complexes in Arabidopsis. Together, our work highlights the divergence of SWI/SNF chromatin remodelers during the eukaryote evolution and provides a comprehensive landscape for understanding the plant SWI/SNF complexes organization, assembly, genomic targeting, and function.

One-sentence summary Comprehensively define the organization, genomic targeting and assembly of three distinct SWI/SNF chromatin remodeling complexes in Arabidopsis

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • The author(s) responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (https://academic.oup.com/plcell/pages/General-Instructions) is: Chenlong Li (lichlong3{at}mail.sysu.edu.cn).

  • We have updated some writing errors, inculding: line 225: "CBAF" to "cBAF"; line 257: "Figure S2G" to "Figure S2, F and G" line 450: "reduction of SYD occupancy at individual loci in swi3d-1" to "reduction of SWI3D occupancy at individual loci in syd-5" line 538: "Supplemental Figure S13" to "Supplemental Figure S12" line 689: "short-day" to "long-day"

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted December 07, 2022.
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Organization, genomic targeting and assembly of three distinct SWI/SNF chromatin remodeling complexes in Arabidopsis
Wei Fu, Yaoguang Yu, Jie Shu, Zewang Yu, Tao Zhu, Yixiong Zhong, Zhihao Zhang, Zhenwei Liang, Yuhai Cui, Chen Chen, Chenlong Li
bioRxiv 2022.11.24.517835; doi: https://doi.org/10.1101/2022.11.24.517835
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Organization, genomic targeting and assembly of three distinct SWI/SNF chromatin remodeling complexes in Arabidopsis
Wei Fu, Yaoguang Yu, Jie Shu, Zewang Yu, Tao Zhu, Yixiong Zhong, Zhihao Zhang, Zhenwei Liang, Yuhai Cui, Chen Chen, Chenlong Li
bioRxiv 2022.11.24.517835; doi: https://doi.org/10.1101/2022.11.24.517835

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