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Comprehensive characterization of three classes of Arabidopsis SWI/SNF chromatin remodelling complexes

Nature Plants volume 8, pages 1423–1439 (2022)Cite this article

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An Author Correction to this article was published on 10 May 2023

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Abstract

Although SWI/SNF chromatin remodelling complexes are known to regulate diverse biological functions in plants, the classification, compositions and functional mechanisms of the complexes remain to be determined. Here we comprehensively characterized SWI/SNF complexes by affinity purification and mass spectrometry in Arabidopsis thaliana, and found three classes of SWI/SNF complexes, which we termed BAS, SAS and MAS (BRM-, SYD- and MINU1/2-associated SWI/SNF complexes). By investigating multiple developmental phenotypes of SWI/SNF mutants, we found that three classes of SWI/SNF complexes have both overlapping and specific functions in regulating development. To investigate how the three classes of SWI/SNF complexes differentially regulate development, we mapped different SWI/SNF components on chromatin at the whole-genome level and determined their effects on chromatin accessibility. While all three classes of SWI/SNF complexes regulate chromatin accessibility at proximal promoter regions, SAS is a major SWI/SNF complex that is responsible for mediating chromatin accessibility at distal promoter regions and intergenic regions. Histone modifications are related to both the association of SWI/SNF complexes with chromatin and the SWI/SNF-dependent chromatin accessibility. Three classes of SWI/SNF-dependent accessibility may enable different sets of transcription factors to access chromatin. These findings lay a foundation for further investigation of the function of three classes of SWI/SNF complexes in plants.

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Fig. 1: Identification and classification of SWI/SNF complexes in Arabidopsis.
Fig. 2: Different developmental defects of BAS, SAS and MAS mutants in leaves, branches and flowers.
Fig. 3: BAS, SAS and MAS complexes function differently in regulation of gene expression.
Fig. 4: Differential occupancy of BAS, SAS and MAS complexes on chromatin.
Fig. 5: Distinct effects on chromatin accessibility of BAS, SAS and MAS complexes.
Fig. 6: Enrichment of different transcription-factor-binding motifs in the accessible regions maintained by BAS, SAS and MAS.
Fig. 7: Different effects of SAS, BAS and MAS complexes on chromatin accessibility at TSS-flanking regions.

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Data availability

A reporting summary for this paper is available as a Supplementary Information file. Raw data of RNA-seq, ChIP–seq and ATAC–seq results have been deposited in GEO (accession number GSE193397). The accession numbers of genes reported in this study are as follows: AT3G01890 (SWP73A), AT5G14170 (SWP73B), AT4G22320 (BCL7A), AT5G55210 (BCL7B), AT1G18450 (ARP4), AT3G60830 (ARP7), AT2G46020 (BRM), AT1G21700 (SWI3C), AT1G20670 (BRD1), AT1G76380 (BRD2), AT5G55040 (BRD13), AT3G03460 (BRIP1), AT5G17510 (BRIP2), AT5G28640 (AN3), AT1G01160 (GIF2), AT4G00850 (GIF3), AT2G28290 (SYD), AT4G34430 (SWI3D), AT5G07940 (SYS1), AT5G07970 (SYS2), AT5G07980 (SYS3), AT3G22990 (LFR), AT3G06010 (MINU1), AT5G19310 (MINU2), AT2G47620 (SWI3A), AT2G33610 (SWI3B), AT3G17590 (BSH), AT3G18380 (SHH2), AT1G50620 (PMS1A), AT3G20280 (PMS1B), AT3G08020 (PMS2A), AT3G52100 (PMS2B), AT1G58025 (BRD5), AT1G32730 (MIS), AT1G06500 (SSM), Os09g0284300 (OsBCL7), Os08g0137200 (OsARP4), Os03g0783000 (OsARP7), Os04g0382100 (OsSWIB), Os02g0114033 (OsCHR707), Os11g0183700 (OsSWI3C), Os12g0176700 (OsCHB701), Os03g0130800 (OsBRD1), Os09g0550000 (OsBRD2), Os12g0465700 (OsDEC), Os03g0733600 (OsGIF1), Os11g0615200 (OsGIF2), Os12g0496900 (OsGIF3), Os06g0255200 (OsCHR720), Os04g0110300 (OsCHB704), Os03g0213300 (OsSYS), Os07g0609766 (OsLFR), Os05g0144300 (OsCHR719), Os04g0480300 (OsCHB703), Os02g0194000 (OsCHB702), Os02g0723700 (OsBSH), Os06g0485100 (OsSHH2), Os06g0309000 (OsPMS1), Os12g0527800 (OsPMS2), Os08g0109500 (OsBRD5), Os08g0129500 (OsMIS) and Os01g0246500 (OsSSM). Source data are provided with this paper.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (32025003) and by the National Key Research and Development Program of China (2016YFA0500801) from the Chinese Ministry of Science and Technology. We thank the Research Platform of Protein Science at Institute of Biophysics, Chinese Academy of Sciences, for providing the technical assistance on the ITC assay.

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Authors and Affiliations

  1. College of Life Sciences, Beijing Normal University, Beijing, China

    Jing Guo

  2. National Institute of Biological Sciences, Beijing, China

    Jing Guo, Guang Cai, Yong-Qiang Li, Yi-Xuan Zhang, Yin-Na Su, Dan-Yang Yuan, Zhao-Chen Zhang, Zhen-Zhen Liu, Xue-Wei Cai, Jing Guo, Lin Li, She Chen & Xin-Jian He

  3. Tsinghua Institute of Multidisciplinary Biomedical Research, Tsinghua University, Beijing, China

    She Chen & Xin-Jian He

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Contributions

J.G. (Beijing Normal University), G.C., Y.-X.Z., Z.-C.Z., Z.-Z.L., J.G. (National Institute of Biological Sciences), L.L. and S.C. performed the experiments. J.G. (Beijing Normal University), Y.-Q.L., Y.-N.S., D.-Y.Y. and X.-W.C. performed the bioinformatics analyses. J.G. (Beijing Normal University) and X.-J.H. designed the experiments. J.G. (Beijing Normal University) and X.-J.H. wrote the manuscript.

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Correspondence to Xin-Jian He.

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Nature Plants thanks Sebastian Sacharowski and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Phylogenetic analysis of SWI/SNF chromatin remodelers in different plant species and identification of SWI/SNF complexes in Oryza sativa.

a, A neighbor-joining tree was generated using the full-length protein sequences of BRM, SYD, MINU1, MINU2, and their orthologues in different plant species. The human SWI/SNF chromatin remodeler BRG1 was introduced as the outgroup. Bootstrap values: % invariant branches during resampling. b, Heatmap visualization of proteins co-purified with GFP-tagged OsBCL7, OsDEC, OsCHB704, OsLFR and OsBSH as determined by AP-MS. The matched queries of a prey protein are normalized by the average matched queries of the total subunits purified by a bait protein. c, Schematic representations of BAS, SAS and MAS complexes in Oryza sativa. Shared subunits are shown in grey. Specific subunits of BAS, SAS and MAS complexes are shown in green, blue and red, respectively.

Extended Data Fig. 2 Interactions between subunits of BAS, SAS, and MAS complexes as determined by Y2H assays.

a, Interactions of BAS complex subunits. The truncated versions of BRM used in Y2H assays. b, Interactions of SAS complex subunits. The truncated SYD versions SYD-ΔC and SYD-C used in Y2H assays are shown on the top panel. c, Interaction of MAS complex subunits. The interactions detected by Y2H assays in this study are highlighted in blue, and the previously published interactions are labelled by red frames. Blank boxes indicate that no interaction was detected.

Extended Data Fig. 3 Developmental phenotypes of SWI/SNF mutants.

a, Schematic representations of mutations in SYS1, SYS2 and SYS3 mediated by CRISPR/Cas9. The translation start sites are marked by +1. The untranslated regions (UTR) and exon regions are indicated with blank and black boxes, respectively. Introns are indicated with fold lines. The mutations validated by Sanger sequencing are illustrated by red boxes. WT: wild type. Scale bar: 100 bp. b, Morphological phenotypes of cotyledons and rosette leaves taken from bolting plants of SWI/SNF mutants and wild type. c, Morphological phenotypes of 5-week-old plants of SWI/SNF mutants and wild type. d, Measurement of the first cauline branching angles in indicated genotypes. P values determined by two-tailed Student’s t-test or Welch’s t-test indicate the difference between the mutants and the wild-type control. n = 23. e, The ratio of abnormal cauline branches of which the growth positions are not at the axils of cauline leaves. n = 15. P values determined by two-tailed Mann Whitney U test indicate the difference between the mutants and the wild-type control. f, Petal number in the indicated genotypes. The average petal number of five flowers was calculated for each plant. The petal numbers of 20 plants were determined for each genotype (except for swp73b, n = 14). P values determined by two-tailed Mann Whitney U test indicate the difference between the mutants and the wild-type control. g, The average length of all the siliques from the main stem was determined for each plant. n = 15. P values determined by two-tailed Student’s t-test or Welch’s t-test indicate the difference between the mutants and the wild-type control. Data are presented as mean values + /- SD in d-g.

Extended Data Fig. 4 Comparison of the effects of SWI/SNF mutations on development and gene expression.

a, Fresh weight of 23-day-old plants of SWI/SNF mutants and wild type. The fresh weight of 15 plants were determined for each genotype. P values determined by two-tailed Student’s t-test or Welch’s t-test indicate the difference between the mutants and the wild-type control. Data are presented as mean values + /- SD. b, Scatter plot with a fitted regression line and a 95% confidence interval band showing the correlation between the plant fresh weight and the differentially expressed genes in SWI/SNF mutants. R represents the Pearson correlation coefficient. P value were determined by two-tailed t-test. c-f, Determination of the correlation of development-related differentially expressed genes between different SWI/SNF mutants. Heatmaps show the Pearson Correlation Coefficient of brm, brd1/2/13, brip1/2, syd, swi3d, sys1/2/3, minu1/2, pms2a/2b based on the expression changes of leaf development-related genes (c), flower development-related genes (d), flowering time-related genes (e), and embryo development-related genes (f).

Extended Data Fig. 5 Comparison of BAS-, SAS- and MAS-occupied TSS-flanking regions and genes as determined by ChIP-seq.

a, Profile plots showing the enrichment of the SWI/SNF components at the genes bound by each component. b, Boxplots showing the enrichment of SWI/SNF components at the TSS-flanking region of their binding genes. The enrichment of SWI/SNF components was calculated at 200-bp bins of the TSS-flanking region. Sample size of each box plot: BRD1 (n = 10928), SWI3C (n = 11110), SYD (n = 7904), SWI3D (n = 10492), SYS1 (n = 8929), MINU2 (n = 10835), PMS2B (n = 13467). In box plots, center lines and box edges are medians and the interquartile range (IQR), respectively. Whiskers extend within 1.5 times the IQR. c, Venn diagrams showing the overlap of genes occupied by indicated SWI/SNF components. The overlapping significance is shown by P values as determined by hypergeometric test (one-tailed). RF (representation factor) represents the number of overlapping genes divided by the expected number of overlapping genes drawn from two independent groups.

Extended Data Fig. 6 Determination of the correlation between the enrichments of BAS, SAS and MAS components at chromatin.

a, b, Heatmaps showing the enrichment of indicated SWI/SNF components at all the SWI/SNF components-occupied genes. The genes are subjected to sorting by the maximum enrichment value of each region of SYD (a) and MINU2 (b) at these genes. c, d, Enrichment of indicated SWI/SNF components at SYD (c) and MINU2 (d) enrichment deciles of the total regions (n = 18552) occupied by SWI/SNF components. In box plots of c and d, center lines and box edges are medians and the interquartile range (IQR), respectively. Whiskers extend within 1.5 times the IQR.

Extended Data Fig. 7 The histone modification and expression levels of genes occupied by BAS, SAS and MAS components.

a, The H3ac, H3K4me3, and H3K27me3 levels at regions occupied by indicated BAS, SAS, and MAS components in the wild-type plants. The sample size of each boxplot: BRD1 (n = 12973), SWI3C (n = 13851), SYD (n = 9687), SWI3D (n = 13099), SYS1 (n = 11875), MINU2 (n = 11729), PMS2B (n = 15207), random (n = 10000). P values for Kruskal-Wallis tests indicate the differences of the histone modification levels within a group (marked by black lines). Lowercase letters above the boxplots show the results of Dunnett’s test, with statistically similar clusters grouped by the same letter. b, The expression levels of genes occupied by indicated BAS, SAS, and MAS components in the wild-type plants. The sample size of each boxplot: BRD1 (n = 12973), SWI3C (n = 13851), SYD (n = 9687), SWI3D (n = 13099), SYS1 (n = 11875), MINU2 (n = 11729), PMS2B (n = 15207), random (n = 10000). P values for Kruskal-Wallis tests indicate the expression differences within a group (marked by black lines). Lowercase letters above the boxplots show the results of Dunnett’s test, with statistically similar clusters grouped by the same letter. c, Heatmap showing the enrichment of H3ac and H3K4me3 at all the SWI/SNF components-occupied genes. The genes are subjected to sorting by the maximum enrichment value of BRD1 (left), SYD (middle), and MINU2 (right)-occupied regions. d, Enrichment of H3ac, H3K4me3, and H3K27me3 at BRD1, SYD and MINU2 enrichment deciles of total regions (n = 18552) occupied by SWI/SNF components. In box plots of a, b and d, center lines and box edges are medians and the interquartile range (IQR), respectively. Whiskers extend within 1.5 times the IQR.

Extended Data Fig. 8 The bromodomains of BRD1, BRD2 and BRD13 bind to acetylated histones and the second PHD domain of PMS2B binds to methylated H3 at lysine 4.

a, Sequence alignment of the bromodomains of HsBRD9, AtBRD1, AtBRD2, AtBRD13, HsBRM, ScSTH1, and AtBRM. The BRD1 bromodomain conserved residues Y207, N251 and Y258 marked with asterisks were subjected to point mutation. b, Coomassie blue staining of the wild-type BRD1, BRD2, and BRD13 bromodomains and of the mutated BRD1 bromodomain (BRD1-M) tagged by HIS. The fusion proteins were purified from E. coli. The experiments were repeated for at least two times with similar results. c,d, ITC binding assays measuring the binding affinity of the bromodomains of BRD1,BRD2, BRD13 and BRD1-M for acetylated and unmodified H3 peptides (c) and acetylated and unmodified H4 peptides (d). e, Schematic representations indicate the domain architecture of PMS1A and PMS2B and the truncated versions of PMS1A and PMS2B purified from E. coli. f, A phylogenetic tree of the PHD domains in PMS1A, PMS1B, PMS2A, PMS2B, and in the known PHD-containing H3K4me3 readers ARID5, SHL and EBS. The RING fingers of PMS2A and PMS2B that are closely related to the conserved PHD finger were included for analysis. g, Coomassie blue staining of the wild-type PMS1A and PMS2B PHD domains and of the mutated PMS2B PHD domain tagged by GST. The proteins were expressed and purified from E. coli. The experiments were repeated for at least two times with similar results. h, Determination of the binding of wild-type PMS1A and PMS2B PHD domains to methylated and unmethylated histone peptides by in vitro binding assays. i, Sequence alignment of the second PHD fingers of PMS2A and PMS2B (PMS2A-PHD2 and PMS2B-PHD2) and the PHD fingers of ARID5, SHL and EBS. Three conserved aromatic residues (Y148, Y155, and W170) in the PMS2B-PHD2 marked with asterisks were mutated to alanine in the mutated version of PMS2B (PMS2B-PHD-M). The experiment was repeated for two times with similar results. j, The effect of the PMS2B-PHD2 mutation on the binding ability of PMS2B for methylated H3 at lysine 4 as determined by in vitro binding assays. The experiment was repeated for two times with similar results.

Source data

Extended Data Fig. 9 Different effects of BAS, SAS and MAS mutations on chromatin accessibility.

a, The number of differential accessible regions (DARs) in indicated SWI/SNF mutants. DARs with increased accessibility (ATAC-up) were represented in red and DARs with decreased accessibility (ATAC-down) were represented in blue. b, The percentage of BAS/SAS/MAS-bound and unbound regions among the regions with decreased accessibility (ATAC-down regions) in corresponding BAS/SAS/MAS mutants. c, The number of genes with increased accessibility and genes with decreased accessibility in indicated SWI/SNF mutants. Genes with increased accessibility (ATAC-up) were represented in red and genes with decreased accessibility (ATAC-down) were represented in blue. d, Boxplots showing H3K27me3 levels at the regions bound by each complex and the regions bound by each complex with decreased (ATAC-down) or maintained (ATAC-maintain) accessibility. The sample size of each box plot: BAS-bound (n = 12392), ATAC-down (n = 1470), ATAC-maintain (n = 10922), SAS-bound (n = 11398), ATAC-down (n = 2195), ATAC-maintain (n = 9203), MAS-bound (n = 11129), ATAC-down (n = 1637), ATAC-maintain (n = 9492), random (n = 10000). In box plots, center lines and box edges are medians and the interquartile range (IQR), respectively. Whiskers extend within 1.5 times the IQR. P values determined by two-tailed Mann Whitney U test indicate the difference between indicated samples.

Extended Data Fig. 10 Different effects of BAS, SAS and MAS mutations on chromatin accessibility.

a, Heatmap depicting the effects of BAS, SAS, and MAS enzyme mutations on chromatin accessibility at genes whose chromatin accessibility is specifically reduced in brm, syd, and minu1/2. WT: wild type. b, Boxplots showing the chromatin accessibility levels in the brm, syd and minu1/2 mutants and the wild type at the 400~1500 bp upstream region of TSS and at the −400~200-bp TSS-flanking region. Those genes with reduced chromatin accessibility specifically in brm, syd, and minu1/2 mutants were independently analyzed. In box plots, center lines and box edges are medians and the interquartile range (IQR), respectively. Whiskers extend within 1.5 times the IQR. P values determined by two-tailed Wilcoxon signed rank test indicate the difference between the mutants and the wild-type control. WT: wild type. P values of reduced and increased signals in indicated mutants are shown in blue and red, respectively.

Supplementary information

Supplementary Information

Supplementary Figs. 1–4 and Supplementary Tables 1–3.

Reporting Summary

Supplementary Data 1

Full list of Arabidopsis proteins identified by affinity purification followed by mass spectrometry analysis.

Supplementary Data 2

Full list of rice proteins identified by affinity purification followed by mass spectrometry analysis.

Supplementary Data 3

DEGs identifed by RNA-seq.

Supplementary Data 4

Expression of development-related genes in SWI/SNF mutants.

Supplementary Data 5

Peaks identified by ChIP–seq.

Supplementary Data 6

DARs identified by ATAC–seq.

Supplementary Data 7

GO analysis of genes with decreased accessibilily in SWI/SNF mutants identified by ATAC–seq.

Supplementary Data 8

Motif analysis of regions with decreased accessibility in SWI/SNF mutants identified by ATAC–seq.

Supplementary Data 9

Primers used in the study.

Source data

Source Data Extended Data Fig. 8

Unprocessed gels and western blots.

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Guo, J., Cai, G., Li, YQ. et al. Comprehensive characterization of three classes of Arabidopsis SWI/SNF chromatin remodelling complexes. Nat. Plants 8, 1423–1439 (2022). https://doi.org/10.1038/s41477-022-01282-z

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