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BRAHMA-interacting proteins BRIP1 and BRIP2 are core subunits of Arabidopsis SWI/SNF complexes

Nature Plants volume 6, pages 996–1007 (2020)Cite this article

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Abstract

Switch defective/sucrose non-fermentable (SWI/SNF) chromatin remodelling complexes are multi-protein machineries that control gene expression by regulating chromatin structure in eukaryotes. However, the full subunit composition of SWI/SNF complexes in plants remains unclear. Here we report that in Arabidopsis thaliana, two homologous glioma tumour suppressor candidate region domain-containing proteins, named BRAHMA-interacting proteins 1 (BRIP1) and BRIP2, are core subunits of plant SWI/SNF complexes. brip1 brip2 double mutants exhibit developmental phenotypes and a transcriptome remarkably similar to those of BRAHMA (BRM) mutants. Genetic interaction tests indicated that BRIP1 and BRIP2 act together with BRM to regulate gene expression. Furthermore, BRIP1 and BRIP2 physically interact with BRM-containing SWI/SNF complexes and extensively co-localize with BRM on chromatin. Simultaneous mutation of BRIP1 and BRIP2 results in decreased BRM occupancy at almost all BRM target loci and substantially reduced abundance of the SWI/SNF assemblies. Together, our work identifies new core subunits of BRM-containing SWI/SNF complexes in plants and uncovers the essential role of these subunits in maintaining the abundance of SWI/SNF complexes in plants.

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Fig. 1: BRIP1 and BRIP2 interact with BRM-containing SWI/SNF complexes.
Fig. 2: brip1 brip2 double mutants show phenotypes similar to brm.
Fig. 3: BRIP1 and BRIP2 co-occupy with BRM genome-wide.
Fig. 4: Loss of BRIP1/2 leads to genome-wide decrease in BRM occupancy.
Fig. 5: BRIP1 and BRIP2 are essential for the integrity of BRM complexes.
Fig. 6: The GLTSCR domain is essential for the function of BRIP2.

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Data availability

The ChIP–seq and RNA-seq datasets have been deposited in the Gene Expression Omnibus (GEO) under accession no. GSE142369. The mass spectrometry proteomics data have been deposited in the ProteomeXchange Consortium under the dataset identifier PXD018815. Source data are provided with this paper.

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Acknowledgements

We thank the ABRC for seeds of tDNA insertion lines, S. Yang and X. Hou (Chinese Academy of Sciences) for the pEAQ-BRM-N-GFP vector and pZPY122-FLAG vector, respectively, and J. Li (Sun Yat-sen University) for the pHBT-HA vector. This work was supported by the National Natural Science Foundation of China to C.L. (no. 31870289) and the Natural Science and Engineering Council of Canada to Y.C. (no. RGPIN/04625-2017).

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Authors and Affiliations

  1. State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-Sen University, Guangzhou, China

    Yaoguang Yu, Zhenwei Liang, Xin Song, Wei Fu, Jianqu Xu, Yawen Lei, Liangbing Yuan, Jiuxiao Ruan, Shangzhi Huang & Chenlong Li

  2. London Research and Development Centre, Agriculture and Agri-Food Canada, London, Ontario, Canada

    Chen Chen & Yuhai Cui

  3. School of Biological Science and Biotechnology, Minnan Normal University, Zhangzhou, China

    Wenqun Fu

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  1. Yaoguang Yu
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Contributions

Y.Y. and C.L. conceived the project. Y.Y. performed most of the experiments. Wenqun Fu constructed the GUS reporter lines. Y.Y., Z.L., L.Y. and C.L. conducted bioinformatics analysis. Y.Y., Z.L., X.S., Wei Fu, Y.L., L.Y., J.X., J.R., C.C., Y.C. and S.H. analysed data. Y.Y. and C.L. wrote the manuscript.

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Correspondence to Chenlong Li.

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Extended data

Extended Data Fig. 1 Physical interaction among BRIP1, BRIP2 and SWI/SNF complex.

a, Bimolecular Fluorescence Complementation assay (BiFC) showing that BRIP1 and BRIP2 interact with SWI/SNF complex core members. An unrelated nuclear protein encoded by AT3G60390 was used as a negative control. error bar = 20 μm. b, Co-immunoprecipitation of BRIP1 with BRM-N (N-terminal of BRM, 1-952 amino acids). BRM-N-GFP was immunoprecipitated by an anti-HA-Agarose antibody from protoplasts co-transfected with BRM-N-GFP and BRIP1-HA. The antibodies used for immunoblot are indicated on the left, and the sizes of the protein markers are indicated on the right. c, Yeast-two hybrid assay to examine the region of BRM that interacts with BRIP1/2. Growth of transformed yeast is shown on permissive SD -Ade/-His/-Leu/-Trp medium.

Source data

Extended Data Fig. 2 Gene structures and Genetic materials.

a, Schematic illustration of the conserved domain of BRIP1 and BRIP2. The numbers indicate the positions of amino acids. At the bottom, the alignment of the sequences of the GLTSCR domain of BRIP1/2 proteins. The amino acids same in both proteins are marked by red. b, Schematic illustration of the locations of the T-DNA insertion sites (dark arrow) of the two brip mutants. The GLTSCR domains are red marked. c, Genotyping of brip1 and brip2 by using the three primers method (LBb1.3+LP + RP). Wild-type (Col-0) was used as a control. d, The mRNA levels of BRIP1 and BRIP2 were determined by RT-PCR in brip1, brip2 and Col-0. GAPDH was amplified as an internal control. Error bars represent s.d. of three biological replicates, as determined by the post hoc Tukey’s HSD test.

Source data

Extended Data Fig. 3 Phenotype of brip1, brip2, brip1 brip2 and brm mutants.

a, Leaf phenotype of 14-day-old seedlings. Scale bars, 5 mm. b, Confocal images of root tips showing nuclear localization of the BRIP1-GFP and BRIP2-GFP in brip1 brip2 double mutant background. The red fluorescent signal is from propidium iodide staining. Scale bars, 50 μm. c, Number of rosette leaf of different plant materials at flowering. d, Silique phenotypes of different materials. Scale bars, 1 cm. Lowercase letters indicate significant differences between genetic backgrounds, as determined by the post hoc Tukey’s HSD test. The number of ‘n = ’ indicates the number of plants that were used. Data are presented as mean values +/− SD.

Source data

Extended Data Fig. 4 brip1brip2 mutants had similar transcriptome to brm mutants.

a, Summary of up- and down-regulated genes in different mutants compared to WT. The number indicates the concrete number of up- and down-regulated genes and the Y-axis showing the percentage of up- and down-regulated genes of all mis-regulated genes. b, Venn diagrams showing statistically significant overlaps between genes up- or down-regulated in brm-3 and those in brip1 brip2. p = 0, Hypergeometric test. c, Scatterplot of FPKM log2 fold change over WT of indicated mutants (y-axis) vs. brm-3 or brm-1 (x-axis) at brm-3 or brm-1 differentially expressed genes. Red lines indicate the line of best fit, and adjusted R value is indicated. Dots are mean values from three biologically independent experiments.

Source data

Extended Data Fig. 5 Plants expressing GFP-tagged BRIP1 or BRIP2 in their respective single mutant background.

a, Pictures showing 21-day-old plants. Scale bars, 1 cm. b, Confocal images of root tips showing nuclear localization of the BRIP1-GFP and BRIP2-GFP in their single mutant background. The red fluorescent signal is from propidium iodide staining. Scale bars, 50 μm. c, Western blot analysis using an anti-GFP antibody shows the accumulation of BRIP1 and BRIP2. For each plot, the antibody used is indicated on the left, and the sizes of the protein markers are indicated on the right. H3 serves as a loading control.

Source data

Extended Data Fig. 6 BRIP1, BRIP2 and BRM show a similar binding pattern.

a, Pie charts showing the distribution of BRM, BRIP1 and BRIP2 peaks at annotated genic and intergenic regions in the genome. b, The average enrichment of BRM, BRIP1 or BRIP2 at its target genes, respectively (n = 7,767, 5,035 and 7,023, respectively). Plotting regions were scaled to the same length as follows: 5′ ends (−3.0 kb to transcription starting site (TSS)) and 3′ ends (transcription stop site (TTS) to downstream 3.0 kb), and the gene body was scaled to 3 kb. Two biological replicates were included. c, GO analysis for biological processes associated with genes occupied by BRM, BRIP1 or BRIP2.

Extended Data Fig. 7 Loss of BRM causes the genome-wide decrease of BRIP1/2 occupancy.

a, On the top, Plot representation of the mean density of BRIP1 or BRIP2 occupancy at all BRIP1 or BRIP2 sites in brm-1 compared with WT. The average BRIP1/2 binding signal within 3 kb genomic regions flanking the summit of BRIP1/2 peaks are shown. Bottom, Heat-map representation of the occupancy of BRIP1 or BRIP1 in WT and brm-1. b, IGV views of BRIP1/2 occupancy at selected loci in WT and brm-1 background. The scale was identical for the different tracks, and gene structures are shown underneath each panel. The gene IDs and the ‘START and END’ positions on the chromosome are shown below. The y-axis scales represent shifted merged MACS2 tag counts for every 10-bp window.

Extended Data Fig. 8 The number of unique peptides identified by Mass spectrometry analyses.

a, Mass spectrometry results showing the total number of unique peptides in the input or IP samples of SWI3C-3×FLAG BRM-GFP brm-1 and SWI3C-3×FLAG BRM-GFP brm-1 brip1 brip2. b, The number of unique peptides of five representative proteins (named by UniProt) in the input samples SWI3C-3×FLAG BRM-GFP brm-1 before FLAG immunoprecipitation was similar to that in SWI3C-3×FLAG BRM-GFP brm-1 brip1 brip2. c, The number of unique peptides of five representative proteins (named by UniProt) in the input samples SWI3C-3×FLAG BRM-GFP brm-1 before GFP immunoprecipitation was similar to that in SWI3C-3×FLAG BRM-GFP brm-1 brip1 brip2. Error bars are presented as mean values from three biological replicates, +/− SD. N.S., not significant (Unpaired, two-tailed Student’s t-test).

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Extended Data Fig. 9 Loss of GLTSCR domain impairs the function of BRIP2.

a, qRT-PCR analyses showing the mRNA level of BRIP2∆GLTSCR-GFP and full length BRIP2-GFP. The expression level of each gene was normalized to that of GAPDH. Error bars are presented as mean values from three biological replicates, +/− SD. ** p < 0.01 (Unpaired, two-tailed Student’s t-test). b, Morphological phenotypes of pBRIP2:BRIP2-GFP brip1 brip2 and pBRIP2:BRIP2∆ GLTSCR-GFP brip1 brip2. Photographs of 35-day-old plants are shown. Scale bar, 1 cm. c, Silique phenotypes of different materials. Scale bars, 1 cm. Lowercase letters indicate significant differences between genetic backgrounds, as determined by the post hoc Tukey’s HSD test. The number of ‘n = ’ indicates the number of plants that were used. Data are presented as mean values +/− SD.

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Extended Data Fig. 10 Phylogenetic analysis of GLTSCR domain-containing proteins among different species.

a, The phylogenetic tree was constructed using the amino-acid sequences of the GLTSCR domain from different species, including Amborella trichopoda, Physcomitrella patens, Arabidopsis thaliana, Arabidopsis lyrate, Brassica napus, Oryza sativa Japonica, Triticum aestivum, Hordeum vulgare subsp. Vulgare, Zea mays, Homo sapiens, Danio rerio, Drosophila melanogaster, Caenorhabditis elegans, Mus musculus. The scale length in the tree is indicated. b, The alignment of sequences of GLTSCR domain across different species. Conserved amino acids are marked in red (100%), green (≥75%), and purple (≥ 50%), respectively.

Supplementary information

Supplementary Information

Supplementary Figs. 1–4.

Reporting Summary

Supplementary Tables

Supplementary Table 1: Summary of SWI/SNF complex core members according to the IP/MS results for BRM. Supplementary Table 2: List of genes misregulated in different mutants. Supplementary Table 3: List of genes occupied by BRM, BRIP1 or BRIP2 in Arabidopsis seedlings. Supplementary Table 4: Summary of IP–MS data. Supplementary Table 5: Oligonucleotides used in this study. Supplementary Table 6: Summary of mapped reads in ChIP–seq.

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Yu, Y., Liang, Z., Song, X. et al. BRAHMA-interacting proteins BRIP1 and BRIP2 are core subunits of Arabidopsis SWI/SNF complexes. Nat. Plants 6, 996–1007 (2020). https://doi.org/10.1038/s41477-020-0734-z

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