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Abstract

SWITCH deficient SUCROSE NONFERMENTING (SWI/SNF) class chromatin remodeling complexes (CRCs) use the energy derived from ATP hydrolysis to facilitate access of proteins to the genomic DNA for transcription, replication, and DNA repair. Uniquely, SWI/SNF CRCs can both slide the histone octamer along the DNA or eject it from the DNA. Given their ability to change the chromatin status quo, SWI/SNF remodelers are critical for cell fate reprogramming with pioneer and other transcription factors, for responses to environmental challenges, and for disease prevention. Recent cryo-electron microscopy and mass spectrometry approaches have uncovered different subtypes of SWI/SNF complexes with unique properties and functions. At the same time, tethering or rapid depletion and inactivation of SWI/SNF have provided novel insight into SWI/SNF requirements for enhancer activity and into balancing chromatin compaction and accessibility in concert with Polycomb complexes. Given their importance, SWI/SNF recruitment to genomic locations by transcription factors and their biochemical activity is tightly controlled. This review focuses on recent advances in our understanding of SWI/SNF CRCs in animals and plants and discusses the multiple nuclear and biological roles of SWI/SNF CRCs and how SWI/SNF activity is altered by complex subunit composition, posttranslational modifications, and the chromatin context to support proper development and response to extrinsic cues.

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2023-05-22
2024-04-24
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Literature Cited

  1. 1.
    Alpsoy A, Dykhuizen EC. 2018. Glioma tumor suppressor candidate region gene 1 (GLTSCR1) and its paralog GLTSCR1-like form SWI/SNF chromatin remodeling subcomplexes. J. Biol. Chem. 293:3892–903
    [Google Scholar]
  2. 2.
    Archacki R, Buszewicz D, Sarnowski TJ, Sarnowska E, Rolicka AT et al. 2013. BRAHMA ATPase of the SWI/SNF chromatin remodeling complex acts as a positive regulator of gibberellin-mediated responses in Arabidopsis. PLOS ONE 8:e58588
    [Google Scholar]
  3. 3.
    Archacki R, Sarnowski TJ, Halibart-Puzio J, Brzeska K, Buszewicz D et al. 2009. Genetic analysis of functional redundancy of BRM ATPase and ATSWI3C subunits of Arabidopsis SWI/SNF chromatin remodelling complexes. Planta 229:1281–92
    [Google Scholar]
  4. 4.
    Archacki R, Yatusevich R, Buszewicz D, Krzyczmonik K, Patryn J et al. 2017. Arabidopsis SWI/SNF chromatin remodeling complex binds both promoters and terminators to regulate gene expression. Nucleic Acids Res. 45:3116–29
    [Google Scholar]
  5. 5.
    Baker RW, Reimer JM, Carman PJ, Turegun B, Arakawa T et al. 2021. Structural insights into assembly and function of the RSC chromatin remodeling complex. Nat. Struct. Mol. Biol. 28:71–80
    [Google Scholar]
  6. 6.
    Barutcu AR, Lajoie BR, Fritz AJ, McCord RP, Nickerson JA et al. 2016. SMARCA4 regulates gene expression and higher order chromatin structure in proliferating mammary epithelial cells. Genome Res. 26:1188–201
    [Google Scholar]
  7. 7.
    Bezhani S, Winter C, Hershman S, Wagner JD, Kennedy JF et al. 2007. Unique, shared, and redundant roles for the Arabidopsis SWI/SNF chromatin remodeling ATPases BRAHMA and SPLAYED. Plant Cell 19:403–16
    [Google Scholar]
  8. 8.
    Bieluszewski T, Galganski L, Sura W, Bieluszewska A, Abram M et al. 2015. AtEAF1 is a potential platform protein for Arabidopsis NuA4 acetyltransferase complex. BMC Plant Biol. 15:75
    [Google Scholar]
  9. 9.
    Blumli S, Wiechens N, Wu MY, Singh V, Gierlinski M et al. 2021. Acute depletion of the ARID1A subunit of SWI/SNF complexes reveals distinct pathways for activation and repression of transcription. Cell Rep. 37:109943
    [Google Scholar]
  10. 10.
    Boulay G, Sandoval GJ, Riggi N, Iyer S, Buisson R et al. 2017. Cancer-specific retargeting of BAF complexes by a prion-like domain. Cell 171:163–78.e19
    [Google Scholar]
  11. 11.
    Brzezinka K, Altmann S, Czesnick H, Nicolas P, Gorka M et al. 2016. Arabidopsis FORGETTER1 mediates stress-induced chromatin memory through nucleosome remodeling. eLife 5:e17061
    [Google Scholar]
  12. 12.
    Buszewicz D, Archacki R, Palusiński A, Kotliński M, Fogtman A et al. 2016. HD2C histone deacetylase and a SWI/SNF chromatin remodelling complex interact and both are involved in mediating the heat stress response in Arabidopsis. Plant Cell Environ. 39:2108–22
    [Google Scholar]
  13. 13.
    Cairns BR, Levinson RS, Yamamoto KR, Kornberg R. 1996. Essential role of Swp73p in the function of yeast Swi/Snf complex. Genes Dev. 10:2131–44
    [Google Scholar]
  14. 14.
    Campi M, D'Andrea L, Emiliani J, Casati P 2012. Participation of chromatin-remodeling proteins in the repair of ultraviolet-B-damaged DNA. Plant Physiol. 158:981–95
    [Google Scholar]
  15. 15.
    Carissimi C, Laudadio I, Cipolletta E, Gioiosa S, Mihailovich M et al. 2015. ARGONAUTE2 cooperates with SWI/SNF complex to determine nucleosome occupancy at human transcription start sites. Nucleic Acids Res. 43:1498–512
    [Google Scholar]
  16. 16.
    Casati P, Campi M, Chu F, Suzuki N, Maltby D et al. 2008. Histone acetylation and chromatin remodeling are required for UV-B-dependent transcriptional activation of regulated genes in maize. Plant Cell 20:827–42
    [Google Scholar]
  17. 17.
    Casati P, Stapleton AE, Blum JE, Walbot V. 2006. Genome-wide analysis of high-altitude maize and gene knockdown stocks implicates chromatin remodeling proteins in response to UV-B. Plant J. 46:613–27
    [Google Scholar]
  18. 18.
    Chakrabortee S, Kayatekin C, Newby GA, Mendillo ML, Lancaster A, Lindquist S. 2016. Luminidependens (LD) is an Arabidopsis protein with prion behavior. PNAS 113:6065–70
    [Google Scholar]
  19. 19.
    Chang L, Azzolin L, Di Biagio D, Zanconato F, Battilana G et al. 2018. The SWI/SNF complex is a mechanoregulated inhibitor of YAP and TAZ. Nature 563:265–69
    [Google Scholar]
  20. 20.
    Clapier CR, Iwasa J, Cairns BR, Peterson CL. 2017. Mechanisms of action and regulation of ATP-dependent chromatin-remodelling complexes. Nat. Rev. Mol. Cell Biol. 18:407–22
    [Google Scholar]
  21. 21.
    Cristini A, Groh M, Kristiansen MS, Gromak N. 2018. RNA/DNA hybrid interactome identifies DXH9 as a molecular player in transcriptional termination and R-loop-associated DNA damage. Cell Rep. 23:1891–905
    [Google Scholar]
  22. 22.
    Damelin M, Simon I, Moy TI, Wilson B, Komili S et al. 2002. The genome-wide localization of Rsc9, a component of the RSC chromatin-remodeling complex, changes in response to stress. Mol. Cell 9:563–73
    [Google Scholar]
  23. 23.
    Davis RB, Kaur T, Moosa MM, Banerjee PR. 2021. FUS oncofusion protein condensates recruit mSWI/SNF chromatin remodeler via heterotypic interactions between prion-like domains. Protein Sci. 30:1454–66
    [Google Scholar]
  24. 24.
    Dennis EM, Garcia DM. 2022. Biochemical principles in prion-based inheritance. Epigenomes 6:4
    [Google Scholar]
  25. 25.
    Depège-Fargeix N, Javelle M, Chambrier P, Frangne N, Gerentes D et al. 2011. Functional characterization of the HD-ZIP IV transcription factor OCL1 from maize. J. Exp. Bot. 62:293–305
    [Google Scholar]
  26. 26.
    Diego-Martin B, Pérez-Alemany J, Candela-Ferre J, Corbalán-Acedo A, Pereyra J et al. 2022. The TRIPLE PHD FINGERS proteins are required for SWI/SNF complex-mediated +1 nucleosome positioning and transcription start site determination in Arabidopsis. Nucleic Acids Res. 50:10399–417
    [Google Scholar]
  27. 27.
    Ding B, Wang G-L. 2015. Chromatin versus pathogens: the function of epigenetics in plant immunity. Front. Plant Sci. 6:675
    [Google Scholar]
  28. 28.
    Du Z, Regan J, Bartom E, Wu W-S, Zhang L et al. 2020. Elucidating the regulatory mechanism of Swi1 prion in global transcription and stress responses. Sci. Rep. 10:21838
    [Google Scholar]
  29. 29.
    Efroni I, Han S-K, Kim HJ, Wu M-F, Steiner E et al. 2013. Regulation of leaf maturation by chromatin-mediated modulation of cytokinin responses. Dev. Cell 24:438–45
    [Google Scholar]
  30. 30.
    Farrona S, Hurtado L, March-Díaz R, Schmitz RJ, Florencio FJ et al. 2011. Brahma is required for proper expression of the floral repressor FLC in Arabidopsis. PLOS ONE 6:e17997
    [Google Scholar]
  31. 31.
    Feng J, Xu X, Fan X, Yi Q, Tang L 2021. BAF57/SMARCE1 interacting with splicing factor SRSF1 regulates mechanical stress-induced alternative splicing of cyclin D1. Genes 12:306
    [Google Scholar]
  32. 32.
    Gañez-Zapater A, Mackowiak SD, Guo Y, Tarbier M, Jordán-Pla A et al. 2022. The SWI/SNF subunit BRG1 affects alternative splicing by changing RNA binding factor interactions with nascent RNA. Mol. Genet. Genom. 297:463–84
    [Google Scholar]
  33. 33.
    Gao X, Tate P, Hu P, Tjian R, Skarnes WC, Wang Z. 2008. ES cell pluripotency and germ-layer formation require the SWI/SNF chromatin remodeling component BAF250a. PNAS 105:6656–61
    [Google Scholar]
  34. 34.
    Gatchalian J, Malik S, Ho J, Lee DS, Kelso TWR et al. 2018. A non-canonical BRD9-containing BAF chromatin remodeling complex regulates naive pluripotency in mouse embryonic stem cells. Nat. Commun. 9:5139
    [Google Scholar]
  35. 35.
    Goncharoff DK, Du Z, Li L. 2018. A brief overview of the Swi1 prion—[SWI+]. FEMS Yeast Res. 18:foy061
    [Google Scholar]
  36. 36.
    Gratkowska-Zmuda DM, Kubala S, Sarnowska E, Cwiek P, Oksinska P et al. 2020. The SWI/SNF ATP-dependent chromatin remodeling complex in Arabidopsis responds to environmental changes in temperature-dependent manner. Int. J. Mol. Sci. 21:762
    [Google Scholar]
  37. 37.
    Gutierrez JI, Brittingham GP, Karadeniz Y, Tran KD, Dutta A et al. 2022. SWI/SNF senses carbon starvation with a pH-sensitive low-complexity sequence. eLife 11:e70344Depending on environmental cues, low-pH-mediated extension of a disordered domain in SNF5 regulates interaction with TFs.
    [Google Scholar]
  38. 38.
    Hainer SJ, Boskovic A, McCannell KN, Rando OJ, Fazzio TG. 2019. Profiling of pluripotency factors in single cells and early embryos. Cell 177:1319–29.e11
    [Google Scholar]
  39. 39.
    Han S-K, Sang Y, Rodrigues A, BIOL425 F2010, Wu M-F et al. 2012. The SWI2/SNF2 chromatin remodeling ATPase BRAHMA represses abscisic acid responses in the absence of the stress stimulus in Arabidopsis. Plant Cell 24:124892–906
    [Google Scholar]
  40. 40.
    Han Y, Reyes AA, Malik S, He Y 2020. Cryo-EM structure of SWI/SNF complex bound to a nucleosome. Nature 579:452–55
    [Google Scholar]
  41. 41.
    Hays E, Nettleton E, Carter C, Morales M, Vo L et al. 2020. The SWI/SNF ATPase BRG1 stimulates DNA end resection and homologous recombination by reducing nucleosome density at DNA double strand breaks and by promoting the recruitment of the CtIP nuclease. Cell Cycle 19:3096–114
    [Google Scholar]
  42. 42.
    He S, Wu Z, Tian Y, Yu Z, Yu J et al. 2020. Structure of nucleosome-bound human BAF complex. Science 367:875–81
    [Google Scholar]
  43. 43.
    Hernández-García J, Diego-Martin B, Kuo PH, Jami-Alahmadi Y, Vashisht AA et al. 2022. Comprehensive identification of SWI/SNF complex subunits underpins deep eukaryotic ancestry and reveals new plant components. Commun. Biol. 5:549This study provides evolutionary evidence for the cBAF–ncBAF dichotomy in plants.
    [Google Scholar]
  44. 44.
    Ho L, Crabtree GR. 2010. Chromatin remodelling during development. Nature 463:474–84
    [Google Scholar]
  45. 45.
    Ho PJ, Lloyd SM, Bao X. 2019. Unwinding chromatin at the right places: how BAF is targeted to specific genomic locations during development. Development 146:dev178780
    [Google Scholar]
  46. 46.
    Hota SK, Rao KS, Blair AP, Khalilimeybodi A, Hu KM et al. 2022. Brahma safeguards canalization of cardiac mesoderm differentiation. Nature 602:129–34
    [Google Scholar]
  47. 47.
    Huang CY, Rangel DS, Qin X, Bui C, Li R et al. 2021. The chromatin-remodeling protein BAF60/SWP73A regulates the plant immune receptor NLRs. Cell Host Microbe 29:425–34.e4
    [Google Scholar]
  48. 48.
    Huber FM, Greenblatt SM, Davenport AM, Martinez C, Xu Y et al. 2017. Histone-binding of DPF2 mediates its repressive role in myeloid differentiation. PNAS 114:6016–21
    [Google Scholar]
  49. 49.
    Ito T, Watanabe H, Yamamichi N, Kondo S, Tando T et al. 2008. Brm transactivates the telomerase reverse transcriptase (TERT) gene and modulates the splicing patterns of its transcripts in concert with p54nrb. Biochem. J. 411:201–9
    [Google Scholar]
  50. 50.
    Iurlaro M, Stadler MB, Masoni F, Jagani Z, Galli GG, Schubeler D. 2021. Mammalian SWI/SNF continuously restores local accessibility to chromatin. Nat. Genet. 53:279–87
    [Google Scholar]
  51. 51.
    Jarończyk K, Sosnowska K, Zaborowski A, Pupel P, Bucholc M et al. 2021. Bromodomain-containing subunits BRD1, BRD2, and BRD13 are required for proper functioning of SWI/SNF complexes in Arabidopsis. Plant Commun. 2:100174
    [Google Scholar]
  52. 52.
    Jégu T, Domenichini S, Blein T, Ariel F, Christ A et al. 2015. A SWI/SNF chromatin remodelling protein controls cytokinin production through the regulation of chromatin architecture. PLOS ONE 10:e0138276
    [Google Scholar]
  53. 53.
    Jégu T, Latrasse D, Delarue M, Hirt H, Domenichini S et al. 2014. The BAF60 subunit of the SWI/SNF chromatin-remodeling complex directly controls the formation of a gene loop at FLOWERING LOCUS C in Arabidopsis. Plant Cell 26:538–51
    [Google Scholar]
  54. 54.
    Jégu T, Veluchamy A, Ramirez-Prado JS, Rizzi-Paillet C, Perez M et al. 2017. The Arabidopsis SWI/SNF protein BAF60 mediates seedling growth control by modulating DNA accessibility. Genome Biol. 18:114
    [Google Scholar]
  55. 55.
    Jerzmanowski A. 2007. SWI/SNF chromatin remodeling and linker histones in plants. Biochim. Biophys. Acta Gene Struct. Expr. 1769:330–45
    [Google Scholar]
  56. 56.
    Jian Y, Shim W-B, Ma Z 2021. Multiple functions of SWI/SNF chromatin remodeling complex in plant-pathogen interactions. Stress Biol. 1:18
    [Google Scholar]
  57. 57.
    Jiang J, Mao N, Hu H, Tang J, Han D et al. 2019. A SWI/SNF subunit regulates chromosomal dissociation of structural maintenance complex 5 during DNA repair in plant cells. PNAS 116:15288–96
    [Google Scholar]
  58. 58.
    Jin R, Klasfeld S, Zhu Y, Fernandez Garcia M, Xiao J et al. 2021. LEAFY is a pioneer transcription factor and licenses cell reprogramming to floral fate. Nat. Commun. 12:626LEAFY is a pioneer TF that licenses cell fate changes via H1 linker histone displacement and SWI/SNF recruitment to target loci.
    [Google Scholar]
  59. 59.
    Johnson KCM, Xia S, Feng X, Li X. 2015. The chromatin remodeler SPLAYED negatively regulates SNC1-mediated immunity. Plant Cell Physiol. 56:1616–23
    [Google Scholar]
  60. 60.
    Judd J, Duarte FM, Lis JT. 2021. Pioneer-like factor GAF cooperates with PBAP (SWI/SNF) and NURF (ISWI) to regulate transcription. Genes Dev. 35:147–56
    [Google Scholar]
  61. 61.
    Kadoch C, Crabtree GR. 2015. Mammalian SWI/SNF chromatin remodeling complexes and cancer: mechanistic insights gained from human genomics. Sci. Adv. 1:e1500447
    [Google Scholar]
  62. 62.
    Kadoch C, Williams RT, Calarco JP, Miller EL, Weber CM et al. 2017. Dynamics of BAF-Polycomb complex opposition on heterochromatin in normal and oncogenic states. Nat. Genet. 49:213–22
    [Google Scholar]
  63. 63.
    Kingston RE, Tamkun JW. 2014. Transcriptional regulation by trithorax-group proteins. Cold Spring Harb. Perspect. Biol. 6:a019349
    [Google Scholar]
  64. 64.
    Kubik S, Bruzzone MJ, Challal D, Dreos R, Mattarocci S et al. 2019. Opposing chromatin remodelers control transcription initiation frequency and start site selection. Nat. Struct. Mol. Biol. 26:744–54
    [Google Scholar]
  65. 65.
    Kwon CS, Chen C, Wagner D. 2005. WUSCHEL is a primary target for transcriptional regulation by SPLAYED in dynamic control of stem cell fate in Arabidopsis. Genes Dev. 19:992–1003
    [Google Scholar]
  66. 66.
    Kwon CS, Wagner D. 2007. Unwinding chromatin for development and growth: a few genes at a time. Trends Genet. 23:403–12
    [Google Scholar]
  67. 67.
    Lai X, Blanc-Mathieu R, GrandVuillemin L, Huang Y, Stigliani A et al. 2021. The LEAFY floral regulator displays pioneer transcription factor properties. Mol. Plant 14:829–37
    [Google Scholar]
  68. 68.
    Li C, Chen C, Gao L, Yang S, Nguyen V et al. 2015. The Arabidopsis SWI2/SNF2 chromatin remodeler BRAHMA regulates Polycomb function during vegetative development and directly activates the flowering repressor gene SVP. PLOS Genet. 11:e1004944
    [Google Scholar]
  69. 69.
    Li C, Gu L, Gao L, Chen C, Wei C-Q et al. 2016. Concerted genomic targeting of H3K27 demethylase REF6 and chromatin-remodeling ATPase BRM in Arabidopsis. Nat. Genet. 48:687–93
    [Google Scholar]
  70. 70.
    Lin X, Gu D, Zhao H, Peng Y, Zhang G et al. 2018. LFR is functionally associated with AS2 to mediate leaf development in Arabidopsis. Plant J. 95(4):598–612 https://doi.org/10.1111/tpj.13973
    [Crossref] [Google Scholar]
  71. 71.
    Lin X, Yuan C, Zhu B, Yuan T, Li X et al. 2021. LFR physically and genetically interacts with SWI/SNF component SWI3B to regulate leaf blade development in Arabidopsis. Front. Plant Sci. 12:717649 Erratum 2022. Front. Plant Sci. 13:901613
    [Google Scholar]
  72. 72.
    Liu C, Wang C, Wang G, Becker C, Zaidem M, Weigel D. 2016. Genome-wide analysis of chromatin packing in Arabidopsis thaliana at single-gene resolution. Genome Res. 26:1057–68
    [Google Scholar]
  73. 73.
    Liu C, Xin Y, Xu L, Cai Z, Xue Y et al. 2018. Arabidopsis ARGONAUTE 1 binds chromatin to promote gene transcription in response to hormones and stresses. Dev. Cell 44:348–61.e7
    [Google Scholar]
  74. 74.
    Malovichko YV, Antonets KS, Maslova AR, Andreeva EA, Inge-Vechtomov SG, Nizhnikov AA 2019. RNA sequencing reveals specific transcriptomic signatures distinguishing effects of the [SWI+] prion and SWI1 deletion in yeast Saccharomyces cerevisiae. Genes 10:212
    [Google Scholar]
  75. 75.
    Marino MM, Rega C, Russo R, Valletta M, Gentile MT et al. 2019. Interactome mapping defines BRG1, a component of the SWI/SNF chromatin remodeling complex, as a new partner of the transcriptional regulator CTCF. J. Biol. Chem. 294:861–73
    [Google Scholar]
  76. 76.
    Mashtalir N, Dao HT, Sankar A, Liu H, Corin AJ et al. 2021. Chromatin landscape signals differentially dictate the activities of mSWI/SNF family complexes. Science 373:306–15A comprehensive analysis of the relationship between chromatin remodeling by BAF complexes and histone modifications.
    [Google Scholar]
  77. 77.
    Mashtalir N, D'Avino AR, Michel BC, Luo J, Pan J et al. 2018. Modular organization and assembly of SWI/SNF family chromatin remodeling complexes. Cell 175:1272–88.e20
    [Google Scholar]
  78. 78.
    Michel BC, D'Avino AR, Cassel SH, Mashtalir N, McKenzie ZM et al. 2018. A non-canonical SWI/SNF complex is a synthetic lethal target in cancers driven by BAF complex perturbation. Nat. Cell Biol. 20:1410–20
    [Google Scholar]
  79. 79.
    Middeljans E, Wan X, Jansen PW, Sharma V, Stunnenberg HG, Logie C. 2012. SS18 together with animal-specific factors defines human BAF-type SWI/SNF complexes. PLOS ONE 7:e33834
    [Google Scholar]
  80. 80.
    Mlynárová L, Nap J-P, Bisseling T. 2007. The SWI/SNF chromatin-remodeling gene AtCHR12 mediates temporary growth arrest in Arabidopsis thaliana upon perceiving environmental stress. Plant J. 51:874–85
    [Google Scholar]
  81. 81.
    Nelissen H, Eeckhout D, Demuynck K, Persiau G, Walton A et al. 2015. Dynamic changes in ANGUSTIFOLIA3 complex composition reveal a growth regulatory mechanism in the maize leaf. Plant Cell 27:1605–19
    [Google Scholar]
  82. 82.
    Nguyen NH, Jung C, Cheong JJ. 2019. Chromatin remodeling for the transcription of type 2C protein phosphatase genes in response to salt stress. Plant Physiol. Biochem. 141:325–31
    [Google Scholar]
  83. 83.
    Ochoa D, Jarnuczak AF, Viéitez C, Gehre M, Soucheray M et al. 2020. The functional landscape of the human phosphoproteome. Nat. Biotechnol. 38:365–73
    [Google Scholar]
  84. 84.
    Padilla-Benavides T, Haokip DT, Yoon Y, Reyes-Gutierrez P, Rivera-Pérez JA, Imbalzano AN. 2020. CK2-dependent phosphorylation of the Brg1 chromatin remodeling enzyme occurs during mitosis. Int. J. Mol. Sci. 21:923
    [Google Scholar]
  85. 85.
    Padilla-Benavides T, Reyes-Gutierrez P, Imbalzano AN 2020. Regulation of the mammalian SWI/SNF family of chromatin remodeling enzymes by phosphorylation during myogenesis. Biology 9:152
    [Google Scholar]
  86. 86.
    Patel AB, Moore CM, Greber BJ, Luo J, Zukin SA et al. 2019. Architecture of the chromatin remodeler RSC and insights into its nucleosome engagement. eLife 8:e54449
    [Google Scholar]
  87. 87.
    Patty BJ, Hainer SJ. 2020. Non-coding RNAs and nucleosome remodeling complexes: an intricate regulatory relationship. Biology 9:213
    [Google Scholar]
  88. 88.
    Peirats-Llobet M, Han S-K, Gonzalez-Guzman M, Jeong CW, Rodriguez L et al. 2016. A direct link between abscisic acid sensing and the chromatin-remodeling ATPase BRAHMA via core ABA signaling pathway components. Mol. Plant 9:136–47
    [Google Scholar]
  89. 89.
    Powers SK, Holehouse AS, Korasick DA, Schreiber KH, Clark NM et al. 2019. Nucleo-cytoplasmic partitioning of ARF proteins controls auxin responses in Arabidopsis thaliana. Mol. Cell 76:177–90.e5
    [Google Scholar]
  90. 90.
    Qi D, Wen Q, Meng Z, Yuan S, Guo H et al. 2020. OsLFR is essential for early endosperm and embryo development by interacting with SWI/SNF complex members in Oryza sativa. Plant J. 104:901–16
    [Google Scholar]
  91. 91.
    Rendina R, Strangi A, Avallone B, Giordano E 2010. Bap170, a subunit of the Drosophila PBAP chromatin remodeling complex, negatively regulates the EGFR signaling. Genetics 186:167–81
    [Google Scholar]
  92. 92.
    Ribeiro-Silva C, Vermeulen W, Lans H. 2019. SWI/SNF: complex complexes in genome stability and cancer. DNA Repair 77:87–95
    [Google Scholar]
  93. 93.
    Ricci WA, Lu Z, Ji L, Marand AP, Ethridge CL et al. 2019. Widespread long-range cis-regulatory elements in the maize genome. Nat. Plants 5:1237–49
    [Google Scholar]
  94. 94.
    Richter R, Kinoshita A, Vincent C, Martinez-Gallegos R, Gao H et al. 2019. Floral regulators FLC and SOC1 directly regulate expression of the B3-type transcription factor TARGET OF FLC AND SVP 1 at the Arabidopsis shoot apex via antagonistic chromatin modifications. PLOS Genet. 15:e1008065
    [Google Scholar]
  95. 95.
    Sabate R, Rousseau F, Schymkowitz J, Ventura S. 2015. What makes a protein sequence a prion?. PLOS Comput. Biol. 11:e1004013
    [Google Scholar]
  96. 96.
    Sakamoto T, Tsujimoto-Inui Y, Sotta N, Hirakawa T, Matsunaga TM et al. 2018. Proteasomal degradation of BRAHMA promotes boron tolerance in Arabidopsis. Nat. Commun. 9:5285
    [Google Scholar]
  97. 97.
    Sang Y, Silva-Ortega CO, Wu S, Yamaguchi N, Wu M-F et al. 2012. Mutations in two non-canonical Arabidopsis SWI2/SNF2 chromatin remodeling ATPases cause embryogenesis and stem cell maintenance defects. Plant J. 72:1000–14
    [Google Scholar]
  98. 98.
    Sarnowska E, Gratkowska DM, Sacharowski SP, Cwiek P, Tohge T et al. 2016. The role of SWI/SNF chromatin remodeling complexes in hormone crosstalk. Trends Plant Sci. 21:594–608
    [Google Scholar]
  99. 99.
    Sarnowska EA, Rolicka AT, Bucior E, Cwiek P, Tohge T et al. 2013. DELLA-interacting SWI3C core subunit of switch/sucrose nonfermenting chromatin remodeling complex modulates gibberellin responses and hormonal cross talk in Arabidopsis. Plant Physiol. 163:305–17
    [Google Scholar]
  100. 100.
    Sarnowski TJ, Ríos G, Jásik J, Świeżewski S, Kaczanowski S et al. 2005. SWI3 subunits of putative SWI/SNF chromatin-remodeling complexes play distinct roles during Arabidopsis development. Plant Cell 17:2454–72
    [Google Scholar]
  101. 101.
    Schick S, Grosche S, Kohl KE, Drpic D, Jaeger MG et al. 2021. Acute BAF perturbation causes immediate changes in chromatin accessibility. Nat. Genet. 53:269–78
    [Google Scholar]
  102. 102.
    Shaked H, Avivi-Ragolsky N, Levy AA. 2006. Involvement of the Arabidopsis SWI2/SNF2 chromatin remodeling gene family in DNA damage response and recombination. Genetics 173:985–94
    [Google Scholar]
  103. 103.
    Shao Z, Raible F, Mollaaghababa R, Guyon JR, Wu CT et al. 1999. Stabilization of chromatin structure by PRC1, a Polycomb complex. Cell 98:37–46
    [Google Scholar]
  104. 104.
    Shinozaki K, Yamaguchi-Shinozaki K. 2000. Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr. Opin. Plant Biol. 3:217–23
    [Google Scholar]
  105. 105.
    Shu J, Chen C, Li C, Thapa RK, Song J et al. 2021. Genome-wide occupancy of Arabidopsis SWI/SNF chromatin remodeler SPLAYED provides insights into its interplay with its close homolog BRAHMA and Polycomb proteins. Plant J. 106:200–13
    [Google Scholar]
  106. 106.
    Skalska L, Begley V, Beltran M, Lukauskas S, Khandelwal G et al. 2021. Nascent RNA antagonizes the interaction of a set of regulatory proteins with chromatin. Mol. Cell 81:2944–59.e10
    [Google Scholar]
  107. 107.
    Smaczniak C, Immink RG, Muiño JM, Blanvillain R, Busscher M et al. 2012. Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. PNAS 109:1560–65
    [Google Scholar]
  108. 108.
    St Pierre R, Collings CK, Samé Guerra DD, Widmer CJ, Bolonduro O et al. 2022. SMARCE1 deficiency generates a targetable mSWI/SNF dependency in clear cell meningioma. Nat. Genet. 54:861–73
    [Google Scholar]
  109. 109.
    Stanton BZ, Hodges C, Calarco JP, Braun SM, Ku WL et al. 2017. Smarca4 ATPase mutations disrupt direct eviction of PRC1 from chromatin. Nat. Genet. 49:282–88
    [Google Scholar]
  110. 110.
    Strader L, Wagner D, Weijers D. 2021. Plant transcription factors—being in the right place with the right company. Curr. Opin. Plant Biol. 65:102136
    [Google Scholar]
  111. 111.
    Su Y, Kwon CS, Bezhani S, Huvermann B, Chen C et al. 2006. The N-terminal ATPase AT-hook-containing region of the Arabidopsis chromatin-remodeling protein SPLAYED is sufficient for biological activity. Plant J. 46:685–99
    [Google Scholar]
  112. 112.
    Sun B, Zhou Y, Cai J, Shang E, Yamaguchi N et al. 2019. Integration of transcriptional repression and Polycomb-mediated silencing of WUSCHEL in floral meristems. Plant Cell 31:1488–505
    [Google Scholar]
  113. 113.
    Thouly C, Le Masson M, Lai X, Carles CC, Vachon G 2020. Unwinding BRAHMA functions in plants. Genes 11:90
    [Google Scholar]
  114. 114.
    Trizzino M, Barbieri E, Petracovici A, Wu S, Welsh SA et al. 2018. The tumor suppressor ARID1A controls global transcription via pausing of RNA Polymerase II. Cell Rep. 23:3933–45
    [Google Scholar]
  115. 115.
    Tsai S, Fournier LA, Chang EY, Wells JP, Minaker SW et al. 2021. ARID1A regulates R-loop associated DNA replication stress. PLOS Genet. 17:e1009238
    [Google Scholar]
  116. 116.
    Valencia AM, Collings CK, Dao HT, St Pierre R, Cheng Y-C et al. 2019. Recurrent SMARCB1 mutations reveal a nucleosome acidic patch interaction site that potentiates mSWI/SNF complex chromatin remodeling. Cell 179:1342–56.e23
    [Google Scholar]
  117. 117.
    Venkataramanan S, Douglass S, Galivanche AR, Johnson TL. 2017. The chromatin remodeling complex Swi/Snf regulates splicing of meiotic transcripts in Saccharomyces cerevisiae. Nucleic Acids Res. 45:7708–21
    [Google Scholar]
  118. 118.
    Vercruyssen L, Verkest A, Gonzalez N, Heyndrickx KS, Eeckhout D et al. 2014. ANGUSTIFOLIA3 binds to SWI/SNF chromatin remodeling complexes to regulate transcription during Arabidopsis leaf development. Plant Cell 26:210–29
    [Google Scholar]
  119. 119.
    Vicente J, Mendiondo GM, Movahedi M, Peirats-Llobet M, Juan Y-T et al. 2017. The Cys-Arg/N-end rule pathway is a general sensor of abiotic stress in flowering plants. Curr. Biol. 27:3183–90.e4
    [Google Scholar]
  120. 120.
    Wagner D, Meyerowitz EM. 2002. SPLAYED, a novel SWI/SNF ATPase homolog, controls reproductive development in Arabidopsis. Curr. Biol. 12:85–94
    [Google Scholar]
  121. 121.
    Wagner FR, Dienemann C, Wang H, Stutzer A, Tegunov D et al. 2020. Structure of SWI/SNF chromatin remodeller RSC bound to a nucleosome. Nature 579:448–51
    [Google Scholar]
  122. 122.
    Waldholm J, Wang Z, Brodin D, Tyagi A, Yu S et al. 2011. SWI/SNF regulates the alternative processing of a specific subset of pre-mRNAs in Drosophila melanogaster. BMC Mol. Biol. 12:46
    [Google Scholar]
  123. 123.
    Walley JW, Rowe HC, Xiao Y, Chehab EW, Kliebenstein DJ et al. 2008. The chromatin remodeler SPLAYED regulates specific stress signaling pathways. PLOS Pathog. 4:e1000237
    [Google Scholar]
  124. 124.
    Wang C, Guo Z, Zhan X, Yang F, Wu M, Zhang X. 2020. Structure of the yeast Swi/Snf complex in a nucleosome free state. Nat. Commun. 11:3398
    [Google Scholar]
  125. 125.
    Wang L, Oh TG, Magida J, Estepa G, Obayomi SMB et al. 2021. Bromodomain containing 9 (BRD9) regulates macrophage inflammatory responses by potentiating glucocorticoid receptor activity. PNAS 118:e2109517118
    [Google Scholar]
  126. 126.
    Wang Z, Ma Z, Castillo-González C, Sun D, Li Y et al. 2018. SWI2/SNF2 ATPase CHR2 remodels pri-miRNAs via Serrate to impede miRNA production. Nature 557:516–21
    [Google Scholar]
  127. 127.
    Wang Z, Yuan T, Yuan C, Niu Y, Sun D, Cui S. 2009. LFR, which encodes a novel nuclear-localized Armadillo-repeat protein, affects multiple developmental processes in the aerial organs in Arabidopsis. Plant Mol. Biol. 69:121–31
    [Google Scholar]
  128. 128.
    Weber CM, Hafner A, Kirkland JG, Braun SMG, Stanton BZ et al. 2021. mSWI/SNF promotes Polycomb repression both directly and through genome-wide redistribution. Nat. Struct. Mol. Biol. 28:501–11Rapid depletion reveals dynamic interplay between opposite and synergistic roles of SWI/SNF and Polycomb activities in embryonic stem cells.
    [Google Scholar]
  129. 129.
    Wei J, Alfajaro MM, DeWeirdt PC, Hanna RE, Lu-Culligan WJ et al. 2021. Genome-wide CRISPR screens reveal host factors critical for SARS-CoV-2 infection. Cell 184:76–91.e13
    [Google Scholar]
  130. 130.
    Wu M-F, Sang Y, Bezhani S, Yamaguchi N, Han S-K et al. 2012. SWI2/SNF2 chromatin remodeling ATPases overcome Polycomb repression and control floral organ identity with the LEAFY and SEPALLATA3 transcription factors. PNAS 109:3576–81
    [Google Scholar]
  131. 131.
    Wu M-F, Yamaguchi N, Xiao J, Bargmann B, Estelle M et al. 2015. Auxin-regulated chromatin switch directs acquisition of flower primordium founder fate. eLife 4:e09269
    [Google Scholar]
  132. 132.
    Xu Y, Guo C, Zhou B, Li C, Wang H et al. 2016. Regulation of vegetative phase change by SWI2/SNF2 chromatin remodeling ATPase BRAHMA. Plant Physiol. 172:2416–28
    [Google Scholar]
  133. 133.
    Xun Q, Mei M, Song Y, Rong C, Liu J et al. 2022. SWI2/SNF2 chromatin remodeling ATPases SPLAYED and BRAHMA control embryo development in rice. Plant Cell Rep. 41:1389–401
    [Google Scholar]
  134. 134.
    Yang J, Xu Y, Wang J, Gao S, Huang Y et al. 2022. The chromatin remodelling ATPase BRAHMA interacts with GATA-family transcription factor GNC to regulate flowering time in Arabidopsis. J. Exp. Bot. 73:835–47
    [Google Scholar]
  135. 135.
    Yang J, Yuan L, Yen M-R, Zheng F, Ji R et al. 2020. SWI3B and HDA6 interact and are required for transposon silencing in Arabidopsis. Plant J. 102:809–22
    [Google Scholar]
  136. 136.
    Yang S, Li C, Zhao L, Gao S, Lu J et al. 2015. The Arabidopsis SWI2/SNF2 chromatin remodeling ATPase BRAHMA targets directly to PINs and is required for root stem cell niche maintenance. Plant Cell 27:1670–80
    [Google Scholar]
  137. 137.
    Yang T, Wang D, Tian G, Sun L, Yang M et al. 2022. Chromatin remodeling complexes regulate genome architecture in Arabidopsis. Plant Cell 34:2638–51CRCs, including SWI/SNF, fine-tune the A/B genome compartmentalization in Arabidopsis through maintenance of nucleosome occupancy and H3K27me3 in B compartments.
    [Google Scholar]
  138. 138.
    Ye Y, Wu H, Chen K, Clapier CR, Verma N et al. 2019. Structure of the RSC complex bound to the nucleosome. Science 366:838–43
    [Google Scholar]
  139. 139.
    Yu S, Jordán-Pla A, Gañez-Zapater A, Jain S, Rolicka A et al. 2018. SWI/SNF interacts with cleavage and polyadenylation factors and facilitates pre-mRNA 3′ end processing. Nucleic Acids Res. 46:8557–73
    [Google Scholar]
  140. 140.
    Yu X, Meng X, Liu Y, Wang X, Wang T-J et al. 2019. The chromatin remodeler ZmCHB101 impacts alternative splicing contexts in response to osmotic stress. Plant Cell Rep. 38:131–45
    [Google Scholar]
  141. 141.
    Yu Y, Fu W, Xu J, Lei Y, Song X et al. 2021. Bromodomain-containing proteins BRD1, BRD2, and BRD13 are core subunits of SWI/SNF complexes and vital for their genomic targeting in Arabidopsis. Mol. Plant 14:888–904
    [Google Scholar]
  142. 142.
    Yu Y, Liang Z, Song X, Fu W, Xu J et al. 2020. BRAHMA-interacting proteins BRIP1 and BRIP2 are core subunits of Arabidopsis SWI/SNF complexes. Nat. Plants 6:996–1007GLTSCR1/1L-homologs BRIP1/2 interact physically and functionally with BRM, linking BRM to a ncBAF-like complex in plants.
    [Google Scholar]
  143. 143.
    Yuan J, Chen K, Zhang W, Chen Z 2022. Structure of human chromatin-remodelling PBAF complex bound to a nucleosome. Nature 605:166–71
    [Google Scholar]
  144. 144.
    Zaret KS. 2020. Pioneer transcription factors initiating gene network changes. Annu. Rev. Genet. 54:367–85
    [Google Scholar]
  145. 145.
    Zeng L, Zhang Q, Li S, Plotnikov AN, Walsh MJ, Zhou MM. 2010. Mechanism and regulation of acetylated histone binding by the tandem PHD finger of DPF3b. Nature 466:258–62
    [Google Scholar]
  146. 146.
    Zhang D, Li Y, Zhang X, Zha P, Lin R. 2017. The SWI2/SNF2 chromatin-remodeling ATPase BRAHMA regulates chlorophyll biosynthesis in Arabidopsis. Mol. Plant 10:155–67
    [Google Scholar]
  147. 147.
    Zhang H, Lang Z, Zhu JK. 2018. Dynamics and function of DNA methylation in plants. Nat. Rev. Mol. Cell Biol. 19:489–506
    [Google Scholar]
  148. 148.
    Zhang J, Lai J, Wang F, Yang S, He Z et al. 2017. A SUMO ligase AtMMS21 regulates the stability of the chromatin remodeler BRAHMA in root development. Plant Physiol. 173:1574–82
    [Google Scholar]
  149. 149.
    Zhao M, Yang S, Chen C-Y, Li C, Shan W et al. 2015. Arabidopsis BREVIPEDICELLUS interacts with the SWI2/SNF2 chromatin remodeling ATPase BRAHMA to regulate KNAT2 and KNAT6 expression in control of inflorescence architecture. PLOS Genet. 11:e1005125
    [Google Scholar]
  150. 150.
    Guo J, Cai G, Li Y-Q, Zhang Y-X, Su Y-N et al. 2022. Comprehensive characterization of three classes of Arabidopsis SWI/SNF chromatin remodelling complexes. Nat. Plants 8:1423–39Identification of the components of three SWI/SNF CRCs in plants that form around the BRM, SYD, or MINU ATPases.
    [Google Scholar]
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