Chromatin attachment to the nuclear matrix represses hypocotyl elongation in Arabidopsis thaliana.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
12 Feb 2024
12 Feb 2024
Historique:
received:
03
07
2023
accepted:
26
01
2024
medline:
13
2
2024
pubmed:
13
2
2024
entrez:
12
2
2024
Statut:
epublish
Résumé
The nuclear matrix is a nuclear compartment that has diverse functions in chromatin regulation and transcription. However, how this structure influences epigenetic modifications and gene expression in plants is largely unknown. In this study, we show that a nuclear matrix binding protein, AHL22, together with the two transcriptional repressors FRS7 and FRS12, regulates hypocotyl elongation by suppressing the expression of a group of genes known as SMALL AUXIN UP RNAs (SAURs) in Arabidopsis thaliana. The transcriptional repression of SAURs depends on their attachment to the nuclear matrix. The AHL22 complex not only brings these SAURs, which contain matrix attachment regions (MARs), to the nuclear matrix, but it also recruits the histone deacetylase HDA15 to the SAUR loci. This leads to the removal of H3 acetylation at the SAUR loci and the suppression of hypocotyl elongation. Taken together, our results indicate that MAR-binding proteins act as a hub for chromatin and epigenetic regulators. Moreover, we present a mechanism by which nuclear matrix attachment to chromatin regulates histone modifications, transcription, and hypocotyl elongation.
Identifiants
pubmed: 38346986
doi: 10.1038/s41467-024-45577-5
pii: 10.1038/s41467-024-45577-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1286Subventions
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : JI 347/6-1
Informations de copyright
© 2024. The Author(s).
Références
Berezney, R. & Coffey, D. S. Identification of a nuclear protein matrix. Biochem Biophys. Res Commun. 60, 1410–1417 (1974).
pubmed: 4214419
doi: 10.1016/0006-291X(74)90355-6
Martelli, A. M. et al. The controversial nuclear matrix: a balanced point of view. Histol. Histopathol. 17, 1193–1205 (2002).
pubmed: 12371147
Tsutsui, K. M., Sano, K. & Tsutsui, K. Dynamic view of the nuclear matrix. Acta Med Okayama 59, 113–120 (2005).
pubmed: 16155636
Bode, J., Stengert-Iber, M., Kay, V., Schlake, T. & Dietz-Pfeilstetter, A. Scaffold/matrix-attached regions: topological switches with multiple regulatory functions. Crit. Rev. Eukaryot. Gene Expr. 6, 115–138 (1996).
pubmed: 8855385
doi: 10.1615/CritRevEukarGeneExpr.v6.i2-3.20
Allen, G. C., Spiker, S. & Thompson, W. F. Use of matrix attachment regions (MARs) to minimize transgene silencing. Plant Mol. Biol. 43, 361–376 (2000).
pubmed: 10999416
doi: 10.1023/A:1006424621037
Gasser, S. M., Amati, B. B., Cardenas, M. E. & Hofmann, J. F. Studies on scaffold attachment sites and their relation to genome function. Int Rev. Cytol. 119, 57–96 (1989).
pubmed: 2695485
doi: 10.1016/S0074-7696(08)60649-X
Bode, J. et al. Scaffold/matrix-attached regions: structural properties creating transcriptionally active loci. Int Rev. Cytol. 162A, 389–454 (1995).
pubmed: 8575884
Heng, H. H. et al. Chromatin loops are selectively anchored using scaffold/matrix-attachment regions. J. Cell Sci. 117, 999–1008 (2004).
pubmed: 14996931
doi: 10.1242/jcs.00976
Girod, P. A. et al. Genome-wide prediction of matrix attachment regions that increase gene expression in mammalian cells. Nat. Methods 4, 747–753 (2007).
pubmed: 17676049
doi: 10.1038/nmeth1076
Chavali, P. L., Funa, K. & Chavali, S. Cis-regulation of microRNA expression by scaffold/matrix-attachment regions. Nucleic Acids Res 39, 6908–6918 (2011).
pubmed: 21586588
pmcid: 3167628
doi: 10.1093/nar/gkr303
Pascuzzi, P. E. et al. In vivo mapping of arabidopsis scaffold/matrix attachment regions reveals link to nucleosome-disfavoring poly(dA:dT) tracts. Plant Cell 26, 102–120 (2014).
pubmed: 24488963
pmcid: 3963562
doi: 10.1105/tpc.113.121194
Tetko, I. V. et al. Spatiotemporal expression control correlates with intragenic scaffold matrix attachment regions (S/MARs) in Arabidopsis thaliana. PLoS Comput Biol. 2, e21 (2006).
pubmed: 16604187
pmcid: 1420657
doi: 10.1371/journal.pcbi.0020021
Aravind, L. & Landsman, D. AT-hook motifs identified in a wide variety of DNA-binding proteins. Nucleic Acids Res 26, 4413–4421 (1998).
pubmed: 9742243
pmcid: 147871
doi: 10.1093/nar/26.19.4413
Razin, S. V., Borunova, V. V., Iarovaia, O. V. & Vassetzky, Y. S. Nuclear matrix and structural and functional compartmentalization of the eucaryotic cell nucleus. Biochemistry 79, 608–618 (2014).
Wang, T. Y., Han, Z. M., Chai, Y. R. & Zhang, J. H. A mini review of MAR-binding proteins. Mol. Biol. Rep. 37, 3553–3560 (2010).
pubmed: 20174991
doi: 10.1007/s11033-010-0003-8
Dickinson, L. A., Joh, T., Kohwi, Y. & Kohwi-Shigematsu, T. A tissue-specific MAR/SAR DNA-binding protein with unusual binding site recognition. Cell 70, 631–645 (1992).
pubmed: 1505028
doi: 10.1016/0092-8674(92)90432-C
Yasui, D., Miyano, M., Cai, S., Varga-Weisz, P. & Kohwi-Shigematsu, T. SATB1 targets chromatin remodelling to regulate genes over long distances. Nature 419, 641–645 (2002).
pubmed: 12374985
doi: 10.1038/nature01084
Cai, S., Han, H. J. & Kohwi-Shigematsu, T. Tissue-specific nuclear architecture and gene expression regulated by SATB1. Nat. Genet 34, 42–51 (2003).
pubmed: 12692553
doi: 10.1038/ng1146
Kumar, P. P. et al. Functional interaction between PML and SATB1 regulates chromatin-loop architecture and transcription of the MHC class I locus. Nat. Cell Biol. 9, 45–56 (2007).
pubmed: 17173041
doi: 10.1038/ncb1516
Han, H. J., Russo, J., Kohwi, Y. & Kohwi-Shigematsu, T. SATB1 reprogrammes gene expression to promote breast tumour growth and metastasis. Nature 452, 187–193 (2008).
pubmed: 18337816
doi: 10.1038/nature06781
Kohwi-Shigematsu, T. et al. SATB1-mediated functional packaging of chromatin into loops. Methods 58, 243–254 (2012).
pubmed: 22782115
pmcid: 4029128
doi: 10.1016/j.ymeth.2012.06.019
Fujimoto, S. et al. Identification of a novel plant MAR DNA binding protein localized on chromosomal surfaces. Plant Mol. Biol. 56, 225–239 (2004).
pubmed: 15604740
doi: 10.1007/s11103-004-3249-5
Lim, P. O. et al. Overexpression of a chromatin architecture-controlling AT-hook protein extends leaf longevity and increases the post-harvest storage life of plants. Plant J. 52, 1140–1153 (2007).
pubmed: 17971039
doi: 10.1111/j.1365-313X.2007.03317.x
Xu, Y. et al. A matrix protein silences transposons and repeats through interaction with retinoblastoma-associated proteins. Curr. Biol. 23, 345–350 (2013).
pubmed: 23394836
doi: 10.1016/j.cub.2013.01.030
Zhao, J., Favero, D. S., Peng, H. & Neff, M. M. Arabidopsis thaliana AHL family modulates hypocotyl growth redundantly by interacting with each other via the PPC/DUF296 domain. Proc. Natl Acad. Sci. USA 110, E4688–E4697 (2013).
pubmed: 24218605
pmcid: 3845178
doi: 10.1073/pnas.1219277110
Street, I. H., Shah, P. K., Smith, A. M., Avery, N. & Neff, M. M. The AT-hook-containing proteins SOB3/AHL29 and ESC/AHL27 are negative modulators of hypocotyl growth in Arabidopsis. Plant J. 54, 1–14 (2008).
pubmed: 18088311
doi: 10.1111/j.1365-313X.2007.03393.x
Favero, D. S. et al. Suppressor of phytochrome B4-#3 represses genes associated with auxin signaling to modulate hypocotyl growth. Plant Physiol. 171, 2701–2716 (2016).
pubmed: 27342309
pmcid: 4972272
doi: 10.1104/pp.16.00405
Favero, D. S., Le, K. N. & Neff, M. M. Brassinosteroid signaling converges with SUPPRESSOR OF PHYTOCHROME B4-#3 to influence the expression of SMALL AUXIN UP RNA genes and hypocotyl growth. Plant J. 89, 1133–1145 (2017).
pubmed: 27984677
pmcid: 5665367
doi: 10.1111/tpj.13451
Xiao, C., Chen, F., Yu, X., Lin, C. & Fu, Y. F. Over-expression of an AT-hook gene, AHL22, delays flowering and inhibits the elongation of the hypocotyl in Arabidopsis thaliana. Plant Mol. Biol. 71, 39–50 (2009).
pubmed: 19517252
doi: 10.1007/s11103-009-9507-9
Van Leene, J. et al. An improved toolbox to unravel the plant cellular machinery by tandem affinity purification of Arabidopsis protein complexes. Nat. Protoc. 10, 169–187 (2015).
pubmed: 25521792
doi: 10.1038/nprot.2014.199
Ritter, A. et al. The transcriptional repressor complex FRS7-FRS12 regulates flowering time and growth in Arabidopsis. Nat. Commun. 8, 15235 (2017).
pubmed: 28492275
pmcid: 5437275
doi: 10.1038/ncomms15235
Yun, J., Kim, Y. S., Jung, J. H., Seo, P. J. & Park, C. M. The AT-hook motif-containing protein AHL22 regulates flowering initiation by modifying FLOWERING LOCUS T chromatin in Arabidopsis. J. Biol. Chem. 287, 15307–15316 (2012).
pubmed: 22442143
pmcid: 3346147
doi: 10.1074/jbc.M111.318477
Wilson, R. H., Hesketh, E. L. & Coverley, D. Preparation of the nuclear matrix for parallel microscopy and biochemical analyses. Cold Spring Harb. Protoc. 2016, pdb prot083758 (2016).
pubmed: 26729903
doi: 10.1101/pdb.prot083758
Zhou, X., Groves, N. R. & Meier, I. Plant nuclear shape is independently determined by the SUN-WIP-WIT2-myosin XI-i complex and CRWN1. Nucleus 6, 144–153 (2015).
pubmed: 25759303
pmcid: 4615252
doi: 10.1080/19491034.2014.1003512
Van Damme, D., Bouget, F. Y., Van Poucke, K., Inze, D. & Geelen, D. Molecular dissection of plant cytokinesis and phragmoplast structure: a survey of GFP-tagged proteins. Plant J. 40, 386–398 (2004).
pubmed: 15469496
doi: 10.1111/j.1365-313X.2004.02222.x
Lee, K. & Seo, P. J. Coordination of matrix attachment and ATP-dependent chromatin remodeling regulate auxin biosynthesis and Arabidopsis hypocotyl elongation. PLoS One 12, e0181804 (2017).
pubmed: 28746399
pmcid: 5529009
doi: 10.1371/journal.pone.0181804
Favero, D. S. et al. AT-Hook Transcription Factors Restrict Petiole Growth by Antagonizing PIFs. Curr. Biol. 30, 1454–1466 e1456 (2020).
pubmed: 32197081
doi: 10.1016/j.cub.2020.02.017
Pathak, R. U., Srinivasan, A. & Mishra, R. K. Genome-wide mapping of matrix attachment regions in Drosophila melanogaster. BMC Genom. 15, 1022 (2014).
doi: 10.1186/1471-2164-15-1022
Dobson, J. R. et al. Identifying nuclear matrix-attached DNA across the genome. J. Cell Physiol. 232, 1295–1305 (2017).
pubmed: 27627025
pmcid: 5325791
doi: 10.1002/jcp.25596
Liu, C. et al. Genome-wide analysis of chromatin packing in Arabidopsis thaliana at single-gene resolution. Genome Res 26, 1057–1068 (2016).
pubmed: 27225844
pmcid: 4971768
doi: 10.1101/gr.204032.116
Zhao, L. et al. HY5 interacts with the histone deacetylase HDA15 to repress hypocotyl cell elongation in photomorphogenesis. Plant Physiol. 180, 1450–1466 (2019).
pubmed: 31061103
pmcid: 6752902
doi: 10.1104/pp.19.00055
Jiang, H. et al. Ectopic application of the repressive histone modification H3K9me2 establishes post-zygotic reproductive isolation in Arabidopsis thaliana. Genes Dev. 31, 1272–1287 (2017).
pubmed: 28743695
pmcid: 5558928
doi: 10.1101/gad.299347.117
Coelho, M. B. et al. Nuclear matrix protein Matrin3 regulates alternative splicing and forms overlapping regulatory networks with PTB. EMBO J. 34, 653–668 (2015).
pubmed: 25599992
pmcid: 4365034
doi: 10.15252/embj.201489852
Filarsky, M. et al. The extended AT-hook is a novel RNA binding motif. RNA Biol. 12, 864–876 (2015).
pubmed: 26156556
pmcid: 4615771
doi: 10.1080/15476286.2015.1060394
Honda, S. et al. Dual chromatin recognition by the histone deacetylase complex HCHC is required for proper DNA methylation in Neurospora crassa. Proc. Natl Acad. Sci. USA 113, E6135–E6144 (2016).
pubmed: 27681634
pmcid: 5068333
doi: 10.1073/pnas.1614279113
Croft, J. A. et al. Differences in the localization and morphology of chromosomes in the human nucleus. J. Cell Biol. 145, 1119–1131 (1999).
pubmed: 10366586
pmcid: 2133153
doi: 10.1083/jcb.145.6.1119
Linnemann, A. K., Platts, A. E. & Krawetz, S. A. Differential nuclear scaffold/matrix attachment marks expressed genes. Hum. Mol. Genet 18, 645–654 (2009).
pubmed: 19017725
doi: 10.1093/hmg/ddn394
Keaton, M. A., Taylor, C. M., Layer, R. M. & Dutta, A. Nuclear scaffold attachment sites within ENCODE regions associate with actively transcribed genes. PLoS One 6, e17912 (2011).
pubmed: 21423757
pmcid: 3056778
doi: 10.1371/journal.pone.0017912
Narwade, N. et al. Mapping of scaffold/matrix attachment regions in human genome: a data mining exercise. Nucleic Acids Res 47, 7247–7261 (2019).
pubmed: 31265077
pmcid: 6698742
doi: 10.1093/nar/gkz562
Ley, D. et al. MAR elements and transposons for improved transgene integration and expression. PLoS One 8, e62784 (2013).
pubmed: 23646143
pmcid: 3640020
doi: 10.1371/journal.pone.0062784
Kostyrko, K. et al. MAR-Mediated transgene integration into permissive chromatin and increased expression by recombination pathway engineering. Biotechnol. Bioeng. 114, 384–396 (2017).
pubmed: 27575535
doi: 10.1002/bit.26086
Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998).
pubmed: 10069079
doi: 10.1046/j.1365-313x.1998.00343.x
Van Leene, J. et al. Isolation of transcription factor complexes from Arabidopsis cell suspension cultures by tandem affinity purification. Methods Mol. Biol. 754, 195–218 (2011).
pubmed: 21720954
doi: 10.1007/978-1-61779-154-3_11
Nelissen, H. et al. Dynamic changes in ANGUSTIFOLIA3 complex composition reveal a growth regulatory mechanism in the maize leaf. Plant Cell 27, 1605–1619 (2015).
pubmed: 26036253
pmcid: 4498210
doi: 10.1105/tpc.15.00269
Kerppola, T. K. Design and implementation of bimolecular fluorescence complementation (BiFC) assays for the visualization of protein interactions in living cells. Nat. Protoc. 1, 1278–1286 (2006).
pubmed: 17406412
pmcid: 2518326
doi: 10.1038/nprot.2006.201
Potok, M. E. et al. Arabidopsis SWR1-associated protein methyl-CpG-binding domain 9 is required for histone H2A.Z deposition. Nat. Commun. 10, 3352 (2019).
pubmed: 31350403
pmcid: 6659704
doi: 10.1038/s41467-019-11291-w
Schagger, H. Tricine-SDS-PAGE. Nat. Protoc. 1, 16–22 (2006).
pubmed: 17406207
doi: 10.1038/nprot.2006.4
Kaspar, S., Weier, D., Weschke, W., Mock, H. P. & Matros, A. Protein analysis of laser capture micro-dissected tissues revealed cell-type specific biological functions in developing barley grains. Anal. Bioanal. Chem. 398, 2883–2893 (2010).
pubmed: 20798931
doi: 10.1007/s00216-010-4120-y
Doll, S., Djalali Farahani-Kofoet, R., Zrenner, R., Henze, A. & Witzel, K. Tissue-specific signatures of metabolites and proteins in asparagus roots and exudates. Hortic. Res 8, 86 (2021).
pubmed: 33795633
pmcid: 8016990
doi: 10.1038/s41438-021-00510-5
Kim, D., Paggi, J. M., Park, C., Bennett, C. & Salzberg, S. L. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat. Biotechnol. 37, 907–915 (2019).
pubmed: 31375807
pmcid: 7605509
doi: 10.1038/s41587-019-0201-4
Liao, Y., Smyth, G. K. & Shi, W. The R package Rsubread is easier, faster, cheaper and better for alignment and quantification of RNA sequencing reads. Nucleic Acids Res 47, e47 (2019).
pubmed: 30783653
pmcid: 6486549
doi: 10.1093/nar/gkz114
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
pubmed: 25516281
pmcid: 4302049
doi: 10.1186/s13059-014-0550-8
Chen, C. et al. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Mol. Plant 13, 1194–1202 (2020).
pubmed: 32585190
doi: 10.1016/j.molp.2020.06.009
Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890 (2018).
pubmed: 30423086
pmcid: 6129281
doi: 10.1093/bioinformatics/bty560
Zang, C. et al. A clustering approach for identification of enriched domains from histone modification ChIP-Seq data. Bioinformatics 25, 1952–1958 (2009).
pubmed: 19505939
pmcid: 2732366
doi: 10.1093/bioinformatics/btp340
Moreno-Romero, J., Jiang, H., Santos-Gonzalez, J. & Kohler, C. Parental epigenetic asymmetry of PRC2-mediated histone modifications in the Arabidopsis endosperm. EMBO J. 35, 1298–1311 (2016).
pubmed: 27113256
pmcid: 4910532
doi: 10.15252/embj.201593534