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Ectopic targeting of CG DNA methylation in Arabidopsis with the bacterial SssI methyltransferase

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Ectopic targeting of CG DNA methylation in Arabidopsis with the bacterial SssI methyltransferase

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dc.contributor.author Liu, Wanlu es_ES
dc.contributor.author Gallego Bartolomé, Javier es_ES
dc.contributor.author Zhou, Yuxing es_ES
dc.contributor.author Zhong, Zhenhui es_ES
dc.contributor.author Wang, Ming es_ES
dc.contributor.author Wongpalee, Somsakul Pop es_ES
dc.contributor.author Gardiner, Jason es_ES
dc.contributor.author Feng, Suhua es_ES
dc.contributor.author Kuo, Peggy Hsuanyu es_ES
dc.contributor.author Jacobsen, Steven E. es_ES
dc.date.accessioned 2023-12-21T19:02:36Z
dc.date.available 2023-12-21T19:02:36Z
dc.date.issued 2021-05-25 es_ES
dc.identifier.issn 2041-1723 es_ES
dc.identifier.uri http://hdl.handle.net/10251/201056
dc.description.abstract [EN] The ability to target epigenetic marks like DNA methylation to specific loci is important in both basic research and in crop plant engineering. However, heritability of targeted DNA methylation, how it impacts gene expression, and which epigenetic features are required for proper establishment are mostly unknown. Here, we show that targeting the CG-specific methyltransferase M.SssI with an artificial zinc finger protein can establish heritable CG methylation and silencing of a targeted locus in Arabidopsis. In addition, we observe highly heritable widespread ectopic CG methylation mainly over euchromatic regions. This hypermethylation shows little effect on transcription while it triggers a mild but significant reduction in the accumulation of H2A.Z and H3K27me3. Moreover, ectopic methylation occurs preferentially at less open chromatin that lacks positive histone marks. These results outline general principles of the heritability and interaction of CG methylation with other epigenomic features that should help guide future efforts to engineer epigenomes. The ability to target DNA methylation to specific loci is important for both basic and applied research. Here, the authors fuse CG-specific methyltransferase SssI with an artificial zinc finger protein for DNA methylation targeting and show the chromatin features favorable for efficient gain of methylation. es_ES
dc.description.sponsorship We thank Mahnaz Akhavan for support with high-throughput sequencing at the University of California at Los Angeles (UCLA) Broad Stem Cell Research Center BioSequencing Core Facility. We also thank Life Science Editors (https://www.lifescienceeditors.com/) for editing assistance. J.G.B. was partially funded by the European Horizon 2020 Framework Programme (H2020-MSCA-IF-2018-835599) and the Spanish Ministry of Science, Innovation, and Universities (RYC2018-024108-I). W.L. was partially supported by the Fundamental Research Funds for the Central Universities (2021QN81016). This work was supported by NIH grant R35 GM130272, and by a Bill & Melinda Gates Foundation grant (OPP1210659) to S.E.J. S.E.J. is an Investigator of the Howard Hughes Medical Institute. es_ES
dc.language Inglés es_ES
dc.publisher Nature Publishing Group es_ES
dc.relation.ispartof Nature Communications es_ES
dc.rights Reconocimiento (by) es_ES
dc.title Ectopic targeting of CG DNA methylation in Arabidopsis with the bacterial SssI methyltransferase es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1038/s41467-021-23346-y es_ES
dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/835599/EU es_ES
dc.relation.projectID info:eu-repo/grantAgreement/NIH//R35 GM130272/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/Fundamental Research Funds for the Central Universities//2021QN81016/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MICINN//RYC2018-024108-I/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/BMGF//OPP1210659/ es_ES
dc.rights.accessRights Abierto es_ES
dc.contributor.affiliation Universitat Politècnica de València. Instituto Universitario Mixto de Biología Molecular y Celular de Plantas - Institut Universitari Mixt de Biologia Molecular i Cel·lular de Plantes es_ES
dc.description.bibliographicCitation Liu, W.; Gallego Bartolomé, J.; Zhou, Y.; Zhong, Z.; Wang, M.; Wongpalee, SP.; Gardiner, J.... (2021). Ectopic targeting of CG DNA methylation in Arabidopsis with the bacterial SssI methyltransferase. Nature Communications. 12(1):1-14. https://doi.org/10.1038/s41467-021-23346-y es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion https://doi.org/10.1038/s41467-021-23346-y es_ES
dc.description.upvformatpinicio 1 es_ES
dc.description.upvformatpfin 14 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 12 es_ES
dc.description.issue 1 es_ES
dc.identifier.pmid 34035251 es_ES
dc.identifier.pmcid PMC8149686 es_ES
dc.relation.pasarela S\505585 es_ES
dc.contributor.funder European Commission es_ES
dc.contributor.funder Bill and Melinda Gates Foundation es_ES
dc.contributor.funder Ministerio de Ciencia e Innovación es_ES
dc.contributor.funder National Institutes of Health, EEUU es_ES
dc.contributor.funder Fundamental Research Funds for the Central Universities es_ES
dc.description.references Du, J., Johnson, L. M., Jacobsen, S. E. & Patel, D. J. DNA methylation pathways and their crosstalk with histone methylation. Nat. Rev. Mol. Cell Biol. 16, 519–532 (2015). es_ES
dc.description.references Feng, S. et al. Conservation and divergence of methylation patterning in plants and animals. Proc. Natl Acad. Sci. USA 107, 8689–8694 (2010). es_ES
dc.description.references Zilberman, D., Gehring, M., Tran, R. K., Ballinger, T. & Henikoff, S. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat. Genet. 39, 61–69 (2007). es_ES
dc.description.references Law, J. A. & Jacobsen, S. E. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11, 204–220 (2010). es_ES
dc.description.references Blevins, T. et al. Identification of Pol IV and RDR2-dependent precursors of 24 nt siRNAs guiding de novo DNA methylation in Arabidopsis. elife 4, e09591 (2015). es_ES
dc.description.references Zhai, J. et al. A one precursor one siRNA Model for Pol IV-Dependent siRNA Biogenesis. Cell 163, 445–455 (2015). es_ES
dc.description.references Li, S. et al. Detection of Pol IV/RDR2-dependent transcripts at the genomic scale in Arabidopsis reveals features and regulation of siRNA biogenesis. Genome Res. 25, 235–245 (2015). es_ES
dc.description.references Xie, Z. et al. Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2, E104 (2004). es_ES
dc.description.references Haag, J. R. et al. In vitro transcription activities of Pol IV, Pol V, and RDR2 reveal coupling of Pol IV and RDR2 for dsRNA synthesis in plant RNA silencing. Mol. Cell 48, 811–818 (2012). es_ES
dc.description.references Qi, Y., Denli, A. M. & Hannon, G. J. Biochemical specialization within Arabidopsis RNA silencing pathways. Mol. Cell 19, 421–428 (2005). es_ES
dc.description.references Zilberman, D., Cao, X. & Jacobsen, S. E. ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299, 716–719 (2003). es_ES
dc.description.references Li, C. F. et al. An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell 126, 93–106 (2006). es_ES
dc.description.references Qi, Y. et al. Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation. Nature 443, 1008–1012 (2006). es_ES
dc.description.references Wierzbicki, A. T., Haag, J. R. & Pikaard, C. S. Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135, 635–648 (2008). es_ES
dc.description.references Zhong, X. et al. Molecular mechanism of action of plant DRM de novo DNA methyltransferases. Cell 157, 1050–1060 (2014). es_ES
dc.description.references Liu, W. et al. RNA-directed DNA methylation involves co-transcriptional small-RNA-guided slicing of polymerase V transcripts in Arabidopsis. Nat. Plants 4, 181–188 (2018). es_ES
dc.description.references Stroud, H. et al. Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat. Struct. Mol. Biol. 21, 64–72 (2014). es_ES
dc.description.references Zemach, A. et al. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153, 193–205 (2013). es_ES
dc.description.references Niederhuth, C. E. et al. Widespread natural variation of DNA methylation within angiosperms. Genome Biol. 17, 194 (2016). es_ES
dc.description.references Zhang, X. et al. Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126, 1189–1201 (2006). es_ES
dc.description.references Zilberman, D. An evolutionary case for functional gene body methylation in plants and animals. Genome Biol. 18, 87 (2017). es_ES
dc.description.references Horvath, R., Laenen, B., Takuno, S. & Slotte, T. Single-cell expression noise and gene-body methylation in Arabidopsis thaliana. Heredity (Edinb.) 123, 81–91 (2019). es_ES
dc.description.references Bewick, A. J. & Schmitz, R. J. Gene body DNA methylation in plants. Curr. Opin. Plant Biol. 36, 103–110 (2017). es_ES
dc.description.references Regulski, M. et al. The maize methylome influences mRNA splice sites and reveals widespread paramutation-like switches guided by small RNA. Genome Res. 23, 1651–1662 (2013). es_ES
dc.description.references Lorincz, M. C., Dickerson, D. R., Schmitt, M. & Groudine, M. Intragenic DNA methylation alters chromatin structure and elongation efficiency in mammalian cells. Nat. Struct. Mol. Biol. 11, 1068–1075 (2004). es_ES
dc.description.references Maunakea, A. K. et al. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 466, 253–257 (2010). es_ES
dc.description.references Neri, F. et al. Intragenic DNA methylation prevents spurious transcription initiation. Nature 543, 72–77 (2017). es_ES
dc.description.references Kawakatsu, T. et al. Epigenomic diversity in a global collection of Arabidopsis thaliana accessions. Cell 166, 492–505 (2016). es_ES
dc.description.references Bewick, A. J. et al. On the origin and evolutionary consequences of gene body DNA methylation. Proc. Natl Acad. Sci. USA 113, 9111–9116 (2016). es_ES
dc.description.references Bewick, A. J., Zhang, Y., Wendte, J. M., Zhang, X. & Schmitz, R. J. Evolutionary and experimental loss of gene body methylation and its consequence to gene expression. G3 (Bethesda) 9, 2441–2445 (2019). es_ES
dc.description.references Zilberman, D., Coleman-Derr, D., Ballinger, T. & Henikoff, S. Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature 456, 125–129 (2008). es_ES
dc.description.references Zhang, X. et al. Whole-genome analysis of histone H3 lysine 27 trimethylation in Arabidopsis. PLoS Biol. 5, e129 (2007). es_ES
dc.description.references Johnson, L. M. et al. SRA- and SET-domain-containing proteins link RNA polymerase V occupancy to DNA methylation. Nature 507, 124–128 (2014). es_ES
dc.description.references Gallego-Bartolome, J. et al. Co-targeting RNA polymerases IV and V promotes efficient de novo DNA methylation in Arabidopsis. Cell 176, 1068–1082.e19 (2019). es_ES
dc.description.references Papikian, A., Liu, W., Gallego-Bartolome, J. & Jacobsen, S. E. Site-specific manipulation of Arabidopsis loci using CRISPR-Cas9 SunTag systems. Nat. Commun. 10, 729 (2019). es_ES
dc.description.references Liu, X. S. et al. Editing DNA methylation in the mammalian genome. Cell 167, 233–247.e17 (2016). es_ES
dc.description.references Gallego-Bartolome, J. DNA methylation in plants: mechanisms and tools for targeted manipulation. N. Phytol. 227, 38–44 (2020). es_ES
dc.description.references Gallego-Bartolome, J. et al. Targeted DNA demethylation of the Arabidopsis genome using the human TET1 catalytic domain. Proc. Natl Acad. Sci. USA 115, E2125–E2134 (2018). es_ES
dc.description.references Lei, Y. et al. Targeted DNA methylation in vivo using an engineered dCas9-MQ1 fusion protein. Nat. Commun. 8, 16026 (2017). es_ES
dc.description.references Carvin, C. D., Parr, R. D. & Kladde, M. P. Site-selective in vivo targeting of cytosine-5 DNA methylation by zinc-finger proteins. Nucleic Acids Res. 31, 6493–6501 (2003). es_ES
dc.description.references Soppe, W. J. J. et al. The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain Gene. Mol. Cell 6, 791–802 (2000). es_ES
dc.description.references Liu, Z.-W. et al. The SET domain proteins SUVH2 and SUVH9 are required for Pol V occupancy at RNA-directed DNA methylation loci. PLoS Genet. 10, e1003948 (2014). es_ES
dc.description.references Cao, X. et al. Conserved plant genes with similarity to mammalian de novo DNA methyltransferases. Proc. Natl Acad. Sci. USA 97, 4979–4984 (2000). es_ES
dc.description.references Guo, Y. et al. RAD: a web application to identify region associated differentially expressed genes. Bioinformatics 10.1093/bioinformatics/btab075 (2021). es_ES
dc.description.references Shen, S. et al. rMATS: robust and flexible detection of differential alternative splicing from replicate RNA-seq data. Proc. Natl Acad. Sci. USA 111, E5593–E5601 (2014). es_ES
dc.description.references Raisner, R. M. et al. Histone variant H2A.Z marks the 5′ ends of both active and inactive genes in euchromatin. Cell 123, 233–248 (2005). es_ES
dc.description.references Barski, A. et al. High-resolution profiling of histone methylations in the human genome. Cell 129, 823–837 (2007). es_ES
dc.description.references Law, J. A. et al. Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature 498, 385–389 (2014). es_ES
dc.description.references Cokus, S. J. et al. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452, 215–219 (2008). es_ES
dc.description.references Boivin, A. & Dura, J. M. In vivo chromatin accessibility correlates with gene silencing in Drosophila. Genetics 150, 1539–1549 (1998). es_ES
dc.description.references Fatemi, M. et al. Footprinting of mammalian promoters: use of a CpG DNA methyltransferase revealing nucleosome positions at a single molecule level. Nucleic Acids Res. 33, e176–e176 (2005). es_ES
dc.description.references Gottschling, D. E. Telomere-proximal DNA in Saccharomyces cerevisiae is refractory to methyltransferase activity in vivo. Proc. Natl Acad. Sci. USA 89, 4062–4065 (1992). es_ES
dc.description.references Singh, J. & Klar, A. J. Active genes in budding yeast display enhanced in vivo accessibility to foreign DNA methylases: a novel in vivo probe for chromatin structure of yeast. Genes Dev. 6, 186–196 (1992). es_ES
dc.description.references Soppe, W. J. J. et al. DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis. EMBO J. 21, 6549–6559 (2002). es_ES
dc.description.references Gong, Z. et al. ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell 111, 803–814 (2002). es_ES
dc.description.references Wendte, J. M. et al. Epimutations are associated with CHROMOMETHYLASE 3-induced de novo DNA methylation. elife 8, 86 (2019). es_ES
dc.description.references Conerly, M. L. et al. Changes in H2A.Z occupancy and DNA methylation during B-cell lymphomagenesis. Genome Res. 20, 1383–1390 (2010). es_ES
dc.description.references Zemach, A., McDaniel, I. E., Silva, P. & Zilberman, D. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328, 916–919 (2010). es_ES
dc.description.references Yang, X. et al. Gene reactivation by 5-aza-2′-deoxycytidine-induced demethylation requires SRCAP-mediated H2A.Z insertion to establish nucleosome depleted regions. PLoS Genet. 8, e1002604 (2012). es_ES
dc.description.references Saze, H., Mittelsten Scheid, O. & Paszkowski, J. Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat. Genet. 34, 65–69 (2003). es_ES
dc.description.references Mathieu, O., Reinders, J., Caikovski, M., Smathajitt, C. & Paszkowski, J. Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation. Cell 130, 851–862 (2007). es_ES
dc.description.references Hofmeister, B. T., Lee, K., Rohr, N. A., Hall, D. W. & Schmitz, R. J. Stable inheritance of DNA methylation allows creation of epigenotype maps and the study of epiallele inheritance patterns in the absence of genetic variation. Genome Biol. 18, 155 (2017). es_ES
dc.description.references Curtis, M. D. & Grossniklaus, U. A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462–469 (2003). es_ES
dc.description.references Potok, M. E. et al. Arabidopsis SWR1-associated protein methyl-CpG-binding domain 9 is required for histone H2A.Z deposition. Nat. Commun. 10, 3352–14 (2019). es_ES
dc.description.references Deal, R. B., Topp, C. N., McKinney, E. C. & Meagher, R. B. Repression of flowering in Arabidopsis requires activation of FLOWERING LOCUS C expression by the histone variant H2A.Z. Plant Cell 19, 74–83 (2007). es_ES
dc.description.references Zhong, Z. et al. DNA methylation-linked chromatin accessibility affects genomic architecture in Arabidopsis. Proc. Natl Acad. Sci. USA 118, e2023347118 (2021). es_ES
dc.description.references Hetzel, J., Duttke, S. H., Benner, C. & Chory, J. Nascent RNA sequencing reveals distinct features in plant transcription. Proc. Natl Acad. Sci. USA 113, 12316–12321 (2016). es_ES
dc.description.references Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y. & Greenleaf, W. J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10, 1213–1218 (2013). es_ES
dc.description.references Xi, Y. & Li, W. BSMAP: whole genome bisulfite sequence MAPping program. BMC Bioinformatics 10, 232 (2009). es_ES
dc.description.references Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576–589 (2010). es_ES
dc.description.references Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009). es_ES
dc.description.references Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009). es_ES
dc.description.references Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008). es_ES
dc.description.references Shen, L., Shao, N., Liu, X. & Nestler, E. ngs.plot: Quick mining and visualization of next-generation sequencing data by integrating genomic databases. BMC Genomics 15, 284 (2014). es_ES
dc.description.references Ramírez, F., Dündar, F., Diehl, S., Grüning, B. A. & Manke, T. deepTools: a flexible platform for exploring deep-sequencing data. Nucleic Acids Res. 42, W187–W191 (2014). es_ES
dc.description.references Gu, Z., Eils, R., Schlesner, M. & Ishaque, N. EnrichedHeatmap: an R/Bioconductor package for comprehensive visualization of genomic signal associations. BMC Genomics 19, 234–237 (2018). es_ES
dc.description.references Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013). es_ES
dc.description.references Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014). es_ES
dc.description.references 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). es_ES


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