{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,2]],"date-time":"2026-10-02T02:50:45Z","timestamp":1790909445476,"version":"4.1.0"},"reference-count":146,"publisher":"eLife Sciences Publications, Ltd","license":[{"start":{"date-parts":[[2023,9,28]],"date-time":"2023-09-28T00:00:00Z","timestamp":1695859200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2023,9,28]],"date-time":"2023-09-28T00:00:00Z","timestamp":1695859200000},"content-version":"am","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2023,9,28]],"date-time":"2023-09-28T00:00:00Z","timestamp":1695859200000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"crossref","award":["R35GM132111"],"award-info":[{"award-number":["R35GM132111"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100012007","name":"The Rockefeller University","doi-asserted-by":"crossref","award":["Women & Science Postdoctoral Fellowship"],"award-info":[{"award-number":["Women & Science Postdoctoral Fellowship"]}],"id":[{"id":"10.13039\/100012007","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["elifesciences.org"],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:p>5-Methylcytosine (5mC) and DNA methyltransferases (DNMTs) are broadly conserved in eukaryotes but are also frequently lost during evolution. The mammalian SNF2 family ATPase HELLS and its plant ortholog DDM1 are critical for maintaining 5mC. Mutations in HELLS, its activator CDCA7, and the de novo DNA methyltransferase DNMT3B, cause immunodeficiency-centromeric instability-facial anomalies (ICF) syndrome, a genetic disorder associated with the loss of DNA methylation. We here examine the coevolution of CDCA7, HELLS and DNMTs. While DNMT3, the maintenance DNA methyltransferase DNMT1, HELLS, and CDCA7 are all highly conserved in vertebrates and green plants, they are frequently co-lost in other evolutionary clades. The presence-absence patterns of these genes are not random; almost all CDCA7 harboring eukaryote species also have HELLS and DNMT1 (or another maintenance methyltransferase, DNMT5). Coevolution of presence-absence patterns (CoPAP) analysis in Ecdysozoa further indicates coevolutionary linkages among CDCA7, HELLS, DNMT1 and its activator UHRF1. We hypothesize that CDCA7 becomes dispensable in species that lost HELLS or DNA methylation, and\/or the loss of CDCA7 triggers the replacement of DNA methylation by other chromatin regulation mechanisms. Our study suggests that a unique specialized role of CDCA7 in HELLS-dependent DNA methylation maintenance is broadly inherited from the last eukaryotic common ancestor.<\/jats:p>","DOI":"10.7554\/elife.86721","type":"journal-article","created":{"date-parts":[[2023,6,5]],"date-time":"2023-06-05T11:50:23Z","timestamp":1685965823000},"update-policy":"https:\/\/doi.org\/10.7554\/elife.86721","source":"Crossref","is-referenced-by-count":17,"title":["Coevolution of the CDCA7-HELLS ICF-related nucleosome remodeling complex and DNA methyltransferases"],"prefix":"10.7554","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4831-4087","authenticated-orcid":true,"given":"Hironori","family":"Funabiki","sequence":"first","affiliation":[{"id":[{"id":"https:\/\/ror.org\/0420db125","id-type":"ROR","asserted-by":"publisher"}],"name":"Laboratory of Chromosome and Cell Biology, The Rockefeller University","place":["New York, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Isabel E","family":"Wassing","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/0420db125","id-type":"ROR","asserted-by":"publisher"}],"name":"Laboratory of Chromosome and Cell Biology, The Rockefeller University","place":["New York, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qingyuan","family":"Jia","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/0420db125","id-type":"ROR","asserted-by":"publisher"}],"name":"Laboratory of Chromosome and Cell Biology, The Rockefeller University","place":["New York, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0150-1440","authenticated-orcid":true,"given":"Ji-Dung","family":"Luo","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/0420db125","id-type":"ROR","asserted-by":"publisher"}],"name":"Bioinformatics Resource Center, The Rockefeller University","place":["New York, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thomas","family":"Carroll","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/0420db125","id-type":"ROR","asserted-by":"publisher"}],"name":"Bioinformatics Resource Center, The Rockefeller University","place":["New York, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"4374","published-online":{"date-parts":[[2023,9,28]]},"reference":[{"key":"bib1","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-018-37407-8","article-title":"Universality of the DNA methylation codes in Eucaryotes","volume":"9","author":"Aliaga","year":"2019","journal-title":"Scientific Reports"},{"key":"bib2","doi-asserted-by":"crossref","first-page":"8033","DOI":"10.1016\/S0021-9258(17)39681-3","article-title":"DNA methylation in the fungi","volume":"259","author":"Antequera","year":"1984","journal-title":"The Journal of Biological Chemistry"},{"key":"bib3","doi-asserted-by":"publisher","first-page":"119","DOI":"10.4161\/cc.11.1.18475","article-title":"The HARE-HTH and associated domains: novel modules in the coordination of epigenetic DNA and protein modifications","volume":"11","author":"Aravind","year":"2012","journal-title":"Cell Cycle"},{"key":"bib4","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1005790","article-title":"The LSH\/DDM1 Homolog MUS-30 is required for Genome Stability, but Not for DNA Methylation in Neurospora crassa","volume":"12","author":"Basenko","year":"2016","journal-title":"PLOS Genetics"},{"key":"bib5","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-020-18009-3","article-title":"Helicase LSH\/Hells regulates kinetochore function, histone H3\/Thr3 phosphorylation and centromere transcription during oocyte meiosis","volume":"11","author":"Baumann","year":"2020","journal-title":"Nature Communications"},{"key":"bib6","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1038\/s41576-018-0081-3","article-title":"Deciphering bacterial epigenomes using modern sequencing technologies","volume":"20","author":"Beaulaurier","year":"2019","journal-title":"Nature Reviews. Genetics"},{"key":"bib7","doi-asserted-by":"publisher","DOI":"10.1186\/s13059-017-1195-1","article-title":"The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants","volume":"18","author":"Bewick","year":"2017","journal-title":"Genome Biology"},{"key":"bib8","doi-asserted-by":"publisher","first-page":"654","DOI":"10.1093\/molbev\/msw264","article-title":"Evolution of DNA Methylation across insects","volume":"34","author":"Bewick","year":"2017","journal-title":"Molecular Biology and Evolution"},{"key":"bib9","doi-asserted-by":"publisher","first-page":"479","DOI":"10.1038\/s41559-019-0810-9","article-title":"Diversity of cytosine methylation across the fungal tree of life","volume":"3","author":"Bewick","year":"2019","journal-title":"Nature Ecology & Evolution"},{"key":"bib10","doi-asserted-by":"publisher","DOI":"10.1186\/s13072-018-0246-5","article-title":"Dnmt1 is essential for egg production and embryo viability in the large milkweed bug, Oncopeltus fasciatus","volume":"12","author":"Bewick","year":"2019","journal-title":"Epigenetics & Chromatin"},{"key":"bib11","doi-asserted-by":"publisher","first-page":"2841","DOI":"10.1093\/bioinformatics\/btl498","article-title":"Meisetz and the birth of the KRAB motif","volume":"22","author":"Birtle","year":"2006","journal-title":"Bioinformatics"},{"key":"bib12","doi-asserted-by":"publisher","first-page":"1755","DOI":"10.1016\/j.cub.2012.07.042","article-title":"Genome-wide and caste-specific DNA methylomes of the ants Camponotus floridanus and Harpegnathos saltator","volume":"22","author":"Bonasio","year":"2012","journal-title":"Current Biology"},{"key":"bib13","doi-asserted-by":"publisher","first-page":"823","DOI":"10.1074\/jbc.M209260200","article-title":"Deficient in DNA methylation 1 (DDM1) defines a novel family of chromatin-remodeling factors","volume":"278","author":"Brzeski","year":"2003","journal-title":"The Journal of Biological Chemistry"},{"key":"bib14","doi-asserted-by":"publisher","first-page":"4979","DOI":"10.1073\/pnas.97.9.4979","article-title":"Conserved plant genes with similarity to mammalian de novo DNA methyltransferases","volume":"97","author":"Cao","year":"2000","journal-title":"PNAS"},{"key":"bib15","article-title":"Copap_Analysis","volume-title":"Software Heritage","author":"Carroll","year":"2023","unstructured":"Carroll T. 2023. Copap_Analysis. Software Heritage. swh:1:rev:6a146eb234dd517cc9744a61e8d7f5679d440164. https:\/\/archive.softwareheritage.org\/swh:1:dir:877abf7f1f55664b43e34813dded8243b67609a5;origin=https:\/\/github.com\/RockefellerUniversity\/Copap_Analysis;visit=swh:1:snp:4d7d8f1dfbcfa677a23ab4509b29e6f4af7efc57;anchor=swh:1:rev:6a146eb234dd517cc9744a61e8d7f5679d440164."},{"key":"bib16","doi-asserted-by":"publisher","first-page":"830","DOI":"10.1128\/MMBR.00016-06","article-title":"Epigenetic gene regulation in the bacterial world","volume":"70","author":"Casades\u00fas","year":"2006","journal-title":"Microbiology and Molecular Biology Reviews"},{"key":"bib17","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2020.02.006","article-title":"Evolutionary persistence of DNA methylation for millions of years after ancient loss of a de novo methyltransferase","volume":"180","author":"Catania","year":"2020","journal-title":"Cell"},{"key":"bib18","doi-asserted-by":"publisher","first-page":"351","DOI":"10.1038\/nrg1601","article-title":"Gardening the genome: DNA methylation in Arabidopsis thaliana","volume":"6","author":"Chan","year":"2005","journal-title":"Nature Reviews. Genetics"},{"key":"bib19","doi-asserted-by":"publisher","first-page":"11552","DOI":"10.1074\/jbc.M410033200","article-title":"R1, A novel repressor of the human monoamine oxidase A","volume":"280","author":"Chen","year":"2005","journal-title":"The Journal of Biological Chemistry"},{"key":"bib20","doi-asserted-by":"publisher","first-page":"310","DOI":"10.1016\/j.molcel.2019.10.011","article-title":"DNA methylation and histone H1 jointly repress transposable elements and aberrant intragenic transcripts","volume":"77","author":"Choi","year":"2020","journal-title":"Molecular Cell"},{"key":"bib21","doi-asserted-by":"publisher","first-page":"617","DOI":"10.1038\/nature09016","article-title":"The Ectocarpus genome and the independent evolution of multicellularity in brown algae","volume":"465","author":"Cock","year":"2010","journal-title":"Nature"},{"key":"bib22","doi-asserted-by":"publisher","first-page":"i389","DOI":"10.1093\/bioinformatics\/bts396","article-title":"Uncovering the co-evolutionary network among prokaryotic genes","volume":"28","author":"Cohen","year":"2012","journal-title":"Bioinformatics"},{"key":"bib23","doi-asserted-by":"publisher","first-page":"W232","DOI":"10.1093\/nar\/gkt471","article-title":"CoPAP: Coevolution of presence-absence patterns","volume":"41","author":"Cohen","year":"2013","journal-title":"Nucleic Acids Research"},{"key":"bib24","doi-asserted-by":"publisher","first-page":"402","DOI":"10.1002\/(SICI)1521-1878(199905)21:5<402::AID-BIES7>3.0.CO;2-B","article-title":"Eukaryotic DNA methylation as an evolutionary device","volume":"21","author":"Colot","year":"1999","journal-title":"BioEssays"},{"key":"bib25","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1146\/annurev-genet-120417-031441","article-title":"piRNA-guided genome defense: from biogenesis to silencing","volume":"52","author":"Czech","year":"2018","journal-title":"Annual Review of Genetics"},{"key":"bib26","doi-asserted-by":"publisher","first-page":"796","DOI":"10.1016\/j.ajhg.2011.04.018","article-title":"Mutations in ZBTB24 are associated with immunodeficiency, centromeric instability, and facial anomalies syndrome type 2","volume":"88","author":"de Greef","year":"2011","journal-title":"American Journal of Human Genetics"},{"key":"bib27","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-018-03724-9","article-title":"Recurrent acquisition of cytosine methyltransferases into eukaryotic retrotransposons","volume":"9","author":"de Mendoza","year":"2018","journal-title":"Nature Communications"},{"key":"bib28","doi-asserted-by":"publisher","first-page":"579","DOI":"10.1146\/annurev-phyto-080615-100308","article-title":"DNA methylation and demethylation in plant immunity","volume":"54","author":"Deleris","year":"2016","journal-title":"Annual Review of Phytopathology"},{"key":"bib29","doi-asserted-by":"publisher","first-page":"251","DOI":"10.1101\/gad.274647.115","article-title":"JMJ24 targets CHROMOMETHYLASE3 for proteasomal degradation in Arabidopsis","volume":"30","author":"Deng","year":"2016","journal-title":"Genes & Development"},{"key":"bib30","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1038\/s41576-019-0117-3","article-title":"Author Correction: Regulation of transposable elements by DNA modifications","volume":"20","author":"Deniz","year":"2019","journal-title":"Nature Reviews. Genetics"},{"key":"bib31","doi-asserted-by":"publisher","first-page":"2940","DOI":"10.1101\/gad.929101","article-title":"Lsh, a member of the SNF2 family, is required for genome-wide methylation","volume":"15","author":"Dennis","year":"2001","journal-title":"Genes & Development"},{"key":"bib32","doi-asserted-by":"publisher","first-page":"R1189","DOI":"10.1016\/j.cub.2020.08.028","article-title":"Evolutionary ecology and interplay of prokaryotic innate and adaptive immune systems","volume":"30","author":"Dimitriu","year":"2020","journal-title":"Current Biology"},{"key":"bib33","doi-asserted-by":"publisher","first-page":"928","DOI":"10.1111\/jipb.12069","article-title":"SLIDE, the protein interacting domain of Imitation Switch remodelers, binds DDT-domain proteins of different subfamilies in chromatin remodeling complexes","volume":"55","author":"Dong","year":"2013","journal-title":"Journal of Integrative Plant Biology"},{"key":"bib34","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1016\/j.molcel.2020.04.029","article-title":"ATP Hydrolysis by the SNF2 Domain of Dnmt5 is coupled to both specific recognition and modification of Hemimethylated DNA","volume":"79","author":"Dumesic","year":"2020","journal-title":"Molecular Cell"},{"key":"bib35","doi-asserted-by":"publisher","DOI":"10.1186\/gb-2013-14-12-r146","article-title":"Lsh regulates LTR retrotransposon repression independently of Dnmt3b function","volume":"14","author":"Dunican","year":"2013","journal-title":"Genome Biology"},{"key":"bib36","doi-asserted-by":"publisher","DOI":"10.1155\/2015\/740637","article-title":"Lsh is essential for maintaining Global DNA Methylation levels in Amphibia and Fish and interacts directly with Dnmt1","volume":"2015","author":"Dunican","year":"2015","journal-title":"BioMed Research International"},{"key":"bib37","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-022-34630-w","article-title":"Muscle5: High-accuracy alignment ensembles enable unbiased assessments of sequence homology and phylogeny","volume":"13","author":"Edgar","year":"2022","journal-title":"Nature Communications"},{"key":"bib38","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1016\/s1521-6616(03)00201-8","article-title":"The ICF syndrome, a DNA methyltransferase 3B deficiency and immunodeficiency disease","volume":"109","author":"Ehrlich","year":"2003","journal-title":"Clinical Immunology"},{"key":"bib39","doi-asserted-by":"publisher","DOI":"10.1186\/1750-1172-1-2","article-title":"Immunodeficiency, centromeric region instability, facial anomalies syndrome (ICF)","volume":"1","author":"Ehrlich","year":"2006","journal-title":"Orphanet Journal of Rare Diseases"},{"key":"bib40","doi-asserted-by":"publisher","first-page":"56","DOI":"10.1007\/s00239-021-10042-0","article-title":"Evolution of DNA methylation across ecdysozoa","volume":"90","author":"Engelhardt","year":"2022","journal-title":"Journal of Molecular Evolution"},{"key":"bib41","doi-asserted-by":"publisher","first-page":"6956","DOI":"10.1093\/nar\/gkr263","article-title":"Nucleosomes protect DNA from DNA methylation in vivo and in vitro","volume":"39","author":"Felle","year":"2011","journal-title":"Nucleic Acids Research"},{"key":"bib42","doi-asserted-by":"publisher","first-page":"8689","DOI":"10.1073\/pnas.1002720107","article-title":"Conservation and divergence of methylation patterning in plants and animals","volume":"107","author":"Feng","year":"2010","journal-title":"PNAS"},{"key":"bib43","doi-asserted-by":"publisher","first-page":"540","DOI":"10.1016\/j.ijbiomac.2020.07.149","article-title":"Evolution of tRNA gene rearrangement in the mitochondrial genome of ichneumonoid wasps (Hymenoptera: Ichneumonoidea)","volume":"164","author":"Feng","year":"2020","journal-title":"International Journal of Biological Macromolecules"},{"key":"bib44","doi-asserted-by":"publisher","first-page":"2887","DOI":"10.1093\/nar\/gkl295","article-title":"Identification of multiple distinct Snf2 subfamilies with conserved structural motifs","volume":"34","author":"Flaus","year":"2006","journal-title":"Nucleic Acids Research"},{"key":"bib45","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms1433","article-title":"Cytosine methylation regulates oviposition in the pathogenic blood fluke Schistosoma mansoni","volume":"2","author":"Geyer","year":"2011","journal-title":"Nature Communications"},{"key":"bib46","doi-asserted-by":"publisher","first-page":"498","DOI":"10.1128\/MCB.00276-12","article-title":"The MYC-associated protein CDCA7 is phosphorylated by AKT to regulate MYC-dependent apoptosis and transformation","volume":"33","author":"Gill","year":"2013","journal-title":"Molecular and Cellular Biology"},{"key":"bib47","doi-asserted-by":"publisher","first-page":"590","DOI":"10.1038\/s41580-019-0159-6","article-title":"The diverse roles of DNA methylation in mammalian development and disease","volume":"20","author":"Greenberg","year":"2019","journal-title":"Nature Reviews. Molecular Cell Biology"},{"key":"bib48","doi-asserted-by":"publisher","first-page":"4657","DOI":"10.1128\/JB.185.15.4657-4661.2003","article-title":"Cytosine Methylation by the Sua I Restriction-Modification System: implications for Genetic Fidelity in a Hyperthermophilic Archaeon","volume":"185","author":"Grogan","year":"2003","journal-title":"Journal of Bacteriology"},{"key":"bib49","doi-asserted-by":"publisher","first-page":"12116","DOI":"10.1093\/nar\/gkaa1003","article-title":"A role for LSH in facilitating DNA methylation by DNMT1 through enhancing UHRF1 chromatin association","volume":"48","author":"Han","year":"2020","journal-title":"Nucleic Acids Research"},{"key":"bib50","doi-asserted-by":"publisher","first-page":"14412","DOI":"10.1073\/pnas.96.25.14412","article-title":"The DNMT3B DNA methyltransferase gene is mutated in the ICF immunodeficiency syndrome","volume":"96","author":"Hansen","year":"1999","journal-title":"PNAS"},{"key":"bib51","doi-asserted-by":"publisher","first-page":"214","DOI":"10.1007\/s13238-019-00682-w","article-title":"The ZBTB24-CDCA7 axis regulates HELLS enrichment at centromeric satellite repeats to facilitate DNA methylation","volume":"11","author":"Hardikar","year":"2020","journal-title":"Protein & Cell"},{"key":"bib52","doi-asserted-by":"publisher","DOI":"10.1128\/Spectrum.00186-21","article-title":"Evaluation of the Properties of the DNA Methyltransferase from Aeropyrum pernix K1","volume":"9","author":"Hayashi","year":"2021","journal-title":"Microbiology Spectrum"},{"key":"bib53","doi-asserted-by":"publisher","first-page":"740","DOI":"10.1038\/35047123","article-title":"A Toll-like receptor recognizes bacterial DNA","volume":"408","author":"Hemmi","year":"2000","journal-title":"Nature"},{"key":"bib54","doi-asserted-by":"publisher","first-page":"237","DOI":"10.1016\/0378-1119(88)90330-7","article-title":"CLUSTAL: a package for performing multiple sequence alignment on a microcomputer","volume":"73","author":"Higgins","year":"1988","journal-title":"Gene"},{"key":"bib55","doi-asserted-by":"publisher","first-page":"518","DOI":"10.1093\/molbev\/msx281","article-title":"UFBoot2: improving the ultrafast bootstrap approximation","volume":"35","author":"Hoang","year":"2018","journal-title":"Molecular Biology and Evolution"},{"key":"bib56","doi-asserted-by":"publisher","first-page":"443","DOI":"10.1101\/gad.1893210","article-title":"The DMM complex prevents spreading of DNA methylation from transposons to nearby genes in Neurospora crassa","volume":"24","author":"Honda","year":"2010","journal-title":"Genes & Development"},{"key":"bib57","doi-asserted-by":"publisher","first-page":"5019","DOI":"10.1093\/nar\/gkh821","article-title":"Lsh, an epigenetic guardian of repetitive elements","volume":"32","author":"Huang","year":"2004","journal-title":"Nucleic Acids Research"},{"key":"bib58","doi-asserted-by":"publisher","first-page":"5607","DOI":"10.1158\/0008-5472.CAN-05-0500","article-title":"Identification of a novel c-Myc protein interactor, JPO2, with transforming activity in medulloblastoma cells","volume":"65","author":"Huang","year":"2005","journal-title":"Cancer Research"},{"key":"bib59","doi-asserted-by":"publisher","first-page":"1286","DOI":"10.1016\/j.cell.2014.01.029","article-title":"Dnmt1-independent CG methylation contributes to nucleosome positioning in diverse eukaryotes","volume":"156","author":"Huff","year":"2014","journal-title":"Cell"},{"key":"bib60","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.57117","article-title":"PRDM9 activity depends on HELLS and promotes local 5-hydroxymethylcytosine enrichment","volume":"9","author":"Imai","year":"2020","journal-title":"eLife"},{"key":"bib61","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gni113","article-title":"Discovery of a novel restriction endonuclease by genome comparison and application of a wheat-germ-based cell-free translation assay: PabI (5\u2019-GTA\/C) from the hyperthermophilic archaeon Pyrococcus abyssi","volume":"33","author":"Ishikawa","year":"2005","journal-title":"Nucleic Acids Research"},{"key":"bib62","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-023-37945-4","article-title":"DNMT1 mutant ants develop normally but have disrupted oogenesis","volume":"14","author":"Ivasyk","year":"2023","journal-title":"Nature Communications"},{"key":"bib63","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1016\/B978-0-12-387685-0.00002-0","article-title":"Natural history of eukaryotic DNA methylation systems","volume":"101","author":"Iyer","year":"2011","journal-title":"Progress in Molecular Biology and Translational Science"},{"key":"bib64","doi-asserted-by":"publisher","first-page":"6027","DOI":"10.1073\/pnas.1303750110","article-title":"Regional control of histone H3 lysine 27 methylation in Neurospora","volume":"110","author":"Jamieson","year":"2013","journal-title":"PNAS"},{"key":"bib65","doi-asserted-by":"publisher","first-page":"E876","DOI":"10.1073\/pnas.1717509115","article-title":"HELLS and CDCA7 comprise a bipartite nucleosome remodeling complex defective in ICF syndrome","volume":"115","author":"Jenness","year":"2018","journal-title":"PNAS"},{"key":"bib66","doi-asserted-by":"publisher","first-page":"56","DOI":"10.1002\/humu.20113","article-title":"DNMT3B mutations and DNA methylation defect define two types of ICF syndrome","volume":"25","author":"Jiang","year":"2005","journal-title":"Human Mutation"},{"key":"bib67","doi-asserted-by":"publisher","first-page":"421","DOI":"10.1016\/s0960-9822(03)00106-4","article-title":"Role of CG and non-CG methylation in immobilization of transposons in Arabidopsis","volume":"13","author":"Kato","year":"2003","journal-title":"Current Biology"},{"key":"bib68","doi-asserted-by":"publisher","first-page":"813","DOI":"10.1016\/j.mam.2012.06.008","article-title":"Epigenetics and the adaptive immune response","volume":"34","author":"Kondilis-Mangum","year":"2013","journal-title":"Molecular Aspects of Medicine"},{"key":"bib69","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msac174","article-title":"TimeTree 5: an expanded resource for species divergence times","volume":"39","author":"Kumar","year":"2022","journal-title":"Molecular Biology and Evolution"},{"key":"bib70","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1093\/molbev\/msaa214","article-title":"Myxosporea (Myxozoa, Cnidaria) lack DNA Cytosine Methylation","volume":"38","author":"Kyger","year":"2021","journal-title":"Molecular Biology and Evolution"},{"key":"bib71","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1008864","article-title":"\u00ad\u00ad\u00ad\u00ad\u00ad\u00adWidespread conservation and lineage-specific diversification of genome-wide DNA methylation patterns across arthropods","volume":"16","author":"Lewis","year":"2020","journal-title":"PLOS Genetics"},{"key":"bib72","doi-asserted-by":"publisher","first-page":"365","DOI":"10.1007\/s00412-017-0626-9","article-title":"The ISWI remodeler in plants: protein complexes, biochemical functions, and developmental roles","volume":"126","author":"Li","year":"2017","journal-title":"Chromosoma"},{"key":"bib73","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-018-20831-1","article-title":"Identification and caste-dependent expression patterns of DNA methylation associated genes in Bombus terrestris","volume":"8","author":"Li","year":"2018","journal-title":"Scientific Reports"},{"key":"bib74","doi-asserted-by":"publisher","first-page":"941","DOI":"10.1111\/1755-0998.13308","article-title":"Chromosome\u2010level genome assembly of the aphid parasitoid Aphidius gifuensis using Oxford Nanopore sequencing and Hi\u2010C technology","volume":"21","author":"Li","year":"2021","journal-title":"Molecular Ecology Resources"},{"key":"bib75","doi-asserted-by":"publisher","first-page":"391","DOI":"10.1016\/j.cub.2015.12.040","article-title":"Robust DNA methylation in the clonal raider ant brain","volume":"26","author":"Libbrecht","year":"2016","journal-title":"Current Biology"},{"key":"bib76","doi-asserted-by":"publisher","first-page":"6404","DOI":"10.1093\/nar\/gkx240","article-title":"The LSH\/HELLS homolog Irc5 contributes to cohesin association with chromatin in yeast","volume":"45","author":"Litwin","year":"2017","journal-title":"Nucleic Acids Research"},{"key":"bib77","doi-asserted-by":"publisher","first-page":"727","DOI":"10.1042\/BST20130028","article-title":"ZF-CxxC domain-containing proteins, CpG islands and the chromatin connection","volume":"41","author":"Long","year":"2013","journal-title":"Biochemical Society Transactions"},{"key":"bib78","doi-asserted-by":"publisher","DOI":"10.1186\/s13059-018-1397-1","article-title":"Ageing-associated DNA methylation dynamics are a molecular readout of lifespan variation among mammalian species","volume":"19","author":"Lowe","year":"2018","journal-title":"Genome Biology"},{"key":"bib79","doi-asserted-by":"publisher","first-page":"D265","DOI":"10.1093\/nar\/gkz991","article-title":"CDD\/SPARCLE: the conserved domain database in 2020","volume":"48","author":"Lu","year":"2020","journal-title":"Nucleic Acids Research"},{"key":"bib80","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1038\/nrg.2017.80","article-title":"The DNA methyltransferase family: a versatile toolkit for epigenetic regulation","volume":"19","author":"Lyko","year":"2018","journal-title":"Nature Reviews. Genetics"},{"key":"bib81","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.30674","article-title":"DDM1 and Lsh remodelers allow methylation of DNA wrapped in nucleosomes","volume":"6","author":"Lyons","year":"2017","journal-title":"eLife"},{"key":"bib82","doi-asserted-by":"publisher","first-page":"2563","DOI":"10.1242\/jcs.02995","article-title":"Transcriptional co-activator p75 binds and tethers the Myc-interacting protein JPO2 to chromatin","volume":"119","author":"Maertens","year":"2006","journal-title":"Journal of Cell Science"},{"key":"bib83","doi-asserted-by":"publisher","first-page":"343","DOI":"10.1038\/nature09784","article-title":"The Polycomb complex PRC2 and its mark in life","volume":"469","author":"Margueron","year":"2011","journal-title":"Nature"},{"key":"bib84","doi-asserted-by":"publisher","first-page":"2012","DOI":"10.1128\/EC.00198-08","article-title":"African trypanosomes contain 5-methylcytosine in nuclear DNA","volume":"7","author":"Militello","year":"2008","journal-title":"Eukaryotic Cell"},{"key":"bib85","doi-asserted-by":"publisher","first-page":"980","DOI":"10.1038\/s41422-020-0359-9","article-title":"Kinetics and mechanisms of mitotic inheritance of DNA methylation and their roles in aging-associated methylome deterioration","volume":"30","author":"Ming","year":"2020","journal-title":"Cell Research"},{"key":"bib86","doi-asserted-by":"publisher","first-page":"1530","DOI":"10.1093\/molbev\/msaa131","article-title":"Corrigendum to: IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era","volume":"37","author":"Minh","year":"2020","journal-title":"Molecular Biology and Evolution"},{"key":"bib87","doi-asserted-by":"publisher","first-page":"1037","DOI":"10.1016\/j.devcel.2022.03.014","article-title":"Paramecium Polycomb repressive complex 2 physically interacts with the small RNA-binding PIWI protein to repress transposable elements","volume":"57","author":"Mir\u00f3-Pina","year":"2022","journal-title":"Developmental Cell"},{"key":"bib88","doi-asserted-by":"publisher","first-page":"D412","DOI":"10.1093\/nar\/gkaa913","article-title":"Pfam: The protein families database in 2021","volume":"49","author":"Mistry","year":"2021","journal-title":"Nucleic Acids Research"},{"key":"bib89","doi-asserted-by":"publisher","first-page":"212","DOI":"10.1038\/35075612","article-title":"Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis","volume":"411","author":"Miura","year":"2001","journal-title":"Nature"},{"key":"bib90","doi-asserted-by":"publisher","first-page":"964","DOI":"10.1038\/ng.3859","article-title":"Widespread adenine N6-methylation of active genes in fungi","volume":"49","author":"Mondo","year":"2017","journal-title":"Nature Genetics"},{"key":"bib91","doi-asserted-by":"publisher","first-page":"115","DOI":"10.3347\/kjp.2017.55.2.115","article-title":"DNA Methylation of Gene expression in Acanthamoeba castellanii Encystation","volume":"55","author":"Moon","year":"2017","journal-title":"The Korean Journal of Parasitology"},{"key":"bib92","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-020-19603-1","article-title":"Recent evolution of a TET-controlled and DPPA3\/STELLA-driven pathway of passive DNA demethylation in mammals","volume":"11","author":"Mulholland","year":"2020","journal-title":"Nature Communications"},{"key":"bib93","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1101\/gr.108498.110","article-title":"LSH and G9a\/GLP complex are required for developmentally programmed DNA methylation","volume":"21","author":"Myant","year":"2011","journal-title":"Genome Research"},{"key":"bib94","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2020.616922","article-title":"Diversity of Fungal DNA Methyltransferases and their association with DNA Methylation patterns","volume":"11","author":"Nai","year":"2020","journal-title":"Frontiers in Microbiology"},{"key":"bib95","doi-asserted-by":"publisher","first-page":"72","DOI":"10.1038\/nature21373","article-title":"Intragenic DNA methylation prevents spurious transcription initiation","volume":"543","author":"Neri","year":"2017","journal-title":"Nature"},{"key":"bib96","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-020-19159-0","article-title":"LSH mediates gene repression through macroH2A deposition","volume":"11","author":"Ni","year":"2020","journal-title":"Nature Communications"},{"key":"bib97","doi-asserted-by":"publisher","first-page":"8024","DOI":"10.1093\/nar\/gkab588","article-title":"LSH catalyzes ATP-driven exchange of histone variants macroH2A1 and macroH2A2","volume":"49","author":"Ni","year":"2021","journal-title":"Nucleic Acids Research"},{"key":"bib98","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-020-15006-4","article-title":"Two distinct modes of DNMT1 recruitment ensure stable maintenance DNA methylation","volume":"11","author":"Nishiyama","year":"2020","journal-title":"Nature Communications"},{"key":"bib99","doi-asserted-by":"publisher","first-page":"1012","DOI":"10.1016\/j.tig.2021.05.002","article-title":"Navigating the DNA methylation landscape of cancer","volume":"37","author":"Nishiyama","year":"2021","journal-title":"Trends in Genetics"},{"key":"bib100","doi-asserted-by":"publisher","first-page":"52","DOI":"10.1016\/j.pedobi.2017.10.001","article-title":"Exploring DNA methylation patterns in copper exposed Folsomia candida and Enchytraeus crypticus","volume":"66","author":"Noordhoek","year":"2018","journal-title":"Pedobiologia"},{"key":"bib101","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1016\/s0092-8674(00)81656-6","article-title":"DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development","volume":"99","author":"Okano","year":"1999","journal-title":"Cell"},{"key":"bib102","doi-asserted-by":"publisher","DOI":"10.15252\/embr.202153062","article-title":"piRNA- and siRNA-mediated transcriptional repression in Drosophila, mice, and yeast: new insights and biodiversity","volume":"22","author":"Onishi","year":"2021","journal-title":"EMBO Reports"},{"key":"bib103","doi-asserted-by":"publisher","first-page":"391","DOI":"10.1038\/s41556-021-00658-1","article-title":"The chromatin remodeler DDM1 prevents transposon mobility through deposition of histone variant H2A.W","volume":"23","author":"Osakabe","year":"2021","journal-title":"Nature Cell Biology"},{"key":"bib104","doi-asserted-by":"publisher","first-page":"21512","DOI":"10.1074\/jbc.M600250200","article-title":"Glucocorticoid and androgen activation of monoamine oxidase a is regulated differently by R1 and Sp1","volume":"281","author":"Ou","year":"2006","journal-title":"Journal of Biological Chemistry"},{"key":"bib105","doi-asserted-by":"publisher","first-page":"D418","DOI":"10.1093\/nar\/gkac993","article-title":"InterPro in 2022","volume":"51","author":"Paysan-Lafosse","year":"2023","journal-title":"Nucleic Acids Research"},{"key":"bib106","doi-asserted-by":"publisher","first-page":"1013","DOI":"10.1016\/j.cub.2017.01.027","article-title":"Evolutionary history of the hymenoptera","volume":"27","author":"Peters","year":"2017","journal-title":"Current Biology"},{"key":"bib107","doi-asserted-by":"publisher","first-page":"558","DOI":"10.1093\/jhered\/esab032","article-title":"A chromosome-level genome assembly of the parasitoid wasp, cotesia glomerata (hymenoptera: braconidae)","volume":"112","author":"Pinto","year":"2021","journal-title":"The Journal of Heredity"},{"key":"bib108","doi-asserted-by":"publisher","first-page":"1119","DOI":"10.1093\/molbev\/msi098","article-title":"Evolutionary diversification of DNA methyltransferases in eukaryotic genomes","volume":"22","author":"Ponger","year":"2005","journal-title":"Molecular Biology and Evolution"},{"key":"bib109","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1016\/0014-5793(85)80042-9","article-title":"A restriction endonuclease SuaI from the thermoacidophilic archaebacterium Sulfolobus acidocaldarius","volume":"192","author":"Prangishvili","year":"1985","journal-title":"FEBS Letters"},{"key":"bib110","doi-asserted-by":"publisher","first-page":"1925","DOI":"10.1534\/genetics.104.031526","article-title":"DNA methylation affects meiotic trans-sensing, not meiotic silencing, in Neurospora","volume":"168","author":"Pratt","year":"2004","journal-title":"Genetics"},{"key":"bib111","doi-asserted-by":"publisher","first-page":"1444","DOI":"10.1093\/nar\/gku1371","article-title":"The ATP binding site of the chromatin remodeling homolog Lsh is required for nucleosome density and de novo DNA methylation at repeat sequences","volume":"43","author":"Ren","year":"2015","journal-title":"Nucleic Acids Research"},{"key":"bib112","doi-asserted-by":"publisher","first-page":"597","DOI":"10.1038\/nrg1655","article-title":"DNA methylation and human disease","volume":"6","author":"Robertson","year":"2005","journal-title":"Nature Reviews. Genetics"},{"key":"bib113","doi-asserted-by":"publisher","first-page":"462","DOI":"10.1126\/science.1150987","article-title":"Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana","volume":"319","author":"Saze","year":"2008","journal-title":"Science"},{"key":"bib114","doi-asserted-by":"publisher","first-page":"579","DOI":"10.1146\/annurev.micro.57.030502.090847","article-title":"DNA mismatch repair: molecular mechanisms and biological function","volume":"57","author":"Schofield","year":"2003","journal-title":"Annual Review of Microbiology"},{"key":"bib115","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-018-34701-3","article-title":"Dnmt1 has an essential function despite the absence of CpG DNA methylation in the red flour beetle Tribolium castaneum","volume":"8","author":"Schulz","year":"2018","journal-title":"Scientific Reports"},{"key":"bib116","doi-asserted-by":"publisher","DOI":"10.26508\/lsa.202101271","article-title":"Phylogenetic profiling resolves early emergence of PRC2 and illuminates its functional core","volume":"5","author":"Sharaf","year":"2022","journal-title":"Life Science Alliance"},{"key":"bib117","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0206667","article-title":"Determination of the presence of 5-methylcytosine in Paramecium tetraurelia","volume":"13","author":"Singh","year":"2018","journal-title":"PLOS ONE"},{"key":"bib118","doi-asserted-by":"publisher","first-page":"398","DOI":"10.1101\/gad.333542.119","article-title":"HELLS and PRDM9 form a pioneer complex to open chromatin at meiotic recombination hot spots","volume":"34","author":"Spruce","year":"2020","journal-title":"Genes & Development"},{"key":"bib119","doi-asserted-by":"publisher","DOI":"10.1242\/dev.194605","article-title":"Maintenance DNA methylation in pre-meiotic germ cells regulates meiotic prophase by facilitating homologous chromosome pairing","volume":"148","author":"Takada","year":"2021","journal-title":"Development"},{"key":"bib120","doi-asserted-by":"publisher","first-page":"2178","DOI":"10.1105\/tpc.19.00944","article-title":"Dual recognition of H3K4me3 and DNA by the ISWI component ARID5 regulates the floral transition in Arabidopsis","volume":"32","author":"Tan","year":"2020","journal-title":"The Plant Cell"},{"key":"bib121","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms8968","article-title":"Multiple cellular proteins interact with LEDGF\/p75 through a conserved unstructured consensus motif","volume":"6","author":"Tesina","year":"2015","journal-title":"Nature Communications"},{"key":"bib122","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms8870","article-title":"Mutations in CDCA7 and HELLS cause immunodeficiency-centromeric instability-facial anomalies syndrome","volume":"6","author":"Thijssen","year":"2015","journal-title":"Nature Communications"},{"key":"bib123","doi-asserted-by":"publisher","first-page":"4673","DOI":"10.1093\/nar\/22.22.4673","article-title":"CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice","volume":"22","author":"Thompson","year":"1994","journal-title":"Nucleic Acids Research"},{"key":"bib124","doi-asserted-by":"publisher","DOI":"10.3390\/epigenomes5030019","article-title":"Evolution of CG methylation maintenance machinery in plants","volume":"5","author":"Tirot","year":"2021","journal-title":"Epigenomes"},{"key":"bib125","doi-asserted-by":"publisher","first-page":"78","DOI":"10.1172\/JCI99751","article-title":"CDCA7 and HELLS mutations undermine nonhomologous end joining in centromeric instability syndrome","volume":"129","author":"Unoki","year":"2019","journal-title":"The Journal of Clinical Investigation"},{"key":"bib126","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-020-74636-2","article-title":"CDCA7 and HELLS suppress DNA:RNA hybrid-associated DNA damage at pericentromeric repeats","volume":"10","author":"Unoki","year":"2020","journal-title":"Scientific Reports"},{"key":"bib127","doi-asserted-by":"publisher","first-page":"349","DOI":"10.1111\/gtc.12850","article-title":"Chromatin remodeling in replication-uncoupled maintenance DNA methylation and chromosome stability: Insights from ICF syndrome studies","volume":"26","author":"Unoki","year":"2021","journal-title":"Genes to Cells"},{"key":"bib128","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1128\/MMBR.00044-12","article-title":"Diverse functions of restriction-modification systems in addition to cellular defense","volume":"77","author":"Vasu","year":"2013","journal-title":"Microbiology and Molecular Biology Reviews"},{"key":"bib129","doi-asserted-by":"publisher","first-page":"2409","DOI":"10.1093\/hmg\/ddy130","article-title":"Comparative methylome analysis of ICF patients identifies heterochromatin loci that require ZBTB24, CDCA7 and HELLS for their methylated state","volume":"27","author":"Velasco","year":"2018","journal-title":"Human Molecular Genetics"},{"key":"bib130","doi-asserted-by":"publisher","first-page":"1926","DOI":"10.1126\/science.8316832","article-title":"Arabidopsis thaliana DNA methylation mutants","volume":"260","author":"Vongs","year":"1993","journal-title":"Science"},{"key":"bib131","doi-asserted-by":"publisher","first-page":"773","DOI":"10.1042\/EBC20190035","article-title":"DNA methylation in disease: Immunodeficiency, Centromeric instability, Facial anomalies syndrome","volume":"63","author":"Vukic","year":"2019","journal-title":"Essays in Biochemistry"},{"key":"bib132","doi-asserted-by":"publisher","first-page":"73","DOI":"10.2174\/1568009013334241","article-title":"Drug target discovery by gene expression analysis: cell cycle genes","volume":"1","author":"Walker","year":"2001","journal-title":"Current Cancer Drug Targets"},{"key":"bib133","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1003872","article-title":"Function and Evolution of DNA Methylation in Nasonia vitripennis","volume":"9","author":"Wang","year":"2013","journal-title":"PLOS Genetics"},{"key":"bib134","doi-asserted-by":"publisher","first-page":"176","DOI":"10.1016\/j.cels.2020.06.006","article-title":"Quantitative translation of Dog-to-Human Aging by conserved remodeling of the DNA Methylome","volume":"11","author":"Wang","year":"2020","journal-title":"Cell Systems"},{"key":"bib135","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0101850","article-title":"Quickly finding Orthologs as reciprocal best hits with BLAT, LAST, and UBLAST: how much do we miss?","volume":"9","author":"Ward","year":"2014","journal-title":"PLOS ONE"},{"key":"bib136","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.62202","article-title":"The essential role of Dnmt1 in gametogenesis in the large milkweed bug Oncopeltus fasciatus","volume":"10","author":"Washington","year":"2021","journal-title":"eLife"},{"key":"bib137","doi-asserted-by":"publisher","first-page":"1189","DOI":"10.1093\/bioinformatics\/btp033","article-title":"Jalview Version 2--a multiple sequence alignment editor and analysis workbench","volume":"25","author":"Waterhouse","year":"2009","journal-title":"Bioinformatics"},{"key":"bib138","doi-asserted-by":"publisher","first-page":"4041","DOI":"10.1093\/hmg\/ddw243","article-title":"Converging disease genes in ICF syndrome: ZBTB24 controls expression of CDCA7 in mammals","volume":"25","author":"Wu","year":"2016","journal-title":"Human Molecular Genetics"},{"key":"bib139","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-021-23809-2","article-title":"The epigenetic regulator LSH maintains fork protection and genomic stability via MacroH2A deposition and RAD51 filament formation","volume":"12","author":"Xu","year":"2021","journal-title":"Nature Communications"},{"key":"bib140","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-019-09496-0","article-title":"RdDM-independent de novo and heterochromatin DNA methylation by plant CMT and DNMT3 orthologs","volume":"10","author":"Yaari","year":"2019","journal-title":"Nature Communications"},{"key":"bib141","doi-asserted-by":"publisher","first-page":"448","DOI":"10.1038\/nature09947","article-title":"Structure and mechanism of the chromatin remodelling factor ISW1a","volume":"472","author":"Yamada","year":"2011","journal-title":"Nature"},{"key":"bib142","doi-asserted-by":"publisher","first-page":"1613","DOI":"10.1101\/gr.172015.114","article-title":"Genome-wide DNA methylation patterns in LSH mutant reveals de-repression of repeat elements and redundant epigenetic silencing pathways","volume":"24","author":"Yu","year":"2014","journal-title":"Genome Research"},{"key":"bib143","doi-asserted-by":"publisher","first-page":"916","DOI":"10.1126\/science.1186366","article-title":"Genome-wide evolutionary analysis of eukaryotic DNA methylation","volume":"328","author":"Zemach","year":"2010","journal-title":"Science"},{"key":"bib144","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1016\/j.cell.2013.02.033","article-title":"The Arabidopsis Nucleosome Remodeler DDM1 Allows DNA Methyltransferases to access H1-Containing Heterochromatin","volume":"153","author":"Zemach","year":"2013","journal-title":"Cell"},{"key":"bib145","doi-asserted-by":"publisher","first-page":"1235","DOI":"10.1095\/biolreprod.110.085720","article-title":"Lymphoid-specific helicase (HELLS) is essential for meiotic progression in mouse spermatocytes","volume":"84","author":"Zeng","year":"2011","journal-title":"Biology of Reproduction"},{"key":"bib146","doi-asserted-by":"publisher","first-page":"3852","DOI":"10.1093\/nar\/gkac196","article-title":"H3K56 deacetylation and H2A.Z deposition are required for aberrant heterochromatin spreading","volume":"50","author":"Zhang","year":"2022","journal-title":"Nucleic Acids Research"}],"container-title":["eLife"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/cdn.elifesciences.org\/articles\/86721\/elife-86721-v1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/cdn.elifesciences.org\/articles\/86721\/elife-86721-v1.xml","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/elifesciences.org\/articles\/86721","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,13]],"date-time":"2023-10-13T19:03:44Z","timestamp":1697223824000},"score":1,"resource":{"primary":{"URL":"https:\/\/elifesciences.org\/articles\/86721"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,9,28]]},"references-count":146,"alternative-id":["10.7554\/eLife.86721"],"URL":"https:\/\/doi.org\/10.7554\/elife.86721","archive":["CLOCKSS"],"relation":{"has-preprint":[{"id-type":"doi","id":"10.7554\/eLife.86721.3","asserted-by":"subject"},{"id-type":"doi","id":"10.1101\/2023.01.30.526367","asserted-by":"subject"}],"references":[{"id-type":"accession","id":"GCF_000648655.2","asserted-by":"subject"},{"id-type":"accession","id":"GCF_009193385.2","asserted-by":"subject"},{"id-type":"accession","id":"GCF_000572035.2","asserted-by":"subject"},{"id-type":"accession","id":"GCF_000806365.1","asserted-by":"subject"},{"id-type":"accession","id":"GCF_001313835.1","asserted-by":"subject"},{"id-type":"accession","id":"GCF_003672135.1","asserted-by":"subject"},{"id-type":"accession","id":"GCF_001263275.1","asserted-by":"subject"},{"id-type":"accession","id":"GCF_910591885.1","asserted-by":"subject"},{"id-type":"accession","id":"GCF_000612105.2","asserted-by":"subject"},{"id-type":"accession","id":"GCF_019457755.1","asserted-by":"subject"},{"id-type":"accession","id":"GCF_014905175.1","asserted-by":"subject"},{"id-type":"accession","id":"GCF_020080835.1","asserted-by":"subject"}],"is-same-as":[{"id-type":"doi","id":"10.7554\/eLife.86721.4","asserted-by":"subject"}],"is-version-of":[{"id-type":"doi","id":"10.7554\/eLife.86721.1","asserted-by":"subject"},{"id-type":"doi","id":"10.7554\/eLife.86721.2","asserted-by":"subject"},{"id-type":"doi","id":"10.7554\/eLife.86721.3","asserted-by":"subject"}]},"ISSN":["2050-084X"],"issn-type":[{"value":"2050-084X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,9,28]]},"assertion":[{"value":"single anonymised","name":"peer_review_transparency","label":"Peer review transparency","group":{"name":"peer_review_taxonomy"}},{"value":"other reviewer(s), editor","name":"peer_review_interaction","label":"Peer review interaction","group":{"name":"peer_review_taxonomy"}},{"value":"review summaries, review reports, author\/editor communication, reviewer identities reviewer opt in, editor identities","name":"peer_review_published","label":"Peer review published","group":{"name":"peer_review_taxonomy"}},{"value":"open (sign in with ORCID iD required)","name":"post_publication_commenting","label":"Post publication commenting","group":{"name":"post_publication_commenting"}}],"article-number":"RP86721"}}