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In the case of birds, dosage compensation is largely absent, with it being restricted to two small Male Hyper-Methylated (MHM) regions on the Z chromosome. To investigate how variation in DNA methylation is regulated on the Z chromosome we utilised a wild x domestic advanced intercross in the chicken, with both hypothalamic methylomes and transcriptomes assayed in 124 individuals. The relatively large numbers of individuals allowed us to identify additional genomic MHM regions on the Z chromosome that were significantly differentially methylated between the sexes. These regions appear to down-regulate local gene expression in males, but not remove it entirely (unlike the lncRNAs identified in the initial MHM regions). These MHM regions were further tested and the most balanced genes appear to show decreased expression in males, whilst methylation appeared to be far more correlated with gene expression in the less balanced, as compared to the most balanced genes. In addition, quantitative trait loci (QTL) that regulate variation in methylation on the Z chromosome, and those loci that regulate methylation on the autosomes that derive from the Z chromosome were mapped. Trans-effect hotspots were also identified that were based on the autosomes but affected the Z, and also one that was based on the Z chromosome but that affected both autosomal and sex chromosome DNA methylation regulation. We show that both cis and trans loci that originate from the Z chromosome never exhibit an interaction with sex, whereas trans loci originating from the autosomes but affecting the Z chromosome always display such an interaction. Our results highlight how additional MHM regions are actually present on the Z chromosome, and they appear to have smaller-scale effects on gene expression in males. Quantitative variation in methylation is also regulated both from the autosomes to the Z chromosome, and from the Z chromosome to the autosomes.<\/jats:p>","DOI":"10.1371\/journal.pgen.1010719","type":"journal-article","created":{"date-parts":[[2024,3,8]],"date-time":"2024-03-08T13:38:47Z","timestamp":1709905127000},"page":"e1010719","update-policy":"https:\/\/doi.org\/10.1371\/journal.pgen.corrections_policy","source":"Crossref","is-referenced-by-count":5,"title":["The regulation of methylation on the Z chromosome and the identification of multiple novel Male Hyper-Methylated regions in the chicken"],"prefix":"10.1371","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1130-374X","authenticated-orcid":true,"given":"Andrey","family":"H\u00f6glund","sequence":"first","affiliation":[]},{"given":"Rie","family":"Henriksen","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1902-3002","authenticated-orcid":true,"given":"Allison M.","family":"Churcher","sequence":"additional","affiliation":[]},{"given":"Carlos M.","family":"Guerrero-Bosagna","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5064-2093","authenticated-orcid":true,"given":"Alvaro","family":"Martinez-Barrio","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1262-4585","authenticated-orcid":true,"given":"Martin","family":"Johnsson","sequence":"additional","affiliation":[]},{"given":"Per","family":"Jensen","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2329-2635","authenticated-orcid":true,"given":"Dominic","family":"Wright","sequence":"additional","affiliation":[]}],"member":"340","published-online":{"date-parts":[[2024,3,8]]},"reference":[{"issue":"6","key":"pgen.1010719.ref001","doi-asserted-by":"crossref","first-page":"901","DOI":"10.1093\/nar\/23.6.901","article-title":"CpG methylation has differential effects on the binding of YY1 and ETS proteins to the bi-directional promoter of the Surf-1 and Surf-2 genes","volume":"23","author":"K Gaston","year":"1995","journal-title":"Nucleic acids research"},{"issue":"6","key":"pgen.1010719.ref002","doi-asserted-by":"crossref","first-page":"988","DOI":"10.1101\/gr.146654.112","article-title":"CG methylated microarrays identify a novel methylated sequence bound by the CEBPB| ATF4 heterodimer that is active in vivo","volume":"23","author":"IK Mann","year":"2013","journal-title":"Genome research"},{"issue":"6337","key":"pgen.1010719.ref003","article-title":"Impact of cytosine methylation on DNA binding specificities of human transcription factors","volume":"356","author":"Y Yin","year":"2017","journal-title":"Science"},{"issue":"12","key":"pgen.1010719.ref004","doi-asserted-by":"crossref","first-page":"1713","DOI":"10.1038\/s41559-020-01310-1","article-title":"The methylation landscape and its role in domestication and gene regulation in the chicken","volume":"4","author":"A H\u00f6glund","year":"2020","journal-title":"Nature Ecology and Evolution"},{"key":"pgen.1010719.ref005","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1201\/9781315208701-6","volume-title":"Epigenetics and Assisted Reproduction","author":"I Nalvarte","year":"2018"},{"issue":"6159","key":"pgen.1010719.ref006","doi-asserted-by":"crossref","first-page":"750","DOI":"10.1126\/science.1242510","article-title":"Extensive variation in chromatin states across humans","volume":"342","author":"M Kasowski","year":"2013","journal-title":"Science"},{"issue":"6159","key":"pgen.1010719.ref007","doi-asserted-by":"crossref","first-page":"744","DOI":"10.1126\/science.1242463","article-title":"Coordinated effects of sequence variation on DNA binding, chromatin structure, and transcription","volume":"342","author":"H Kilpinen","year":"2013","journal-title":"Science"},{"issue":"6159","key":"pgen.1010719.ref008","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1126\/science.1242429","article-title":"Identification of genetic variants that affect histone modifications in human cells","volume":"342","author":"G McVicker","year":"2013","journal-title":"Science"},{"key":"pgen.1010719.ref009","volume-title":"Seminars in cell & developmental biology","author":"C Guerrero-Bosagna","year":"2019"},{"issue":"1","key":"pgen.1010719.ref010","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1186\/s12711-018-0384-z","article-title":"Epigenetics and early domestication: differences in hypothalamic DNA methylation between red junglefowl divergently selected for high or low fear of humans","volume":"50","author":"J B\u00e9lteky","year":"2018","journal-title":"Genetics Selection Evolution"},{"key":"pgen.1010719.ref011","volume-title":"Sex chromosomes and sex-linked genes","author":"S. 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