{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,29]],"date-time":"2026-07-29T23:13:30Z","timestamp":1785366810695,"version":"3.55.0"},"update-to":[{"DOI":"10.1371\/journal.pbio.3002605","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2024,5,29]],"date-time":"2024-05-29T00:00:00Z","timestamp":1716940800000}}],"reference-count":101,"publisher":"Public Library of Science (PLoS)","issue":"4","license":[{"start":{"date-parts":[[2024,4,30]],"date-time":"2024-04-30T00:00:00Z","timestamp":1714435200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"NIH","award":["5R01GM101255"],"award-info":[{"award-number":["5R01GM101255"]}]}],"content-domain":{"domain":["www.plosbiology.org"],"crossmark-restriction":false},"short-container-title":["PLoS Biol"],"abstract":"<jats:p>Although sex chromosomes have evolved from autosomes, they often have unusual regulatory regimes that are sex- and cell-type-specific such as dosage compensation (DC) and meiotic sex chromosome inactivation (MSCI). The molecular mechanisms and evolutionary forces driving these unique transcriptional programs are critical for genome evolution but have been, in the case of MSCI in <jats:italic>Drosophila<\/jats:italic>, subject to continuous debate. Here, we take advantage of the younger sex chromosomes in <jats:italic>D<\/jats:italic>. <jats:italic>miranda<\/jats:italic> (XR and the neo-X) to infer how former autosomes acquire sex-chromosome-specific regulatory programs using single-cell and bulk RNA sequencing and ribosome profiling, in a comparative evolutionary context. We show that contrary to mammals and worms, the X down-regulation through germline progression is most consistent with the shutdown of DC instead of MSCI, resulting in half gene dosage at the end of meiosis for all 3 X\u2019s. Moreover, lowly expressed germline and meiotic genes on the neo-X are ancestrally lowly expressed, instead of acquired suppression after sex linkage. For the young neo-X, DC is incomplete across all tissue and cell types and this dosage imbalance is rescued by contributions from Y-linked gametologs which produce transcripts that are translated to compensate both gene and protein dosage. We find an excess of previously autosomal testis genes becoming Y-specific, showing that the neo-Y and its masculinization likely resolve sexual antagonism. Multicopy neo-sex genes are predominantly expressed during meiotic stages of spermatogenesis, consistent with their amplification being driven to interfere with mendelian segregation. Altogether, this study reveals germline regulation of evolving sex chromosomes and elucidates the consequences these unique regulatory mechanisms have on the evolution of sex chromosome architecture.<\/jats:p>","DOI":"10.1371\/journal.pbio.3002605","type":"journal-article","created":{"date-parts":[[2024,4,30]],"date-time":"2024-04-30T19:31:11Z","timestamp":1714505471000},"page":"e3002605","update-policy":"https:\/\/doi.org\/10.1371\/journal.pbio.corrections_policy","source":"Crossref","is-referenced-by-count":19,"title":["Single-cell RNA-seq of Drosophila miranda testis reveals the evolution and trajectory of germline sex chromosome regulation"],"prefix":"10.1371","volume":"22","author":[{"given":"Kevin H-C.","family":"Wei","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kamalakar","family":"Chatla","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9724-9467","authenticated-orcid":true,"given":"Doris","family":"Bachtrog","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2024,4,30]]},"reference":[{"key":"pbio.3002605.ref001","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1038\/nrg3366","article-title":"Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration","volume":"14","author":"D. Bachtrog","year":"2013","journal-title":"Nat Rev Genet"},{"key":"pbio.3002605.ref002","doi-asserted-by":"crossref","first-page":"e1001711","DOI":"10.1371\/journal.pbio.1001711","article-title":"The epigenome of evolving Drosophila neo-sex chromosomes: dosage compensation and heterochromatin formation","volume":"11","author":"Q Zhou","year":"2013","journal-title":"PLoS Biol"},{"key":"pbio.3002605.ref003","doi-asserted-by":"crossref","first-page":"20200093","DOI":"10.1098\/rstb.2020.0093","article-title":"The timing of genetic degeneration of sex chromosomes","volume":"376","author":"D. Charlesworth","year":"2021","journal-title":"Philos Trans R Soc Lond B Biol Sci"},{"key":"pbio.3002605.ref004","doi-asserted-by":"crossref","first-page":"5618","DOI":"10.1073\/pnas.75.11.5618","article-title":"Model for evolution of Y chromosomes and dosage compensation","volume":"75","author":"B. Charlesworth","year":"1978","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pbio.3002605.ref005","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1016\/S0960-9822(02)00448-7","article-title":"The evolution of chromosomal sex determination and dosage compensation","volume":"6","author":"B. Charlesworth","year":"1996","journal-title":"Curr Biol"},{"key":"pbio.3002605.ref006","doi-asserted-by":"crossref","first-page":"645","DOI":"10.1038\/nrg1914","article-title":"Evolution on the X chromosome: unusual patterns and processes","volume":"7","author":"B Vicoso","year":"2006","journal-title":"Nat Rev Genet"},{"key":"pbio.3002605.ref007","article-title":"Sex chromosomes and sex-linked genes","author":"S. Ohno","year":"2013","journal-title":"Springer Science & Business Media"},{"key":"pbio.3002605.ref008","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1016\/j.tig.2009.03.005","article-title":"X, Y and Z of sex-chromosome dosage compensation","volume":"25","author":"JE Mank","year":"2009","journal-title":"Trends Genet"},{"key":"pbio.3002605.ref009","doi-asserted-by":"crossref","first-page":"2133","DOI":"10.1111\/j.1558-5646.2011.01316.x","article-title":"Some inconvenient truths about sex chromosome dosage compensation and the potential role of sexual conflict","volume":"65","author":"JE Mank","year":"2011","journal-title":"Evolution"},{"key":"pbio.3002605.ref010","first-page":"7","article-title":"Dosage compensation in Drosophila","author":"JC Lucchesi","year":"2015","journal-title":"Cold Spring Harb Perspect Biol"},{"key":"pbio.3002605.ref011","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1038\/nsmb.1644","article-title":"Drosophila MSL complex globally acetylates H4K16 on the male X chromosome for dosage compensation","volume":"16","author":"ME Gelbart","year":"2009","journal-title":"Nat Struct Mol Biol"},{"key":"pbio.3002605.ref012","doi-asserted-by":"crossref","first-page":"1399","DOI":"10.1242\/dev.029645","article-title":"Drosophila dosage compensation: a complex voyage to the X chromosome","volume":"136","author":"ME Gelbart","year":"2009","journal-title":"Development"},{"key":"pbio.3002605.ref013","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1242\/dev.129.2.479","article-title":"X-chromosome silencing in the germline of C. elegans","volume":"129","author":"WG Kelly","year":"2002","journal-title":"Development"},{"key":"pbio.3002605.ref014","doi-asserted-by":"crossref","first-page":"1823","DOI":"10.1242\/dev.000018","article-title":"Meiotic sex chromosome inactivation","volume":"134","author":"JMA Turner","year":"2007","journal-title":"Development"},{"key":"pbio.3002605.ref015","doi-asserted-by":"crossref","first-page":"e1000466","DOI":"10.1371\/journal.pgen.1000466","article-title":"Female meiotic sex chromosome inactivation in chicken","volume":"5","author":"S Schoenmakers","year":"2009","journal-title":"PLoS Genet"},{"key":"pbio.3002605.ref016","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1016\/S0074-7696(08)60928-6","article-title":"The behavior of the XY pair in mammals","volume":"38","author":"AJ Solari","year":"1974","journal-title":"Int Rev Cytol"},{"key":"pbio.3002605.ref017","doi-asserted-by":"crossref","first-page":"2135","DOI":"10.1016\/j.cub.2004.11.032","article-title":"BRCA1, histone H2AX phosphorylation, and male meiotic sex chromosome inactivation","volume":"14","author":"JMA Turner","year":"2004","journal-title":"Curr Biol"},{"key":"pbio.3002605.ref018","doi-asserted-by":"crossref","first-page":"9730","DOI":"10.1073\/pnas.0700323104","article-title":"Sex chromosome silencing in the marsupial male germ line","volume":"104","author":"SH Namekawa","year":"2007","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pbio.3002605.ref019","doi-asserted-by":"crossref","first-page":"e31485","DOI":"10.1371\/journal.pone.0031485","article-title":"Human male meiotic sex chromosome inactivation","volume":"7","author":"M de Vries","year":"2012","journal-title":"PLoS ONE"},{"key":"pbio.3002605.ref020","doi-asserted-by":"crossref","first-page":"e1010040","DOI":"10.1371\/journal.pgen.1010040","article-title":"Strategies for meiotic sex chromosome dynamics and telomeric elongation in Marsupials","volume":"18","author":"L Mar\u00edn-Gual","year":"2022","journal-title":"PLoS Genet"},{"key":"pbio.3002605.ref021","doi-asserted-by":"crossref","first-page":"1641","DOI":"10.1534\/genetics.116.191130","article-title":"Plasticity in the Meiotic Epigenetic Landscape of Sex Chromosomes in Caenorhabditis Species","volume":"203","author":"BJ Larson","year":"2016","journal-title":"Genetics"},{"key":"pbio.3002605.ref022","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1007\/BF00356023","article-title":"Sex chromosomes, recombination, and chromatin conformation","volume":"102","author":"BD McKee","year":"1993","journal-title":"Chromosoma"},{"key":"pbio.3002605.ref023","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1038\/nrg2505","article-title":"The consequences of asynapsis for mammalian meiosis","volume":"10","author":"PS Burgoyne","year":"2009","journal-title":"Nat Rev Genet"},{"key":"pbio.3002605.ref024","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1016\/S0168-9525(03)00058-1","article-title":"Sexual antagonism and X inactivation\u2014the SAXI hypothesis","volume":"19","author":"CI Wu","year":"2003","journal-title":"Trends Genet"},{"key":"pbio.3002605.ref025","doi-asserted-by":"crossref","first-page":"e293","DOI":"10.1371\/journal.pbio.0050293","article-title":"A sex-ratio meiotic drive system in Drosophila simulans. II: an X-linked distorter","volume":"5","author":"Y Tao","year":"2007","journal-title":"PLoS Biol"},{"key":"pbio.3002605.ref026","doi-asserted-by":"crossref","first-page":"794","DOI":"10.1038\/ng.126","article-title":"The mouse X chromosome is enriched for multicopy testis genes showing postmeiotic expression","volume":"40","author":"JL Mueller","year":"2008","journal-title":"Nat Genet"},{"key":"pbio.3002605.ref027","doi-asserted-by":"crossref","first-page":"3699","DOI":"10.1016\/j.cub.2019.08.057","article-title":"A neofunctionalized X-linked ampliconic gene family is essential for male fertility and equal sex ratio in mice","volume":"29","author":"AN Kruger","year":"2019","journal-title":"Curr Biol"},{"key":"pbio.3002605.ref028","doi-asserted-by":"crossref","first-page":"e273","DOI":"10.1371\/journal.pbio.0050273","article-title":"X chromosome inactivation during Drosophila spermatogenesis","volume":"5","author":"W Hense","year":"2007","journal-title":"PLoS Biol"},{"key":"pbio.3002605.ref029","doi-asserted-by":"crossref","first-page":"e1000731","DOI":"10.1371\/journal.pgen.1000731","article-title":"Stage-specific expression profiling of Drosophila spermatogenesis suggests that meiotic sex chromosome inactivation drives genomic relocation of testis-expressed genes","volume":"5","author":"MD Vibranovski","year":"2009","journal-title":"PLoS Genet"},{"key":"pbio.3002605.ref030","doi-asserted-by":"crossref","first-page":"e1001126","DOI":"10.1371\/journal.pbio.1001126","article-title":"Sex chromosome-specific regulation in the Drosophila male germline but little evidence for chromosomal dosage compensation or meiotic inactivation","volume":"9","author":"CD Meiklejohn","year":"2011","journal-title":"PLoS Biol"},{"key":"pbio.3002605.ref031","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1186\/1741-7007-9-29","article-title":"Lack of global meiotic sex chromosome inactivation, and paucity of tissue-specific gene expression on the Drosophila X chromosome","volume":"9","author":"LM Mikhaylova","year":"2011","journal-title":"BMC Biol"},{"key":"pbio.3002605.ref032","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1186\/1741-7007-10-49","article-title":"Re-analysis of the larval testis data on meiotic sex chromosome inactivation revealed evidence for tissue-specific gene expression related to the drosophila X chromosome","volume":"10","author":"MD Vibranovski","year":"2012","journal-title":"BMC Biol"},{"key":"pbio.3002605.ref033","doi-asserted-by":"crossref","first-page":"104","DOI":"10.7150\/jgen.8178","article-title":"Meiotic sex chromosome inactivation","volume":"2","author":"MD Vibranovski","year":"2014","journal-title":"Drosophila. J Genomics"},{"key":"pbio.3002605.ref034","doi-asserted-by":"crossref","first-page":"e1002499","DOI":"10.1371\/journal.pbio.1002499","article-title":"Sex Chromosome-wide Transcriptional Suppression and Compensatory Cis-Regulatory Evolution Mediate Gene Expression in the Drosophila Male Germline","volume":"14","author":"EL Landeen","year":"2016","journal-title":"PLoS Biol"},{"key":"pbio.3002605.ref035","doi-asserted-by":"crossref","first-page":"e1009728","DOI":"10.1371\/journal.pgen.1009728","article-title":"Single-cell RNA-sequencing reveals pre-meiotic X-chromosome dosage compensation in Drosophila testis","volume":"17","author":"E Witt","year":"2021","journal-title":"PLoS Genet"},{"key":"pbio.3002605.ref036","doi-asserted-by":"crossref","first-page":"892","DOI":"10.1038\/s41467-021-20897-y","article-title":"Dynamic sex chromosome expression in Drosophila male germ cells","volume":"12","author":"S Mahadevaraju","year":"2021","journal-title":"Nat Commun"},{"key":"pbio.3002605.ref037","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1016\/S0925-4773(98)00009-4","article-title":"An analysis of maleless and histone H4 acetylation in Drosophila melanogaster spermatogenesis","volume":"71","author":"L Rastelli","year":"1998","journal-title":"Mech Dev"},{"key":"pbio.3002605.ref038","doi-asserted-by":"crossref","first-page":"3203","DOI":"10.1093\/nar\/gkac109","article-title":"Comparison of genome architecture at two stages of male germline cell differentiation in Drosophila","volume":"50","author":"AA Ilyin","year":"2022","journal-title":"Nucleic Acids Res"},{"key":"pbio.3002605.ref039","doi-asserted-by":"crossref","first-page":"1854","DOI":"10.1101\/gr.604902","article-title":"Retroposed new genes out of the X in Drosophila","volume":"12","author":"E Betr\u00e1n","year":"2002","journal-title":"Genome Res"},{"key":"pbio.3002605.ref040","doi-asserted-by":"crossref","first-page":"697","DOI":"10.1126\/science.1079190","article-title":"Paucity of genes on the Drosophila X chromosome showing male-biased expression","volume":"299","author":"M Parisi","year":"2003","journal-title":"Science"},{"key":"pbio.3002605.ref041","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1242\/dev.00914","article-title":"Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans","volume":"131","author":"V Reinke","year":"2004","journal-title":"Development"},{"key":"pbio.3002605.ref042","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1038\/nature06330","article-title":"Demasculinization of X chromosomes in the Drosophila genus","volume":"450","author":"D Sturgill","year":"2007","journal-title":"Nature"},{"key":"pbio.3002605.ref043","doi-asserted-by":"crossref","first-page":"735","DOI":"10.2307\/2408385","article-title":"SEX CHROMOSOMES AND THE EVOLUTION OF SEXUAL DIMORPHISM","volume":"38","author":"WR Rice","year":"1984","journal-title":"Evolution"},{"key":"pbio.3002605.ref044","first-page":"1510","article-title":"The genomic location of sexually antagonistic variation: some cautionary comments","volume":"64","author":"JD Fry","year":"2010","journal-title":"Evolution"},{"key":"pbio.3002605.ref045","doi-asserted-by":"crossref","first-page":"3743","DOI":"10.1111\/j.1558-5646.2012.01728.x","article-title":"The effects of selection and genetic drift on the genomic distribution of sexually antagonistic alleles","volume":"66","author":"C Mullon","year":"2012","journal-title":"Evolution"},{"key":"pbio.3002605.ref046","doi-asserted-by":"crossref","first-page":"2888","DOI":"10.1111\/j.1558-5646.2009.00764.x","article-title":"Maintenance or loss of genetic variation under sexual and parental antagonism at a sex-linked locus","volume":"63","author":"MM Patten","year":"2009","journal-title":"Evolution"},{"key":"pbio.3002605.ref047","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1002\/bies.20034","article-title":"Battle of the Xs","volume":"26","author":"B Oliver","year":"2004","journal-title":"Bioessays"},{"key":"pbio.3002605.ref048","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1016\/S0169-5347(98)01567-5","article-title":"The Y chromosome as a battle ground for sexual selection","volume":"14","author":"ER Roldan","year":"1999","journal-title":"Trends Ecol Evol"},{"key":"pbio.3002605.ref049","doi-asserted-by":"crossref","first-page":"675","DOI":"10.1126\/science.278.5338.675","article-title":"Functional coherence of the human Y chromosome","volume":"278","author":"BT Lahn","year":"1997","journal-title":"Science"},{"key":"pbio.3002605.ref050","doi-asserted-by":"crossref","first-page":"13225","DOI":"10.1073\/pnas.231484998","article-title":"Identification of five new genes on the Y chromosome of Drosophila melanogaster","volume":"98","author":"AB Carvalho","year":"2001","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pbio.3002605.ref051","doi-asserted-by":"crossref","first-page":"1030","DOI":"10.1126\/science.1998119","article-title":"The evolution of sex chromosomes","volume":"251","author":"B. Charlesworth","year":"1991","journal-title":"Science"},{"key":"pbio.3002605.ref052","doi-asserted-by":"crossref","first-page":"e1002078","DOI":"10.1371\/journal.pbio.1002078","article-title":"Numerous Transitions of Sex Chromosomes in Diptera","volume":"13","author":"B Vicoso","year":"2015","journal-title":"PLoS Biol"},{"key":"pbio.3002605.ref053","doi-asserted-by":"crossref","first-page":"846","DOI":"10.1126\/science.1239552","article-title":"Dosage compensation via transposable element mediated rewiring of a regulatory network","volume":"342","author":"CE Ellison","year":"2013","journal-title":"Science"},{"key":"pbio.3002605.ref054","doi-asserted-by":"crossref","first-page":"853","DOI":"10.1101\/gad.215426.113","article-title":"Conservation and de novo acquisition of dosage compensation on newly evolved sex chromosomes in Drosophila","volume":"27","author":"AA Alekseyenko","year":"2013","journal-title":"Genes Dev"},{"key":"pbio.3002605.ref055","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1038\/416323a","article-title":"Reduced adaptation of a non-recombining neo-Y chromosome","volume":"416","author":"D Bachtrog","year":"2002","journal-title":"Nature"},{"key":"pbio.3002605.ref056","doi-asserted-by":"crossref","first-page":"1329","DOI":"10.1093\/gbe\/evr103","article-title":"Nonrandom gene loss from the Drosophila miranda neo-Y chromosome","volume":"3","author":"VB Kaiser","year":"2011","journal-title":"Genome Biol Evol"},{"key":"pbio.3002605.ref057","doi-asserted-by":"crossref","first-page":"e2006348","DOI":"10.1371\/journal.pbio.2006348","article-title":"De novo assembly of a young Drosophila Y chromosome using single-molecule sequencing and chromatin conformation capture","volume":"16","author":"S Mahajan","year":"2018","journal-title":"PLoS Biol"},{"key":"pbio.3002605.ref058","doi-asserted-by":"crossref","first-page":"5537","DOI":"10.1038\/s41467-020-19134-9","article-title":"Epigenetic conflict on a degenerating Y chromosome increases mutational burden in Drosophila males","volume":"11","author":"KH-C Wei","year":"2020","journal-title":"Nat Commun"},{"key":"pbio.3002605.ref059","first-page":"4","article-title":"Non-allelic gene conversion enables rapid evolutionary change at multiple regulatory sites encoded by transposable elements","author":"CE Ellison","year":"2015","journal-title":"Elife"},{"key":"pbio.3002605.ref060","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1297-9686-21-3-283","article-title":"Variation of sperm length and heteromorphism in drosophilid species","volume":"21","author":"D Joly","year":"1989","journal-title":"Genet Sel Evol"},{"key":"pbio.3002605.ref061","doi-asserted-by":"crossref","first-page":"797","DOI":"10.2307\/2411155","article-title":"IS THE PRODUCTION OF MULTIPLE SPERM TYPES ADAPTIVE?","volume":"51","author":"RR Snook","year":"1997","journal-title":"Evolution"},{"key":"pbio.3002605.ref062","first-page":"8","article-title":"Testis single-cell RNA-seq reveals the dynamics of de novo gene transcription and germline mutational bias in Drosophila","author":"E Witt","year":"2019","journal-title":"Elife"},{"key":"pbio.3002605.ref063","doi-asserted-by":"crossref","first-page":"540","DOI":"10.1042\/BST0360540","article-title":"Comet and cup genes in Drosophila spermatogenesis: the first demonstration of post-meiotic transcription","volume":"36","author":"C Barreau","year":"2008","journal-title":"Biochem Soc Trans"},{"key":"pbio.3002605.ref064","doi-asserted-by":"crossref","first-page":"933","DOI":"10.1016\/0022-1910(94)90131-7","article-title":"Polymorphism in the sperm heteromorphic species of the Drosophila obscura group","volume":"40","author":"D Joly","year":"1994","journal-title":"J Insect Physiol"},{"key":"pbio.3002605.ref065","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1038\/nature12235","article-title":"Reversal of an ancient sex chromosome to an autosome in Drosophila","volume":"499","author":"B Vicoso","year":"2013","journal-title":"Nature"},{"key":"pbio.3002605.ref066","doi-asserted-by":"crossref","first-page":"1189","DOI":"10.1093\/gbe\/evs093","article-title":"Sex-biased transcriptome evolution in Drosophila","volume":"4","author":"R Assis","year":"2012","journal-title":"Genome Biol Evol"},{"key":"pbio.3002605.ref067","doi-asserted-by":"crossref","first-page":"1476","DOI":"10.1016\/j.cub.2010.06.076","article-title":"Dosage compensation and demasculinization of X chromosomes in Drosophila","volume":"20","author":"D Bachtrog","year":"2010","journal-title":"Curr Biol"},{"key":"pbio.3002605.ref068","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/j.molcel.2007.08.011","article-title":"MSL complex is attracted to genes marked by H3K36 trimethylation using a sequence-independent mechanism","volume":"28","author":"E Larschan","year":"2007","journal-title":"Mol Cell"},{"key":"pbio.3002605.ref069","doi-asserted-by":"crossref","first-page":"1153","DOI":"10.1101\/gr.211433.116","article-title":"Clustering of Drosophila housekeeping promoters facilitates their expression","volume":"27","author":"M Corrales","year":"2017","journal-title":"Genome Res"},{"key":"pbio.3002605.ref070","doi-asserted-by":"crossref","first-page":"1073","DOI":"10.1038\/ng1429","article-title":"Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise","volume":"36","author":"JT Mendell","year":"2004","journal-title":"Nat Genet"},{"key":"pbio.3002605.ref071","doi-asserted-by":"crossref","first-page":"735","DOI":"10.1261\/rna.060541.116","article-title":"High-resolution profiling of NMD targets in yeast reveals translational fidelity as a basis for substrate selection","volume":"23","author":"A Celik","year":"2017","journal-title":"RNA"},{"key":"pbio.3002605.ref072","doi-asserted-by":"crossref","first-page":"897","DOI":"10.1101\/gr.088609.108","article-title":"General gene movement off the X chromosome in the Drosophila genus","volume":"19","author":"MD Vibranovski","year":"2009","journal-title":"Genome Res"},{"key":"pbio.3002605.ref073","doi-asserted-by":"crossref","first-page":"1587","DOI":"10.1038\/s41559-019-1009-9","article-title":"Massive gene amplification on a recently formed Drosophila Y chromosome","volume":"3","author":"D Bachtrog","year":"2019","journal-title":"Nat Ecol Evol"},{"key":"pbio.3002605.ref074","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1093\/genetics\/101.1.57","article-title":"Defective Histone Transition during Spermiogenesis in Heterozygous SEGREGATION DISTORTER Males of DROSOPHILA MELANOGASTER","volume":"101","author":"E Hauschteck-Jungen","year":"1982","journal-title":"Genetics"},{"key":"pbio.3002605.ref075","doi-asserted-by":"crossref","first-page":"831","DOI":"10.1534\/genetics.114.173948","article-title":"Sex-ratio meiotic drive and Y-linked resistance in Drosophila affinis","volume":"199","author":"RL Unckless","year":"2015","journal-title":"Genetics"},{"key":"pbio.3002605.ref076","first-page":"20191430","article-title":"Meiotic drive mechanisms: lessons from Drosophila","volume":"286","author":"C Courret","year":"2019","journal-title":"Proc Biol Sci"},{"key":"pbio.3002605.ref077","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1016\/j.devcel.2018.07.004","article-title":"The hpRNA\/RNAi Pathway Is Essential to Resolve Intragenomic Conflict in the Drosophila Male Germline","volume":"46","author":"C-J Lin","year":"2018","journal-title":"Dev Cell"},{"key":"pbio.3002605.ref078","doi-asserted-by":"crossref","first-page":"1613","DOI":"10.1038\/s41559-021-01592-z","article-title":"Rapid evolutionary dynamics of an expanding family of meiotic drive factors and their hpRNA suppressors","volume":"5","author":"J Vedanayagam","year":"2021","journal-title":"Nat Ecol Evol"},{"key":"pbio.3002605.ref079","doi-asserted-by":"crossref","first-page":"1604","DOI":"10.1038\/s41559-021-01543-8","article-title":"Satellite DNA-mediated diversification of a sex-ratio meiotic drive gene family in Drosophila","volume":"5","author":"CA Muirhead","year":"2021","journal-title":"Nat Ecol Evol"},{"key":"pbio.3002605.ref080","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1073\/pnas.69.1.182","article-title":"The role of X-chromosome inactivation during spermatogenesis (Drosophila-allocycly-chromosome evolution-male sterility-dosage compensation)","volume":"69","author":"E Lifschytz","year":"1972","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pbio.3002605.ref081","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1007\/BF00288489","article-title":"Chromatin organization in the male germ line of Drosophila hydei","volume":"94","author":"H Kremer","year":"1986","journal-title":"Chromosoma"},{"key":"pbio.3002605.ref082","doi-asserted-by":"crossref","first-page":"742","DOI":"10.1126\/science.1221428","article-title":"Drosophila dosage compensation involves enhanced Pol II recruitment to male X-linked promoters","volume":"337","author":"T Conrad","year":"2012","journal-title":"Science"},{"key":"pbio.3002605.ref083","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1126\/science.1231815","article-title":"Comment on \u201cDrosophila dosage compensation involves enhanced Pol II recruitment to male X-linked promoters.\u201d","author":"F Ferrari","year":"2013","journal-title":"Science"},{"key":"pbio.3002605.ref084","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1016\/j.celrep.2013.09.037","article-title":"\u201cJump start and gain\u201d model for dosage compensation in Drosophila based on direct sequencing of nascent transcripts","volume":"5","author":"F Ferrari","year":"2013","journal-title":"Cell Rep"},{"key":"pbio.3002605.ref085","article-title":"Chromosome-specific maturation of the epigenome in the Drosophila male germline","author":"J Anderson","year":"2023","journal-title":"eLife"},{"key":"pbio.3002605.ref086","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1016\/0012-1606(86)90007-2","article-title":"Mutations affecting dosage compensation in Drosophila melanogaster: effects in the germline","volume":"118","author":"D Bachiller","year":"1986","journal-title":"Dev Biol"},{"key":"pbio.3002605.ref087","first-page":"8","article-title":"Single cell transcriptome atlas of the Drosophila larval brain","author":"C Brunet Avalos","year":"2019","journal-title":"Elife"},{"key":"pbio.3002605.ref088","doi-asserted-by":"crossref","first-page":"eabk2432","DOI":"10.1126\/science.abk2432","article-title":"Fly Cell Atlas: A single-nucleus transcriptomic atlas of the adult fruit fly","volume":"375","author":"H Li","year":"2022","journal-title":"Science"},{"key":"pbio.3002605.ref089","doi-asserted-by":"crossref","first-page":"e1010268","DOI":"10.1371\/journal.pgen.1010268","article-title":"Sex-specific variation in R-loop formation in Drosophila melanogaster","volume":"18","author":"TJ Stanek","year":"2022","journal-title":"PLoS Genet"},{"key":"pbio.3002605.ref090","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1038\/nmeth.4197","article-title":"Salmon provides fast and bias-aware quantification of transcript expression","volume":"14","author":"R Patro","year":"2017","journal-title":"Nat Methods"},{"key":"pbio.3002605.ref091","doi-asserted-by":"crossref","first-page":"3573","DOI":"10.1016\/j.cell.2021.04.048","article-title":"Integrated analysis of multimodal single-cell data","volume":"184","author":"Y Hao","year":"2021","journal-title":"Cell"},{"key":"pbio.3002605.ref092","doi-asserted-by":"crossref","first-page":"6854","DOI":"10.1038\/s41467-021-27136-4","article-title":"A transposon expression burst accompanies the activation of Y-chromosome fertility genes during Drosophila spermatogenesis","volume":"12","author":"MA Lawlor","year":"2021","journal-title":"Nat Commun"},{"key":"pbio.3002605.ref093","doi-asserted-by":"crossref","first-page":"1754","DOI":"10.1093\/bioinformatics\/btp324","article-title":"Fast and accurate short read alignment with Burrows-Wheeler transform","volume":"25","author":"H Li","year":"2009","journal-title":"Bioinformatics"},{"key":"pbio.3002605.ref094","doi-asserted-by":"crossref","first-page":"R137","DOI":"10.1186\/gb-2008-9-9-r137","article-title":"Model-based analysis of ChIP-Seq (MACS)","volume":"9","author":"Y Zhang","year":"2008","journal-title":"Genome Biol"},{"key":"pbio.3002605.ref095","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1093\/bioinformatics\/btq033","article-title":"BEDTools: a flexible suite of utilities for comparing genomic features","volume":"26","author":"AR Quinlan","year":"2010","journal-title":"Bioinformatics"},{"key":"pbio.3002605.ref096","first-page":"8","article-title":"Dynamic turnover of centromeres drives karyotype evolution in Drosophila","author":"R Bracewell","year":"2019","journal-title":"Elife"},{"key":"pbio.3002605.ref097","doi-asserted-by":"crossref","first-page":"e1004159","DOI":"10.1371\/journal.pgen.1004159","article-title":"Sex-specific embryonic gene expression in species with newly evolved sex chromosomes","volume":"10","author":"SE Lott","year":"2014","journal-title":"PLoS Genet"},{"key":"pbio.3002605.ref098","first-page":"10","article-title":"Establishment of H3K9me3-dependent heterochromatin during embryogenesis in Drosophila miranda","author":"KH-C Wei","year":"2021","journal-title":"Elife"},{"key":"pbio.3002605.ref099","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1093\/bioinformatics\/bts635","article-title":"STAR: ultrafast universal RNA-seq aligner","volume":"29","author":"A Dobin","year":"2013","journal-title":"Bioinformatics"},{"key":"pbio.3002605.ref100","doi-asserted-by":"crossref","first-page":"e108","DOI":"10.1093\/nar\/gkt214","article-title":"The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote","volume":"41","author":"Y Liao","year":"2013","journal-title":"Nucleic Acids Res"},{"key":"pbio.3002605.ref101","article-title":"Data from: Evolution and dynamics of germline sex chromosome regulation in D. miranda [Dataset].","author":"K. Wei","year":"2024","journal-title":"Dryad"}],"updated-by":[{"DOI":"10.1371\/journal.pbio.3002605","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2024,5,29]],"date-time":"2024-05-29T00:00:00Z","timestamp":1716940800000}}],"container-title":["PLOS Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pbio.3002605","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,5,29]],"date-time":"2024-05-29T17:49:37Z","timestamp":1717004977000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pbio.3002605"}},"subtitle":[],"editor":[{"given":"Erin S.","family":"Kelleher","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2024,4,30]]},"references-count":101,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2024,4,30]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pbio.3002605","relation":{"new_version":[{"id-type":"doi","id":"10.1371\/journal.pbio.3002605","asserted-by":"object"}]},"ISSN":["1545-7885"],"issn-type":[{"value":"1545-7885","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,4,30]]}}}