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Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2022,12,6]]},"abstract":"<jats:p>\n                    Mammalian sex chromosomes are highly conserved, and sex is determined by\n                    <jats:italic>SRY<\/jats:italic>\n                    on the Y chromosome. Two exceptional rodent groups in which some species lack a Y chromosome and\n                    <jats:italic>Sry<\/jats:italic>\n                    offer insights into how novel sex genes can arise and replace\n                    <jats:italic>Sry<\/jats:italic>\n                    , leading to sex chromosome turnover. However, intensive study over three decades has failed to reveal the identity of novel sex genes in either of these lineages. We here report our discovery of a male-specific duplication of an enhancer of\n                    <jats:italic>Sox9<\/jats:italic>\n                    in the Amami spiny rat\n                    <jats:italic>Tokudaia osimensis<\/jats:italic>\n                    , in which males and females have only a single X chromosome (XO\/XO) and the Y chromosome and\n                    <jats:italic>Sry<\/jats:italic>\n                    are completely lost. We performed a comprehensive survey to detect sex-specific genomic regions in the spiny rat. Sex-related genomic differences were limited to a male-specific duplication of a 17-kb unit located 430 kb upstream of\n                    <jats:italic>Sox9<\/jats:italic>\n                    on an autosome. Hi-C analysis using male spiny rat cells showed the duplicated region has potential chromatin interaction with\n                    <jats:italic>Sox9<\/jats:italic>\n                    . The duplicated unit harbored a 1,262-bp element homologous to mouse enhancer 14 (Enh14), a candidate\n                    <jats:italic>Sox9<\/jats:italic>\n                    enhancer that is functionally redundant in mice. Transgenic reporter mice showed that the spiny rat Enh14 can function as an embryonic testis enhancer in mice. Embryonic gonads of XX mice in which Enh14 was replaced by the duplicated spiny rat Enh14 showed increased\n                    <jats:italic>Sox9<\/jats:italic>\n                    expression and decreased\n                    <jats:italic>Foxl2<\/jats:italic>\n                    expression. We propose that male-specific duplication of this\n                    <jats:italic>Sox9<\/jats:italic>\n                    enhancer substituted for\n                    <jats:italic>Sry<\/jats:italic>\n                    function, defining a novel Y chromosome in the spiny rat.\n                  <\/jats:p>","DOI":"10.1073\/pnas.2211574119","type":"journal-article","created":{"date-parts":[[2022,11,28]],"date-time":"2022-11-28T17:14:31Z","timestamp":1669655671000},"update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":50,"title":["Turnover of mammal sex chromosomes in the\n                    <i>Sry<\/i>\n                    -deficient Amami spiny rat is due to male-specific upregulation of\n                    <i>Sox9<\/i>"],"prefix":"10.1073","volume":"119","author":[{"given":"Miho","family":"Terao","sequence":"first","affiliation":[{"name":"Department of Systems BioMedicine, National Research Institute for Child Health and Development, Setagaya-ku, Tokyo 157-8535, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuya","family":"Ogawa","sequence":"additional","affiliation":[{"name":"Department of Systems BioMedicine, National Research Institute for Child Health and Development, Setagaya-ku, Tokyo 157-8535, Japan"},{"name":"Department of National Center for Child Health and Development, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Bunkyo-ku, Tokyo 113-8510, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuji","family":"Takada","sequence":"additional","affiliation":[{"name":"Department of Systems BioMedicine, National Research Institute for Child Health and Development, Setagaya-ku, Tokyo 157-8535, Japan"},{"name":"Department of National Center for Child Health and Development, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Bunkyo-ku, Tokyo 113-8510, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5013-0052","authenticated-orcid":false,"given":"Rei","family":"Kajitani","sequence":"additional","affiliation":[{"name":"School of Life Science and Technology, Tokyo Institute of Technology, Meguro-ku, Tokyo 152-8550, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6164-1878","authenticated-orcid":false,"given":"Miki","family":"Okuno","sequence":"additional","affiliation":[{"name":"School of Life Science and Technology, Tokyo Institute of Technology, Meguro-ku, Tokyo 152-8550, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6096-064X","authenticated-orcid":false,"given":"Yuta","family":"Mochimaru","sequence":"additional","affiliation":[{"name":"School of Life Science and Technology, Tokyo Institute of Technology, Meguro-ku, Tokyo 152-8550, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6503-3880","authenticated-orcid":false,"given":"Kentaro","family":"Matsuoka","sequence":"additional","affiliation":[{"name":"School of Life Science and Technology, Tokyo Institute of Technology, Meguro-ku, Tokyo 152-8550, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6113-557X","authenticated-orcid":false,"given":"Takehiko","family":"Itoh","sequence":"additional","affiliation":[{"name":"School of Life Science and Technology, Tokyo Institute of Technology, Meguro-ku, Tokyo 152-8550, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0728-7548","authenticated-orcid":false,"given":"Atsushi","family":"Toyoda","sequence":"additional","affiliation":[{"name":"Comparative Genomics Laboratory, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan"},{"name":"Advanced Genomics Center, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tomohiro","family":"Kono","sequence":"additional","affiliation":[{"name":"Department of Bioscience, Tokyo University of Agriculture, Setagaya-ku, Tokyo 156-8502, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Takamichi","family":"Jogahara","sequence":"additional","affiliation":[{"name":"Faculty of Law, Economics and Management, Okinawa University, Naha, Okinawa 902-8521, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shusei","family":"Mizushima","sequence":"additional","affiliation":[{"name":"Division of Reproductive and Developmental Biology, Department of Biological Sciences, Faculty of Science, Hokkaido University, Kita-ku, Sapporo, Hokkaido 060-0810, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Asato","family":"Kuroiwa","sequence":"additional","affiliation":[{"name":"Division of Reproductive and Developmental Biology, Department of Biological Sciences, Faculty of Science, Hokkaido University, Kita-ku, Sapporo, Hokkaido 060-0810, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"341","published-online":{"date-parts":[[2022,11,28]]},"reference":[{"key":"e_1_3_4_1_2","doi-asserted-by":"publisher","DOI":"10.1038\/351117a0"},{"key":"e_1_3_4_2_2","doi-asserted-by":"publisher","DOI":"10.1266\/jjg.52.247"},{"key":"e_1_3_4_3_2","doi-asserted-by":"publisher","DOI":"10.1007\/s003350010228"},{"key":"e_1_3_4_4_2","doi-asserted-by":"publisher","DOI":"10.1038\/ng1095-117"},{"key":"e_1_3_4_5_2","first-page":"86","article-title":"Fertile males with two X chromosomes in Ellobius tancrei (Rodentia, Mammalia)","volume":"115","author":"Fredga K.","year":"1991","unstructured":"K. Fredga, E. A. Lyapunova, Fertile males with two X chromosomes in Ellobius tancrei (Rodentia, Mammalia). Hereditas 115, 86\u201397 (1991).","journal-title":"Hereditas"},{"key":"e_1_3_4_6_2","doi-asserted-by":"publisher","DOI":"10.1007\/s10577-010-9142-y"},{"key":"e_1_3_4_7_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0108779"},{"key":"e_1_3_4_8_2","doi-asserted-by":"publisher","DOI":"10.1038\/srep32874"},{"key":"e_1_3_4_9_2","doi-asserted-by":"publisher","DOI":"10.1007\/s10577-006-1093-y"},{"key":"e_1_3_4_10_2","doi-asserted-by":"publisher","DOI":"10.1007\/s10577-008-1199-5"},{"key":"e_1_3_4_11_2","doi-asserted-by":"publisher","DOI":"10.3106\/041.035.0404"},{"key":"e_1_3_4_12_2","doi-asserted-by":"publisher","DOI":"10.1038\/90046"},{"key":"e_1_3_4_13_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.gendis.2014.09.004"},{"key":"e_1_3_4_14_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.biocel.2017.03.005"},{"key":"e_1_3_4_15_2","doi-asserted-by":"publisher","DOI":"10.1136\/jmedgenet-2014-102864"},{"key":"e_1_3_4_16_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-018-07784-9"},{"key":"e_1_3_4_17_2","doi-asserted-by":"publisher","DOI":"10.1002\/ajmg.a.37101"},{"key":"e_1_3_4_18_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature06944"},{"key":"e_1_3_4_19_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2009.11.021"},{"key":"e_1_3_4_20_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1006520"},{"key":"e_1_3_4_21_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.aas9408"},{"key":"e_1_3_4_22_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-018-35746-0"},{"key":"e_1_3_4_23_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature19800"},{"key":"e_1_3_4_24_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41588-019-0466-z"},{"key":"e_1_3_4_25_2","doi-asserted-by":"publisher","DOI":"10.1159\/000519244"},{"key":"e_1_3_4_26_2","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms5157"},{"key":"e_1_3_4_27_2","doi-asserted-by":"publisher","DOI":"10.1007\/s00412-010-0275-8"},{"key":"e_1_3_4_28_2","doi-asserted-by":"publisher","DOI":"10.1159\/000071608"},{"key":"e_1_3_4_29_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1242544"},{"key":"e_1_3_4_30_2","doi-asserted-by":"publisher","DOI":"10.1126\/sciadv.1602179"},{"key":"e_1_3_4_31_2","doi-asserted-by":"publisher","DOI":"10.1159\/000504313"},{"key":"e_1_3_4_32_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cels.2016.07.002"},{"key":"e_1_3_4_33_2","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btp324"},{"key":"e_1_3_4_34_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2014.11.021"},{"key":"e_1_3_4_35_2","first-page":"1029","article-title":"A fast algorithm for matrix balancing","volume":"33","author":"Knight P. A.","year":"2013","unstructured":"P. A. Knight, D. Ruiz, A fast algorithm for matrix balancing. IMAJNA 33, 1029\u20131047 (2013).","journal-title":"IMAJNA"},{"key":"e_1_3_4_36_2","doi-asserted-by":"publisher","DOI":"10.1101\/gr.212803.116"},{"key":"e_1_3_4_37_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cels.2015.07.012"},{"key":"e_1_3_4_38_2","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btu743"},{"key":"e_1_3_4_39_2","doi-asserted-by":"publisher","DOI":"10.1006\/dbio.2000.9989"}],"container-title":["Proceedings of the National Academy of Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pnas.org\/doi\/pdf\/10.1073\/pnas.2211574119","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,9,21]],"date-time":"2023-09-21T08:38:10Z","timestamp":1695285490000},"score":1,"resource":{"primary":{"URL":"https:\/\/pnas.org\/doi\/10.1073\/pnas.2211574119"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,11,28]]},"references-count":39,"journal-issue":{"issue":"49","published-print":{"date-parts":[[2022,12,6]]}},"alternative-id":["10.1073\/pnas.2211574119"],"URL":"https:\/\/doi.org\/10.1073\/pnas.2211574119","relation":{},"ISSN":["0027-8424","1091-6490"],"issn-type":[{"value":"0027-8424","type":"print"},{"value":"1091-6490","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,11,28]]},"assertion":[{"value":"2022-07-07","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2022-10-17","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2022-11-28","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e2211574119"}}