{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,23]],"date-time":"2026-03-23T14:50:21Z","timestamp":1774277421402,"version":"3.50.1"},"reference-count":67,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2016,7,18]],"date-time":"2016-07-18T00:00:00Z","timestamp":1468800000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2016,7,18]],"date-time":"2016-07-18T00:00:00Z","timestamp":1468800000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Most mammalian species have heteromorphic sex chromosomes in males, except for a few enigmatic groups such as the mole voles <jats:italic>Ellobius<\/jats:italic>, which do not have the Y chromosome and <jats:italic>Sry<\/jats:italic> gene. The <jats:bold><jats:italic>Ellobius<\/jats:italic><\/jats:bold> (XX \u2640\u2642\"Equation missing\") system of sex chromosomes has no analogues among other animals. The structure and meiotic behaviour of the two X chromosomes were investigated for males of the sibling species <jats:bold><jats:italic>Ellobius<\/jats:italic><\/jats:bold><jats:italic> talpinus<\/jats:italic> and <jats:bold><jats:italic>Ellobius<\/jats:italic><\/jats:bold><jats:italic> tancrei<\/jats:italic>. Their sex chromosomes, despite their identical G-structure, demonstrate short synaptic fragments and crossover-associated MLH1 foci in both telomeric regions only. The chromatin undergoes modifications in the meiotic sex chromosomes. SUMO-1 marks a small nucleolus-like body of the meiotic XX. ATR and ubiH2A are localized in the asynaptic area and the histone \u03b3H2AFX covers the entire XX bivalent. The distribution of some markers of chromatin inactivation differentiates sex chromosomes of mole voles from those of other mammals. Sex chromosomes of both studied species have identical recombination and meiotic inactivation patterns. In <jats:italic>Ellobius<\/jats:italic>, similar chromosome morphology masks the functional heteromorphism of the male sex chromosomes, which can be seen at meiosis.<\/jats:p>","DOI":"10.1038\/srep29949","type":"journal-article","created":{"date-parts":[[2016,7,18]],"date-time":"2016-07-18T09:57:32Z","timestamp":1468835852000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":37,"title":["Unique sex chromosome systems in Ellobius: How do male XX chromosomes recombine and undergo pachytene chromatin inactivation?"],"prefix":"10.1038","volume":"6","author":[{"given":"Sergey","family":"Matveevsky","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Irina","family":"Bakloushinskaya","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Oxana","family":"Kolomiets","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2016,7,18]]},"reference":[{"key":"BFsrep29949_CR1","doi-asserted-by":"crossref","unstructured":"Ohno, S. Sex chromosomes and sex-linked genes. (Springer-Verlag, 1967).","DOI":"10.1007\/978-3-642-88178-7"},{"key":"BFsrep29949_CR2","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1038\/sj.hdy.6800697","volume":"95","author":"D \u0421harlesworth","year":"2005","unstructured":"\u0421harlesworth, D., Charlesworth, B. & Marais, G. Steps in the evolution of heteromorphic sex chromosomes. Heredity 95, 118\u2013128 (2005).","journal-title":"Heredity"},{"key":"BFsrep29949_CR3","doi-asserted-by":"crossref","first-page":"901","DOI":"10.1016\/j.cell.2006.02.024","volume":"124","author":"JAM Graves","year":"2006","unstructured":"Graves, J. A. M. Sex chromosome specialization and degeneration in mammals. Cell 124, 901\u2013914 (2006).","journal-title":"Cell"},{"key":"BFsrep29949_CR4","doi-asserted-by":"crossref","first-page":"331","DOI":"10.2307\/1312947","volume":"46","author":"WR Rice","year":"1996","unstructured":"Rice, W. R. Evolution of the Y sex chromosome in animals. Bioscience 46, 331\u2013343 (1996).","journal-title":"Bioscience"},{"key":"BFsrep29949_CR5","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1038\/346240a0","volume":"346","author":"AH Sinclair","year":"1990","unstructured":"Sinclair, A. H. et al. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346, 240\u2013244 (1990).","journal-title":"Nature"},{"key":"BFsrep29949_CR6","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1038\/351117a0","volume":"351","author":"P Koopman","year":"1991","unstructured":"Koopman, P., Gubbay, J., Vivian, N., Goodfellow, P. & Lovell-Badge, R. Male development of chromosomally female mice transgenic for Sry. Nature 351, 117\u2013121 (1991).","journal-title":"Nature"},{"key":"BFsrep29949_CR7","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1007\/BF00274192","volume":"61","author":"PS Burgoyne","year":"1982","unstructured":"Burgoyne, P. S. Genetic similarity and crossing over in the X and Y chromosomes of humans. Hum. Genet. 61, 85\u201390 (1982).","journal-title":"Hum. Genet."},{"key":"BFsrep29949_CR8","doi-asserted-by":"crossref","unstructured":"Patel, H. R., Delbridge, M. L. & Graves, J. A. M. Organization and evolution of the marsupial X chromosome. In Marsupial Genetics and Genomics (eds Deakin, J. E. et al. ) Ch. 8, 151\u2013171 (Springer, 2010).","DOI":"10.1007\/978-90-481-9023-2_8"},{"key":"BFsrep29949_CR9","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1038\/261225a0","volume":"261","author":"K Fredga","year":"1976","unstructured":"Fredga, K., Gropp, A., Winking, H. & Frank, F. Fertile XX- and XY-type females in the wood lemming Myopus schisticolor. Nature 261, 225\u2013227 (1976).","journal-title":"Nature"},{"key":"BFsrep29949_CR10","first-page":"1049","volume":"277","author":"F Veyrunes","year":"2010","unstructured":"Veyrunes, F. et al. A novel sex determination system in a close relative of the house mouse. Proc Biol Sci 277, 1049\u20131056 (2010).","journal-title":"Proc Biol Sci"},{"key":"BFsrep29949_CR11","doi-asserted-by":"crossref","first-page":"35","DOI":"10.11646\/zootaxa.3493.1.3","volume":"3493","author":"R Castiglia","year":"2012","unstructured":"Castiglia, R. & Annesi, F. Cytotaxonomic considerations on the sex chromosome variation observed within Acomys ngurui Verheyen et al. 2011 (Rodentia, Muridae). Zootaxa 3493, 35\u201338 (2012).","journal-title":"Zootaxa"},{"key":"BFsrep29949_CR12","doi-asserted-by":"crossref","first-page":"43","DOI":"10.3897\/compcytogen.v8i1.6716","volume":"8","author":"ER Steinberg","year":"2014","unstructured":"Steinberg, E. R., Nieves, M. & Mudry, M. D. Multiple sex chromosome systems in howler monkeys (Platyrrhini, Alouatta). Compar Cytogenet 8, 43\u201369 (2014).","journal-title":"Compar Cytogenet"},{"key":"BFsrep29949_CR13","doi-asserted-by":"crossref","first-page":"1197","DOI":"10.1038\/nm.f.1895","volume":"14","author":"MM Matzuk","year":"2008","unstructured":"Matzuk, M. M. & Lamb, D. J. The biology of infertility: research advances and clinical challenges. Nature medicine 14, 1197\u20131213 (2008).","journal-title":"Nature medicine"},{"key":"BFsrep29949_CR14","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1016\/j.fertnstert.2012.06.019","volume":"98","author":"M Maiburg","year":"2012","unstructured":"Maiburg, M., Repping, S. & Giltay, J. The genetic origin of Klinefelter syndrome and its effect on spermatogenesis. Fertil Steril. 98, 253\u2013260 (2012).","journal-title":"Fertil Steril."},{"key":"BFsrep29949_CR15","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1210\/jc.2007-0447","volume":"92","author":"E Vorona","year":"2007","unstructured":"Vorona, E., Zitzmann, M., Gromoll, J., Sch\u00fcring, A. N. & Nieschlag, E. Clinical, endocrinological, and epigenetic features of the 46, XX male syndrome, compared with 47, XXY Klinefelter patients. J Clin Endocrinol Metab. 92, 58\u201365 (2007).","journal-title":"J Clin Endocrinol Metab."},{"key":"BFsrep29949_CR16","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1186\/1750-1172-1-42","volume":"1","author":"J Visootsak","year":"2006","unstructured":"Visootsak, J. & Graham J. M. Klinefelter syndrome and other sex chromosomal aneuploidies. Orphanet J Rare Dis. 1, 42 (2006).","journal-title":"Orphanet J Rare Dis."},{"key":"BFsrep29949_CR17","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1186\/s13039-015-0128-5","volume":"8","author":"I Szczerbal","year":"2015","unstructured":"Szczerbal, I., Stachowiak, M., Dzimira, S., Sliwa, K. & Switonski, M. The first case of 38, XX (SRY-positive) disorder of sex development in a cat. Molec Cytogenet. 8, 22 (2015).","journal-title":"Molec Cytogenet."},{"key":"BFsrep29949_CR18","doi-asserted-by":"crossref","first-page":"685","DOI":"10.1590\/S0004-27302010000800004","volume":"54","author":"C Alves","year":"2010","unstructured":"Alves, C., Braid, Z., Coeli, F. B. & Mello, M. P. D. 46, XX male-testicular disorder of sexual differentiation (DSD): hormonal, molecular and cytogenetic studies. Arq Bras Endocrinol Metabol 54, 685\u2013689 (2010).","journal-title":"Arq Bras Endocrinol Metabol"},{"key":"BFsrep29949_CR19","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1007\/s00412-010-0275-8","volume":"119","author":"A Kuroiwa","year":"2010","unstructured":"Kuroiwa, A., Ishiguchi, Y., Yamada, F., Shintaro, A. & Matsuda, Y. The process of a Y-loss event in an XO\/XO mammal, the Ryukyu spiny rat. Chromosoma 119, 519\u2013526 (2010).","journal-title":"Chromosoma"},{"key":"BFsrep29949_CR20","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1159\/000104771","volume":"1","author":"W Just","year":"2007","unstructured":"Just, W. et al. Ellobius lutescens: sex determination and sex chromosome. Sexual Devel. 1, 211\u2013221 (2007).","journal-title":"Sexual Devel."},{"key":"BFsrep29949_CR21","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1007\/BF00121845","volume":"52\/53","author":"NN Vorontsov","year":"1980","unstructured":"Vorontsov, N. N., Lyapunova, E. A., Borissov, Y. M. & Dovgal, V. E. Variability of sex chromosomes in mammals. Genetica 52\/53, 361\u2013372 (1980).","journal-title":"Genetica"},{"key":"BFsrep29949_CR22","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1007\/BF00127245","volume":"84","author":"OL Kolomiets","year":"1991","unstructured":"Kolomiets, O. L., Vorontsov, N. N., Lyapunova, E. A. & Mazurova, T. F. Ultrastructure, meiotic behavior, and evolution of sex chromosomes of the genus Ellobius. Genetica 84, 179\u2013189 (1991).","journal-title":"Genetica"},{"key":"BFsrep29949_CR23","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1159\/000336459","volume":"136","author":"IYu Bakloushinskaya","year":"2012","unstructured":"Bakloushinskaya, I.Yu. et al. A comparative analysis of the mole vole sibling species Ellobius tancrei and E. talpinus (Cricetidae, Rodentia) through chromosome painting and examination of synaptonemal complex structures in hybrids. Cytogenet Genome Res 136, 199\u2013207 (2012).","journal-title":"Cytogenet Genome Res"},{"key":"BFsrep29949_CR24","doi-asserted-by":"crossref","first-page":"55","DOI":"10.3897\/compcytogen.v4i1.25","volume":"4","author":"OL Kolomiets","year":"2010","unstructured":"Kolomiets, O. L., Matveevsky, S. N. & Bakloushinskaya, I. Y. Sexual dimorphism in prophase I of meiosis in the Northern mole vole (Ellobius talpinus Pallas, 1770) with isomorphic (XX) chromosomes in males and females. Compar Cytogenet 4, 55\u201366 (2010).","journal-title":"Compar Cytogenet"},{"key":"BFsrep29949_CR25","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1016\/S0074-7696(08)60928-6","volume":"38","author":"AJ Solari","year":"1974","unstructured":"Solari, A. J. The behavior of the XY pair in mammals. Int Rev Cytol 38, 273\u2013317 (1974).","journal-title":"Int Rev Cytol"},{"key":"BFsrep29949_CR26","doi-asserted-by":"crossref","first-page":"4097","DOI":"10.1242\/jcs.00111","volume":"115","author":"JM Turner","year":"2002","unstructured":"Turner, J. M. et al. Meiotic sex chromosome inactivation in male mice with targeted disruptions of Xist. J. Cell Sci. 115, 4097\u20134105 (2002).","journal-title":"J. Cell Sci."},{"key":"BFsrep29949_CR27","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1146\/annurev-genet-112414-055145","volume":"49","author":"JM Turner","year":"2015","unstructured":"Turner, J. M. Meiotic silencing in mammals. Annu. Rev. Genet. 49, 395\u2013412 (2015).","journal-title":"Annu. Rev. Genet."},{"key":"BFsrep29949_CR28","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/S0022-5193(88)80022-5","volume":"133","author":"E Jablonka","year":"1988","unstructured":"Jablonka, E. & Lamb, M. J. Meiotic pairing constraints and the activity of sex chromosomes. J Theor Biol 133, 23\u201336 (1988).","journal-title":"J Theor Biol"},{"key":"BFsrep29949_CR29","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1007\/s004120050356","volume":"108","author":"PB Moens","year":"1999","unstructured":"Moens, P. B. et al. The association of ATR protein with mouse meiotic chromosome cores. Chromosoma 108, 95\u2013102 (1999).","journal-title":"Chromosoma"},{"key":"BFsrep29949_CR30","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1038\/85830","volume":"27","author":"SK Mahadevaiah","year":"2001","unstructured":"Mahadevaiah, S. K. et al. Recombinational DNA double-strand breaks in mice precede synapsis. Nat Genet 27, 271\u2013276 (2001).","journal-title":"Nat Genet"},{"key":"BFsrep29949_CR31","doi-asserted-by":"crossref","first-page":"1041","DOI":"10.1128\/MCB.25.3.1041-1053.2005","volume":"25","author":"WM Baarends","year":"2005","unstructured":"Baarends, W. M. et al. Silencing of unpaired chromatin and histone H2A ubiquitination in mammalian meiosis. Mol Cell Biol 25, 1041\u20131053 (2005).","journal-title":"Mol Cell Biol"},{"key":"BFsrep29949_CR32","doi-asserted-by":"crossref","first-page":"2046","DOI":"10.1101\/gad.1214604","volume":"18","author":"G Gill","year":"2004","unstructured":"Gill, G. SUMO and ubiquitin in the nucleus: different functions, similar mechanisms? Genes Dev. 18, 2046\u20132059 (2004).","journal-title":"Genes Dev."},{"key":"BFsrep29949_CR33","doi-asserted-by":"crossref","first-page":"e19255","DOI":"10.1371\/journal.pone.0019255","volume":"6","author":"Q Yang","year":"2011","unstructured":"Yang, Q. et al. Synapsis and meiotic recombination in male Chinese muntjac (Muntiacus reevesi). PLoS One 6, e19255 (2011).","journal-title":"PLoS One"},{"key":"BFsrep29949_CR34","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1007\/s00412-007-0116-6","volume":"116","author":"PD Waters","year":"2007","unstructured":"Waters, P. D., Ruiz-Herrera, A., Dobigny, G., Garcia Caldes, M. & Robinson, T. J. Sex chromosomes of basal placental mammals. Chromosoma 116, 511\u2013518 (2007).","journal-title":"Chromosoma"},{"key":"BFsrep29949_CR35","first-page":"2013","volume":"280","author":"J Segura","year":"2013","unstructured":"Segura, J. et al. Evolution of recombination in eutherian mammals: insights into mechanisms that affect recombination rates and crossover interference. Proc Biol Sci 280, 2013 1945 (2013).","journal-title":"Proc Biol Sci"},{"key":"BFsrep29949_CR36","doi-asserted-by":"crossref","first-page":"1569","DOI":"10.1093\/genetics\/151.4.1569","volume":"151","author":"LK Anderson","year":"1999","unstructured":"Anderson, L. K., Reeves, A., Webb, L. M. & Ashley, T. Distribution of crossing over on mouse synaptonemal complexes using immunofluorescent localization of MLH1 protein. Genetics 151, 1569\u20131579 (1999).","journal-title":"Genetics"},{"key":"BFsrep29949_CR37","doi-asserted-by":"crossref","first-page":"2583","DOI":"10.1093\/hmg\/ddn158","volume":"17","author":"J Lian","year":"2008","unstructured":"Lian, J. et al. Variation in crossover interference levels on individual chromosomes from human males. Hum Mol Genet 17, 2583\u20132594 (2008).","journal-title":"Hum Mol Genet"},{"key":"BFsrep29949_CR38","doi-asserted-by":"crossref","first-page":"1353","DOI":"10.1086\/344714","volume":"71","author":"L Froenicke","year":"2002","unstructured":"Froenicke, L., Anderson, L. K., Wienberg, J. & Ashley, T. Male mouse recombination maps for each autosome identified by chromosome painting. Am J Hum Genet 71, 1353\u20131368 (2002).","journal-title":"Am J Hum Genet"},{"key":"BFsrep29949_CR39","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1159\/000350444","volume":"140","author":"M Vozdova","year":"2013","unstructured":"Vozdova, M. et al. A comparative study of meiotic recombination in cattle (Bos taurus) and three wildebeest species (Connochaetes gnou, C. taurinus taurinus and C. t. albojubatus). Cytogenet Genome Res 140, 36\u201345 (2013).","journal-title":"Cytogenet Genome Res"},{"key":"BFsrep29949_CR40","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1159\/000439452","volume":"146","author":"J Fr\u00f6hlich","year":"2015","unstructured":"Fr\u00f6hlich, J. et al. Variation of meiotic recombination rates and MLH1 foci distribution in spermatocytes of cattle, sheep and goats. Cytogenet Genome Res 146, 211\u2013221 (2015).","journal-title":"Cytogenet Genome Res"},{"key":"BFsrep29949_CR41","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1007\/s13353-014-0193-1","volume":"55","author":"M Vozdova","year":"2014","unstructured":"Vozdova, M. et al. Impact of Robertsonian translocation on meiosis and reproduction: an impala (Aepyceros melampus) model. J Appl Genet 55, 249\u2013258 (2014).","journal-title":"J Appl Genet"},{"key":"BFsrep29949_CR42","doi-asserted-by":"crossref","first-page":"e99123","DOI":"10.1371\/journal.pone.0099123","volume":"9","author":"N Mary","year":"2014","unstructured":"Mary, N. et al. Meiotic recombination analyses of individual chromosomes in male domestic pigs (Sus scrofa domestica). PLoS One 9, e99123 (2014).","journal-title":"PLoS One"},{"key":"BFsrep29949_CR43","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1086\/382138","volume":"74","author":"F Sun","year":"2004","unstructured":"Sun, F. et al. Human male recombination maps for individual chromosomes. Am J Hum Genet 74, 521\u2013531 (2004).","journal-title":"Am J Hum Genet"},{"key":"BFsrep29949_CR44","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1159\/000357152","volume":"142","author":"A Al-Jaru","year":"2014","unstructured":"Al-Jaru, A., Goodwin, W., Skidmore, J. & Khazanehdari, K. Distribution of MLH1 foci in horse male synaptonemal complex. Cytogenet Genome Res 142, 87\u201394 (2014).","journal-title":"Cytogenet Genome Res"},{"key":"BFsrep29949_CR45","doi-asserted-by":"crossref","first-page":"1431","DOI":"10.1101\/gr.6520107","volume":"17","author":"D Homolka","year":"2007","unstructured":"Homolka, D., Ivanek, R., Capkova, J., Jansa, P. & Forejt, J. Chromosomal rearrangement interferes with meiotic X chromosome inactivation. Genome Res 17, 1431\u20131437 (2007).","journal-title":"Genome Res"},{"key":"BFsrep29949_CR46","doi-asserted-by":"crossref","first-page":"2423","DOI":"10.1101\/gad.10.19.2423","volume":"10","author":"KS Keegan","year":"1996","unstructured":"Keegan, K. S. et al. The Atr and Atm protein kinases associate with different sites along meiotically pairing chromosomes. Genes Dev. 10, 2423\u20132437 (1996).","journal-title":"Genes Dev."},{"key":"BFsrep29949_CR47","doi-asserted-by":"crossref","first-page":"2135","DOI":"10.1016\/j.cub.2004.11.032","volume":"14","author":"JM Turner","year":"2004","unstructured":"Turner, J. M. et al. BRCA1, histone H2AX phosphorylation, and male meiotic sex chromosome inactivation. Curr Biol 14, 2135\u20132142 (2004).","journal-title":"Curr Biol"},{"key":"BFsrep29949_CR48","doi-asserted-by":"crossref","first-page":"1376","DOI":"10.1101\/gad.329705","volume":"19","author":"FA de Vries","year":"2005","unstructured":"de Vries, F. A. et al. Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev 19, 1376\u20131389 (2005).","journal-title":"Genes Dev"},{"key":"BFsrep29949_CR49","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1016\/S1534-5807(03)00093-5","volume":"4","author":"O Fernandez-Capetillo","year":"2003","unstructured":"Fernandez-Capetillo, O. et al. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev Cell 4, 497\u2013508 (2003).","journal-title":"Dev Cell"},{"key":"BFsrep29949_CR50","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1038\/ng1484","volume":"37","author":"JM Turner","year":"2005","unstructured":"Turner, J. M. et al. Silencing of unsynapsed meiotic chromosomes in the mouse. Nat Genet 37, 41\u201347 (2005).","journal-title":"Nat Genet"},{"key":"BFsrep29949_CR51","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1007\/s00412-004-0311-7","volume":"113","author":"RS Rogers","year":"2004","unstructured":"Rogers, R. S., Inselman, A., Handel, M. A. & Matunis, M. J. SUMO modified proteins localize to the XY body of pachytene spermatocytes. Chromosoma 113, 233\u2013243 (2004).","journal-title":"Chromosoma"},{"key":"BFsrep29949_CR52","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1016\/j.ydbio.2008.06.020","volume":"321","author":"S La Salle","year":"2008","unstructured":"La Salle, S., Sun, F., Zhang, X. D., Matunis, M. J. & Handel, M. A. Developmental control of sumoylation pathway proteins in mouse male germ cells. Dev Biol 321, 227\u2013237 (2008).","journal-title":"Dev Biol"},{"key":"BFsrep29949_CR53","doi-asserted-by":"crossref","first-page":"1002009","DOI":"10.1371\/journal.pgen.1000625","volume":"5","author":"M Manterola","year":"2009","unstructured":"Manterola, M. et al. A high incidence of meiotic silencing of unsynapsed chromatin is not associated with substantial pachytene loss in heterozygous male mice carrying multiple simple Robertsonian translocations. PLOS Genet 5, 1002009 (2009).","journal-title":"PLOS Genet"},{"key":"BFsrep29949_CR54","unstructured":"Matveevsky, S. N. Signs of sexual dimorphism in meiosis and karyotype variability of mole vole Ellobius (Rodentia, Mammalia). PhD thesis. NI Vavilov Institute of General Genetics of Russian Academy of Science (Moscow, 2011)."},{"key":"BFsrep29949_CR55","first-page":"26","volume":"2","author":"J Cao","year":"2012","unstructured":"Cao, J. & Yan, Q. Histone ubiquitination and deubiquitination in transcription, DNA damage response, and cancer. Front Oncol 2, 26 (2012).","journal-title":"Front Oncol"},{"key":"BFsrep29949_CR56","doi-asserted-by":"crossref","first-page":"1341","DOI":"10.1091\/mbc.5.12.1341","volume":"5","author":"C Richler","year":"1994","unstructured":"Richler, C. et al. Splicing components are excluded from the transcriptionally inactive XY body in male meiotic nuclei. Mol Biol Cell 5, 1341\u20131352 (1994).","journal-title":"Mol Biol Cell"},{"key":"BFsrep29949_CR57","doi-asserted-by":"crossref","first-page":"930","DOI":"10.1038\/nature06944","volume":"453","author":"R Sekido","year":"2008","unstructured":"Sekido, R. & Lovell-Badge, R. Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453, 930\u2013934 (2008).","journal-title":"Nature"},{"key":"BFsrep29949_CR58","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1007\/s10577-011-9269-5","volume":"20","author":"S Bagheri-Fam","year":"2012","unstructured":"Bagheri-Fam, S. et al. Sox9 gene regulation and the loss of the XY\/XX sex-determining mechanism in the mole vole Ellobius lutescens . Chromosome research 20, 191\u2013199 (2012).","journal-title":"Chromosome research"},{"key":"BFsrep29949_CR59","doi-asserted-by":"crossref","first-page":"1891","DOI":"10.1242\/dev.01087","volume":"131","author":"MC Chaboissier","year":"2004","unstructured":"Chaboissier, M. C. et al. Functional analysis of Sox8 and Sox9 during sex determination in the mouse. Development 131, 1891\u20131901 (2004).","journal-title":"Development"},{"key":"BFsrep29949_CR60","doi-asserted-by":"crossref","first-page":"e108779","DOI":"10.1371\/journal.pone.0108779","volume":"9","author":"R Kimura","year":"2014","unstructured":"Kimura, R., Murata, C., Kuroki, Y. & Kuroiwa, A. Mutations in the testis-specific enhancer of SOX9 in the SRY independent sex-determining mechanism in the genus Tokudaia. PLoS ONE 9, e108779 (2014).","journal-title":"PLoS ONE"},{"key":"BFsrep29949_CR61","doi-asserted-by":"crossref","first-page":"026015","DOI":"10.1117\/1.JBO.17.2.026015","volume":"17","author":"NK Reitan","year":"2012","unstructured":"Reitan, N. K., Sporsheim, B., Bj\u00f8rk\u00f8y, A., Strand, S., Davies, C. & de L. Quantitative 3-D colocalization analysis as a tool to study the intracellular trafficking and dissociation of pDNA-chitosan polyplexes. J Biomed Opt 17, 026015 (2012).","journal-title":"J Biomed Opt"},{"key":"BFsrep29949_CR62","doi-asserted-by":"crossref","first-page":"4070","DOI":"10.1523\/JNEUROSCI.0346-04.2004","volume":"24","author":"Q Li","year":"2004","unstructured":"Li, Q. et al. A syntaxin 1, Galpha(o), and N-type calcium channel complex at a presynaptic nerve terminal: analysis by quantitative immunocolocalization. J. Neurosci. 24, 4070\u20134081 (2004).","journal-title":"J. Neurosci."},{"key":"BFsrep29949_CR63","unstructured":"Rasband, W. S. ImageJ. National U. S. Institutes of Health, Bethesda, Maryland, USA. Available at: http:\/\/imagej.nih.gov\/ij\/ (1997\u20132016)."},{"key":"BFsrep29949_CR64","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1038\/nmeth.2089","volume":"9","author":"CA Schneider","year":"2012","unstructured":"Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9, 671\u2013675 (2012).","journal-title":"Nat Methods"},{"key":"BFsrep29949_CR65","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1038\/nprot.2008.31","volume":"3","author":"AP French","year":"2008","unstructured":"French, A. P., Mills, S., Swarup, R., Bennett, M. J. & Pridmore, T. P. Colocalization of fluorescent markers in confocal microscope images of plant cells. Nat Protoc 3, 619\u2013628 (2008).","journal-title":"Nat Protoc"},{"key":"BFsrep29949_CR66","doi-asserted-by":"crossref","first-page":"149","DOI":"10.3389\/fnana.2010.00149","volume":"4","author":"B Barak","year":"2010","unstructured":"Barak, B. et al. Tomosyn expression pattern in the mouse hippocampus suggests both presynaptic and postsynaptic functions. Front Neuroanat 4, 149 (2010).","journal-title":"Front Neuroanat"},{"key":"BFsrep29949_CR67","doi-asserted-by":"crossref","first-page":"2475","DOI":"10.1074\/jbc.M112.432617","volume":"288","author":"S Fargue","year":"2013","unstructured":"Fargue, S., Lewin, J., Rumsby, G. & Danpure, C. J. Four of the most common mutations in primary hyperoxaluria type 1 unmask the cryptic mitochondrial targeting sequence of alanine:glyoxylate aminotransferase encoded by the polymorphic minor allele. J Biol Chem 288, 2475\u20132484 (2013).","journal-title":"J Biol Chem"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/srep29949.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep29949","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep29949.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,5]],"date-time":"2023-01-05T06:39:12Z","timestamp":1672900752000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/srep29949"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,7,18]]},"references-count":67,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2016,7,28]]}},"alternative-id":["BFsrep29949"],"URL":"https:\/\/doi.org\/10.1038\/srep29949","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,7,18]]},"assertion":[{"value":"26 February 2016","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"27 June 2016","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 July 2016","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing financial interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"29949"}}