{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,12]],"date-time":"2025-10-12T03:47:46Z","timestamp":1760240866579,"version":"build-2065373602"},"reference-count":43,"publisher":"MDPI AG","issue":"20","license":[{"start":{"date-parts":[[2019,10,15]],"date-time":"2019-10-15T00:00:00Z","timestamp":1571097600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Spanish Ministerio de Ciencia e Innovaci\u00f3n","award":["RTI2018-096847-B-C21","AGL2014- 51860-C2-1-P"],"award-info":[{"award-number":["RTI2018-096847-B-C21","AGL2014- 51860-C2-1-P"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Solea senegalensis is a flatfish belonging to the Soleidae family within the Pleuronectiformes order. It has a karyotype of 2n = 42 (FN = 60; 6M + 4 SM + 8 St + 24 T) and a XX\/XY system. The first pair of metacentric chromosomes has been proposed as a proto sex-chromosome originated by a Robertsonian fusion between acrocentric chromosomes. In order to elucidate a possible evolutionary origin of this chromosome 1, studies of genomic synteny were carried out with eight fish species. A total of 88 genes annotated within of 14 BACs located in the chromosome 1 of S. senegalensis were used to elaborate syntenic maps. Six BACs (BAC5K5, BAC52C17, BAC53B20, BAC84K7, BAC56H24, and BAC48P7) were distributed in, at least, 5 chromosomes in the species studied, and a group of four genes from BAC53B20 (grsf1, rufy3, slc4a4 and npffr2) and genes from BAC48K7 (dmrt2, dmrt3, dmrt1, c9orf117, kank1 and fbp1) formed a conserved cluster in all species. The analysis of repetitive sequences showed that the number of retroelements and simple repeat per BAC showed its highest value in the subcentromeric region where 53B20, 16E16 and 48K7 BACs were localized. This region contains all the dmrt genes, which are associated with sex determination in some species. In addition, the presence of a satellite \u201cchromosome Y\u201d (motif length: 860 bp) was detected in this region. These findings allowed to trace an evolutionary trend for the large metacentric chromosome of S. senegalensis, throughout different rearrangements, which could be at an initial phase of differentiation as sex chromosome.<\/jats:p>","DOI":"10.3390\/ijms20205111","type":"journal-article","created":{"date-parts":[[2019,10,16]],"date-time":"2019-10-16T03:32:54Z","timestamp":1571196774000},"page":"5111","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":12,"title":["Evolution of the Proto Sex-Chromosome in Solea senegalensis"],"prefix":"10.3390","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4475-2170","authenticated-orcid":false,"given":"Mar\u00eda","family":"Rodr\u00edguez","sequence":"first","affiliation":[{"name":"\u00c1rea de Gen\u00e9tica, Facultad de Ciencias del Mar y Ambientales, INMAR, Universidad de C\u00e1diz, 11510 C\u00e1diz, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Bel\u00e9n","family":"Molina","sequence":"additional","affiliation":[{"name":"\u00c1rea de Gen\u00e9tica, Facultad de Ciencias del Mar y Ambientales, INMAR, Universidad de C\u00e1diz, 11510 C\u00e1diz, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Manuel","family":"Merlo","sequence":"additional","affiliation":[{"name":"\u00c1rea de Gen\u00e9tica, Facultad de Ciencias del Mar y Ambientales, INMAR, Universidad de C\u00e1diz, 11510 C\u00e1diz, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8967-4519","authenticated-orcid":false,"given":"Alberto","family":"Arias-P\u00e9rez","sequence":"additional","affiliation":[{"name":"\u00c1rea de Gen\u00e9tica, Facultad de Ciencias del Mar y Ambientales, INMAR, Universidad de C\u00e1diz, 11510 C\u00e1diz, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5269-2182","authenticated-orcid":false,"given":"Silvia","family":"Portela-Bens","sequence":"additional","affiliation":[{"name":"\u00c1rea de Gen\u00e9tica, Facultad de Ciencias del Mar y Ambientales, INMAR, Universidad de C\u00e1diz, 11510 C\u00e1diz, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Aglaya","family":"Garc\u00eda-Angulo","sequence":"additional","affiliation":[{"name":"\u00c1rea de Gen\u00e9tica, Facultad de Ciencias del Mar y Ambientales, INMAR, Universidad de C\u00e1diz, 11510 C\u00e1diz, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ismael","family":"Cross","sequence":"additional","affiliation":[{"name":"\u00c1rea de Gen\u00e9tica, Facultad de Ciencias del Mar y Ambientales, INMAR, Universidad de C\u00e1diz, 11510 C\u00e1diz, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1672-3054","authenticated-orcid":false,"given":"Thomas","family":"Liehr","sequence":"additional","affiliation":[{"name":"Molcular Cytogenetics, University Clinic Jena Institute of Human Genetics, 07747 Jena, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Laureana","family":"Rebordinos","sequence":"additional","affiliation":[{"name":"\u00c1rea de Gen\u00e9tica, Facultad de Ciencias del Mar y Ambientales, INMAR, Universidad de C\u00e1diz, 11510 C\u00e1diz, Spain"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2019,10,15]]},"reference":[{"key":"ref_1","unstructured":"Nelson, J.S. (2006). Fishes of the World, John Willey & Sons, Inc.. [4th ed.]."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1007\/s00412-017-0648-3","article-title":"Tracking the evolutionary pathway of sex chromosomes among fishes: Characterizing the unique XX\/XY1Y2 system in Hoplias malabaricus (Teleostei, Characiformes)","volume":"127","author":"Sember","year":"2018","journal-title":"Chromosoma"},{"key":"ref_3","first-page":"217","article-title":"Centromeric satellite DNA in flatfish (order Pleuronectiformes) and its relation to speciation processes","volume":"108","author":"Robles","year":"2017","journal-title":"J. Hered."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1038\/ng.2890","article-title":"Whole-genome sequenced of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle","volume":"46","author":"Chen","year":"2014","journal-title":"Nat. Genet."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1007\/s10126-014-9589-5","article-title":"First haploid genetic map base don microsatellite markers in Senegalense sole (Solea senegalensis, Kaup, 1858)","volume":"17","author":"Hermida","year":"2015","journal-title":"Mar. Biotecnol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1038\/s41467-018-08014-y","article-title":"The evolution of sex determination associated with a chromosomal inversion","volume":"10","author":"Natri","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_7","first-page":"340","article-title":"Genetic architecture of sex determination in fish: Applications to sex ratio control in aquaculture","volume":"5","author":"Ribas","year":"2014","journal-title":"Front. Genet."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1016\/j.ygcen.2015.10.004","article-title":"Evolution of the sex-determining gene in teleostean genus Oryzias","volume":"239","author":"Matsuda","year":"2016","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"4157","DOI":"10.1038\/ncomms5157","article-title":"Co-option of sox3 as the male-determining factor on the Y chromosome in fish Oryzias dancena","volume":"5","author":"Takehana","year":"2014","journal-title":"Nat. Commun."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2955","DOI":"10.1073\/pnas.1018392109","article-title":"A Y-linked anti-M\u00fcllerian hormone duplication takes over a critical role in sex determination","volume":"109","author":"Hattori","year":"2012","journal-title":"Proc. Nat. Acad. Sci. USA"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Kamiya, T., Kai, W., Tasumi, S., Oka, A., Matsunaga, T., Mizuno, N., Fujita, M., Suetake, H., Suzuki, S., and Hosoya, S. (2012). A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (fugu). PLoS Genet., 8.","DOI":"10.1371\/journal.pgen.1002798"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"486","DOI":"10.1111\/eva.12032","article-title":"The sexually dimorphic on the Y-chromosome gene (sdY) is a conserved male-specific Y-chromosome sequence in many salmonids","volume":"6","author":"Yano","year":"2013","journal-title":"Evol. Appl."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Pennell, M.W., Kirkpatrick, M., Otto, S.P., Vamosi, J.C., Peichel, C.L., Valenzuela, N., and Kitano, J. (2015). Y fuse? Sex chromosome fusions in fishes and reptiles. PLoS Genet., 11.","DOI":"10.1371\/journal.pgen.1005237"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Xu, D., Sember, A., Zhu, Q., De Oliveira, E.A., Liehr, T., Al-Rikabi, A.B.H., Xiao, Z., Song, H., and Cioffi, M.B. (2019). Deciphering the origin and evolution of the X1X2Y system in two closely-related Oplegnathus species (Oplegnathidae and Centrarchiformes). Int. J. Mol Sci., 20.","DOI":"10.3390\/ijms20143571"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1007\/s00412-016-0589-2","article-title":"Integrated gene mapping and synteny studies give insights into the evolution of a sex proto-chromosome in Solea senegalensis","volume":"126","author":"Merlo","year":"2017","journal-title":"Chromosoma"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Garc\u00eda-Angulo, A., Merlo, M.A., Portela-Bens, S., Rodr\u00edguez, M.E., Garc\u00eda, E., Al-Rikabi, A., Liehr, T., and Rebordinos, L. (2018). Evidence for a Robertsonian fusion in Solea senegalensis (Kaup, 1858) revealed by zoo-FISH and comparative genome analysis. BMC Genomics, 19.","DOI":"10.1186\/s12864-018-5216-6"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1007\/s00412-015-0569-y","article-title":"Dynamics of vertebrate sex chromosome evolution: From equal size to giants and dwarfs","volume":"125","author":"Schartl","year":"2016","journal-title":"Chromosoma"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1016\/j.gene.2012.04.062","article-title":"Swimy locus on Y chromosome of the platyfish (Xiphophorus maculatus) is derived from a novel DNA transposon Zisupton","volume":"503","author":"Zhou","year":"2012","journal-title":"Gene"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1007\/s10577-015-9490-8","article-title":"Transposable elements and early evolution of sex chromosome in fish","volume":"23","author":"Chalopin","year":"2015","journal-title":"Chromosome Res."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"2173","DOI":"10.1534\/genetics.108.088559","article-title":"Molecular cytogenetic evidence of rearrangements on the Y chromosome of the threespine stickleback fish","volume":"179","author":"Ross","year":"2008","journal-title":"Genetics"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1038\/nature751","article-title":"DMY is a Y-specific DM-domain gene required for male development in the medaka fish","volume":"417","author":"Matsuda","year":"2002","journal-title":"Nature"},{"key":"ref_22","first-page":"245","article-title":"Caracterizaciones citogen\u00e9tica e isoenzim\u00e1tica del lengauado Solea senegalensis Kaup, 1858","volume":"18","author":"Vega","year":"2002","journal-title":"Bol. Inst. Esp. Oceanogr."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1139\/gen-2016-0143","article-title":"Analysis of the histone cluster in Senegalese sole (Solea senegalensis): Evidence for a divergent evolution of two canonical histone cluster","volume":"60","author":"Merlo","year":"2017","journal-title":"Genome"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1534\/genetics.111.127324","article-title":"Genome evolution and meiotic maps by massively parallel DNA sequencing: Spotted gar, an outgroup for the teleost genome duplication","volume":"188","author":"Amores","year":"2011","journal-title":"Genetics"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Harrington, R.C., Faircloth, B.C., Eytan, R.I., Smith, W.L., Near, T.J., Alfaro, M.E., and Friedman, M. (2016). Phylogenomic analysis of carangimorph fishes reveals flatfish asymmetry arose in blink of evolutionary eye. BMC Evol. Biol., 16.","DOI":"10.1186\/s12862-016-0786-x"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Shi, W., Chen, S., Kong, X., Si, L., Gong, L., Zhang, Y., and Yu, H. (2018). Flatfish monophyly refereed by the relationship of Psettodes in Carangimorphariae. BMC Genom., 19.","DOI":"10.1186\/s12864-018-4788-5"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1038\/ng.3526","article-title":"The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons","volume":"48","author":"Braasch","year":"2016","journal-title":"Nat. Genet."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"602","DOI":"10.1093\/oxfordjournals.molbev.a026142","article-title":"Distribution of dinucleotide microsatellites in the Drosophila melanogaster genome","volume":"16","author":"Bachtrog","year":"1999","journal-title":"Mol. Biol. Evol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1139\/G08-024","article-title":"Microsatellite accumulation on the Y chromosome in Silene latifolia","volume":"51","author":"Kubat","year":"2008","journal-title":"Genome"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1038\/hdy.2009.17","article-title":"The role of repetitive DNA in structure and evolution of sex chromosomes in plants","volume":"103","author":"Kejnovsky","year":"2009","journal-title":"Heredity"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Kejnovsk\u00fd, E., Michalovova, M., Steflova, P., Kejnovska, I., Manzano, S., Hobza, R., Kubat, Z., Kovarik, J., Jamilena, M., and Vyskot, B. (2013). Expansion of microsatellites on evolutionary young Y chromosome. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0045519"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"6470","DOI":"10.1073\/pnas.93.13.6470","article-title":"Microsatellite spreading in the human genome: Evolutionary mechanisms and structural implications","volume":"93","author":"Nadir","year":"1996","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2038","DOI":"10.1101\/gr.122937.111","article-title":"A matter of life or death: How microsatellites emerge in and vanish from the human genome","volume":"21","author":"Kelkar","year":"2011","journal-title":"Genome Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1441","DOI":"10.1101\/gr.184001","article-title":"Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): Frequency, length variation, transposon association, and genetic marker potential","volume":"11","author":"Temnykh","year":"2001","journal-title":"Genome Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"194","DOI":"10.1038\/ng822","article-title":"Microsatellites are preferentially associated with nonrepetitive DNA in plant genomes","volume":"30","author":"Morgante","year":"2002","journal-title":"Nat. Genet."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1534\/genetics.114.161158","article-title":"Genetics of sexual development: An evolutionary playground for fish","volume":"196","author":"Heule","year":"2014","journal-title":"Genetics"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1016\/S0168-9525(02)02666-5","article-title":"The rise and fall of SRY","volume":"18","author":"Graves","year":"2002","journal-title":"Trends Genet."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"6472","DOI":"10.1073\/pnas.0609054104","article-title":"Gene organization of the liverworth Y chromosome reveals distinct sex chromosom evolution in a haploid system","volume":"104","author":"Yamato","year":"2007","journal-title":"Proc. Natl Acad Sci USA"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1038\/371215a0","article-title":"The evolutionary dynamics of repetitive DNA in eukaryotes","volume":"371","author":"Charlesworth","year":"1994","journal-title":"Nature"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/S0378-1119(97)00044-9","article-title":"Human BAC library: Construction and rapid screening","volume":"191","author":"Asakawa","year":"1997","journal-title":"Gene"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1159\/000355001","article-title":"A preliminary genetic map in Solea senegalensis (Pleuronectiformes, Soleidae) using BAC-FISH and next-generation sequencing","volume":"141","author":"Merlo","year":"2013","journal-title":"Cytogenet. Genome Res."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1647","DOI":"10.1093\/bioinformatics\/bts199","article-title":"Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data","volume":"28","author":"Kearse","year":"2012","journal-title":"Bioinformatics"},{"key":"ref_43","unstructured":"Smit, A.F.A., Hubley, R., and Green, P. (2018, May 24). RepeatMasker Open-4.0. (2013\u20132015). Available online: http:\/\/www.repeatmasker.org."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/20\/20\/5111\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:26:29Z","timestamp":1760189189000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/20\/20\/5111"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,10,15]]},"references-count":43,"journal-issue":{"issue":"20","published-online":{"date-parts":[[2019,10]]}},"alternative-id":["ijms20205111"],"URL":"https:\/\/doi.org\/10.3390\/ijms20205111","relation":{},"ISSN":["1422-0067"],"issn-type":[{"type":"electronic","value":"1422-0067"}],"subject":[],"published":{"date-parts":[[2019,10,15]]}}}