Heterochiasmy and the establishment of gsdf as a novel sex determining gene in Atlantic halibut
Atlantic Halibut (Hippoglossus hippoglossus) has a X/Y genetic sex determination system, but the sex determining factor is not known. We produced a high-quality genome assembly from a male and identified parts of chromosome 13 as the Y chromosome due to sequence divergence between sexes and segregat...
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| Veröffentlicht in: | PLoS genetics 2022-02, Vol.18 (2), p.e1010011-e1010011 |
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| creator | Edvardsen, Rolf Brudvik Wallerman, Ola Furmanek, Tomasz Kleppe, Lene Jern, Patric Wallberg, Andreas Kjærner-Semb, Erik Mæhle, Stig Olausson, Sara Karolina Sundström, Elisabeth Harboe, Torstein Mangor-Jensen, Ragnfrid Møgster, Margareth Perrichon, Prescilla Norberg, Birgitta Rubin, Carl-Johan |
| description | Atlantic Halibut (Hippoglossus hippoglossus) has a X/Y genetic sex determination system, but the sex determining factor is not known. We produced a high-quality genome assembly from a male and identified parts of chromosome 13 as the Y chromosome due to sequence divergence between sexes and segregation of sex genotypes in pedigrees. Linkage analysis revealed that all chromosomes exhibit heterochiasmy, i.e. male-only and female-only meiotic recombination regions (MRR/FRR). We show that FRR/MRR intervals differ in nucleotide diversity and repeat class content and that this is true also for other Pleuronectidae species. We further show that remnants of a Gypsy-like transposable element insertion on chr13 promotes early male specific expression of gonadal somatic cell derived factor (gsdf). Less than 4.5 MYA, this male-determining element evolved on an autosomal FRR segment featuring pre-existing male meiotic recombination barriers, thereby creating a Y chromosome. Our findings indicate that heterochiasmy may facilitate the evolution of genetic sex determination systems relying on linkage of sexually antagonistic loci to a sex-determining factor. |
| doi_str_mv | 10.1371/journal.pgen.1010011 |
| format | Article |
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We produced a high-quality genome assembly from a male and identified parts of chromosome 13 as the Y chromosome due to sequence divergence between sexes and segregation of sex genotypes in pedigrees. Linkage analysis revealed that all chromosomes exhibit heterochiasmy, i.e. male-only and female-only meiotic recombination regions (MRR/FRR). We show that FRR/MRR intervals differ in nucleotide diversity and repeat class content and that this is true also for other Pleuronectidae species. We further show that remnants of a Gypsy-like transposable element insertion on chr13 promotes early male specific expression of gonadal somatic cell derived factor (gsdf). Less than 4.5 MYA, this male-determining element evolved on an autosomal FRR segment featuring pre-existing male meiotic recombination barriers, thereby creating a Y chromosome. Our findings indicate that heterochiasmy may facilitate the evolution of genetic sex determination systems relying on linkage of sexually antagonistic loci to a sex-determining factor.</description><identifier>ISSN: 1553-7404</identifier><identifier>ISSN: 1553-7390</identifier><identifier>EISSN: 1553-7404</identifier><identifier>DOI: 10.1371/journal.pgen.1010011</identifier><identifier>PMID: 35134055</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Biology and Life Sciences ; Chromosome 13 ; Divergence ; DNA Transposable Elements ; Embryo, Nonmammalian ; Evolution ; Female ; Females ; Fish ; Fish Proteins - genetics ; Flounder - embryology ; Flounder - genetics ; Gender differences ; Gene Expression ; Genetic aspects ; Genetic engineering ; Genetic recombination ; Genome ; Genomes ; Genomics ; Genotypes ; Halibut ; Insertion ; Linkage analysis ; Male ; Males ; Meiosis ; Promoter Regions, Genetic ; Proteins ; Recombination ; Recombination, Genetic ; Repetitive Sequences, Nucleic Acid ; Reptiles & amphibians ; Research and Analysis Methods ; Sex Chromosomes ; Sex determination ; Sex Determination Processes ; Sex determination, Genetic ; Sexes ; Transposons ; Y Chromosome ; Y chromosomes ; Zoological research</subject><ispartof>PLoS genetics, 2022-02, Vol.18 (2), p.e1010011-e1010011</ispartof><rights>COPYRIGHT 2022 Public Library of Science</rights><rights>2022 Edvardsen et al. 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We produced a high-quality genome assembly from a male and identified parts of chromosome 13 as the Y chromosome due to sequence divergence between sexes and segregation of sex genotypes in pedigrees. Linkage analysis revealed that all chromosomes exhibit heterochiasmy, i.e. male-only and female-only meiotic recombination regions (MRR/FRR). We show that FRR/MRR intervals differ in nucleotide diversity and repeat class content and that this is true also for other Pleuronectidae species. We further show that remnants of a Gypsy-like transposable element insertion on chr13 promotes early male specific expression of gonadal somatic cell derived factor (gsdf). Less than 4.5 MYA, this male-determining element evolved on an autosomal FRR segment featuring pre-existing male meiotic recombination barriers, thereby creating a Y chromosome. Our findings indicate that heterochiasmy may facilitate the evolution of genetic sex determination systems relying on linkage of sexually antagonistic loci to a sex-determining factor.</description><subject>Animals</subject><subject>Biology and Life Sciences</subject><subject>Chromosome 13</subject><subject>Divergence</subject><subject>DNA Transposable Elements</subject><subject>Embryo, Nonmammalian</subject><subject>Evolution</subject><subject>Female</subject><subject>Females</subject><subject>Fish</subject><subject>Fish Proteins - genetics</subject><subject>Flounder - embryology</subject><subject>Flounder - genetics</subject><subject>Gender differences</subject><subject>Gene Expression</subject><subject>Genetic aspects</subject><subject>Genetic engineering</subject><subject>Genetic recombination</subject><subject>Genome</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Genotypes</subject><subject>Halibut</subject><subject>Insertion</subject><subject>Linkage analysis</subject><subject>Male</subject><subject>Males</subject><subject>Meiosis</subject><subject>Promoter Regions, Genetic</subject><subject>Proteins</subject><subject>Recombination</subject><subject>Recombination, Genetic</subject><subject>Repetitive Sequences, Nucleic Acid</subject><subject>Reptiles & amphibians</subject><subject>Research and Analysis Methods</subject><subject>Sex Chromosomes</subject><subject>Sex determination</subject><subject>Sex Determination Processes</subject><subject>Sex determination, Genetic</subject><subject>Sexes</subject><subject>Transposons</subject><subject>Y Chromosome</subject><subject>Y chromosomes</subject><subject>Zoological 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and the establishment of gsdf as a novel sex determining gene in Atlantic halibut</title><author>Edvardsen, Rolf Brudvik ; Wallerman, Ola ; Furmanek, Tomasz ; Kleppe, Lene ; Jern, Patric ; Wallberg, Andreas ; Kjærner-Semb, Erik ; Mæhle, Stig ; Olausson, Sara Karolina ; Sundström, Elisabeth ; Harboe, Torstein ; Mangor-Jensen, Ragnfrid ; Møgster, Margareth ; Perrichon, Prescilla ; Norberg, Birgitta ; Rubin, Carl-Johan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c763t-7eb1909c2734380ae0de1e69efa192061ace43e6712e35f248a053bf0af0a6c23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Animals</topic><topic>Biology and Life Sciences</topic><topic>Chromosome 13</topic><topic>Divergence</topic><topic>DNA Transposable Elements</topic><topic>Embryo, Nonmammalian</topic><topic>Evolution</topic><topic>Female</topic><topic>Females</topic><topic>Fish</topic><topic>Fish Proteins - 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Genet</addtitle><date>2022-02-08</date><risdate>2022</risdate><volume>18</volume><issue>2</issue><spage>e1010011</spage><epage>e1010011</epage><pages>e1010011-e1010011</pages><issn>1553-7404</issn><issn>1553-7390</issn><eissn>1553-7404</eissn><abstract>Atlantic Halibut (Hippoglossus hippoglossus) has a X/Y genetic sex determination system, but the sex determining factor is not known. We produced a high-quality genome assembly from a male and identified parts of chromosome 13 as the Y chromosome due to sequence divergence between sexes and segregation of sex genotypes in pedigrees. Linkage analysis revealed that all chromosomes exhibit heterochiasmy, i.e. male-only and female-only meiotic recombination regions (MRR/FRR). We show that FRR/MRR intervals differ in nucleotide diversity and repeat class content and that this is true also for other Pleuronectidae species. We further show that remnants of a Gypsy-like transposable element insertion on chr13 promotes early male specific expression of gonadal somatic cell derived factor (gsdf). Less than 4.5 MYA, this male-determining element evolved on an autosomal FRR segment featuring pre-existing male meiotic recombination barriers, thereby creating a Y chromosome. Our findings indicate that heterochiasmy may facilitate the evolution of genetic sex determination systems relying on linkage of sexually antagonistic loci to a sex-determining factor.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>35134055</pmid><doi>10.1371/journal.pgen.1010011</doi><orcidid>https://orcid.org/0000-0001-8577-9604</orcidid><orcidid>https://orcid.org/0000-0003-1037-7904</orcidid><orcidid>https://orcid.org/0000-0002-1410-878X</orcidid><orcidid>https://orcid.org/0000-0002-9081-9663</orcidid><orcidid>https://orcid.org/0000-0001-8238-5052</orcidid><orcidid>https://orcid.org/0000-0001-8430-8042</orcidid><orcidid>https://orcid.org/0000-0003-1550-5725</orcidid><orcidid>https://orcid.org/0000-0003-3393-5825</orcidid><orcidid>https://orcid.org/0000-0001-9526-8541</orcidid><orcidid>https://orcid.org/0000-0001-7160-6710</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1553-7404 |
| ispartof | PLoS genetics, 2022-02, Vol.18 (2), p.e1010011-e1010011 |
| issn | 1553-7404 1553-7390 1553-7404 |
| language | eng |
| recordid | cdi_plos_journals_2640116613 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; SWEPUB Freely available online; Public Library of Science (PLoS) |
| subjects | Animals Biology and Life Sciences Chromosome 13 Divergence DNA Transposable Elements Embryo, Nonmammalian Evolution Female Females Fish Fish Proteins - genetics Flounder - embryology Flounder - genetics Gender differences Gene Expression Genetic aspects Genetic engineering Genetic recombination Genome Genomes Genomics Genotypes Halibut Insertion Linkage analysis Male Males Meiosis Promoter Regions, Genetic Proteins Recombination Recombination, Genetic Repetitive Sequences, Nucleic Acid Reptiles & amphibians Research and Analysis Methods Sex Chromosomes Sex determination Sex Determination Processes Sex determination, Genetic Sexes Transposons Y Chromosome Y chromosomes Zoological research |
| title | Heterochiasmy and the establishment of gsdf as a novel sex determining gene in Atlantic halibut |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-02T07%3A07%3A52IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Heterochiasmy%20and%20the%20establishment%20of%20gsdf%20as%20a%20novel%20sex%20determining%20gene%20in%20Atlantic%20halibut&rft.jtitle=PLoS%20genetics&rft.au=Edvardsen,%20Rolf%20Brudvik&rft.date=2022-02-08&rft.volume=18&rft.issue=2&rft.spage=e1010011&rft.epage=e1010011&rft.pages=e1010011-e1010011&rft.issn=1553-7404&rft.eissn=1553-7404&rft_id=info:doi/10.1371/journal.pgen.1010011&rft_dat=%3Cgale_plos_%3EA695460953%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2640116613&rft_id=info:pmid/35134055&rft_galeid=A695460953&rft_doaj_id=oai_doaj_org_article_3d73bb22b0ce4159b350b64d31bc151f&rfr_iscdi=true |