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Satellitome analysis on the pale-breasted thrush Turdus leucomelas (Passeriformes; Turdidae) uncovers the putative co-evolution of sex chromosomes and satellite DNAs
Do all birds' sex chromosomes follow the same canonical one-way direction of evolution? We combined cytogenetic and genomic approaches to analyze the process of the W chromosomal differentiation in two selected Passeriform species, named the Pale-breasted Thrush Turdus leucomelas and the Rufous...
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description | Do all birds' sex chromosomes follow the same canonical one-way direction of evolution? We combined cytogenetic and genomic approaches to analyze the process of the W chromosomal differentiation in two selected Passeriform species, named the Pale-breasted Thrush
Turdus leucomelas
and the Rufous-bellied thrush
T. rufiventris
. We characterized the full catalog of satellite DNAs (satellitome) of
T. leucomelas
, and the 10 TleSatDNA classes obtained together with 16 microsatellite motifs were in situ mapped in both species. Additionally, using Comparative Genomic Hybridization (CGH) assays, we investigated their intragenomic variations. The W chromosomes of both species did not accumulate higher amounts of both heterochromatin and repetitive sequences. However, while
T. leucomelas
showed a heterochromatin-poor W chromosome with a very complex evolutionary history,
T. rufiventris
showed a small and partially heterochromatic W chromosome that represents a differentiated version of its original autosomal complement (Z chromosome). The combined approach of CGH and sequential satDNA mapping suggest the occurrence of a former W-autosomal translocation event in
T. leucomelas
, which had an impact on the W chromosome in terms of sequence gains and losses. At the same time, an autosome, which is present in both males and females in a polymorphic state, lost sequences and integrated previously W-specific ones. This putative W-autosomal translocation, however, did not result in the emergence of a multiple-sex chromosome system. Instead, the generation of a neo-W chromosome suggests an unexpected evolutionary trajectory that deviates from the standard canonical model of sex chromosome evolution. |
doi_str_mv | 10.1038/s41598-024-71635-5 |
format | article |
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Turdus leucomelas
and the Rufous-bellied thrush
T. rufiventris
. We characterized the full catalog of satellite DNAs (satellitome) of
T. leucomelas
, and the 10 TleSatDNA classes obtained together with 16 microsatellite motifs were in situ mapped in both species. Additionally, using Comparative Genomic Hybridization (CGH) assays, we investigated their intragenomic variations. The W chromosomes of both species did not accumulate higher amounts of both heterochromatin and repetitive sequences. However, while
T. leucomelas
showed a heterochromatin-poor W chromosome with a very complex evolutionary history,
T. rufiventris
showed a small and partially heterochromatic W chromosome that represents a differentiated version of its original autosomal complement (Z chromosome). The combined approach of CGH and sequential satDNA mapping suggest the occurrence of a former W-autosomal translocation event in
T. leucomelas
, which had an impact on the W chromosome in terms of sequence gains and losses. At the same time, an autosome, which is present in both males and females in a polymorphic state, lost sequences and integrated previously W-specific ones. This putative W-autosomal translocation, however, did not result in the emergence of a multiple-sex chromosome system. Instead, the generation of a neo-W chromosome suggests an unexpected evolutionary trajectory that deviates from the standard canonical model of sex chromosome evolution.</description><identifier>ISSN: 2045-2322</identifier><identifier>EISSN: 2045-2322</identifier><identifier>DOI: 10.1038/s41598-024-71635-5</identifier><identifier>PMID: 39232109</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/208/1405 ; 631/208/182 ; 631/208/212 ; Animals ; Chromosomes ; Coevolution ; Comparative Genomic Hybridization ; Cytogenetics ; DNA, Satellite - genetics ; Evolution ; Evolution, Molecular ; Evolutionary genetics ; Female ; Gene mapping ; Genomics ; Heterochromatin ; Heterochromatin - genetics ; Humanities and Social Sciences ; Hybridization ; In Situ Hybridization, Fluorescence ; Male ; Microsatellite Repeats - genetics ; Molecular cytogenetics ; multidisciplinary ; Neo sex chromosomes ; Passeriformes - genetics ; satDNA ; Science ; Science (multidisciplinary) ; Sex chromosomes ; Sex Chromosomes - genetics ; Translocation ; Turdus leucomelas ; W chromosomes ; Z chromosomes</subject><ispartof>Scientific reports, 2024-09, Vol.14 (1), p.20656-14, Article 20656</ispartof><rights>The Author(s) 2024</rights><rights>2024. The Author(s).</rights><rights>The Author(s) 2024. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>The Author(s) 2024 2024</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c422t-f1edc19008570423867233968bca6aa91c3b6f7e69533bef4fac8ec8bc3c13413</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/3100711591/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/3100711591?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39232109$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Souza, Guilherme Mota</creatorcontrib><creatorcontrib>Kretschmer, Rafael</creatorcontrib><creatorcontrib>Toma, Gustavo Akira</creatorcontrib><creatorcontrib>de Oliveira, Alan Moura</creatorcontrib><creatorcontrib>Deon, Geize Aparecida</creatorcontrib><creatorcontrib>Setti, Princia Grejo</creatorcontrib><creatorcontrib>Zeni dos Santos, Rodrigo</creatorcontrib><creatorcontrib>Goes, Caio Augusto Gomes</creatorcontrib><creatorcontrib>Del Valle Garnero, Analía</creatorcontrib><creatorcontrib>Gunski, Ricardo José</creatorcontrib><creatorcontrib>de Oliveira, Edivaldo Herculano Correa</creatorcontrib><creatorcontrib>Porto-Foresti, Fabio</creatorcontrib><creatorcontrib>Liehr, Thomas</creatorcontrib><creatorcontrib>Utsunomia, Ricardo</creatorcontrib><creatorcontrib>de Bello Cioffi, Marcelo</creatorcontrib><title>Satellitome analysis on the pale-breasted thrush Turdus leucomelas (Passeriformes; Turdidae) uncovers the putative co-evolution of sex chromosomes and satellite DNAs</title><title>Scientific reports</title><addtitle>Sci Rep</addtitle><addtitle>Sci Rep</addtitle><description>Do all birds' sex chromosomes follow the same canonical one-way direction of evolution? We combined cytogenetic and genomic approaches to analyze the process of the W chromosomal differentiation in two selected Passeriform species, named the Pale-breasted Thrush
Turdus leucomelas
and the Rufous-bellied thrush
T. rufiventris
. We characterized the full catalog of satellite DNAs (satellitome) of
T. leucomelas
, and the 10 TleSatDNA classes obtained together with 16 microsatellite motifs were in situ mapped in both species. Additionally, using Comparative Genomic Hybridization (CGH) assays, we investigated their intragenomic variations. The W chromosomes of both species did not accumulate higher amounts of both heterochromatin and repetitive sequences. However, while
T. leucomelas
showed a heterochromatin-poor W chromosome with a very complex evolutionary history,
T. rufiventris
showed a small and partially heterochromatic W chromosome that represents a differentiated version of its original autosomal complement (Z chromosome). The combined approach of CGH and sequential satDNA mapping suggest the occurrence of a former W-autosomal translocation event in
T. leucomelas
, which had an impact on the W chromosome in terms of sequence gains and losses. At the same time, an autosome, which is present in both males and females in a polymorphic state, lost sequences and integrated previously W-specific ones. This putative W-autosomal translocation, however, did not result in the emergence of a multiple-sex chromosome system. Instead, the generation of a neo-W chromosome suggests an unexpected evolutionary trajectory that deviates from the standard canonical model of sex chromosome evolution.</description><subject>631/208/1405</subject><subject>631/208/182</subject><subject>631/208/212</subject><subject>Animals</subject><subject>Chromosomes</subject><subject>Coevolution</subject><subject>Comparative Genomic Hybridization</subject><subject>Cytogenetics</subject><subject>DNA, Satellite - genetics</subject><subject>Evolution</subject><subject>Evolution, Molecular</subject><subject>Evolutionary genetics</subject><subject>Female</subject><subject>Gene mapping</subject><subject>Genomics</subject><subject>Heterochromatin</subject><subject>Heterochromatin - genetics</subject><subject>Humanities and Social Sciences</subject><subject>Hybridization</subject><subject>In Situ Hybridization, Fluorescence</subject><subject>Male</subject><subject>Microsatellite Repeats - genetics</subject><subject>Molecular cytogenetics</subject><subject>multidisciplinary</subject><subject>Neo sex chromosomes</subject><subject>Passeriformes - genetics</subject><subject>satDNA</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Sex chromosomes</subject><subject>Sex Chromosomes - genetics</subject><subject>Translocation</subject><subject>Turdus leucomelas</subject><subject>W chromosomes</subject><subject>Z chromosomes</subject><issn>2045-2322</issn><issn>2045-2322</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNp9kk1v1DAQhiMEolXpH-CALHFpDwF_JrE4oKp8VaoAiXK2HGey61U2Xjzxiv4g_ifezVJaDvhia-adZ8b2WxTPGX3FqGheo2RKNyXlsqxZJVSpHhXHnEpVcsH543vno-IUcUXzUlxLpp8WR0LnBKP6uPj1zU4wDH4KayB2tMMteiRhJNMSyMYOULYRLE7Q5UhMuCQ3KXYJyQDJ5ZrBIjn7ahEh-j7ENeCbvcJ3Fs5JGl3YQsSZliY7-S0QF0rYhiFNPvcJPUH4SdwyhnXATMQ8RkfwMBaQd58v8FnxpLcDwulhPym-f3h_c_mpvP7y8ery4rp0kvOp7Bl0jmlKG1VTyUVT1VwIXTWts5W1mjnRVn0NlVZCtNDL3roGXE4Lx4Rk4qS4mrldsCuziX5t460J1pt9IMSFsXHybgADspYtb1wreis5OM2VqFk-KmgboXestzNrk9p1ngvGKdrhAfRhZvRLswhbw5ioVf7iTDg7EGL4kQAns_bo8rPYEUJCIxilmmUf7Jq9_Ee6Cinm75xVNctm2an4rHIxIEbo76Zh1OxcZWZXmewqs3eVUbnoxf173JX88VAWiFmAOTUuIP7t_R_sb3Ew2zI</recordid><startdate>20240904</startdate><enddate>20240904</enddate><creator>Souza, Guilherme Mota</creator><creator>Kretschmer, Rafael</creator><creator>Toma, Gustavo Akira</creator><creator>de Oliveira, Alan Moura</creator><creator>Deon, Geize Aparecida</creator><creator>Setti, Princia Grejo</creator><creator>Zeni dos Santos, Rodrigo</creator><creator>Goes, Caio Augusto Gomes</creator><creator>Del Valle Garnero, Analía</creator><creator>Gunski, Ricardo José</creator><creator>de Oliveira, Edivaldo Herculano Correa</creator><creator>Porto-Foresti, Fabio</creator><creator>Liehr, Thomas</creator><creator>Utsunomia, Ricardo</creator><creator>de Bello Cioffi, Marcelo</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><general>Nature Portfolio</general><scope>C6C</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20240904</creationdate><title>Satellitome analysis on the pale-breasted thrush Turdus leucomelas (Passeriformes; Turdidae) uncovers the putative co-evolution of sex chromosomes and satellite DNAs</title><author>Souza, Guilherme Mota ; Kretschmer, Rafael ; Toma, Gustavo Akira ; de Oliveira, Alan Moura ; Deon, Geize Aparecida ; Setti, Princia Grejo ; Zeni dos Santos, Rodrigo ; Goes, Caio Augusto Gomes ; Del Valle Garnero, Analía ; Gunski, Ricardo José ; de Oliveira, Edivaldo Herculano Correa ; Porto-Foresti, Fabio ; Liehr, Thomas ; Utsunomia, Ricardo ; de Bello Cioffi, Marcelo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c422t-f1edc19008570423867233968bca6aa91c3b6f7e69533bef4fac8ec8bc3c13413</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>631/208/1405</topic><topic>631/208/182</topic><topic>631/208/212</topic><topic>Animals</topic><topic>Chromosomes</topic><topic>Coevolution</topic><topic>Comparative Genomic Hybridization</topic><topic>Cytogenetics</topic><topic>DNA, Satellite - genetics</topic><topic>Evolution</topic><topic>Evolution, Molecular</topic><topic>Evolutionary genetics</topic><topic>Female</topic><topic>Gene mapping</topic><topic>Genomics</topic><topic>Heterochromatin</topic><topic>Heterochromatin - genetics</topic><topic>Humanities and Social Sciences</topic><topic>Hybridization</topic><topic>In Situ Hybridization, Fluorescence</topic><topic>Male</topic><topic>Microsatellite Repeats - genetics</topic><topic>Molecular cytogenetics</topic><topic>multidisciplinary</topic><topic>Neo sex chromosomes</topic><topic>Passeriformes - genetics</topic><topic>satDNA</topic><topic>Science</topic><topic>Science (multidisciplinary)</topic><topic>Sex chromosomes</topic><topic>Sex Chromosomes - genetics</topic><topic>Translocation</topic><topic>Turdus leucomelas</topic><topic>W chromosomes</topic><topic>Z chromosomes</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Souza, Guilherme Mota</creatorcontrib><creatorcontrib>Kretschmer, Rafael</creatorcontrib><creatorcontrib>Toma, Gustavo Akira</creatorcontrib><creatorcontrib>de Oliveira, Alan Moura</creatorcontrib><creatorcontrib>Deon, Geize Aparecida</creatorcontrib><creatorcontrib>Setti, Princia Grejo</creatorcontrib><creatorcontrib>Zeni dos Santos, Rodrigo</creatorcontrib><creatorcontrib>Goes, Caio Augusto Gomes</creatorcontrib><creatorcontrib>Del Valle Garnero, Analía</creatorcontrib><creatorcontrib>Gunski, Ricardo José</creatorcontrib><creatorcontrib>de Oliveira, Edivaldo Herculano Correa</creatorcontrib><creatorcontrib>Porto-Foresti, Fabio</creatorcontrib><creatorcontrib>Liehr, Thomas</creatorcontrib><creatorcontrib>Utsunomia, Ricardo</creatorcontrib><creatorcontrib>de Bello Cioffi, Marcelo</creatorcontrib><collection>SpringerOpen</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biological Sciences</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>ProQuest Science Journals</collection><collection>ProQuest Biological Science Journals</collection><collection>Publicly Available Content (ProQuest)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Scientific reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Souza, Guilherme Mota</au><au>Kretschmer, Rafael</au><au>Toma, Gustavo Akira</au><au>de Oliveira, Alan Moura</au><au>Deon, Geize Aparecida</au><au>Setti, Princia Grejo</au><au>Zeni dos Santos, Rodrigo</au><au>Goes, Caio Augusto Gomes</au><au>Del Valle Garnero, Analía</au><au>Gunski, Ricardo José</au><au>de Oliveira, Edivaldo Herculano Correa</au><au>Porto-Foresti, Fabio</au><au>Liehr, Thomas</au><au>Utsunomia, Ricardo</au><au>de Bello Cioffi, Marcelo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Satellitome analysis on the pale-breasted thrush Turdus leucomelas (Passeriformes; Turdidae) uncovers the putative co-evolution of sex chromosomes and satellite DNAs</atitle><jtitle>Scientific reports</jtitle><stitle>Sci Rep</stitle><addtitle>Sci Rep</addtitle><date>2024-09-04</date><risdate>2024</risdate><volume>14</volume><issue>1</issue><spage>20656</spage><epage>14</epage><pages>20656-14</pages><artnum>20656</artnum><issn>2045-2322</issn><eissn>2045-2322</eissn><abstract>Do all birds' sex chromosomes follow the same canonical one-way direction of evolution? We combined cytogenetic and genomic approaches to analyze the process of the W chromosomal differentiation in two selected Passeriform species, named the Pale-breasted Thrush
Turdus leucomelas
and the Rufous-bellied thrush
T. rufiventris
. We characterized the full catalog of satellite DNAs (satellitome) of
T. leucomelas
, and the 10 TleSatDNA classes obtained together with 16 microsatellite motifs were in situ mapped in both species. Additionally, using Comparative Genomic Hybridization (CGH) assays, we investigated their intragenomic variations. The W chromosomes of both species did not accumulate higher amounts of both heterochromatin and repetitive sequences. However, while
T. leucomelas
showed a heterochromatin-poor W chromosome with a very complex evolutionary history,
T. rufiventris
showed a small and partially heterochromatic W chromosome that represents a differentiated version of its original autosomal complement (Z chromosome). The combined approach of CGH and sequential satDNA mapping suggest the occurrence of a former W-autosomal translocation event in
T. leucomelas
, which had an impact on the W chromosome in terms of sequence gains and losses. At the same time, an autosome, which is present in both males and females in a polymorphic state, lost sequences and integrated previously W-specific ones. This putative W-autosomal translocation, however, did not result in the emergence of a multiple-sex chromosome system. Instead, the generation of a neo-W chromosome suggests an unexpected evolutionary trajectory that deviates from the standard canonical model of sex chromosome evolution.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>39232109</pmid><doi>10.1038/s41598-024-71635-5</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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source | Publicly Available Content (ProQuest); PubMed Central; Free Full-Text Journals in Chemistry; Springer Nature - nature.com Journals - Fully Open Access |
subjects | 631/208/1405 631/208/182 631/208/212 Animals Chromosomes Coevolution Comparative Genomic Hybridization Cytogenetics DNA, Satellite - genetics Evolution Evolution, Molecular Evolutionary genetics Female Gene mapping Genomics Heterochromatin Heterochromatin - genetics Humanities and Social Sciences Hybridization In Situ Hybridization, Fluorescence Male Microsatellite Repeats - genetics Molecular cytogenetics multidisciplinary Neo sex chromosomes Passeriformes - genetics satDNA Science Science (multidisciplinary) Sex chromosomes Sex Chromosomes - genetics Translocation Turdus leucomelas W chromosomes Z chromosomes |
title | Satellitome analysis on the pale-breasted thrush Turdus leucomelas (Passeriformes; Turdidae) uncovers the putative co-evolution of sex chromosomes and satellite DNAs |
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