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Long-term persistence of supernumerary B chromosomes in multiple species of Astyanax fish
Eukaryote genomes frequently harbor supernumerary B chromosomes in addition to the "standard" A chromosome set. B chromosomes are thought to arise as byproducts of genome rearrangements and have mostly been considered intraspecific oddities. However, their evolutionary transcendence beyond...
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Published in: | BMC biology 2021-03, Vol.19 (1), p.52-52, Article 52 |
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creator | Silva, Duílio Mazzoni Zerbinato de Andrade Ruiz-Ruano, Francisco J Utsunomia, Ricardo Martín-Peciña, María Castro, Jonathan Pena Freire, Paula Paccielli Carvalho, Robson Francisco Hashimoto, Diogo T Suh, Alexander Oliveira, Claudio Porto-Foresti, Fábio Artoni, Roberto Ferreira Foresti, Fausto Camacho, Juan Pedro M |
description | Eukaryote genomes frequently harbor supernumerary B chromosomes in addition to the "standard" A chromosome set. B chromosomes are thought to arise as byproducts of genome rearrangements and have mostly been considered intraspecific oddities. However, their evolutionary transcendence beyond species level has remained untested.
Here we reveal that the large metacentric B chromosomes reported in several fish species of the genus Astyanax arose in a common ancestor at least 4 million years ago. We generated transcriptomes of A. scabripinnis and A. paranae 0B and 1B individuals and used these assemblies as a reference for mapping all gDNA and RNA libraries to quantify coverage differences between B-lacking and B-carrying genomes. We show that the B chromosomes of A. scabripinnis and A. paranae share 19 protein-coding genes, of which 14 and 11 were also present in the B chromosomes of A. bockmanni and A. fasciatus, respectively. Our search for B-specific single-nucleotide polymorphisms (SNPs) identified the presence of B-derived transcripts in B-carrying ovaries, 80% of which belonged to nobox, a gene involved in oogenesis regulation. Importantly, the B chromosome nobox paralog is expressed > 30× more than the A chromosome paralog. This indicates that the normal regulation of this gene is altered in B-carrying females, which could potentially facilitate B inheritance at higher rates than Mendelian law prediction.
Taken together, our results demonstrate the long-term survival of B chromosomes despite their lack of regular pairing and segregation during meiosis and that they can endure episodes of population divergence leading to species formation. |
doi_str_mv | 10.1186/s12915-021-00991-9 |
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Here we reveal that the large metacentric B chromosomes reported in several fish species of the genus Astyanax arose in a common ancestor at least 4 million years ago. We generated transcriptomes of A. scabripinnis and A. paranae 0B and 1B individuals and used these assemblies as a reference for mapping all gDNA and RNA libraries to quantify coverage differences between B-lacking and B-carrying genomes. We show that the B chromosomes of A. scabripinnis and A. paranae share 19 protein-coding genes, of which 14 and 11 were also present in the B chromosomes of A. bockmanni and A. fasciatus, respectively. Our search for B-specific single-nucleotide polymorphisms (SNPs) identified the presence of B-derived transcripts in B-carrying ovaries, 80% of which belonged to nobox, a gene involved in oogenesis regulation. Importantly, the B chromosome nobox paralog is expressed > 30× more than the A chromosome paralog. This indicates that the normal regulation of this gene is altered in B-carrying females, which could potentially facilitate B inheritance at higher rates than Mendelian law prediction.
Taken together, our results demonstrate the long-term survival of B chromosomes despite their lack of regular pairing and segregation during meiosis and that they can endure episodes of population divergence leading to species formation.</description><identifier>ISSN: 1741-7007</identifier><identifier>EISSN: 1741-7007</identifier><identifier>DOI: 10.1186/s12915-021-00991-9</identifier><identifier>PMID: 33740955</identifier><language>eng</language><publisher>England: BioMed Central Ltd</publisher><subject>Animals ; Astyanax ; B chromosomes ; Characidae - genetics ; Chromosome Mapping ; Chromosomes ; Chromosomes - genetics ; Evolution ; Female ; Genome ; Genomics ; Identification and classification ; Male ; Polymorphism, Single Nucleotide ; Species Specificity ; Transcriptomics</subject><ispartof>BMC biology, 2021-03, Vol.19 (1), p.52-52, Article 52</ispartof><rights>COPYRIGHT 2021 BioMed Central Ltd.</rights><rights>The Author(s) 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c640t-f4ff4f46054faafd7b69a55564c217a28c403cda151e9d7c855ced3584827bb43</citedby><cites>FETCH-LOGICAL-c640t-f4ff4f46054faafd7b69a55564c217a28c403cda151e9d7c855ced3584827bb43</cites><orcidid>0000-0001-8845-3845 ; 0000-0002-8808-2498 ; 0000-0003-0887-1081 ; 0000-0002-7010-8880 ; 0000-0003-4565-6065 ; 0000-0002-4901-7714 ; 0000-0002-2528-9846 ; 0000-0003-0649-8279 ; 0000-0002-5391-301X ; 0000-0002-2507-9814 ; 0000-0002-2610-2254 ; 0000-0002-8979-9992</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7976721/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7976721/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,37013,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33740955$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-441099$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Silva, Duílio Mazzoni Zerbinato de Andrade</creatorcontrib><creatorcontrib>Ruiz-Ruano, Francisco J</creatorcontrib><creatorcontrib>Utsunomia, Ricardo</creatorcontrib><creatorcontrib>Martín-Peciña, María</creatorcontrib><creatorcontrib>Castro, Jonathan Pena</creatorcontrib><creatorcontrib>Freire, Paula Paccielli</creatorcontrib><creatorcontrib>Carvalho, Robson Francisco</creatorcontrib><creatorcontrib>Hashimoto, Diogo T</creatorcontrib><creatorcontrib>Suh, Alexander</creatorcontrib><creatorcontrib>Oliveira, Claudio</creatorcontrib><creatorcontrib>Porto-Foresti, Fábio</creatorcontrib><creatorcontrib>Artoni, Roberto Ferreira</creatorcontrib><creatorcontrib>Foresti, Fausto</creatorcontrib><creatorcontrib>Camacho, Juan Pedro M</creatorcontrib><title>Long-term persistence of supernumerary B chromosomes in multiple species of Astyanax fish</title><title>BMC biology</title><addtitle>BMC Biol</addtitle><description>Eukaryote genomes frequently harbor supernumerary B chromosomes in addition to the "standard" A chromosome set. B chromosomes are thought to arise as byproducts of genome rearrangements and have mostly been considered intraspecific oddities. However, their evolutionary transcendence beyond species level has remained untested.
Here we reveal that the large metacentric B chromosomes reported in several fish species of the genus Astyanax arose in a common ancestor at least 4 million years ago. We generated transcriptomes of A. scabripinnis and A. paranae 0B and 1B individuals and used these assemblies as a reference for mapping all gDNA and RNA libraries to quantify coverage differences between B-lacking and B-carrying genomes. We show that the B chromosomes of A. scabripinnis and A. paranae share 19 protein-coding genes, of which 14 and 11 were also present in the B chromosomes of A. bockmanni and A. fasciatus, respectively. Our search for B-specific single-nucleotide polymorphisms (SNPs) identified the presence of B-derived transcripts in B-carrying ovaries, 80% of which belonged to nobox, a gene involved in oogenesis regulation. Importantly, the B chromosome nobox paralog is expressed > 30× more than the A chromosome paralog. This indicates that the normal regulation of this gene is altered in B-carrying females, which could potentially facilitate B inheritance at higher rates than Mendelian law prediction.
Taken together, our results demonstrate the long-term survival of B chromosomes despite their lack of regular pairing and segregation during meiosis and that they can endure episodes of population divergence leading to species formation.</description><subject>Animals</subject><subject>Astyanax</subject><subject>B chromosomes</subject><subject>Characidae - genetics</subject><subject>Chromosome Mapping</subject><subject>Chromosomes</subject><subject>Chromosomes - genetics</subject><subject>Evolution</subject><subject>Female</subject><subject>Genome</subject><subject>Genomics</subject><subject>Identification and classification</subject><subject>Male</subject><subject>Polymorphism, Single Nucleotide</subject><subject>Species Specificity</subject><subject>Transcriptomics</subject><issn>1741-7007</issn><issn>1741-7007</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNqNkl2L1DAYhYso7rr6B7yQgjcKds1n094sjOvXwMCCHwtehTR9M5OlbWqS6u6_NzNdly14IQ00vHnOITmcLHuO0SnGVfk2YFJjXiCCC4TqGhf1g-wYC4YLgZB4eG9_lD0J4QohwoWgj7MjSgVDNefH2Y-NG7ZFBN_nI_hgQ4RBQ-5MHqY0GKYevPI3-btc77zrXXA9hNwOeT910Y4d5GEEbdMsSVYh3qhBXefGht3T7JFRXYBnt_-T7PvHD9_OPxebi0_r89Wm0CVDsTDMpMVKxJlRyrSiKWvFOS-ZJlgoUmmGqG4V5hjqVuiKcw0t5RWriGgaRk-y9ezbOnUlR2_7dF_plJWHgfNbqXy0ugOpWSkaULhp24oRzZVCmjVMGMRNnfbJ683sFX7DODULt_f2cnVwmybJGE6BJ_xsxhPbQ6thiF51C9XyZLA7uXW_pKhFKQhOBq9uDbz7OUGIsrdBQ9epAdwUJOGIMioI3T_z5YxuVXqJHYxLjnqPy1WZ0sIpGJqo039Q6Wuht9oNYGyaLwSvF4LERLiOWzWFINdfv_w_e3G5ZMnMau9C8GDuUsFI7tsr5_bK1F55aK_c5_nifp53kr91pX8AjZvqBg</recordid><startdate>20210319</startdate><enddate>20210319</enddate><creator>Silva, Duílio Mazzoni Zerbinato de Andrade</creator><creator>Ruiz-Ruano, Francisco J</creator><creator>Utsunomia, Ricardo</creator><creator>Martín-Peciña, María</creator><creator>Castro, Jonathan Pena</creator><creator>Freire, Paula Paccielli</creator><creator>Carvalho, Robson Francisco</creator><creator>Hashimoto, Diogo T</creator><creator>Suh, Alexander</creator><creator>Oliveira, Claudio</creator><creator>Porto-Foresti, Fábio</creator><creator>Artoni, Roberto Ferreira</creator><creator>Foresti, Fausto</creator><creator>Camacho, Juan Pedro M</creator><general>BioMed Central Ltd</general><general>BioMed Central</general><general>BMC</general><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>IOV</scope><scope>ISR</scope><scope>7X8</scope><scope>5PM</scope><scope>ACNBI</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>D8T</scope><scope>DF2</scope><scope>ZZAVC</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-8845-3845</orcidid><orcidid>https://orcid.org/0000-0002-8808-2498</orcidid><orcidid>https://orcid.org/0000-0003-0887-1081</orcidid><orcidid>https://orcid.org/0000-0002-7010-8880</orcidid><orcidid>https://orcid.org/0000-0003-4565-6065</orcidid><orcidid>https://orcid.org/0000-0002-4901-7714</orcidid><orcidid>https://orcid.org/0000-0002-2528-9846</orcidid><orcidid>https://orcid.org/0000-0003-0649-8279</orcidid><orcidid>https://orcid.org/0000-0002-5391-301X</orcidid><orcidid>https://orcid.org/0000-0002-2507-9814</orcidid><orcidid>https://orcid.org/0000-0002-2610-2254</orcidid><orcidid>https://orcid.org/0000-0002-8979-9992</orcidid></search><sort><creationdate>20210319</creationdate><title>Long-term persistence of supernumerary B chromosomes in multiple species of Astyanax fish</title><author>Silva, Duílio Mazzoni Zerbinato de Andrade ; 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B chromosomes are thought to arise as byproducts of genome rearrangements and have mostly been considered intraspecific oddities. However, their evolutionary transcendence beyond species level has remained untested.
Here we reveal that the large metacentric B chromosomes reported in several fish species of the genus Astyanax arose in a common ancestor at least 4 million years ago. We generated transcriptomes of A. scabripinnis and A. paranae 0B and 1B individuals and used these assemblies as a reference for mapping all gDNA and RNA libraries to quantify coverage differences between B-lacking and B-carrying genomes. We show that the B chromosomes of A. scabripinnis and A. paranae share 19 protein-coding genes, of which 14 and 11 were also present in the B chromosomes of A. bockmanni and A. fasciatus, respectively. Our search for B-specific single-nucleotide polymorphisms (SNPs) identified the presence of B-derived transcripts in B-carrying ovaries, 80% of which belonged to nobox, a gene involved in oogenesis regulation. Importantly, the B chromosome nobox paralog is expressed > 30× more than the A chromosome paralog. This indicates that the normal regulation of this gene is altered in B-carrying females, which could potentially facilitate B inheritance at higher rates than Mendelian law prediction.
Taken together, our results demonstrate the long-term survival of B chromosomes despite their lack of regular pairing and segregation during meiosis and that they can endure episodes of population divergence leading to species formation.</abstract><cop>England</cop><pub>BioMed Central Ltd</pub><pmid>33740955</pmid><doi>10.1186/s12915-021-00991-9</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0001-8845-3845</orcidid><orcidid>https://orcid.org/0000-0002-8808-2498</orcidid><orcidid>https://orcid.org/0000-0003-0887-1081</orcidid><orcidid>https://orcid.org/0000-0002-7010-8880</orcidid><orcidid>https://orcid.org/0000-0003-4565-6065</orcidid><orcidid>https://orcid.org/0000-0002-4901-7714</orcidid><orcidid>https://orcid.org/0000-0002-2528-9846</orcidid><orcidid>https://orcid.org/0000-0003-0649-8279</orcidid><orcidid>https://orcid.org/0000-0002-5391-301X</orcidid><orcidid>https://orcid.org/0000-0002-2507-9814</orcidid><orcidid>https://orcid.org/0000-0002-2610-2254</orcidid><orcidid>https://orcid.org/0000-0002-8979-9992</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Astyanax B chromosomes Characidae - genetics Chromosome Mapping Chromosomes Chromosomes - genetics Evolution Female Genome Genomics Identification and classification Male Polymorphism, Single Nucleotide Species Specificity Transcriptomics |
title | Long-term persistence of supernumerary B chromosomes in multiple species of Astyanax fish |
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