Long-term persistence of supernumerary B chromosomes in multiple species of Astyanax fish
Autor(a) principal: | |
---|---|
Data de Publicação: | 2021 |
Outros Autores: | , , , , , , , , , , , , |
Tipo de documento: | Artigo |
Idioma: | eng |
Título da fonte: | Repositório Institucional da UNESP |
Texto Completo: | http://dx.doi.org/10.1186/s12915-021-00991-9 http://hdl.handle.net/11449/207477 |
Resumo: | Background: 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. Results: 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. Conclusions: 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. |
id |
UNSP_eb1de5d200e1500035d47d18bbd1344a |
---|---|
oai_identifier_str |
oai:repositorio.unesp.br:11449/207477 |
network_acronym_str |
UNSP |
network_name_str |
Repositório Institucional da UNESP |
repository_id_str |
2946 |
spelling |
Long-term persistence of supernumerary B chromosomes in multiple species of Astyanax fishAstyanaxB chromosomesEvolutionGenomicsTranscriptomicsBackground: 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. Results: 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. Conclusions: 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.Consejería de Conocimiento, Investigación y Universidad, Junta de AndalucíaConsejería de Economía, Conocimiento, Empresas y Universidad, Junta de AndalucíaConsejería de Economía, Innovación, Ciencia y Empleo, Junta de AndalucíaConsejería de Salud y Familias, Junta de AndalucíaJunta de AndalucíaDepartamento de Biologia Estrutural e Funcional Instituto de Biociências de Botucatu Universidade Estadual Paulista UNESP Distrito de Rubião JuniorDepartment of Organismal Biology – Systematic Biology Evolutionary Biology Centre Uppsala UniversityDepartamento de Genética Universidad de GranadaSchool of Biological Sciences University of East Anglia, Norwich Research ParkDepartamento de Genética Instituto de Ciências Biológicas e da Saúde ICBS Universidade Federal Rural do Rio de JaneiroDepartamento de Ciências Biológicas Faculdade de Ciências Universidade Estadual Paulista UNESP Campus de BauruDepartamento de Genética e Evolução Universidade Federal de São Carlos UFSCARDepartamento de Biologia Estrutural Molecular e Genética Universidade Estadual de Ponta Grossa UEPGDepartamento de Imunologia Instituto de Ciências Biomédicas Universidade de São Paulo USPCentro de Aquicultura Universidade Estadual Paulista UNESP, Campus JaboticabalDepartamento de Biologia Estrutural e Funcional Instituto de Biociências de Botucatu Universidade Estadual Paulista UNESP Distrito de Rubião JuniorDepartamento de Ciências Biológicas Faculdade de Ciências Universidade Estadual Paulista UNESP Campus de BauruCentro de Aquicultura Universidade Estadual Paulista UNESP, Campus JaboticabalUniversidade Estadual Paulista (Unesp)Uppsala UniversityUniversidad de GranadaUniversity of East AngliaUniversidade Federal Rural do Rio de JaneiroUniversidade Federal de São Carlos (UFSCar)Universidade Estadual de Ponta Grossa (UEPG)Universidade de São Paulo (USP)Silva, Duílio Mazzoni Zerbinato de Andrade [UNESP]Ruiz-Ruano, Francisco J.Utsunomia, Ricardo [UNESP]Martín-Peciña, MaríaCastro, Jonathan PenaFreire, Paula Paccielli [UNESP]Carvalho, Robson Francisco [UNESP]Hashimoto, Diogo T. [UNESP]Suh, AlexanderOliveira, Claudio [UNESP]Porto-Foresti, Fábio [UNESP]Artoni, Roberto FerreiraForesti, Fausto [UNESP]Camacho, Juan Pedro M.2021-06-25T10:55:52Z2021-06-25T10:55:52Z2021-12-01info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.1186/s12915-021-00991-9BMC Biology, v. 19, n. 1, 2021.1741-7007http://hdl.handle.net/11449/20747710.1186/s12915-021-00991-92-s2.0-85102821966Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengBMC Biologyinfo:eu-repo/semantics/openAccess2024-04-23T15:24:02Zoai:repositorio.unesp.br:11449/207477Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestrepositoriounesp@unesp.bropendoar:29462024-04-23T15:24:02Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false |
dc.title.none.fl_str_mv |
Long-term persistence of supernumerary B chromosomes in multiple species of Astyanax fish |
title |
Long-term persistence of supernumerary B chromosomes in multiple species of Astyanax fish |
spellingShingle |
Long-term persistence of supernumerary B chromosomes in multiple species of Astyanax fish Silva, Duílio Mazzoni Zerbinato de Andrade [UNESP] Astyanax B chromosomes Evolution Genomics Transcriptomics |
title_short |
Long-term persistence of supernumerary B chromosomes in multiple species of Astyanax fish |
title_full |
Long-term persistence of supernumerary B chromosomes in multiple species of Astyanax fish |
title_fullStr |
Long-term persistence of supernumerary B chromosomes in multiple species of Astyanax fish |
title_full_unstemmed |
Long-term persistence of supernumerary B chromosomes in multiple species of Astyanax fish |
title_sort |
Long-term persistence of supernumerary B chromosomes in multiple species of Astyanax fish |
author |
Silva, Duílio Mazzoni Zerbinato de Andrade [UNESP] |
author_facet |
Silva, Duílio Mazzoni Zerbinato de Andrade [UNESP] Ruiz-Ruano, Francisco J. Utsunomia, Ricardo [UNESP] Martín-Peciña, María Castro, Jonathan Pena Freire, Paula Paccielli [UNESP] Carvalho, Robson Francisco [UNESP] Hashimoto, Diogo T. [UNESP] Suh, Alexander Oliveira, Claudio [UNESP] Porto-Foresti, Fábio [UNESP] Artoni, Roberto Ferreira Foresti, Fausto [UNESP] Camacho, Juan Pedro M. |
author_role |
author |
author2 |
Ruiz-Ruano, Francisco J. Utsunomia, Ricardo [UNESP] Martín-Peciña, María Castro, Jonathan Pena Freire, Paula Paccielli [UNESP] Carvalho, Robson Francisco [UNESP] Hashimoto, Diogo T. [UNESP] Suh, Alexander Oliveira, Claudio [UNESP] Porto-Foresti, Fábio [UNESP] Artoni, Roberto Ferreira Foresti, Fausto [UNESP] Camacho, Juan Pedro M. |
author2_role |
author author author author author author author author author author author author author |
dc.contributor.none.fl_str_mv |
Universidade Estadual Paulista (Unesp) Uppsala University Universidad de Granada University of East Anglia Universidade Federal Rural do Rio de Janeiro Universidade Federal de São Carlos (UFSCar) Universidade Estadual de Ponta Grossa (UEPG) Universidade de São Paulo (USP) |
dc.contributor.author.fl_str_mv |
Silva, Duílio Mazzoni Zerbinato de Andrade [UNESP] Ruiz-Ruano, Francisco J. Utsunomia, Ricardo [UNESP] Martín-Peciña, María Castro, Jonathan Pena Freire, Paula Paccielli [UNESP] Carvalho, Robson Francisco [UNESP] Hashimoto, Diogo T. [UNESP] Suh, Alexander Oliveira, Claudio [UNESP] Porto-Foresti, Fábio [UNESP] Artoni, Roberto Ferreira Foresti, Fausto [UNESP] Camacho, Juan Pedro M. |
dc.subject.por.fl_str_mv |
Astyanax B chromosomes Evolution Genomics Transcriptomics |
topic |
Astyanax B chromosomes Evolution Genomics Transcriptomics |
description |
Background: 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. Results: 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. Conclusions: 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. |
publishDate |
2021 |
dc.date.none.fl_str_mv |
2021-06-25T10:55:52Z 2021-06-25T10:55:52Z 2021-12-01 |
dc.type.status.fl_str_mv |
info:eu-repo/semantics/publishedVersion |
dc.type.driver.fl_str_mv |
info:eu-repo/semantics/article |
format |
article |
status_str |
publishedVersion |
dc.identifier.uri.fl_str_mv |
http://dx.doi.org/10.1186/s12915-021-00991-9 BMC Biology, v. 19, n. 1, 2021. 1741-7007 http://hdl.handle.net/11449/207477 10.1186/s12915-021-00991-9 2-s2.0-85102821966 |
url |
http://dx.doi.org/10.1186/s12915-021-00991-9 http://hdl.handle.net/11449/207477 |
identifier_str_mv |
BMC Biology, v. 19, n. 1, 2021. 1741-7007 10.1186/s12915-021-00991-9 2-s2.0-85102821966 |
dc.language.iso.fl_str_mv |
eng |
language |
eng |
dc.relation.none.fl_str_mv |
BMC Biology |
dc.rights.driver.fl_str_mv |
info:eu-repo/semantics/openAccess |
eu_rights_str_mv |
openAccess |
dc.source.none.fl_str_mv |
Scopus reponame:Repositório Institucional da UNESP instname:Universidade Estadual Paulista (UNESP) instacron:UNESP |
instname_str |
Universidade Estadual Paulista (UNESP) |
instacron_str |
UNESP |
institution |
UNESP |
reponame_str |
Repositório Institucional da UNESP |
collection |
Repositório Institucional da UNESP |
repository.name.fl_str_mv |
Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP) |
repository.mail.fl_str_mv |
repositoriounesp@unesp.br |
_version_ |
1834483921557913600 |