Genomic Differences Between the Sexes in a Fish Species Seen Through Satellite DNAs

Detalhes bibliográficos
Autor(a) principal: Crepaldi, Carolina [UNESP]
Data de Publicação: 2021
Outros Autores: Martí, Emiliano [UNESP], Gonçalves, Évelin Mariani [UNESP], Martí, Dardo Andrea, Parise-Maltempi, Patricia Pasquali [UNESP]
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.3389/fgene.2021.728670
http://hdl.handle.net/11449/222644
Resumo: Neotropical fishes have highly diversified karyotypic and genomic characteristics and present many diverse sex chromosome systems, with various degrees of sex chromosome differentiation. Knowledge on their sex-specific composition and evolution, however, is still limited. Satellite DNAs (satDNAs) are tandemly repeated sequences with pervasive genomic distribution and distinctive evolutionary pathways, and investigating satDNA content might shed light into how genome architecture is organized in fishes and in their sex chromosomes. The present study investigated the satellitome of Megaleporinus elongatus, a freshwater fish with a proposed Z1Z1Z2Z2/Z1W1Z2W2 multiple sex chromosome system that encompasses a highly heterochromatic and differentiated W1 chromosome. The species satellitome comprises of 140 different satDNA families, including previously isolated sequences and new families found in this study. This diversity is remarkable considering the relatively low proportion that satDNAs generally account for the M. elongatus genome (around only 5%). Differences between the sexes in regards of satDNA content were also evidenced, as these sequences are 14% more abundant in the female genome. The occurrence of sex-biased signatures of satDNA evolution in the species is tightly linked to satellite enrichment associated with W1 in females. Although both sexes share practically all satDNAs, the overall massive amplification of only a few of them accompanied the W1 differentiation. We also investigated the expansion and diversification of the two most abundant satDNAs of M. elongatus, MelSat01-36 and MelSat02-26, both highly amplified sequences in W1 and, in MelSat02-26’s case, also harbored by Z2 and W2 chromosomes. We compared their occurrences in M. elongatus and the sister species M. macrocephalus (with a standard ZW sex chromosome system) and concluded that both satDNAs have led to the formation of highly amplified arrays in both species; however, they formed species-specific organization on female-restricted sex chromosomes. Our results show how satDNA composition is highly diversified in M. elongatus, in which their accumulation is significantly contributing to W1 differentiation and not satDNA diversity per se. Also, the evolutionary behavior of these repeats may be associated with genome plasticity and satDNA variability between the sexes and between closely related species, influencing how seemingly homeologous heteromorphic sex chromosomes undergo independent satDNA evolution.
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spelling Genomic Differences Between the Sexes in a Fish Species Seen Through Satellite DNAsanostomidaeconcerted evolutionfish sex chromosomesmegaleporinusneotropical fishsatDNA evolutionsatellitomeNeotropical fishes have highly diversified karyotypic and genomic characteristics and present many diverse sex chromosome systems, with various degrees of sex chromosome differentiation. Knowledge on their sex-specific composition and evolution, however, is still limited. Satellite DNAs (satDNAs) are tandemly repeated sequences with pervasive genomic distribution and distinctive evolutionary pathways, and investigating satDNA content might shed light into how genome architecture is organized in fishes and in their sex chromosomes. The present study investigated the satellitome of Megaleporinus elongatus, a freshwater fish with a proposed Z1Z1Z2Z2/Z1W1Z2W2 multiple sex chromosome system that encompasses a highly heterochromatic and differentiated W1 chromosome. The species satellitome comprises of 140 different satDNA families, including previously isolated sequences and new families found in this study. This diversity is remarkable considering the relatively low proportion that satDNAs generally account for the M. elongatus genome (around only 5%). Differences between the sexes in regards of satDNA content were also evidenced, as these sequences are 14% more abundant in the female genome. The occurrence of sex-biased signatures of satDNA evolution in the species is tightly linked to satellite enrichment associated with W1 in females. Although both sexes share practically all satDNAs, the overall massive amplification of only a few of them accompanied the W1 differentiation. We also investigated the expansion and diversification of the two most abundant satDNAs of M. elongatus, MelSat01-36 and MelSat02-26, both highly amplified sequences in W1 and, in MelSat02-26’s case, also harbored by Z2 and W2 chromosomes. We compared their occurrences in M. elongatus and the sister species M. macrocephalus (with a standard ZW sex chromosome system) and concluded that both satDNAs have led to the formation of highly amplified arrays in both species; however, they formed species-specific organization on female-restricted sex chromosomes. Our results show how satDNA composition is highly diversified in M. elongatus, in which their accumulation is significantly contributing to W1 differentiation and not satDNA diversity per se. Also, the evolutionary behavior of these repeats may be associated with genome plasticity and satDNA variability between the sexes and between closely related species, influencing how seemingly homeologous heteromorphic sex chromosomes undergo independent satDNA evolution.Departamento de Biologia Geral e Aplicada Instituto de Biociências (IB) Universidade Estadual Paulista (UNESP)Laboratorio de Genética Evolutiva Instituto de Biología Subtropical (IBS) Universidad Nacional de Misiones (UNaM) CONICETDepartamento de Biologia Geral e Aplicada Instituto de Biociências (IB) Universidade Estadual Paulista (UNESP)Universidade Estadual Paulista (UNESP)CONICETCrepaldi, Carolina [UNESP]Martí, Emiliano [UNESP]Gonçalves, Évelin Mariani [UNESP]Martí, Dardo AndreaParise-Maltempi, Patricia Pasquali [UNESP]2022-04-28T19:45:56Z2022-04-28T19:45:56Z2021-09-30info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.3389/fgene.2021.728670Frontiers in Genetics, v. 12.1664-8021http://hdl.handle.net/11449/22264410.3389/fgene.2021.7286702-s2.0-85117091247Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengFrontiers in Geneticsinfo:eu-repo/semantics/openAccess2022-04-28T19:45:56Zoai:repositorio.unesp.br:11449/222644Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-08-05T18:15:50.174218Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv Genomic Differences Between the Sexes in a Fish Species Seen Through Satellite DNAs
title Genomic Differences Between the Sexes in a Fish Species Seen Through Satellite DNAs
spellingShingle Genomic Differences Between the Sexes in a Fish Species Seen Through Satellite DNAs
Crepaldi, Carolina [UNESP]
anostomidae
concerted evolution
fish sex chromosomes
megaleporinus
neotropical fish
satDNA evolution
satellitome
title_short Genomic Differences Between the Sexes in a Fish Species Seen Through Satellite DNAs
title_full Genomic Differences Between the Sexes in a Fish Species Seen Through Satellite DNAs
title_fullStr Genomic Differences Between the Sexes in a Fish Species Seen Through Satellite DNAs
title_full_unstemmed Genomic Differences Between the Sexes in a Fish Species Seen Through Satellite DNAs
title_sort Genomic Differences Between the Sexes in a Fish Species Seen Through Satellite DNAs
author Crepaldi, Carolina [UNESP]
author_facet Crepaldi, Carolina [UNESP]
Martí, Emiliano [UNESP]
Gonçalves, Évelin Mariani [UNESP]
Martí, Dardo Andrea
Parise-Maltempi, Patricia Pasquali [UNESP]
author_role author
author2 Martí, Emiliano [UNESP]
Gonçalves, Évelin Mariani [UNESP]
Martí, Dardo Andrea
Parise-Maltempi, Patricia Pasquali [UNESP]
author2_role author
author
author
author
dc.contributor.none.fl_str_mv Universidade Estadual Paulista (UNESP)
CONICET
dc.contributor.author.fl_str_mv Crepaldi, Carolina [UNESP]
Martí, Emiliano [UNESP]
Gonçalves, Évelin Mariani [UNESP]
Martí, Dardo Andrea
Parise-Maltempi, Patricia Pasquali [UNESP]
dc.subject.por.fl_str_mv anostomidae
concerted evolution
fish sex chromosomes
megaleporinus
neotropical fish
satDNA evolution
satellitome
topic anostomidae
concerted evolution
fish sex chromosomes
megaleporinus
neotropical fish
satDNA evolution
satellitome
description Neotropical fishes have highly diversified karyotypic and genomic characteristics and present many diverse sex chromosome systems, with various degrees of sex chromosome differentiation. Knowledge on their sex-specific composition and evolution, however, is still limited. Satellite DNAs (satDNAs) are tandemly repeated sequences with pervasive genomic distribution and distinctive evolutionary pathways, and investigating satDNA content might shed light into how genome architecture is organized in fishes and in their sex chromosomes. The present study investigated the satellitome of Megaleporinus elongatus, a freshwater fish with a proposed Z1Z1Z2Z2/Z1W1Z2W2 multiple sex chromosome system that encompasses a highly heterochromatic and differentiated W1 chromosome. The species satellitome comprises of 140 different satDNA families, including previously isolated sequences and new families found in this study. This diversity is remarkable considering the relatively low proportion that satDNAs generally account for the M. elongatus genome (around only 5%). Differences between the sexes in regards of satDNA content were also evidenced, as these sequences are 14% more abundant in the female genome. The occurrence of sex-biased signatures of satDNA evolution in the species is tightly linked to satellite enrichment associated with W1 in females. Although both sexes share practically all satDNAs, the overall massive amplification of only a few of them accompanied the W1 differentiation. We also investigated the expansion and diversification of the two most abundant satDNAs of M. elongatus, MelSat01-36 and MelSat02-26, both highly amplified sequences in W1 and, in MelSat02-26’s case, also harbored by Z2 and W2 chromosomes. We compared their occurrences in M. elongatus and the sister species M. macrocephalus (with a standard ZW sex chromosome system) and concluded that both satDNAs have led to the formation of highly amplified arrays in both species; however, they formed species-specific organization on female-restricted sex chromosomes. Our results show how satDNA composition is highly diversified in M. elongatus, in which their accumulation is significantly contributing to W1 differentiation and not satDNA diversity per se. Also, the evolutionary behavior of these repeats may be associated with genome plasticity and satDNA variability between the sexes and between closely related species, influencing how seemingly homeologous heteromorphic sex chromosomes undergo independent satDNA evolution.
publishDate 2021
dc.date.none.fl_str_mv 2021-09-30
2022-04-28T19:45:56Z
2022-04-28T19:45:56Z
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/10.3389/fgene.2021.728670
Frontiers in Genetics, v. 12.
1664-8021
http://hdl.handle.net/11449/222644
10.3389/fgene.2021.728670
2-s2.0-85117091247
url http://dx.doi.org/10.3389/fgene.2021.728670
http://hdl.handle.net/11449/222644
identifier_str_mv Frontiers in Genetics, v. 12.
1664-8021
10.3389/fgene.2021.728670
2-s2.0-85117091247
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Frontiers in Genetics
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
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