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

Autores
Crepaldi, Carolina; Martí, Emiliano; Gonçalves, Évelin Mariani; Marti, Dardo Andrea; Parise Maltempi, Patricia Pasquali
Año de publicación
2021
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
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.
Fil: Crepaldi, Carolina. Universidade Estadual Paulista Julio de Mesquita Filho; Brasil
Fil: Martí, Emiliano. Universidade Estadual Paulista Julio de Mesquita Filho; Brasil
Fil: Gonçalves, Évelin Mariani. Universidade Estadual Paulista Julio de Mesquita Filho; Brasil
Fil: Marti, Dardo Andrea. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Instituto de Biología Subtropical. Universidad Nacional de Misiones. Instituto de Biología Subtropical; Argentina
Fil: Parise Maltempi, Patricia Pasquali. Universidade Estadual Paulista Julio de Mesquita Filho; Brasil
Materia
ANOSTOMIDAE
CONCERTED EVOLUTION
FISH SEX CHROMOSOMES
MEGALEPORINUS
NEOTROPICAL FISH
SATDNA EVOLUTION
SATELLITOME
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/211919

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network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Genomic Differences Between the Sexes in a Fish Species Seen Through Satellite DNAsCrepaldi, CarolinaMartí, EmilianoGonçalves, Évelin MarianiMarti, Dardo AndreaParise Maltempi, Patricia PasqualiANOSTOMIDAECONCERTED EVOLUTIONFISH SEX CHROMOSOMESMEGALEPORINUSNEOTROPICAL FISHSATDNA EVOLUTIONSATELLITOMEhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Neotropical 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.Fil: Crepaldi, Carolina. Universidade Estadual Paulista Julio de Mesquita Filho; BrasilFil: Martí, Emiliano. Universidade Estadual Paulista Julio de Mesquita Filho; BrasilFil: Gonçalves, Évelin Mariani. Universidade Estadual Paulista Julio de Mesquita Filho; BrasilFil: Marti, Dardo Andrea. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Instituto de Biología Subtropical. Universidad Nacional de Misiones. Instituto de Biología Subtropical; ArgentinaFil: Parise Maltempi, Patricia Pasquali. Universidade Estadual Paulista Julio de Mesquita Filho; BrasilFrontiers Media2021-09info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/211919Crepaldi, Carolina; Martí, Emiliano; Gonçalves, Évelin Mariani; Marti, Dardo Andrea; Parise Maltempi, Patricia Pasquali; Genomic Differences Between the Sexes in a Fish Species Seen Through Satellite DNAs; Frontiers Media; Frontiers in Genetics; 12; 9-2021; 1-111664-8021CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.3389/fgene.2021.728670info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:43:32Zoai:ri.conicet.gov.ar:11336/211919instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 10:43:33.094CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
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
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
dc.creator.none.fl_str_mv Crepaldi, Carolina
Martí, Emiliano
Gonçalves, Évelin Mariani
Marti, Dardo Andrea
Parise Maltempi, Patricia Pasquali
author Crepaldi, Carolina
author_facet Crepaldi, Carolina
Martí, Emiliano
Gonçalves, Évelin Mariani
Marti, Dardo Andrea
Parise Maltempi, Patricia Pasquali
author_role author
author2 Martí, Emiliano
Gonçalves, Évelin Mariani
Marti, Dardo Andrea
Parise Maltempi, Patricia Pasquali
author2_role author
author
author
author
dc.subject.none.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
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv 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.
Fil: Crepaldi, Carolina. Universidade Estadual Paulista Julio de Mesquita Filho; Brasil
Fil: Martí, Emiliano. Universidade Estadual Paulista Julio de Mesquita Filho; Brasil
Fil: Gonçalves, Évelin Mariani. Universidade Estadual Paulista Julio de Mesquita Filho; Brasil
Fil: Marti, Dardo Andrea. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Nordeste. Instituto de Biología Subtropical. Universidad Nacional de Misiones. Instituto de Biología Subtropical; Argentina
Fil: Parise Maltempi, Patricia Pasquali. Universidade Estadual Paulista Julio de Mesquita Filho; Brasil
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
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/211919
Crepaldi, Carolina; Martí, Emiliano; Gonçalves, Évelin Mariani; Marti, Dardo Andrea; Parise Maltempi, Patricia Pasquali; Genomic Differences Between the Sexes in a Fish Species Seen Through Satellite DNAs; Frontiers Media; Frontiers in Genetics; 12; 9-2021; 1-11
1664-8021
CONICET Digital
CONICET
url http://hdl.handle.net/11336/211919
identifier_str_mv Crepaldi, Carolina; Martí, Emiliano; Gonçalves, Évelin Mariani; Marti, Dardo Andrea; Parise Maltempi, Patricia Pasquali; Genomic Differences Between the Sexes in a Fish Species Seen Through Satellite DNAs; Frontiers Media; Frontiers in Genetics; 12; 9-2021; 1-11
1664-8021
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.3389/fgene.2021.728670
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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