Cytogenomic analysis unveils mixed molecular evolution and recurrent chromosomal rearrangements shaping the multigene families on Schistocerca grasshopper genomes

Detalhes bibliográficos
Autor(a) principal: Martí, Emiliano [UNESP]
Data de Publicação: 2021
Outros Autores: Milani, Diogo [UNESP], Bardella, Vanessa B. [UNESP], Albuquerque, Lucas [UNESP], Song, Hojun, Palacios-Gimenez, Octavio M., Cabral-de-Mello, Diogo C. [UNESP]
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.1111/evo.14287
http://hdl.handle.net/11449/221894
Resumo: Multigene families are essential components of eukaryotic genomes and play key roles either structurally and functionally. Their modes of evolution remain elusive even in the era of genomics, because multiple multigene family sequences coexist in genomes, particularly in large repetitive genomes. Here, we investigate how the multigene families 18S rDNA, U2 snDNA, and H3 histone evolved in 10 species of Schistocerca grasshoppers with very large and repeat-enriched genomes. Using sequenced genomes and fluorescence in situ hybridization mapping, we find substantial differences between species, including the number of chromosomal clusters, changes in sequence abundance and nucleotide composition, pseudogenization, and association with transposable elements (TEs). The intragenomic analysis of Schistocerca gregaria using long-read sequencing and genome assembly unveils conservation for H3 histone and recurrent pseudogenization for 18S rDNA and U2 snDNA, likely promoted by association with TEs and sequence truncation. Remarkably, TEs were frequently associated with truncated copies, were also among the most abundant in the genome, and revealed signatures of recent activity. Our findings suggest a combined effect of concerted and birth-and-death models driving the evolution of multigene families in Schistocerca over the last 8 million years, and the occurrence of intra- and interchromosomal rearrangements shaping their chromosomal distribution. Despite the conserved karyotype in Schistocerca, our analysis highlights the extensive reorganization of repetitive DNAs in Schistocerca, contributing to the advance of comparative genomics for this important grasshopper genus.
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spelling Cytogenomic analysis unveils mixed molecular evolution and recurrent chromosomal rearrangements shaping the multigene families on Schistocerca grasshopper genomesBirth-and-deathconcerted evolutionFISHlarge genomesrepetitive DNAstransposable elementsMultigene families are essential components of eukaryotic genomes and play key roles either structurally and functionally. Their modes of evolution remain elusive even in the era of genomics, because multiple multigene family sequences coexist in genomes, particularly in large repetitive genomes. Here, we investigate how the multigene families 18S rDNA, U2 snDNA, and H3 histone evolved in 10 species of Schistocerca grasshoppers with very large and repeat-enriched genomes. Using sequenced genomes and fluorescence in situ hybridization mapping, we find substantial differences between species, including the number of chromosomal clusters, changes in sequence abundance and nucleotide composition, pseudogenization, and association with transposable elements (TEs). The intragenomic analysis of Schistocerca gregaria using long-read sequencing and genome assembly unveils conservation for H3 histone and recurrent pseudogenization for 18S rDNA and U2 snDNA, likely promoted by association with TEs and sequence truncation. Remarkably, TEs were frequently associated with truncated copies, were also among the most abundant in the genome, and revealed signatures of recent activity. Our findings suggest a combined effect of concerted and birth-and-death models driving the evolution of multigene families in Schistocerca over the last 8 million years, and the occurrence of intra- and interchromosomal rearrangements shaping their chromosomal distribution. Despite the conserved karyotype in Schistocerca, our analysis highlights the extensive reorganization of repetitive DNAs in Schistocerca, contributing to the advance of comparative genomics for this important grasshopper genus.National Science FoundationDepartamento de Biologia Geral e Aplicada UNESP – Univ Estadual Paulista Instituto de Biociências/IBDepartment of Entomology Texas A&M UniversityDepartment of Organismal Biology – Systematic Biology Evolutionary Biology Centre Uppsala UniversityPopulation Ecology Group Institute of Ecology and Evolution Friedrich Schiller University JenaDepartamento de Biologia Geral e Aplicada UNESP – Univ Estadual Paulista Instituto de Biociências/IBNational Science Foundation: IOS-1253493Universidade Estadual Paulista (UNESP)Texas A&M UniversityUppsala UniversityFriedrich Schiller University JenaMartí, Emiliano [UNESP]Milani, Diogo [UNESP]Bardella, Vanessa B. [UNESP]Albuquerque, Lucas [UNESP]Song, HojunPalacios-Gimenez, Octavio M.Cabral-de-Mello, Diogo C. [UNESP]2022-04-28T19:41:07Z2022-04-28T19:41:07Z2021-08-01info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/article2027-2041http://dx.doi.org/10.1111/evo.14287Evolution, v. 75, n. 8, p. 2027-2041, 2021.1558-56460014-3820http://hdl.handle.net/11449/22189410.1111/evo.142872-s2.0-85109095887Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengEvolutioninfo:eu-repo/semantics/openAccess2022-04-28T19:41:07Zoai:repositorio.unesp.br:11449/221894Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-08-05T16:11:20.335960Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv Cytogenomic analysis unveils mixed molecular evolution and recurrent chromosomal rearrangements shaping the multigene families on Schistocerca grasshopper genomes
title Cytogenomic analysis unveils mixed molecular evolution and recurrent chromosomal rearrangements shaping the multigene families on Schistocerca grasshopper genomes
spellingShingle Cytogenomic analysis unveils mixed molecular evolution and recurrent chromosomal rearrangements shaping the multigene families on Schistocerca grasshopper genomes
Martí, Emiliano [UNESP]
Birth-and-death
concerted evolution
FISH
large genomes
repetitive DNAs
transposable elements
title_short Cytogenomic analysis unveils mixed molecular evolution and recurrent chromosomal rearrangements shaping the multigene families on Schistocerca grasshopper genomes
title_full Cytogenomic analysis unveils mixed molecular evolution and recurrent chromosomal rearrangements shaping the multigene families on Schistocerca grasshopper genomes
title_fullStr Cytogenomic analysis unveils mixed molecular evolution and recurrent chromosomal rearrangements shaping the multigene families on Schistocerca grasshopper genomes
title_full_unstemmed Cytogenomic analysis unveils mixed molecular evolution and recurrent chromosomal rearrangements shaping the multigene families on Schistocerca grasshopper genomes
title_sort Cytogenomic analysis unveils mixed molecular evolution and recurrent chromosomal rearrangements shaping the multigene families on Schistocerca grasshopper genomes
author Martí, Emiliano [UNESP]
author_facet Martí, Emiliano [UNESP]
Milani, Diogo [UNESP]
Bardella, Vanessa B. [UNESP]
Albuquerque, Lucas [UNESP]
Song, Hojun
Palacios-Gimenez, Octavio M.
Cabral-de-Mello, Diogo C. [UNESP]
author_role author
author2 Milani, Diogo [UNESP]
Bardella, Vanessa B. [UNESP]
Albuquerque, Lucas [UNESP]
Song, Hojun
Palacios-Gimenez, Octavio M.
Cabral-de-Mello, Diogo C. [UNESP]
author2_role author
author
author
author
author
author
dc.contributor.none.fl_str_mv Universidade Estadual Paulista (UNESP)
Texas A&M University
Uppsala University
Friedrich Schiller University Jena
dc.contributor.author.fl_str_mv Martí, Emiliano [UNESP]
Milani, Diogo [UNESP]
Bardella, Vanessa B. [UNESP]
Albuquerque, Lucas [UNESP]
Song, Hojun
Palacios-Gimenez, Octavio M.
Cabral-de-Mello, Diogo C. [UNESP]
dc.subject.por.fl_str_mv Birth-and-death
concerted evolution
FISH
large genomes
repetitive DNAs
transposable elements
topic Birth-and-death
concerted evolution
FISH
large genomes
repetitive DNAs
transposable elements
description Multigene families are essential components of eukaryotic genomes and play key roles either structurally and functionally. Their modes of evolution remain elusive even in the era of genomics, because multiple multigene family sequences coexist in genomes, particularly in large repetitive genomes. Here, we investigate how the multigene families 18S rDNA, U2 snDNA, and H3 histone evolved in 10 species of Schistocerca grasshoppers with very large and repeat-enriched genomes. Using sequenced genomes and fluorescence in situ hybridization mapping, we find substantial differences between species, including the number of chromosomal clusters, changes in sequence abundance and nucleotide composition, pseudogenization, and association with transposable elements (TEs). The intragenomic analysis of Schistocerca gregaria using long-read sequencing and genome assembly unveils conservation for H3 histone and recurrent pseudogenization for 18S rDNA and U2 snDNA, likely promoted by association with TEs and sequence truncation. Remarkably, TEs were frequently associated with truncated copies, were also among the most abundant in the genome, and revealed signatures of recent activity. Our findings suggest a combined effect of concerted and birth-and-death models driving the evolution of multigene families in Schistocerca over the last 8 million years, and the occurrence of intra- and interchromosomal rearrangements shaping their chromosomal distribution. Despite the conserved karyotype in Schistocerca, our analysis highlights the extensive reorganization of repetitive DNAs in Schistocerca, contributing to the advance of comparative genomics for this important grasshopper genus.
publishDate 2021
dc.date.none.fl_str_mv 2021-08-01
2022-04-28T19:41:07Z
2022-04-28T19:41:07Z
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/10.1111/evo.14287
Evolution, v. 75, n. 8, p. 2027-2041, 2021.
1558-5646
0014-3820
http://hdl.handle.net/11449/221894
10.1111/evo.14287
2-s2.0-85109095887
url http://dx.doi.org/10.1111/evo.14287
http://hdl.handle.net/11449/221894
identifier_str_mv Evolution, v. 75, n. 8, p. 2027-2041, 2021.
1558-5646
0014-3820
10.1111/evo.14287
2-s2.0-85109095887
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Evolution
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 2027-2041
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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