B chromosomes of multiple species have intense evolutionary dynamics and accumulated genes related to important biological processes

Bibliographic Details
Main Author: Ahmad, Syed F. [UNESP]
Publication Date: 2020
Other Authors: Jehangir, Maryam [UNESP], Cardoso, Adauto L. [UNESP], Wolf, Ivan R. [UNESP], Margarido, Vladimir P., Cabral-De-Mello, Diogo C. [UNESP], O'Neill, Rachel, Valente, Guilherme T. [UNESP], Martins, Cesar [UNESP]
Format: Article
Language: eng
Source: Repositório Institucional da UNESP
Download full: http://dx.doi.org/10.1186/s12864-020-07072-1
http://hdl.handle.net/11449/207990
Summary: Background: One of the biggest challenges in chromosome biology is to understand the occurrence and complex genetics of the extra, non-essential karyotype elements, commonly known as supernumerary or B chromosomes (Bs). The non-Mendelian inheritance and non-pairing abilities of B chromosomes make them an interesting model for genomics studies, thus bringing to bear different questions about their genetic composition, evolutionary survival, maintenance and functional role inside the cell. This study uncovers these phenomena in multiple species that we considered as representative organisms of both vertebrate and invertebrate models for B chromosome analysis. Results: We sequenced the genomes of three animal species including two fishes Astyanax mexicanus and Astyanax correntinus, and a grasshopper Abracris flavolineata, each with and without Bs, and identified their B-localized genes and repeat contents. We detected unique sequences occurring exclusively on Bs and discovered various evolutionary patterns of genomic rearrangements associated to Bs. In situ hybridization and quantitative polymerase chain reactions further validated our genomic approach confirming detection of sequences on Bs. The functional annotation of B sequences showed that the B chromosome comprises regions of gene fragments, novel genes, and intact genes, which encode a diverse set of functions related to important biological processes such as metabolism, morphogenesis, reproduction, transposition, recombination, cell cycle and chromosomes functions which might be important for their evolutionary success. Conclusions: This study reveals the genomic structure, composition and function of Bs, which provide new insights for theories of B chromosome evolution. The selfish behavior of Bs seems to be favored by gained genes/sequences.
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spelling B chromosomes of multiple species have intense evolutionary dynamics and accumulated genes related to important biological processesEvolutionExtra chromosomeGenomeNext generation sequencingSupernumerary chromosomeBackground: One of the biggest challenges in chromosome biology is to understand the occurrence and complex genetics of the extra, non-essential karyotype elements, commonly known as supernumerary or B chromosomes (Bs). The non-Mendelian inheritance and non-pairing abilities of B chromosomes make them an interesting model for genomics studies, thus bringing to bear different questions about their genetic composition, evolutionary survival, maintenance and functional role inside the cell. This study uncovers these phenomena in multiple species that we considered as representative organisms of both vertebrate and invertebrate models for B chromosome analysis. Results: We sequenced the genomes of three animal species including two fishes Astyanax mexicanus and Astyanax correntinus, and a grasshopper Abracris flavolineata, each with and without Bs, and identified their B-localized genes and repeat contents. We detected unique sequences occurring exclusively on Bs and discovered various evolutionary patterns of genomic rearrangements associated to Bs. In situ hybridization and quantitative polymerase chain reactions further validated our genomic approach confirming detection of sequences on Bs. The functional annotation of B sequences showed that the B chromosome comprises regions of gene fragments, novel genes, and intact genes, which encode a diverse set of functions related to important biological processes such as metabolism, morphogenesis, reproduction, transposition, recombination, cell cycle and chromosomes functions which might be important for their evolutionary success. Conclusions: This study reveals the genomic structure, composition and function of Bs, which provide new insights for theories of B chromosome evolution. The selfish behavior of Bs seems to be favored by gained genes/sequences.Department of Structural and Functional Biology Institute of Bioscience at Botucatu Sao Paulo State University (UNESP)Western Paraná State University (UNIOESTE) Center for Biology Science and HealthDepartment of General and Applied Biology Institute of Biosciences Sao Paulo State University (UNESP)Department of Molecular and Cell Biology University of Connecticut (UCONN)Institute for Systems Genomics University of Connecticut (UCONN)Bioprocess and Biotechnology Department Agronomical Science Faculty Sao Paulo State University - UNESPDepartment of Structural and Functional Biology Institute of Bioscience at Botucatu Sao Paulo State University (UNESP)Department of General and Applied Biology Institute of Biosciences Sao Paulo State University (UNESP)Bioprocess and Biotechnology Department Agronomical Science Faculty Sao Paulo State University - UNESPUniversidade Estadual Paulista (Unesp)Center for Biology Science and HealthUniversity of Connecticut (UCONN)Ahmad, Syed F. [UNESP]Jehangir, Maryam [UNESP]Cardoso, Adauto L. [UNESP]Wolf, Ivan R. [UNESP]Margarido, Vladimir P.Cabral-De-Mello, Diogo C. [UNESP]O'Neill, RachelValente, Guilherme T. [UNESP]Martins, Cesar [UNESP]2021-06-25T11:04:31Z2021-06-25T11:04:31Z2020-09-23info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.1186/s12864-020-07072-1BMC Genomics, v. 21, n. 1, 2020.1471-2164http://hdl.handle.net/11449/20799010.1186/s12864-020-07072-12-s2.0-85091539666Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengBMC Genomicsinfo:eu-repo/semantics/openAccess2021-10-23T18:47:10Zoai:repositorio.unesp.br:11449/207990Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462021-10-23T18:47:10Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv B chromosomes of multiple species have intense evolutionary dynamics and accumulated genes related to important biological processes
title B chromosomes of multiple species have intense evolutionary dynamics and accumulated genes related to important biological processes
spellingShingle B chromosomes of multiple species have intense evolutionary dynamics and accumulated genes related to important biological processes
Ahmad, Syed F. [UNESP]
Evolution
Extra chromosome
Genome
Next generation sequencing
Supernumerary chromosome
title_short B chromosomes of multiple species have intense evolutionary dynamics and accumulated genes related to important biological processes
title_full B chromosomes of multiple species have intense evolutionary dynamics and accumulated genes related to important biological processes
title_fullStr B chromosomes of multiple species have intense evolutionary dynamics and accumulated genes related to important biological processes
title_full_unstemmed B chromosomes of multiple species have intense evolutionary dynamics and accumulated genes related to important biological processes
title_sort B chromosomes of multiple species have intense evolutionary dynamics and accumulated genes related to important biological processes
author Ahmad, Syed F. [UNESP]
author_facet Ahmad, Syed F. [UNESP]
Jehangir, Maryam [UNESP]
Cardoso, Adauto L. [UNESP]
Wolf, Ivan R. [UNESP]
Margarido, Vladimir P.
Cabral-De-Mello, Diogo C. [UNESP]
O'Neill, Rachel
Valente, Guilherme T. [UNESP]
Martins, Cesar [UNESP]
author_role author
author2 Jehangir, Maryam [UNESP]
Cardoso, Adauto L. [UNESP]
Wolf, Ivan R. [UNESP]
Margarido, Vladimir P.
Cabral-De-Mello, Diogo C. [UNESP]
O'Neill, Rachel
Valente, Guilherme T. [UNESP]
Martins, Cesar [UNESP]
author2_role author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Universidade Estadual Paulista (Unesp)
Center for Biology Science and Health
University of Connecticut (UCONN)
dc.contributor.author.fl_str_mv Ahmad, Syed F. [UNESP]
Jehangir, Maryam [UNESP]
Cardoso, Adauto L. [UNESP]
Wolf, Ivan R. [UNESP]
Margarido, Vladimir P.
Cabral-De-Mello, Diogo C. [UNESP]
O'Neill, Rachel
Valente, Guilherme T. [UNESP]
Martins, Cesar [UNESP]
dc.subject.por.fl_str_mv Evolution
Extra chromosome
Genome
Next generation sequencing
Supernumerary chromosome
topic Evolution
Extra chromosome
Genome
Next generation sequencing
Supernumerary chromosome
description Background: One of the biggest challenges in chromosome biology is to understand the occurrence and complex genetics of the extra, non-essential karyotype elements, commonly known as supernumerary or B chromosomes (Bs). The non-Mendelian inheritance and non-pairing abilities of B chromosomes make them an interesting model for genomics studies, thus bringing to bear different questions about their genetic composition, evolutionary survival, maintenance and functional role inside the cell. This study uncovers these phenomena in multiple species that we considered as representative organisms of both vertebrate and invertebrate models for B chromosome analysis. Results: We sequenced the genomes of three animal species including two fishes Astyanax mexicanus and Astyanax correntinus, and a grasshopper Abracris flavolineata, each with and without Bs, and identified their B-localized genes and repeat contents. We detected unique sequences occurring exclusively on Bs and discovered various evolutionary patterns of genomic rearrangements associated to Bs. In situ hybridization and quantitative polymerase chain reactions further validated our genomic approach confirming detection of sequences on Bs. The functional annotation of B sequences showed that the B chromosome comprises regions of gene fragments, novel genes, and intact genes, which encode a diverse set of functions related to important biological processes such as metabolism, morphogenesis, reproduction, transposition, recombination, cell cycle and chromosomes functions which might be important for their evolutionary success. Conclusions: This study reveals the genomic structure, composition and function of Bs, which provide new insights for theories of B chromosome evolution. The selfish behavior of Bs seems to be favored by gained genes/sequences.
publishDate 2020
dc.date.none.fl_str_mv 2020-09-23
2021-06-25T11:04:31Z
2021-06-25T11:04:31Z
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/s12864-020-07072-1
BMC Genomics, v. 21, n. 1, 2020.
1471-2164
http://hdl.handle.net/11449/207990
10.1186/s12864-020-07072-1
2-s2.0-85091539666
url http://dx.doi.org/10.1186/s12864-020-07072-1
http://hdl.handle.net/11449/207990
identifier_str_mv BMC Genomics, v. 21, n. 1, 2020.
1471-2164
10.1186/s12864-020-07072-1
2-s2.0-85091539666
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv BMC Genomics
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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