First characterization of PIWI-interacting RNA clusters in a cichlid fish with a B chromosome

Detalhes bibliográficos
Autor(a) principal: Oliveira, Jordana Inácio Nascimento [UNESP]
Data de Publicação: 2022
Outros Autores: Cardoso, Adauto Lima [UNESP], Wolf, Ivan Rodrigo [UNESP], de Oliveira, Rogério Antônio [UNESP], Martins, Cesar [UNESP]
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
DOI: 10.1186/s12915-022-01403-2
Texto Completo: http://dx.doi.org/10.1186/s12915-022-01403-2
http://hdl.handle.net/11449/247632
Resumo: Background: B chromosomes are extra elements found in several eukaryote species. Usually, they do not express a phenotype in the host. However, advances in bioinformatics over the last decades have allowed us to describe several genes and molecular functions related to B chromosomes. These advances enable investigations of the relationship between the B chromosome and the host to understand how this element has been preserved in genomes. However, considering that transposable elements (TEs) are highly abundant in this supernumerary chromosome, there is a lack of knowledge concerning the dynamics of TE control in B-carrying cells. Thus, the present study characterized PIWI-interacting RNA (piRNA) clusters and pathways responsible for silencing the mobilization of TEs in gonads of the cichlid fish Astatotilapia latifasciata carrying the B chromosome. Results: Through small RNA-seq and genome assembly, we predicted and annotated piRNA clusters in the A. latifasciata genome for the first time. We observed that these clusters had biased expression related to sex and the presence of the B chromosome. Furthermore, three piRNA clusters, named curupira, were identified in the B chromosome. Two of them were expressed exclusively in gonads of samples with the B chromosome. The composition of these curupira sequences was derived from LTR, LINE, and DNA elements, representing old and recent transposition events in the A. latifasciata genome and the B chromosome. The presence of the B chromosome also affected the expression of piRNA pathway genes. The mitochondrial cardiolipin hydrolase-like (pld6) gene is present in the B chromosome, as previously reported, and an increase in its expression was detected in gonads with the B chromosome. Conclusions: Due to the high abundance of TEs in the B chromosome, it was possible to investigate the origin of piRNA from these jumping genes. We hypothesize that the B chromosome has evolved its own genomic guardians to prevent uncontrolled TE mobilization. Furthermore, we also detected an expression bias in the presence of the B chromosome over A. latifasciata piRNA clusters and pathway genes.
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spelling First characterization of PIWI-interacting RNA clusters in a cichlid fish with a B chromosomeAfrican cichlid fishArms raceGenome evolutionpiRNAsSmall noncoding RNAsSupernumerary chromosomeTransposable elementsBackground: B chromosomes are extra elements found in several eukaryote species. Usually, they do not express a phenotype in the host. However, advances in bioinformatics over the last decades have allowed us to describe several genes and molecular functions related to B chromosomes. These advances enable investigations of the relationship between the B chromosome and the host to understand how this element has been preserved in genomes. However, considering that transposable elements (TEs) are highly abundant in this supernumerary chromosome, there is a lack of knowledge concerning the dynamics of TE control in B-carrying cells. Thus, the present study characterized PIWI-interacting RNA (piRNA) clusters and pathways responsible for silencing the mobilization of TEs in gonads of the cichlid fish Astatotilapia latifasciata carrying the B chromosome. Results: Through small RNA-seq and genome assembly, we predicted and annotated piRNA clusters in the A. latifasciata genome for the first time. We observed that these clusters had biased expression related to sex and the presence of the B chromosome. Furthermore, three piRNA clusters, named curupira, were identified in the B chromosome. Two of them were expressed exclusively in gonads of samples with the B chromosome. The composition of these curupira sequences was derived from LTR, LINE, and DNA elements, representing old and recent transposition events in the A. latifasciata genome and the B chromosome. The presence of the B chromosome also affected the expression of piRNA pathway genes. The mitochondrial cardiolipin hydrolase-like (pld6) gene is present in the B chromosome, as previously reported, and an increase in its expression was detected in gonads with the B chromosome. Conclusions: Due to the high abundance of TEs in the B chromosome, it was possible to investigate the origin of piRNA from these jumping genes. We hypothesize that the B chromosome has evolved its own genomic guardians to prevent uncontrolled TE mobilization. Furthermore, we also detected an expression bias in the presence of the B chromosome over A. latifasciata piRNA clusters and pathway genes.Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)Department of Structural and Functional Biology Institute of Bioscience at Botucatu São Paulo State University (UNESP), SPDepartment of Biostatistics Plant Biology Parasitology and Zoology Institute of Bioscience at Botucatu São Paulo State University (UNESP), SPDepartment of Structural and Functional Biology Institute of Bioscience at Botucatu São Paulo State University (UNESP), SPDepartment of Biostatistics Plant Biology Parasitology and Zoology Institute of Bioscience at Botucatu São Paulo State University (UNESP), SPFAPESP: 2015/16661-1FAPESP: 2016/09320-6CNPq: 304111/2020-1Universidade Estadual Paulista (UNESP)Oliveira, Jordana Inácio Nascimento [UNESP]Cardoso, Adauto Lima [UNESP]Wolf, Ivan Rodrigo [UNESP]de Oliveira, Rogério Antônio [UNESP]Martins, Cesar [UNESP]2023-07-29T13:21:30Z2023-07-29T13:21:30Z2022-12-01info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.1186/s12915-022-01403-2BMC Biology, v. 20, n. 1, 2022.1741-7007http://hdl.handle.net/11449/24763210.1186/s12915-022-01403-22-s2.0-85138212827Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengBMC Biologyinfo:eu-repo/semantics/openAccess2023-07-29T13:21:30Zoai:repositorio.unesp.br:11449/247632Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-08-05T18:50:33.096857Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv First characterization of PIWI-interacting RNA clusters in a cichlid fish with a B chromosome
title First characterization of PIWI-interacting RNA clusters in a cichlid fish with a B chromosome
spellingShingle First characterization of PIWI-interacting RNA clusters in a cichlid fish with a B chromosome
First characterization of PIWI-interacting RNA clusters in a cichlid fish with a B chromosome
Oliveira, Jordana Inácio Nascimento [UNESP]
African cichlid fish
Arms race
Genome evolution
piRNAs
Small noncoding RNAs
Supernumerary chromosome
Transposable elements
Oliveira, Jordana Inácio Nascimento [UNESP]
African cichlid fish
Arms race
Genome evolution
piRNAs
Small noncoding RNAs
Supernumerary chromosome
Transposable elements
title_short First characterization of PIWI-interacting RNA clusters in a cichlid fish with a B chromosome
title_full First characterization of PIWI-interacting RNA clusters in a cichlid fish with a B chromosome
title_fullStr First characterization of PIWI-interacting RNA clusters in a cichlid fish with a B chromosome
First characterization of PIWI-interacting RNA clusters in a cichlid fish with a B chromosome
title_full_unstemmed First characterization of PIWI-interacting RNA clusters in a cichlid fish with a B chromosome
First characterization of PIWI-interacting RNA clusters in a cichlid fish with a B chromosome
title_sort First characterization of PIWI-interacting RNA clusters in a cichlid fish with a B chromosome
author Oliveira, Jordana Inácio Nascimento [UNESP]
author_facet Oliveira, Jordana Inácio Nascimento [UNESP]
Oliveira, Jordana Inácio Nascimento [UNESP]
Cardoso, Adauto Lima [UNESP]
Wolf, Ivan Rodrigo [UNESP]
de Oliveira, Rogério Antônio [UNESP]
Martins, Cesar [UNESP]
Cardoso, Adauto Lima [UNESP]
Wolf, Ivan Rodrigo [UNESP]
de Oliveira, Rogério Antônio [UNESP]
Martins, Cesar [UNESP]
author_role author
author2 Cardoso, Adauto Lima [UNESP]
Wolf, Ivan Rodrigo [UNESP]
de Oliveira, Rogério Antônio [UNESP]
Martins, Cesar [UNESP]
author2_role author
author
author
author
dc.contributor.none.fl_str_mv Universidade Estadual Paulista (UNESP)
dc.contributor.author.fl_str_mv Oliveira, Jordana Inácio Nascimento [UNESP]
Cardoso, Adauto Lima [UNESP]
Wolf, Ivan Rodrigo [UNESP]
de Oliveira, Rogério Antônio [UNESP]
Martins, Cesar [UNESP]
dc.subject.por.fl_str_mv African cichlid fish
Arms race
Genome evolution
piRNAs
Small noncoding RNAs
Supernumerary chromosome
Transposable elements
topic African cichlid fish
Arms race
Genome evolution
piRNAs
Small noncoding RNAs
Supernumerary chromosome
Transposable elements
description Background: B chromosomes are extra elements found in several eukaryote species. Usually, they do not express a phenotype in the host. However, advances in bioinformatics over the last decades have allowed us to describe several genes and molecular functions related to B chromosomes. These advances enable investigations of the relationship between the B chromosome and the host to understand how this element has been preserved in genomes. However, considering that transposable elements (TEs) are highly abundant in this supernumerary chromosome, there is a lack of knowledge concerning the dynamics of TE control in B-carrying cells. Thus, the present study characterized PIWI-interacting RNA (piRNA) clusters and pathways responsible for silencing the mobilization of TEs in gonads of the cichlid fish Astatotilapia latifasciata carrying the B chromosome. Results: Through small RNA-seq and genome assembly, we predicted and annotated piRNA clusters in the A. latifasciata genome for the first time. We observed that these clusters had biased expression related to sex and the presence of the B chromosome. Furthermore, three piRNA clusters, named curupira, were identified in the B chromosome. Two of them were expressed exclusively in gonads of samples with the B chromosome. The composition of these curupira sequences was derived from LTR, LINE, and DNA elements, representing old and recent transposition events in the A. latifasciata genome and the B chromosome. The presence of the B chromosome also affected the expression of piRNA pathway genes. The mitochondrial cardiolipin hydrolase-like (pld6) gene is present in the B chromosome, as previously reported, and an increase in its expression was detected in gonads with the B chromosome. Conclusions: Due to the high abundance of TEs in the B chromosome, it was possible to investigate the origin of piRNA from these jumping genes. We hypothesize that the B chromosome has evolved its own genomic guardians to prevent uncontrolled TE mobilization. Furthermore, we also detected an expression bias in the presence of the B chromosome over A. latifasciata piRNA clusters and pathway genes.
publishDate 2022
dc.date.none.fl_str_mv 2022-12-01
2023-07-29T13:21:30Z
2023-07-29T13:21:30Z
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/s12915-022-01403-2
BMC Biology, v. 20, n. 1, 2022.
1741-7007
http://hdl.handle.net/11449/247632
10.1186/s12915-022-01403-2
2-s2.0-85138212827
url http://dx.doi.org/10.1186/s12915-022-01403-2
http://hdl.handle.net/11449/247632
identifier_str_mv BMC Biology, v. 20, n. 1, 2022.
1741-7007
10.1186/s12915-022-01403-2
2-s2.0-85138212827
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
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dc.identifier.doi.none.fl_str_mv 10.1186/s12915-022-01403-2