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

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...

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Autores principales: Oliveira, Jordana Inácio Nascimento, Cardoso, Adauto Lima, Wolf, Ivan Rodrigo, de Oliveira, Rogério Antônio, Martins, Cesar
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9490952/
https://www.ncbi.nlm.nih.gov/pubmed/36127679
http://dx.doi.org/10.1186/s12915-022-01403-2
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author Oliveira, Jordana Inácio Nascimento
Cardoso, Adauto Lima
Wolf, Ivan Rodrigo
de Oliveira, Rogério Antônio
Martins, Cesar
author_facet Oliveira, Jordana Inácio Nascimento
Cardoso, Adauto Lima
Wolf, Ivan Rodrigo
de Oliveira, Rogério Antônio
Martins, Cesar
author_sort Oliveira, Jordana Inácio Nascimento
collection PubMed
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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01403-2.
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spelling pubmed-94909522022-09-22 First characterization of PIWI-interacting RNA clusters in a cichlid fish with a B chromosome Oliveira, Jordana Inácio Nascimento Cardoso, Adauto Lima Wolf, Ivan Rodrigo de Oliveira, Rogério Antônio Martins, Cesar BMC Biol Research Article 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01403-2. BioMed Central 2022-09-21 /pmc/articles/PMC9490952/ /pubmed/36127679 http://dx.doi.org/10.1186/s12915-022-01403-2 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Oliveira, Jordana Inácio Nascimento
Cardoso, Adauto Lima
Wolf, Ivan Rodrigo
de Oliveira, Rogério Antônio
Martins, Cesar
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
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
title_full_unstemmed First characterization of PIWI-interacting RNA clusters in a cichlid fish with a B chromosome
title_short 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
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9490952/
https://www.ncbi.nlm.nih.gov/pubmed/36127679
http://dx.doi.org/10.1186/s12915-022-01403-2
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