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Clustering of Sex-Biased Genes and Transposable Elements in the Genome of the Medaka Fish Oryzias latipes

Although genes with similar expression patterns are sometimes found in the same genomic regions, almost nothing is known about the relative organization in genomes of genes and transposable elements (TEs), which might influence each other at the regulatory level. In this study, we used transcriptomi...

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Autores principales: Dechaud, Corentin, Miyake, Sho, Martinez-Bengochea, Anabel, Schartl, Manfred, Volff, Jean-Nicolas, Naville, Magali
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8633743/
https://www.ncbi.nlm.nih.gov/pubmed/34623422
http://dx.doi.org/10.1093/gbe/evab230
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author Dechaud, Corentin
Miyake, Sho
Martinez-Bengochea, Anabel
Schartl, Manfred
Volff, Jean-Nicolas
Naville, Magali
author_facet Dechaud, Corentin
Miyake, Sho
Martinez-Bengochea, Anabel
Schartl, Manfred
Volff, Jean-Nicolas
Naville, Magali
author_sort Dechaud, Corentin
collection PubMed
description Although genes with similar expression patterns are sometimes found in the same genomic regions, almost nothing is known about the relative organization in genomes of genes and transposable elements (TEs), which might influence each other at the regulatory level. In this study, we used transcriptomic data from male and female gonads of the Japanese medaka Oryzias latipes to define sexually biased genes and TEs and analyze their relative genomic localization. We identified 20,588 genes expressed in the adult gonads of O. latipes. Around 39% of these genes are differentially expressed between male and female gonads. We further analyzed the expression of TEs using the program SQuIRE and showed that more TE copies are overexpressed in testis than in ovaries (36% vs. 10%, respectively). We then developed a method to detect genomic regions enriched in testis- or ovary-biased genes. This revealed that sex-biased genes and TEs are not randomly distributed in the genome and a part of them form clusters with the same expression bias. We also found a correlation of expression between TE copies and their closest genes, which increases with decreasing intervening distance. Such a genomic organization suggests either that TEs hijack the regulatory sequences of neighboring sexual genes, allowing their expression in germ line cells and consequently new insertions to be transmitted to the next generation, or that TEs are involved in the regulation of sexual genes, and might therefore through their mobility participate in the rewiring of sex regulatory networks.
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spelling pubmed-86337432021-12-01 Clustering of Sex-Biased Genes and Transposable Elements in the Genome of the Medaka Fish Oryzias latipes Dechaud, Corentin Miyake, Sho Martinez-Bengochea, Anabel Schartl, Manfred Volff, Jean-Nicolas Naville, Magali Genome Biol Evol Research Article Although genes with similar expression patterns are sometimes found in the same genomic regions, almost nothing is known about the relative organization in genomes of genes and transposable elements (TEs), which might influence each other at the regulatory level. In this study, we used transcriptomic data from male and female gonads of the Japanese medaka Oryzias latipes to define sexually biased genes and TEs and analyze their relative genomic localization. We identified 20,588 genes expressed in the adult gonads of O. latipes. Around 39% of these genes are differentially expressed between male and female gonads. We further analyzed the expression of TEs using the program SQuIRE and showed that more TE copies are overexpressed in testis than in ovaries (36% vs. 10%, respectively). We then developed a method to detect genomic regions enriched in testis- or ovary-biased genes. This revealed that sex-biased genes and TEs are not randomly distributed in the genome and a part of them form clusters with the same expression bias. We also found a correlation of expression between TE copies and their closest genes, which increases with decreasing intervening distance. Such a genomic organization suggests either that TEs hijack the regulatory sequences of neighboring sexual genes, allowing their expression in germ line cells and consequently new insertions to be transmitted to the next generation, or that TEs are involved in the regulation of sexual genes, and might therefore through their mobility participate in the rewiring of sex regulatory networks. Oxford University Press 2021-10-08 /pmc/articles/PMC8633743/ /pubmed/34623422 http://dx.doi.org/10.1093/gbe/evab230 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Dechaud, Corentin
Miyake, Sho
Martinez-Bengochea, Anabel
Schartl, Manfred
Volff, Jean-Nicolas
Naville, Magali
Clustering of Sex-Biased Genes and Transposable Elements in the Genome of the Medaka Fish Oryzias latipes
title Clustering of Sex-Biased Genes and Transposable Elements in the Genome of the Medaka Fish Oryzias latipes
title_full Clustering of Sex-Biased Genes and Transposable Elements in the Genome of the Medaka Fish Oryzias latipes
title_fullStr Clustering of Sex-Biased Genes and Transposable Elements in the Genome of the Medaka Fish Oryzias latipes
title_full_unstemmed Clustering of Sex-Biased Genes and Transposable Elements in the Genome of the Medaka Fish Oryzias latipes
title_short Clustering of Sex-Biased Genes and Transposable Elements in the Genome of the Medaka Fish Oryzias latipes
title_sort clustering of sex-biased genes and transposable elements in the genome of the medaka fish oryzias latipes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8633743/
https://www.ncbi.nlm.nih.gov/pubmed/34623422
http://dx.doi.org/10.1093/gbe/evab230
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