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Transcriptome assemblies for studying sex-biased gene expression in the guppy, Poecilia reticulata

BACKGROUND: Sexually dimorphic phenotypes are generally associated with differential gene expression between the sexes. The study of molecular evolution and genomic location of these differentially expressed, or sex-biased, genes is important for understanding inter-sexual divergence under sex-speci...

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Autores principales: Sharma, Eshita, Künstner, Axel, Fraser, Bonnie A, Zipprich, Gideon, Kottler, Verena A, Henz, Stefan R, Weigel, Detlef, Dreyer, Christine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4059875/
https://www.ncbi.nlm.nih.gov/pubmed/24886435
http://dx.doi.org/10.1186/1471-2164-15-400
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author Sharma, Eshita
Künstner, Axel
Fraser, Bonnie A
Zipprich, Gideon
Kottler, Verena A
Henz, Stefan R
Weigel, Detlef
Dreyer, Christine
author_facet Sharma, Eshita
Künstner, Axel
Fraser, Bonnie A
Zipprich, Gideon
Kottler, Verena A
Henz, Stefan R
Weigel, Detlef
Dreyer, Christine
author_sort Sharma, Eshita
collection PubMed
description BACKGROUND: Sexually dimorphic phenotypes are generally associated with differential gene expression between the sexes. The study of molecular evolution and genomic location of these differentially expressed, or sex-biased, genes is important for understanding inter-sexual divergence under sex-specific selection pressures. Teleost fish provide a unique opportunity to examine this divergence in the presence of variable sex-determination mechanisms of recent origin. The guppy, Poecilia reticulata, displays sexual dimorphism in size, ornaments, and behavior, traits shaped by natural and sexual selection in the wild. RESULTS: To gain insight into molecular mechanisms underlying the guppy’s sexual dimorphism, we assembled a reference transcriptome combining genome-independent as well as genome-guided assemblies and analyzed sex-biased gene expression between different tissues of adult male and female guppies. We found tissue-associated sex-biased expression of genes related to pigmentation, signal transduction, and spermatogenesis in males; and growth, cell-division, extra-cellular matrix organization, nutrient transport, and folliculogenesis in females. While most sex-biased genes were randomly distributed across linkage groups, we observed accumulation of ovary-biased genes on the sex linkage group, LG12. Both testis-biased and ovary-biased genes showed a significantly higher rate of non-synonymous to synonymous substitutions (d(N)/d(S)) compared to unbiased genes. However, in somatic tissues only female-biased genes, including those co-expressed in multiple tissues, showed elevated ratios of non-synonymous substitutions. CONCLUSIONS: Our work identifies a set of annotated gene products that are candidate factors affecting sexual dimorphism in guppies. The differential genomic distribution of gonad-biased genes provides evidence for sex-specific selection pressures acting on the nascent sex chromosomes of the guppy. The elevated rates of evolution of testis-biased and female-biased genes indicate differing evolution under distinct selection pressures on the reproductive versus non-reproductive tissues. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-400) contains supplementary material, which is available to authorized users.
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spelling pubmed-40598752014-06-19 Transcriptome assemblies for studying sex-biased gene expression in the guppy, Poecilia reticulata Sharma, Eshita Künstner, Axel Fraser, Bonnie A Zipprich, Gideon Kottler, Verena A Henz, Stefan R Weigel, Detlef Dreyer, Christine BMC Genomics Research Article BACKGROUND: Sexually dimorphic phenotypes are generally associated with differential gene expression between the sexes. The study of molecular evolution and genomic location of these differentially expressed, or sex-biased, genes is important for understanding inter-sexual divergence under sex-specific selection pressures. Teleost fish provide a unique opportunity to examine this divergence in the presence of variable sex-determination mechanisms of recent origin. The guppy, Poecilia reticulata, displays sexual dimorphism in size, ornaments, and behavior, traits shaped by natural and sexual selection in the wild. RESULTS: To gain insight into molecular mechanisms underlying the guppy’s sexual dimorphism, we assembled a reference transcriptome combining genome-independent as well as genome-guided assemblies and analyzed sex-biased gene expression between different tissues of adult male and female guppies. We found tissue-associated sex-biased expression of genes related to pigmentation, signal transduction, and spermatogenesis in males; and growth, cell-division, extra-cellular matrix organization, nutrient transport, and folliculogenesis in females. While most sex-biased genes were randomly distributed across linkage groups, we observed accumulation of ovary-biased genes on the sex linkage group, LG12. Both testis-biased and ovary-biased genes showed a significantly higher rate of non-synonymous to synonymous substitutions (d(N)/d(S)) compared to unbiased genes. However, in somatic tissues only female-biased genes, including those co-expressed in multiple tissues, showed elevated ratios of non-synonymous substitutions. CONCLUSIONS: Our work identifies a set of annotated gene products that are candidate factors affecting sexual dimorphism in guppies. The differential genomic distribution of gonad-biased genes provides evidence for sex-specific selection pressures acting on the nascent sex chromosomes of the guppy. The elevated rates of evolution of testis-biased and female-biased genes indicate differing evolution under distinct selection pressures on the reproductive versus non-reproductive tissues. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-400) contains supplementary material, which is available to authorized users. BioMed Central 2014-05-26 /pmc/articles/PMC4059875/ /pubmed/24886435 http://dx.doi.org/10.1186/1471-2164-15-400 Text en © Sharma et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Sharma, Eshita
Künstner, Axel
Fraser, Bonnie A
Zipprich, Gideon
Kottler, Verena A
Henz, Stefan R
Weigel, Detlef
Dreyer, Christine
Transcriptome assemblies for studying sex-biased gene expression in the guppy, Poecilia reticulata
title Transcriptome assemblies for studying sex-biased gene expression in the guppy, Poecilia reticulata
title_full Transcriptome assemblies for studying sex-biased gene expression in the guppy, Poecilia reticulata
title_fullStr Transcriptome assemblies for studying sex-biased gene expression in the guppy, Poecilia reticulata
title_full_unstemmed Transcriptome assemblies for studying sex-biased gene expression in the guppy, Poecilia reticulata
title_short Transcriptome assemblies for studying sex-biased gene expression in the guppy, Poecilia reticulata
title_sort transcriptome assemblies for studying sex-biased gene expression in the guppy, poecilia reticulata
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4059875/
https://www.ncbi.nlm.nih.gov/pubmed/24886435
http://dx.doi.org/10.1186/1471-2164-15-400
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