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

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          Abstract

          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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          Most cited references86

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          Streaming fragment assignment for real-time analysis of sequencing experiments

          We present eXpress, a software package for highly efficient probabilistic assignment of ambiguously mapping sequenced fragments. eXpress uses a streaming algorithm with linear run time and constant memory use. It can determine abundances of sequenced molecules in real time, and can be applied to ChIP-seq, metagenomics and other large-scale sequencing data. We demonstrate its use on RNA-seq data, showing greater efficiency than other quantification methods.
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            Moderated statistical tests for assessing differences in tag abundance.

            Digital gene expression (DGE) technologies measure gene expression by counting sequence tags. They are sensitive technologies for measuring gene expression on a genomic scale, without the need for prior knowledge of the genome sequence. As the cost of sequencing DNA decreases, the number of DGE datasets is expected to grow dramatically. Various tests of differential expression have been proposed for replicated DGE data using binomial, Poisson, negative binomial or pseudo-likelihood (PL) models for the counts, but none of the these are usable when the number of replicates is very small. We develop tests using the negative binomial distribution to model overdispersion relative to the Poisson, and use conditional weighted likelihood to moderate the level of overdispersion across genes. Not only is our strategy applicable even with the smallest number of libraries, but it also proves to be more powerful than previous strategies when more libraries are available. The methodology is equally applicable to other counting technologies, such as proteomic spectral counts. An R package can be accessed from http://bioinf.wehi.edu.au/resources/
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              The rapid evolution of reproductive proteins.

              Many genes that mediate sexual reproduction, such as those involved in gamete recognition, diverge rapidly, often as a result of adaptive evolution. This widespread phenomenon might have important consequences, such as the establishment of barriers to fertilization that might lead to speciation. Sequence comparisons and functional studies are beginning to show the extent to which the rapid divergence of reproductive proteins is involved in the speciation process.
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                Author and article information

                Contributors
                eshita.sharma@tuebingen.mpg.de
                axel.kuenstner@tuebingen.mpg.de
                bonnie.fraser@tuebingen.mpg.de
                g.zipprich@dkfz-heidelberg.de
                verena.kottler@tuebingen.mpg.de
                stefan.henz@tuebingen.mpg.de
                detlef.weigel@tuebingen.mpg.de
                christine.dreyer@tuebingen.mpg.de
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                26 May 2014
                26 May 2014
                2014
                : 15
                : 1
                : 400
                Affiliations
                [ ]Department of Molecular Biology, Max Planck Institute for Developmental Biology, Spemannstrasse 37, 72076 Tübingen, Germany
                [ ]Bioinformatics and Statistical Genetics Core, Wellcome Trust Centre for Human Genetics, Roosevelt Drive, OX3 7BN Oxford, UK
                [ ]Division of Theoretical Bioinformatics, German Cancer Research Center, Im Neuenheimer Feld 280, 69120 Heidelberg, Germany
                Article
                6114
                10.1186/1471-2164-15-400
                4059875
                24886435
                e4e09b19-64f3-4462-8258-1b7d0e2edc7a
                © 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.

                History
                : 6 January 2014
                : 9 May 2014
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2014

                Genetics
                guppy,de novo transcriptome,genome-guided transcriptome,sex-biased genes,sexual dimorphism,rna-seq,coding sequence evolution

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