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Comparing the transcriptomes of embryos from domesticated and wild Atlantic salmon (Salmo salar L.) stocks and examining factors that influence heritability of gene expression

BACKGROUND: Due to selective breeding, domesticated and wild Atlantic salmon are genetically diverged, which raises concerns about farmed escapees having the potential to alter the genetic composition of wild populations and thereby disrupting local adaptation. Documenting transcriptional difference...

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Autores principales: Bicskei, Beatrix, Taggart, John B., Glover, Kevin A., Bron, James E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4797325/
https://www.ncbi.nlm.nih.gov/pubmed/26987528
http://dx.doi.org/10.1186/s12711-016-0200-6
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author Bicskei, Beatrix
Taggart, John B.
Glover, Kevin A.
Bron, James E.
author_facet Bicskei, Beatrix
Taggart, John B.
Glover, Kevin A.
Bron, James E.
author_sort Bicskei, Beatrix
collection PubMed
description BACKGROUND: Due to selective breeding, domesticated and wild Atlantic salmon are genetically diverged, which raises concerns about farmed escapees having the potential to alter the genetic composition of wild populations and thereby disrupting local adaptation. Documenting transcriptional differences between wild and domesticated stocks under controlled conditions is one way to explore the consequences of domestication and selection. We compared the transcriptomes of wild and domesticated Atlantic salmon embryos, by using a custom 44k oligonucleotide microarray to identify perturbed gene pathways between the two stocks, and to document the inheritance patterns of differentially-expressed genes by examining gene expression in their reciprocal hybrids. RESULTS: Data from 24 array interrogations were analysed: four reciprocal cross types (W♀ × W♂, D♀ × W♂; W♀ × D♂, D♀ × D♂) × six biological replicates. A common set of 31,491 features on the microarrays passed quality control, of which about 62 % were assigned a KEGG Orthology number. A total of 6037 distinct genes were identified for gene-set enrichment/pathway analysis. The most highly enriched functional groups that were perturbed between the two stocks were cellular signalling and immune system, ribosome and RNA transport, and focal adhesion and gap junction pathways, relating to cell communication and cell adhesion molecules. Most transcripts that were differentially expressed between the stocks were governed by additive gene interaction (33 to 42 %). Maternal dominance and over-dominance were also prevalent modes of inheritance, with no convincing evidence for a stock effect. CONCLUSIONS: Our data indicate that even at this relatively early developmental stage, transcriptional differences exist between the two stocks and affect pathways that are relevant to wild versus domesticated environments. Many of the identified differentially perturbed pathways are involved in organogenesis, which is expected to be an active process at the eyed egg stage. The dominant effects are more largely due to the maternal line than to the origin of the stock. This finding is particularly relevant in the context of potential introgression between farmed and wild fish, since female escapees tend to have a higher spawning success rate compared to males. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12711-016-0200-6) contains supplementary material, which is available to authorized users.
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spelling pubmed-47973252016-03-19 Comparing the transcriptomes of embryos from domesticated and wild Atlantic salmon (Salmo salar L.) stocks and examining factors that influence heritability of gene expression Bicskei, Beatrix Taggart, John B. Glover, Kevin A. Bron, James E. Genet Sel Evol Research Article BACKGROUND: Due to selective breeding, domesticated and wild Atlantic salmon are genetically diverged, which raises concerns about farmed escapees having the potential to alter the genetic composition of wild populations and thereby disrupting local adaptation. Documenting transcriptional differences between wild and domesticated stocks under controlled conditions is one way to explore the consequences of domestication and selection. We compared the transcriptomes of wild and domesticated Atlantic salmon embryos, by using a custom 44k oligonucleotide microarray to identify perturbed gene pathways between the two stocks, and to document the inheritance patterns of differentially-expressed genes by examining gene expression in their reciprocal hybrids. RESULTS: Data from 24 array interrogations were analysed: four reciprocal cross types (W♀ × W♂, D♀ × W♂; W♀ × D♂, D♀ × D♂) × six biological replicates. A common set of 31,491 features on the microarrays passed quality control, of which about 62 % were assigned a KEGG Orthology number. A total of 6037 distinct genes were identified for gene-set enrichment/pathway analysis. The most highly enriched functional groups that were perturbed between the two stocks were cellular signalling and immune system, ribosome and RNA transport, and focal adhesion and gap junction pathways, relating to cell communication and cell adhesion molecules. Most transcripts that were differentially expressed between the stocks were governed by additive gene interaction (33 to 42 %). Maternal dominance and over-dominance were also prevalent modes of inheritance, with no convincing evidence for a stock effect. CONCLUSIONS: Our data indicate that even at this relatively early developmental stage, transcriptional differences exist between the two stocks and affect pathways that are relevant to wild versus domesticated environments. Many of the identified differentially perturbed pathways are involved in organogenesis, which is expected to be an active process at the eyed egg stage. The dominant effects are more largely due to the maternal line than to the origin of the stock. This finding is particularly relevant in the context of potential introgression between farmed and wild fish, since female escapees tend to have a higher spawning success rate compared to males. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12711-016-0200-6) contains supplementary material, which is available to authorized users. BioMed Central 2016-03-17 /pmc/articles/PMC4797325/ /pubmed/26987528 http://dx.doi.org/10.1186/s12711-016-0200-6 Text en © Bicskei et al. 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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
Bicskei, Beatrix
Taggart, John B.
Glover, Kevin A.
Bron, James E.
Comparing the transcriptomes of embryos from domesticated and wild Atlantic salmon (Salmo salar L.) stocks and examining factors that influence heritability of gene expression
title Comparing the transcriptomes of embryos from domesticated and wild Atlantic salmon (Salmo salar L.) stocks and examining factors that influence heritability of gene expression
title_full Comparing the transcriptomes of embryos from domesticated and wild Atlantic salmon (Salmo salar L.) stocks and examining factors that influence heritability of gene expression
title_fullStr Comparing the transcriptomes of embryos from domesticated and wild Atlantic salmon (Salmo salar L.) stocks and examining factors that influence heritability of gene expression
title_full_unstemmed Comparing the transcriptomes of embryos from domesticated and wild Atlantic salmon (Salmo salar L.) stocks and examining factors that influence heritability of gene expression
title_short Comparing the transcriptomes of embryos from domesticated and wild Atlantic salmon (Salmo salar L.) stocks and examining factors that influence heritability of gene expression
title_sort comparing the transcriptomes of embryos from domesticated and wild atlantic salmon (salmo salar l.) stocks and examining factors that influence heritability of gene expression
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4797325/
https://www.ncbi.nlm.nih.gov/pubmed/26987528
http://dx.doi.org/10.1186/s12711-016-0200-6
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