The initiation of puberty in Atlantic salmon brings about large changes in testicular gene expression that are modulated by the energy status

BACKGROUND: When puberty starts before males reach harvest size, animal welfare and sustainability issues occur in Atlantic salmon (Salmo salar) aquaculture. Hallmarks of male puberty are an increased proliferation activity in the testis and elevated androgen production. Examining transcriptional ch...

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Published in:BMC Genomics
Main Authors: Crespo, Diego, Bogerd, Jan, Sambroni, Elisabeth, LeGac, Florence, Andersson, Eva, Edvardsen, Rolf B., Bergman, Elisabeth Jönsson, Björnsson, Björn Thrandur, Taranger, Geir Lasse, Schulz, Rüdiger W.
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Language:English
Published: BioMed Central 2019
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Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6558769/
http://www.ncbi.nlm.nih.gov/pubmed/31185904
https://doi.org/10.1186/s12864-019-5869-9
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spelling ftpubmed:oai:pubmedcentral.nih.gov:6558769 2023-05-15T15:31:55+02:00 The initiation of puberty in Atlantic salmon brings about large changes in testicular gene expression that are modulated by the energy status Crespo, Diego Bogerd, Jan Sambroni, Elisabeth LeGac, Florence Andersson, Eva Edvardsen, Rolf B. Bergman, Elisabeth Jönsson Björnsson, Björn Thrandur Taranger, Geir Lasse Schulz, Rüdiger W. 2019-06-11 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6558769/ http://www.ncbi.nlm.nih.gov/pubmed/31185904 https://doi.org/10.1186/s12864-019-5869-9 en eng BioMed Central http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6558769/ http://www.ncbi.nlm.nih.gov/pubmed/31185904 http://dx.doi.org/10.1186/s12864-019-5869-9 © The Author(s). 2019 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. CC0 PDM CC-BY Research Article Text 2019 ftpubmed https://doi.org/10.1186/s12864-019-5869-9 2019-06-16T00:28:04Z BACKGROUND: When puberty starts before males reach harvest size, animal welfare and sustainability issues occur in Atlantic salmon (Salmo salar) aquaculture. Hallmarks of male puberty are an increased proliferation activity in the testis and elevated androgen production. Examining transcriptional changes in salmon testis during the transition from immature to maturing testes may help understanding the regulation of puberty, potentially leading to procedures to modulate its start. Since differences in body weight influence, via unknown mechanisms, the chances for entering puberty, we used two feed rations to create body weight differences. RESULTS: Maturing testes were characterized by an elevated proliferation activity of Sertoli cells and of single undifferentiated spermatogonia. Pituitary gene expression data suggest increased Gnrh receptor and gonadotropin gene expression, potentially responsible for the elevated circulating androgen levels in maturing fish. Transcriptional changes in maturing testes included a broad variety of signaling systems (e.g. Tgfβ, Wnt, insulin/Igf, nuclear receptors), but also, activation of metabolic pathways such as anaerobic metabolism and protection against ROS. Feed restriction lowered the incidence of puberty. In males maturing despite feed restriction, plasma androgen levels were higher than in maturing fish receiving the full ration. A group of 449 genes that were up-regulated in maturing fully fed fish, was up-regulated more prominently in testis from fish maturing under caloric restriction. Moreover, 421 genes were specifically up-regulated in testes from fish maturing under caloric restriction, including carbon metabolism genes, a pathway relevant for nucleotide biosynthesis and for placing epigenetic marks. CONCLUSIONS: Undifferentiated spermatogonia and Sertoli cell populations increased at the beginning of puberty, which was associated with the up-regulation of metabolic pathways (e.g. anaerobic and ROS pathways) known from other stem cell systems. The higher androgen ... Text Atlantic salmon Salmo salar PubMed Central (PMC) BMC Genomics 20 1
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Research Article
spellingShingle Research Article
Crespo, Diego
Bogerd, Jan
Sambroni, Elisabeth
LeGac, Florence
Andersson, Eva
Edvardsen, Rolf B.
Bergman, Elisabeth Jönsson
Björnsson, Björn Thrandur
Taranger, Geir Lasse
Schulz, Rüdiger W.
The initiation of puberty in Atlantic salmon brings about large changes in testicular gene expression that are modulated by the energy status
topic_facet Research Article
description BACKGROUND: When puberty starts before males reach harvest size, animal welfare and sustainability issues occur in Atlantic salmon (Salmo salar) aquaculture. Hallmarks of male puberty are an increased proliferation activity in the testis and elevated androgen production. Examining transcriptional changes in salmon testis during the transition from immature to maturing testes may help understanding the regulation of puberty, potentially leading to procedures to modulate its start. Since differences in body weight influence, via unknown mechanisms, the chances for entering puberty, we used two feed rations to create body weight differences. RESULTS: Maturing testes were characterized by an elevated proliferation activity of Sertoli cells and of single undifferentiated spermatogonia. Pituitary gene expression data suggest increased Gnrh receptor and gonadotropin gene expression, potentially responsible for the elevated circulating androgen levels in maturing fish. Transcriptional changes in maturing testes included a broad variety of signaling systems (e.g. Tgfβ, Wnt, insulin/Igf, nuclear receptors), but also, activation of metabolic pathways such as anaerobic metabolism and protection against ROS. Feed restriction lowered the incidence of puberty. In males maturing despite feed restriction, plasma androgen levels were higher than in maturing fish receiving the full ration. A group of 449 genes that were up-regulated in maturing fully fed fish, was up-regulated more prominently in testis from fish maturing under caloric restriction. Moreover, 421 genes were specifically up-regulated in testes from fish maturing under caloric restriction, including carbon metabolism genes, a pathway relevant for nucleotide biosynthesis and for placing epigenetic marks. CONCLUSIONS: Undifferentiated spermatogonia and Sertoli cell populations increased at the beginning of puberty, which was associated with the up-regulation of metabolic pathways (e.g. anaerobic and ROS pathways) known from other stem cell systems. The higher androgen ...
format Text
author Crespo, Diego
Bogerd, Jan
Sambroni, Elisabeth
LeGac, Florence
Andersson, Eva
Edvardsen, Rolf B.
Bergman, Elisabeth Jönsson
Björnsson, Björn Thrandur
Taranger, Geir Lasse
Schulz, Rüdiger W.
author_facet Crespo, Diego
Bogerd, Jan
Sambroni, Elisabeth
LeGac, Florence
Andersson, Eva
Edvardsen, Rolf B.
Bergman, Elisabeth Jönsson
Björnsson, Björn Thrandur
Taranger, Geir Lasse
Schulz, Rüdiger W.
author_sort Crespo, Diego
title The initiation of puberty in Atlantic salmon brings about large changes in testicular gene expression that are modulated by the energy status
title_short The initiation of puberty in Atlantic salmon brings about large changes in testicular gene expression that are modulated by the energy status
title_full The initiation of puberty in Atlantic salmon brings about large changes in testicular gene expression that are modulated by the energy status
title_fullStr The initiation of puberty in Atlantic salmon brings about large changes in testicular gene expression that are modulated by the energy status
title_full_unstemmed The initiation of puberty in Atlantic salmon brings about large changes in testicular gene expression that are modulated by the energy status
title_sort initiation of puberty in atlantic salmon brings about large changes in testicular gene expression that are modulated by the energy status
publisher BioMed Central
publishDate 2019
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6558769/
http://www.ncbi.nlm.nih.gov/pubmed/31185904
https://doi.org/10.1186/s12864-019-5869-9
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6558769/
http://www.ncbi.nlm.nih.gov/pubmed/31185904
http://dx.doi.org/10.1186/s12864-019-5869-9
op_rights © The Author(s). 2019
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.
op_rightsnorm CC0
PDM
CC-BY
op_doi https://doi.org/10.1186/s12864-019-5869-9
container_title BMC Genomics
container_volume 20
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