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

Abstract 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 transcript...

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Main Authors: Crespo, Diego, Bogerd, Jan, Sambroni, Elisabeth, LeGac, Florence, Andersson, Eva, Edvardsen, Rolf, Bergman, Elisabeth, Björnsson, Björn, Taranger, Geir, Schulz, Rüdiger
Format: Article in Journal/Newspaper
Language:unknown
Published: Figshare 2019
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Online Access:https://dx.doi.org/10.6084/m9.figshare.c.4538153
https://springernature.figshare.com/collections/The_initiation_of_puberty_in_Atlantic_salmon_brings_about_large_changes_in_testicular_gene_expression_that_are_modulated_by_the_energy_status/4538153
id ftdatacite:10.6084/m9.figshare.c.4538153
record_format openpolar
spelling ftdatacite:10.6084/m9.figshare.c.4538153 2023-05-15T15:32:21+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 Bergman, Elisabeth Björnsson, Björn Taranger, Geir Schulz, Rüdiger 2019 https://dx.doi.org/10.6084/m9.figshare.c.4538153 https://springernature.figshare.com/collections/The_initiation_of_puberty_in_Atlantic_salmon_brings_about_large_changes_in_testicular_gene_expression_that_are_modulated_by_the_energy_status/4538153 unknown Figshare https://dx.doi.org/10.1186/s12864-019-5869-9 CC BY 4.0 https://creativecommons.org/licenses/by/4.0 CC-BY Biochemistry Medicine Cell Biology Genetics FOS Biological sciences Molecular Biology Physiology Evolutionary Biology 59999 Environmental Sciences not elsewhere classified FOS Earth and related environmental sciences Ecology Developmental Biology Inorganic Chemistry FOS Chemical sciences 111714 Mental Health FOS Health sciences Computational Biology Collection article 2019 ftdatacite https://doi.org/10.6084/m9.figshare.c.4538153 https://doi.org/10.1186/s12864-019-5869-9 2021-11-05T12:55:41Z Abstract 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 levels in males maturing under caloric restriction may be responsible for the stronger up-regulation of a common set of (449) maturation-associated genes, and the specific up-regulation of another set of (421) genes. The latter opened regulatory and/or metabolic options for initiating puberty despite feed restriction. As a means to reduce the incidence of male puberty in salmon, however, caloric restriction seems unsuitable. Article in Journal/Newspaper Atlantic salmon Salmo salar DataCite Metadata Store (German National Library of Science and Technology)
institution Open Polar
collection DataCite Metadata Store (German National Library of Science and Technology)
op_collection_id ftdatacite
language unknown
topic Biochemistry
Medicine
Cell Biology
Genetics
FOS Biological sciences
Molecular Biology
Physiology
Evolutionary Biology
59999 Environmental Sciences not elsewhere classified
FOS Earth and related environmental sciences
Ecology
Developmental Biology
Inorganic Chemistry
FOS Chemical sciences
111714 Mental Health
FOS Health sciences
Computational Biology
spellingShingle Biochemistry
Medicine
Cell Biology
Genetics
FOS Biological sciences
Molecular Biology
Physiology
Evolutionary Biology
59999 Environmental Sciences not elsewhere classified
FOS Earth and related environmental sciences
Ecology
Developmental Biology
Inorganic Chemistry
FOS Chemical sciences
111714 Mental Health
FOS Health sciences
Computational Biology
Crespo, Diego
Bogerd, Jan
Sambroni, Elisabeth
LeGac, Florence
Andersson, Eva
Edvardsen, Rolf
Bergman, Elisabeth
Björnsson, Björn
Taranger, Geir
Schulz, Rüdiger
The initiation of puberty in Atlantic salmon brings about large changes in testicular gene expression that are modulated by the energy status
topic_facet Biochemistry
Medicine
Cell Biology
Genetics
FOS Biological sciences
Molecular Biology
Physiology
Evolutionary Biology
59999 Environmental Sciences not elsewhere classified
FOS Earth and related environmental sciences
Ecology
Developmental Biology
Inorganic Chemistry
FOS Chemical sciences
111714 Mental Health
FOS Health sciences
Computational Biology
description Abstract 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 levels in males maturing under caloric restriction may be responsible for the stronger up-regulation of a common set of (449) maturation-associated genes, and the specific up-regulation of another set of (421) genes. The latter opened regulatory and/or metabolic options for initiating puberty despite feed restriction. As a means to reduce the incidence of male puberty in salmon, however, caloric restriction seems unsuitable.
format Article in Journal/Newspaper
author Crespo, Diego
Bogerd, Jan
Sambroni, Elisabeth
LeGac, Florence
Andersson, Eva
Edvardsen, Rolf
Bergman, Elisabeth
Björnsson, Björn
Taranger, Geir
Schulz, Rüdiger
author_facet Crespo, Diego
Bogerd, Jan
Sambroni, Elisabeth
LeGac, Florence
Andersson, Eva
Edvardsen, Rolf
Bergman, Elisabeth
Björnsson, Björn
Taranger, Geir
Schulz, Rüdiger
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 Figshare
publishDate 2019
url https://dx.doi.org/10.6084/m9.figshare.c.4538153
https://springernature.figshare.com/collections/The_initiation_of_puberty_in_Atlantic_salmon_brings_about_large_changes_in_testicular_gene_expression_that_are_modulated_by_the_energy_status/4538153
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_relation https://dx.doi.org/10.1186/s12864-019-5869-9
op_rights CC BY 4.0
https://creativecommons.org/licenses/by/4.0
op_rightsnorm CC-BY
op_doi https://doi.org/10.6084/m9.figshare.c.4538153
https://doi.org/10.1186/s12864-019-5869-9
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