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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| Format: | Article |
| Language: | English |
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BMC
2019-06-01
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| Series: | BMC Genomics |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s12864-019-5869-9 |
| _version_ | 1818282258551799808 |
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| author | Diego Crespo Jan Bogerd Elisabeth Sambroni Florence LeGac Eva Andersson Rolf B. Edvardsen Elisabeth Jönsson Bergman Björn Thrandur Björnsson Geir Lasse Taranger Rüdiger W. Schulz |
| author_facet | Diego Crespo Jan Bogerd Elisabeth Sambroni Florence LeGac Eva Andersson Rolf B. Edvardsen Elisabeth Jönsson Bergman Björn Thrandur Björnsson Geir Lasse Taranger Rüdiger W. Schulz |
| author_sort | Diego Crespo |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-13T00:18:09Z |
| format | Article |
| id | doaj.art-00f667dee27e4a8aad6840e54f67cbd9 |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-12-13T00:18:09Z |
| publishDate | 2019-06-01 |
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| series | BMC Genomics |
| spelling | doaj.art-00f667dee27e4a8aad6840e54f67cbd92022-12-22T00:05:42ZengBMCBMC Genomics1471-21642019-06-0120111710.1186/s12864-019-5869-9The initiation of puberty in Atlantic salmon brings about large changes in testicular gene expression that are modulated by the energy statusDiego Crespo0Jan Bogerd1Elisabeth Sambroni2Florence LeGac3Eva Andersson4Rolf B. Edvardsen5Elisabeth Jönsson Bergman6Björn Thrandur Björnsson7Geir Lasse Taranger8Rüdiger W. Schulz9Division Developmental Biology, Department Biology, Science Faculty, Reproductive Biology Group, Utrecht UniversityDivision Developmental Biology, Department Biology, Science Faculty, Reproductive Biology Group, Utrecht UniversityINRA, UPR 1037 Laboratory of Fish Physiology and Genomics (LPGP), BIOSIT, OUEST-genopoleINRA, UPR 1037 Laboratory of Fish Physiology and Genomics (LPGP), BIOSIT, OUEST-genopoleResearch Group Reproduction and Developmental Biology, Institute of Marine ResearchResearch Group Reproduction and Developmental Biology, Institute of Marine ResearchFish Endocrinology Laboratory, Department of Biological and Environmental Sciences, University of GothenburgFish Endocrinology Laboratory, Department of Biological and Environmental Sciences, University of GothenburgResearch Group Reproduction and Developmental Biology, Institute of Marine ResearchDivision Developmental Biology, Department Biology, Science Faculty, Reproductive Biology Group, Utrecht UniversityAbstract 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.http://link.springer.com/article/10.1186/s12864-019-5869-9PubertyAndrogensNutritionSpermatogenesisTestisTranscriptomics |
| spellingShingle | Diego Crespo Jan Bogerd Elisabeth Sambroni Florence LeGac Eva Andersson Rolf B. Edvardsen Elisabeth Jönsson Bergman Björn Thrandur Björnsson Geir Lasse Taranger Rüdiger W. Schulz The initiation of puberty in Atlantic salmon brings about large changes in testicular gene expression that are modulated by the energy status BMC Genomics Puberty Androgens Nutrition Spermatogenesis Testis Transcriptomics |
| title | 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_short | 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 |
| topic | Puberty Androgens Nutrition Spermatogenesis Testis Transcriptomics |
| url | http://link.springer.com/article/10.1186/s12864-019-5869-9 |
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