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

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          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.

          Electronic supplementary material

          The online version of this article (10.1186/s12864-019-5869-9) contains supplementary material, which is available to authorized users.

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          Most cited references73

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          Gene Ontology: tool for the unification of biology

          Genomic sequencing has made it clear that a large fraction of the genes specifying the core biological functions are shared by all eukaryotes. Knowledge of the biological role of such shared proteins in one organism can often be transferred to other organisms. The goal of the Gene Ontology Consortium is to produce a dynamic, controlled vocabulary that can be applied to all eukaryotes even as knowledge of gene and protein roles in cells is accumulating and changing. To this end, three independent ontologies accessible on the World-Wide Web (http://www.geneontology.org) are being constructed: biological process, molecular function and cellular component.
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            A Comprehensive Roadmap of Murine Spermatogenesis Defined by Single-Cell RNA-Seq

            Spermatogenesis requires intricate interactions between the germline and somatic cells. Within a given cross section of a seminiferous tubule, multiple germ and somatic cell types co-occur. This cellular heterogeneity has made it difficult to profile distinct cell types at different stages of development. To address this challenge, we collected single-cell RNA sequencing data from ∼35,000 cells from the adult mouse testis and identified all known germ and somatic cells, as well as two unexpected somatic cell types. Our analysis revealed a continuous developmental trajectory of germ cells from spermatogonia to spermatids and identified candidate transcriptional regulators at several transition points during differentiation. Focused analyses delineated four subtypes of spermatogonia and nine subtypes of Sertoli cells; the latter linked to histologically defined developmental stages over the seminiferous epithelial cycle. Overall, this high-resolution cellular atlas represents a community resource and foundation of knowledge to study germ cell development and in vivo gametogenesis.
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              Chromatin and transcription transitions of mammalian adult germline stem cells and spermatogenesis.

              Adult germline stem cells (AGSCs) self-renew (Thy1(+) enriched) or commit to gametogenesis (Kit(+) enriched). To better understand how chromatin regulates AGSC biology and gametogenesis, we derived stage-specific high-resolution profiles of DNA methylation, 5hmC, histone modifications/variants, and RNA-seq in AGSCs and during spermatogenesis. First, we define striking signaling and transcriptional differences between AGSC types, involving key self-renewal and proliferation pathways. Second, key pluripotency factors (e.g., Nanog) are silent in AGSCs and bear particular chromatin/DNAme attributes that may "poise" them for reactivation after fertilization. Third, AGSCs display chromatin "poising/bivalency" of enhancers and promoters for embryonic transcription factors. Remarkably, gametogenesis occurs without significant changes in DNAme and instead involves transcription of DNA-methylated promoters bearing high RNAPol2, H3K9ac, H3K4me3, low CG content, and (often) 5hmC. Furthermore, key findings were confirmed in human sperm. Here, we reveal AGSC signaling asymmetries and chromatin/DNAme strategies in AGSCs to poise key transcription factors and to activate DNA-methylated promoters during gametogenesis. Copyright © 2014 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                +31-30-2533046 , r.w.schulz@uu.nl
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                11 June 2019
                11 June 2019
                2019
                : 20
                : 475
                Affiliations
                [1 ]ISNI 0000000120346234, GRID grid.5477.1, Division Developmental Biology, Department Biology, Science Faculty, , Reproductive Biology Group, Utrecht University, ; Kruyt Building, room O 806, Padualaan 8, 3584 CH Utrecht, The Netherlands
                [2 ]GRID grid.462699.6, INRA, UPR 1037 Laboratory of Fish Physiology and Genomics (LPGP), , BIOSIT, OUEST-genopole, ; Bât. 16, Campus de Beaulieu, 35042 Rennes CEDEX, France
                [3 ]ISNI 0000 0004 0427 3161, GRID grid.10917.3e, Research Group Reproduction and Developmental Biology, , Institute of Marine Research, ; Bergen, Norway
                [4 ]ISNI 0000 0000 9919 9582, GRID grid.8761.8, Fish Endocrinology Laboratory, Department of Biological and Environmental Sciences, , University of Gothenburg, ; S-40590 Gothenburg, Sweden
                Author information
                http://orcid.org/0000-0001-9115-669X
                Article
                5869
                10.1186/s12864-019-5869-9
                6558769
                31185904
                cace3997-c0cb-4179-9dd9-3f1d6c782206
                © 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.

                History
                : 30 April 2019
                : 31 May 2019
                Funding
                Funded by: Norwegian Ministry of Fisheries and Coastal Affairs
                Award ID: 12622
                Award Recipient :
                Funded by: European Research Council
                Award ID: LIFECYCLE FP7-222719
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2019

                Genetics
                puberty,androgens,nutrition,spermatogenesis,testis,transcriptomics
                Genetics
                puberty, androgens, nutrition, spermatogenesis, testis, transcriptomics

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