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

Diego Crespo,Elisabeth Sambroni,Geir Lasse Taranger,Björn Thrandur Björnsson,Elisabeth Jönsson Bergman,Jan Bogerd,Florence Legac,Rolf B Edvardsen,Rüdiger W Schulz,Eva Andersson

doi:10.1186/s12864-019-5869-9

Abstract

BackgroundWhen 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.ResultsMaturing 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.ConclusionsUndifferentiated 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.

Highlights

When puberty starts before males reach harvest size, animal welfare and sustainability issues occur in Atlantic salmon (Salmo salar) aquaculture
While androgens potently stimulate spermatogenesis in fish [10, 11, 15, 16], the relative androgen independence of piscine spermatogenesis may reflect the biological activities of Folliclestimulating hormone (Fsh)-regulated growth factors such as Insulin-like 3 (Insl3) and Wnt5a produced by Leydig cells [17, 18], or Anti-Müllerian hormone (Amh) and Igf3 produced by Sertoli cells [19,20,21]
Quantifying selected pituitary gene transcripts showed that fshb, lhb, and gnrhr4 mRNA levels were all significantly higher in Restricted ration maturing (RRmat) than in Restricted ration immature (RRimm) males (Table 1), while these differences were not significant between Normal ration maturing (NRmat) and Normal ration immature (NRimm) fish (Table 1)

Summary

Introduction

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. Loss of the androgen receptor does reduce testis weight in zebrafish, some functional sperm are still produced [10, 11]. These observations differ from the situation in mice, where spermatogenesis fails in the absence of Lh or androgen signaling [12, 13], unless rescued by strong FSH receptor activation, which increases transcript levels of several genes regulated by androgens [14]. The two gonadotropins target testicular signaling systems that regulate vertebrate spermatogenesis, but our knowledge on the composition and functioning of these testicular signaling systems is far from complete [22]

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