Entry into puberty is reflected in changes in hormone production but not in testicular receptor expression in Atlantic salmon (Salmo salar)

Abstract Background Puberty in male Atlantic salmon in aquaculture can start as early as after the first winter in seawater, stunts growth and entails welfare problems due to the maturation-associated loss of osmoregulation capacity in seawater. A better understanding of the regulation of puberty is...

Full description

Bibliographic Details
Main Authors: Rüdiger W. Schulz, Geir Lasse Taranger, Jan Bogerd, Wouter Nijenhuis, Birgitta Norberg, Rune Male, Eva Andersson
Format: Article
Language:English
Published: BMC 2019-06-01
Series:Reproductive Biology and Endocrinology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12958-019-0493-8
id doaj-9d3aa4dbba924196a9ad1b36a9bd5661
record_format Article
spelling doaj-9d3aa4dbba924196a9ad1b36a9bd56612020-11-25T03:02:44ZengBMCReproductive Biology and Endocrinology1477-78272019-06-0117111610.1186/s12958-019-0493-8Entry into puberty is reflected in changes in hormone production but not in testicular receptor expression in Atlantic salmon (Salmo salar)Rüdiger W. Schulz0Geir Lasse Taranger1Jan Bogerd2Wouter Nijenhuis3Birgitta Norberg4Rune Male5Eva Andersson6Research Group Reproduction and Developmental Biology, Institute of Marine ResearchResearch Group Reproduction and Developmental Biology, Institute of Marine ResearchReproductive Biology Group, Division Developmental Biology, Department Biology, Science Faculty, Utrecht UniversityReproductive Biology Group, Division Developmental Biology, Department Biology, Science Faculty, Utrecht UniversityResearch Group Reproduction and Developmental Biology, Institute of Marine ResearchDepartment of Biological Sciences, University of BergenResearch Group Reproduction and Developmental Biology, Institute of Marine ResearchAbstract Background Puberty in male Atlantic salmon in aquaculture can start as early as after the first winter in seawater, stunts growth and entails welfare problems due to the maturation-associated loss of osmoregulation capacity in seawater. A better understanding of the regulation of puberty is the basis for developing improved cultivation approaches that avoid these problems. Our aim here was to identify morphological and molecular markers signaling the initiation of, and potential involvement in, testis maturation. Methods In the first experiment, we monitored for the first time in large Atlantic salmon males several reproductive parameters during 17 months including the first reproductive cycle. Since testicular growth accelerated after the Winter solstice, we focused in the second experiment on the 5 months following the winter solstice, exposing fish from February 1 onwards to the natural photoperiod (NL) or to continuous additional light (LL). Results In the first experiment, testis weight, plasma androgens and pituitary gonadotropin transcript levels increased with the appearance of type B spermatogonia in the testis, but testicular transcript levels for gonadotropin or androgen receptors did not change while being clearly detectable. In the second experiment, all males kept under NL had been recruited into puberty until June. However, recruitment into puberty was blocked in ~ 40% of the males exposed to LL. The first morphological sign of recruitment was an increased proliferation activity of single spermatogonia and Sertoli cells. Irrespective of the photoperiod, this early sign of testis maturation was accompanied by elevated pituitary gnrhr4 and fshb and testicular igf3 transcript levels as well as increased plasma androgen levels. The transition into puberty occurred again with stable testicular gonadotropin and androgen receptor transcript levels. Conclusions The sensitivity to reproductive hormones is already established before puberty starts and up-regulation of testicular hormone receptor expression is not required to facilitate entry into puberty. The increased availability of receptor ligands, on the other hand, may result from an up-regulation of pituitary Gnrh receptor expression, eventually activating testicular growth factor and sex steroid release and driving germ and Sertoli cell proliferation and differentiation.http://link.springer.com/article/10.1186/s12958-019-0493-8PhotoperiodPubertySpermatogenesisGonadotropinsAndrogensGrowth factors
collection DOAJ
language English
format Article
sources DOAJ
author Rüdiger W. Schulz
Geir Lasse Taranger
Jan Bogerd
Wouter Nijenhuis
Birgitta Norberg
Rune Male
Eva Andersson
spellingShingle Rüdiger W. Schulz
Geir Lasse Taranger
Jan Bogerd
Wouter Nijenhuis
Birgitta Norberg
Rune Male
Eva Andersson
Entry into puberty is reflected in changes in hormone production but not in testicular receptor expression in Atlantic salmon (Salmo salar)
Reproductive Biology and Endocrinology
Photoperiod
Puberty
Spermatogenesis
Gonadotropins
Androgens
Growth factors
author_facet Rüdiger W. Schulz
Geir Lasse Taranger
Jan Bogerd
Wouter Nijenhuis
Birgitta Norberg
Rune Male
Eva Andersson
author_sort Rüdiger W. Schulz
title Entry into puberty is reflected in changes in hormone production but not in testicular receptor expression in Atlantic salmon (Salmo salar)
title_short Entry into puberty is reflected in changes in hormone production but not in testicular receptor expression in Atlantic salmon (Salmo salar)
title_full Entry into puberty is reflected in changes in hormone production but not in testicular receptor expression in Atlantic salmon (Salmo salar)
title_fullStr Entry into puberty is reflected in changes in hormone production but not in testicular receptor expression in Atlantic salmon (Salmo salar)
title_full_unstemmed Entry into puberty is reflected in changes in hormone production but not in testicular receptor expression in Atlantic salmon (Salmo salar)
title_sort entry into puberty is reflected in changes in hormone production but not in testicular receptor expression in atlantic salmon (salmo salar)
publisher BMC
series Reproductive Biology and Endocrinology
issn 1477-7827
publishDate 2019-06-01
description Abstract Background Puberty in male Atlantic salmon in aquaculture can start as early as after the first winter in seawater, stunts growth and entails welfare problems due to the maturation-associated loss of osmoregulation capacity in seawater. A better understanding of the regulation of puberty is the basis for developing improved cultivation approaches that avoid these problems. Our aim here was to identify morphological and molecular markers signaling the initiation of, and potential involvement in, testis maturation. Methods In the first experiment, we monitored for the first time in large Atlantic salmon males several reproductive parameters during 17 months including the first reproductive cycle. Since testicular growth accelerated after the Winter solstice, we focused in the second experiment on the 5 months following the winter solstice, exposing fish from February 1 onwards to the natural photoperiod (NL) or to continuous additional light (LL). Results In the first experiment, testis weight, plasma androgens and pituitary gonadotropin transcript levels increased with the appearance of type B spermatogonia in the testis, but testicular transcript levels for gonadotropin or androgen receptors did not change while being clearly detectable. In the second experiment, all males kept under NL had been recruited into puberty until June. However, recruitment into puberty was blocked in ~ 40% of the males exposed to LL. The first morphological sign of recruitment was an increased proliferation activity of single spermatogonia and Sertoli cells. Irrespective of the photoperiod, this early sign of testis maturation was accompanied by elevated pituitary gnrhr4 and fshb and testicular igf3 transcript levels as well as increased plasma androgen levels. The transition into puberty occurred again with stable testicular gonadotropin and androgen receptor transcript levels. Conclusions The sensitivity to reproductive hormones is already established before puberty starts and up-regulation of testicular hormone receptor expression is not required to facilitate entry into puberty. The increased availability of receptor ligands, on the other hand, may result from an up-regulation of pituitary Gnrh receptor expression, eventually activating testicular growth factor and sex steroid release and driving germ and Sertoli cell proliferation and differentiation.
topic Photoperiod
Puberty
Spermatogenesis
Gonadotropins
Androgens
Growth factors
url http://link.springer.com/article/10.1186/s12958-019-0493-8
work_keys_str_mv AT rudigerwschulz entryintopubertyisreflectedinchangesinhormoneproductionbutnotintesticularreceptorexpressioninatlanticsalmonsalmosalar
AT geirlassetaranger entryintopubertyisreflectedinchangesinhormoneproductionbutnotintesticularreceptorexpressioninatlanticsalmonsalmosalar
AT janbogerd entryintopubertyisreflectedinchangesinhormoneproductionbutnotintesticularreceptorexpressioninatlanticsalmonsalmosalar
AT wouternijenhuis entryintopubertyisreflectedinchangesinhormoneproductionbutnotintesticularreceptorexpressioninatlanticsalmonsalmosalar
AT birgittanorberg entryintopubertyisreflectedinchangesinhormoneproductionbutnotintesticularreceptorexpressioninatlanticsalmonsalmosalar
AT runemale entryintopubertyisreflectedinchangesinhormoneproductionbutnotintesticularreceptorexpressioninatlanticsalmonsalmosalar
AT evaandersson entryintopubertyisreflectedinchangesinhormoneproductionbutnotintesticularreceptorexpressioninatlanticsalmonsalmosalar
_version_ 1724688759612506112