Pituitary Gonadotropin Gene Expression During Induced Onset of Postsmolt Maturation in Male Atlantic Salmon: In Vivo and Tissue Culture Studies

• Published in: Frontiers in endocrinology (Lausanne) 2022-03, Vol.13, p.826920-826920
• Main Authors: Crespo, Diego, Skaftnesmo, Kai Ove, Kjærner-Semb, Erik, Yilmaz, Ozlem, Norberg, Birgitta, Olausson, Sara, Vogelsang, Petra, Bogerd, Jan, Kleppe, Lene, Edvardsen, Rolf B, Andersson, Eva, Wargelius, Anna, Hansen, Tom J, Fjelldal, Per Gunnar, Schulz, Rüdiger W
• Format: Article
• Language: English
• Subjects: Animals; Atlantic salmon; Endocrinology; follicle-stimulating hormone; Gene Expression; Gonadotropins - metabolism; Gonadotropins - pharmacology; Gonadotropins, Pituitary - genetics; Male; pituitary; puberty; Salmo salar - genetics; Salmo salar - metabolism; Sexual Maturation - genetics; transcriptomics
• ISSN: 1664-2392; 1664-2392
• DOI: 10.3389/fendo.2022.826920

Precocious male maturation causes reduced welfare and increased production costs in Atlantic salmon ( ) aquaculture. The pituitary produces and releases follicle-stimulating hormone (Fsh), the gonadotropin triggering puberty in male salmonids. However, little is known about how Fsh production is regulated in Atlantic salmon. We examined, and , transcriptional changes of gonadotropin-related genes accompanying the initial steps of testis maturation, in pituitaries of males exposed to photoperiod and temperature conditions promoting maturation (constant light and 16°C). Pituitary , and transcripts increased in maturing males (gonado-somatic index > 0.1%). RNA sequencing (RNAseq) analysis using pituitaries from genetically similar males carrying the same genetic predisposition to mature, but differing by responding or not responding to stimulatory environmental conditions, revealed 144 differentially expressed genes, ~2/3rds being up-regulated in responders, including and other pituitary hormones, steroid-related and other puberty-associated transcripts. Functional enrichment analyses confirmed gene involvement in hormone/steroid production and gonad development. In studies, whole pituitaries were exposed to a selection of hormones and growth factors. Gonadotropin-releasing hormone (Gnrh), 17β-estradiol (E ) and 11-ketotestosterone (11-KT) up-regulated and , while was up-regulated by Gnrh but down-regulated by 11-KT in pituitaries from immature males. Also pituitaries from maturing males responded to Gnrh and sex steroids by increased and transcript levels, but expression remained unchanged. Growth factors (inhibin A, activin A and insulin-like growth factor 1) did not change , or transcript levels in pituitaries either from immature or maturing males. Additional pituitary studies on candidates identified by RNAseq showed that these transcripts were preferentially regulated by Gnrh and sex steroids, but not by growth factors, and that Gnrh/sex steroids were less effective when incubating pituitaries from maturing males. Our results suggest that a yet to be characterized mechanism up-regulating expression in the salmon pituitary is activated in response to stimulatory environmental conditions prior to morphological signs of testis maturation, and that the transcriptional program associated with this mechanism becomes unresponsive or less responsive to most stimulators once males had entered pubertal developmental .