Functional divergence of thyrotropin beta-subunit paralogs gives new insights into salmon smoltification metamorphosis

Abstract

Smoltification is a metamorphic event in salmon life history, which initiates downstream migration and pre-adapts juvenile salmon for seawater entry. While a number of reports concern thyroid hormones and smoltification, few and inconclusive studies have addressed the potential role of thyrotropin (TSH). TSH is composed of a α-subunit common to gonadotropins, and a β-subunit conferring hormone specificity. We report the presence and functional divergence of duplicated TSH β-subunit paralogs (tshβa and tshβb) in Atlantic salmon. Phylogeny and synteny analyses allowed us to infer that they originated from teleost-specific whole genome duplication. Expression profiles of both paralogs in the pituitary were measured by qPCR throughout smoltification in Atlantic salmon from the endangered Loire-Allier population raised in a conservation hatchery. This revealed a striking peak of tshβb expression in April, concomitant with downstream migration initiation, while tshβa expression remained relatively constant. In situ hybridization showed two distinct pituitary cell populations, tshβa cells in the anterior adenohypophysis, and tshβb cells near to the pituitary stalk, a location comparable to the pars tuberalis TSH cells involved in seasonal physiology and behaviour in birds and mammals. Functional divergence of tshβ paralogs in Atlantic salmon supports a specific role of tshβb in smoltification.

RNA profiling identifies novel, photoperiod-history dependent markers associated with enhanced saltwater performance in juvenile Atlantic salmon

“…Smolting is a hormonally controlled process and photoperiod-dependent changes in the secretion of anterior pituitary trophic hormones (ACTH, GH and TSH), together with cortisol and IGF-1, have been reported [2,15,19,50,51]. Importantly, the same hormones are not influenced by increased day length in salmon juveniles below a threshold body size for smolting [2,4,52,53].…”

Differential Regulation of the Expression of the Two Thyrotropin Beta Subunit Paralogs by Salmon Pituitary Cells In Vitro

“…In birds and mammals, PT-TSH acts retrogradely on hypothalamic area and is involved in the brain regulation of seasonal life-traits, such as reproduction, migration and hibernation [for reviews: ( 22 – 24 )]. A similar potential role in the seasonal regulation of smoltification could be hypothesized for the tshβb paralog in salmon ( 17 ). While in birds and mammals, both pituitary TSH cell populations express the same single tshβ gene, the two TSH cell populations in Atlantic salmon express distinct tshβa and tshβb paralogs.…”

“…Our recent studies in Atlantic salmon, Salmo salar , revealed a remarkable functional divergence of the duplicated tshβ paralogs, with a striking peak of pituitary tshβb transcripts at the time of smoltification, in early April, concomitantly with the change in rheotaxism and initiation of downstream migration, whereas no change was observed for tshβa . While previous studies by many authors in salmonids had only concerned the “classical” tshβa paralog, the demonstration of another paralog and its expression peak at smoltification provided the first evidence for the involvement of TSH in smoltification metamorphosis ( 17 ).…”

“…Furthermore, as shown by in situ hybridization, the two Atlantic salmon tshβ paralogs are expressed by two different cell populations in the pituitary: tshβa cells are abundant and located in the anterior adenohypophysis, while tshβb cells are less numerous, well detected only at the time of smoltification, and located in the dorsal adenohypophysis near to the pituitary stalk ( 17 ). This differential localization and abundance of TSH cells in salmon could be compared to the situation in mammals and birds, which present a “classical” TSH cell population in the pituitary pars distalis (PD) and a less numerous TSH cell population in the pars tuberalis (PT) adjacent to the pituitary stalk [mammals ( 18 – 20 ); birds ( 21 )].…”

An integrative view of mammalian seasonal neuroendocrinology

“…In addition, genome duplication in fish may have allowed for some level of plasticity through specialisation of paralogues along the putative TSH/DIO/T3 axis. Fleming et al reported the expression of two distinct Tshß subunits in the salmon pituitary, one of which ( Tshßb) exhibits a marked induction as daylength increases from late winter onwards and a specific pattern of expression in the dorsal region near the pituitary stalk, a location comparable to the PT in mammals. Differential tissue expression and a response to photoperiod has also been reported for Dio2 paralogues in salmon .…”