Conservation of the photoperiodic neuroendocrine axis among vertebrates: Evidence from the teleost fish, Gasterosteus aculeatus

O’Brien, Conor S; Bourdo, Ryan; Bradshaw, William E.; Holzapfel, Christina; Cresko, William A.

doi:10.1016/j.ygcen.2012.03.010

Cited by 29 publications

(28 citation statements)

References 65 publications

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“…First, as in birds and mammals and echoing other recent reports in teleosts [24,25], photoperiodic induction of dio2b gene expression is seen during smoltification, consistent with the view that this is an ancestral mechanism involved in the timing of seasonal life history transitions. This applies both to cyclical changes such as seasonal breeding as well as to seasonally gated unidirectional events such as puberty and metamorphosis, or in this case, smoltification.…”

Section: Discussionsupporting

confidence: 86%

Functional Divergence of Type 2 Deiodinase Paralogs in the Atlantic Salmon

et al. 2015

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Thyroid hormone (TH) is an ancestral signal linked to seasonal life history transitions throughout vertebrates. TH action depends upon tissue-localized regulation of levels of active TH (triiodothyronine, T3), through spatiotemporal expression of thyroid hormone deiodinase (dio) genes. We investigated the dio gene family in juvenile Atlantic salmon (Salmo salar) parr, which prepare for seaward migration in the spring (smoltification) through TH-dependent changes in physiology. We identified two type 2 deiodinase paralogs, dio2a and dio2b, responsible for conversion of thyroxine (T4) to T3. During smoltification, dio2b was induced in the brain and gills in zones of cell proliferation following increasing day length. Contrastingly, dio2a expression was induced in the gills by transfer to salt water (SW), with the magnitude of the response proportional to the plasma chloride level. This response reflected a selective enrichment for osmotic response elements (OREs) in the dio2a promoter region. Transcriptomic profiling of gill tissue from fish transferred to SW plus or minus the deiodinase inhibitor, iopanoic acid, revealed SW-induced increases in cellular respiration as the principal consequence of gill dio2 activity. Divergent evolution of dio2 paralogs supports organ-specific timing of the TH-dependent events governing the phenotypic plasticity required for migration to sea.

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Section: Discussionsupporting

confidence: 86%

Functional Divergence of Type 2 Deiodinase Paralogs in the Atlantic Salmon

et al. 2015

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“…The lhb mRNA levels started to increase already after a few days of exposure to long day [21]. Paradoxically, the mRNA levels of lhb and fshb in castrated males were higher under short rather than under long day, though the difference was not significant for fshb in 2011.…”

Section: Discussionmentioning

confidence: 86%

Androgen feedback effects on LH and FSH, and photoperiodic control of reproduction in male three-spined sticklebacks, Gasterosteus aculeatus

Shao

Arvidsson

Trombley

et al. 2013

General and Comparative Endocrinology

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, M. et al. (2013) "Androgen feedback effects on LH and FSH, and photoperiodic control of reproduction in male three-spined sticklebacks, Gasterosteus aculeatus" General and Comparative Endocrinology, Access to the published version may require subscription. Sexual maturation in the stickleback is controlled by photoperiod. The aim of this study was to find out whether changes in feedback effects exerted by sex steroids could mediate the photoperiodic effect, which is regarded to be of an all-or-nothing character. To that end, males were castrated and treated with different doses of testosterone (T) and in one experiment also with the aromatase inhibitor fadrozole (AI) and kept under different photoperiods. In control fish, long day (LD 16:8) stimulated maturation, associated with more hypertrophied kidneys (a secondary sexual character) and higher levels of pituitary lhb and fshb mRNA than under short day conditions (LD 8:16). Under LD 8:16, low doses of T suppressed both lhb and fshb mRNA levels. However, with the use of high doses of T and/or longer photoperiods the inhibitory effects on lhb and fshb mRNA levels became less clear or instead positive effects were observed. Under intermediate photoperiod conditions, the negative feedback effect of a low dose of T on fshb was more prominent with shorter photoperiods, whereas no such shift was observed for lhb mRNA. The inhibitory effect of the low dose of T on lhb mRNA levels under LD 8:16 was abolished by AI, whereas the stimulatory effect of the high dose of T was not. The negative feedback effects were more marked under short days than under long days, whereas positive feedback effects were more marked under long days. The suppression of both fshb and lhb mRNA levels by low androgen levels, especially under short days, may inhibit maturation completely unless a rise of androgens above threshold levels would allow complete maturation. 1.IntroductionIn order to reproduce at the optimal time of the year, organisms use endogenous cycles and environmental cues, the most important of which being the photoperiod [18]. In vertebrates, the circulating levels of the pituitary gonadotropic hormones (GtHs), LH and FSH, are higher under stimulatory than under non-stimulatory photoperiods, resulting in increased gonadal acitivity. The pituitary is under control from the brain, especially the hypothalamus, and by gonadal hormones which exert feedback effects on the brain-pituitary-gonad (BPG) axis. In mammals and birds, several studies have shown changes in steroid feedback effects on the BPG axis by photoperiod, but also gonad-independent effects, i.e. higher circulating GTH levels in castrated animals kept under a stimulatory photoperiod are known [16]. This has been studied very little in poikilothermic vertebrates.Photoperiod is an important factor in synchronizing reproduction also in fishes, including the three-spined stickleback which is perhaps the fish where the mechanisms of photoperiodic effects have been studied most extensively [2,3,7,8,9]. At sexual maturat...

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“…It is well established that pituitary gonadotrophins (Fsh and Lh) regulate steroidogenesis and ovarian growth in fishes (Tyler & Sumpter, ; Trudeau, ; Yaron et al ., ; Rosenfeld et al ., ; Zohar et al ., ; O'Brien et al ., ). In H .…”

Section: Discussionmentioning

confidence: 99%

“…Spawning is induced by warm or cool temperature conditions. A dependence on either photoperiod or temperature, or both factors, has been documented for various species (de Vlaming, ; Sundararaj & Vasal, ; Billard, ; Sundararaj, ; Lam, ; Horvath, ; Munro, ; Borg, ; O'Brien et al ., ). The manipulation of these factors can accelerate or decelerate gametogenic and growth activities and the strategy has acquired aquaculture importance (Tyler & Sumpter, ; Davies et al ., ; Rodríguez et al ., ; Biswas & Takeuchi, ; Rad et al ., ; Bradshaw & Holzapfel, , ).…”

Section: Introductionmentioning

confidence: 99%

Effects of altered photoperiod and temperature on expression levels of gonadotrophin subunit mRNAs in the female stinging catfish Heteropneustes fossilis

Acharjee

Chaube

Joy

2017

Journal of Fish Biology

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Differential effects of photoperiod and temperature on the temporal modulation of gonadotrophin subunit genes (glycoprotein α, gpα), follicle-stimulating hormone β (fshβ) and luteinizing hormone β (lhβ) expression were investigated in the stinging catfish Heteropneustes fossilis. Female H. fossilis were exposed to varying photoperiod and temperature conditions for 14 and 28 days in the early preparatory phase of the annual reproductive cycle. Gonadotrophin subunit gene expression, gonado-somatic index (I ), ovarian histology and plasma steroid hormone levels were evaluated. The exposure of H. fossilis to long photoperiod (LP) of 16 h light or high temperature (HT) at 28 ± 2° C (mean ± s.e.), alone or in combination, resulted in significant increases in gpα, fshβ and lhβ messenger (m)RNA levels, I , plasma oestradiol-17β (E ), testosterone (T) and progesterone (P ) levels. The ovaries were filled with advanced yolky oocytes. On the other hand, the short photoperiod (SP) of 8 h light exposure decreased the transcript levels with higher inhibition in the normal temperature (NT) group at 18 ± 2° C (mean ± s.e.) than the HT group at 28 ± 2° C. Furthermore, the inhibition reached the highest level in total darkness (TD) of 24 h light deprivation under NT conditions at 18 ± 2° C. Consequently, the SP and TD treatments inhibited the I , plasma E and T levels and ovarian development. The exposure to high temperature at 28 ± 2° C also modified the short photoperiod effect by elevating plasma E level. The plasma T level changed only mildly while the plasma P level showed the greatest fluctuations; the level reached the nadir in the SP + HT group but increased in the SP + NT group on day 28. A two-way ANOVA of the data showed differential effects of photoperiod and temperature; photoperiod produced a highly significant effect on fshβ expression while temperature had a highly significant effect both on lhβ and gpα levels. Thus, the differential expression of the gpα by the environmental variables ensures temporal synchronization of ovarian development and spawning.

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Conservation of the photoperiodic neuroendocrine axis among vertebrates: Evidence from the teleost fish, Gasterosteus aculeatus

Cited by 29 publications

References 65 publications

Functional Divergence of Type 2 Deiodinase Paralogs in the Atlantic Salmon

Functional Divergence of Type 2 Deiodinase Paralogs in the Atlantic Salmon

Androgen feedback effects on LH and FSH, and photoperiodic control of reproduction in male three-spined sticklebacks, Gasterosteus aculeatus

Effects of altered photoperiod and temperature on expression levels of gonadotrophin subunit mRNAs in the female stinging catfish Heteropneustes fossilis

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