Abstract
The acquisition of reproductive competence requires the activation of the brain-pituitary-gonad (BPG) axis, which in most vertebrates, including fishes, is initiated by changes in photoperiod. In the European sea bass long-term exposure to continuous light (LL) alters the rhythm of reproductive hormones, delays spermatogenesis and reduces the incidence of precocious males. In contrast, an early shift from long to short photoperiod (AP) accelerates spermatogenesis. However, how photoperiod affects key genes in the brain to trigger the onset of puberty is still largely unknown. Here, we investigated if the integration of the light stimulus by clock proteins is sufficient to activate key genes that trigger the BPG axis in the European sea bass. We found that the clock genes clock, npas2, bmal1 and the BPG genes gnrh, kiss and kissr share conserved transcription factor frameworks in their promoters, suggesting co-regulation. Other gene promoters of the BGP axis were also predicted to be co-regulated by the same frameworks. Co-regulation was confirmed through gene expression analysis of brains from males exposed to LL or AP photoperiod compared to natural conditions: LL fish had suppressed gnrh1, kiss2, galr1b and esr1, while AP fish had stimulated npas2, gnrh1, gnrh2, kiss2, kiss1rb and galr1b compared to NP. It is concluded that fish exposed to different photoperiods present significant expression differences in some clock and reproductive axis related genes well before the first detectable endocrine and morphological responses of the BPG axis.
Highlights
Puberty is a process by which a juvenile animal acquires reproductive competence [1]
We show that photoperiod regimes affect the brain mRNA expression of circadian and reproductive axis related genes prior to the activation of the endocrine brain-pituitary-gonadal axis (BPG) axis, suggesting that puberty onset requires coordination and possibly co-regulation of clock and BGP axis genes
The 1.5 Kb putative promoter sequences of the genes analysed in this study were retrieved from the zebrafish zv9 genome assembly at Ensembl database—kiss1 (Chr.11: 24248322–24249833), kiss2 (Chr.4:15894109–15895771, kiss1rb (Chr.2: 33512576– 33514087), kiss2rb (Chr.5: 72415097–72416608), arntl1a (Chr.25: 18397999–18399503), arntl1b (Chr.7:67978425–67979898), clock (Chr. 20: 22200972–22202477), clock3 (Chr.1: 18174667–18176172), npas2 (Chr.5: 24573559–14575064) and gnrh2 (Chr.21: 14027250– 14028860)—and from the European sea bass genome assembly—kiss1 (LG1A:1602662–1606367), kiss2 (LGx:1084174–1087770), kiss1rb (LG10:16049229–16063479), kiss2rb (LG20:15036333–15040834), arntl1a (LG5:15033014– 15038159), arntl1b (LG6:23295633–23321243), clock (LG7:16250759–16266546), clock3 (LG4:20865175–20889027), npas2 (LG14:11922193–11945535) and gnrh2 (LG1A:10673952– 10675997)
Summary
Puberty is a process by which a juvenile animal acquires reproductive competence [1]. During this process major hormonal, physical and behavioural changes occur. Puberty initiates in the brain and requires the activation of cellular mechanisms that control and regulate different levels of the brain-pituitary-gonadal axis (BPG). An increase in hypothalamic kisspeptin (KISS1) stimulates the production of gonadotropin-releasing hormone (GNRH) and PLOS ONE | DOI:10.1371/journal.pone.0144158. Photoperiod Regulation of Clock and Reproduction Related Gene. Foundation for Science and Technology of Portugal (FCT) under fellowship (SFRH/BPD/66742/2009). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript
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