Photoperiod is an important environmental factor that influence seasonal reproduction behavior in bird. Birds translates photoperiodic information into neuroendocrine signals through deep brain photoreceptors (DBPs). OPN5 has been considered as candidate DBPs involving in regulation of seasonal reproduction in birds. However, little is known about the effect of OPN5 in non-seasonal breeding birds. Thus, we pondered on whether OPN5 regulating follicular development through TSH-DIO2/DIO3 system responds to different photoperiods in non-seasonal laying ducks. As an ideal non-seasonal breeding bird, a total of 120 mountain ducks were randomly divided into three groups and treated respectively to a different photoperiod: group S (8 L:18D), group C (17 L:7D), and group L (24 L:0D). The ducks were caged in a fully enclosed shelter with the same feeding conditions for each group, free water and limited feeding (150 g per duck each day). Samples were collected from each group at d 0, d 5, d 8, d 20, and d 35 (n = 8). The ducks in 24 h photoperiod had the highest laying rate and the lowest feed-to-egg ratio, while the ducks in 8 h photoperiod had the lowest laying rate and the highest feed-to-egg ratio. Long-day photoperiod for 24 h significantly increased the ovarian index and GnRH, LH, E2, and P4 levels in serum; short-day photoperiod for 8 h increased PRL and testosterone levels in serum. Compared with 8 h photoperiod, long-day photoperiod significantly or highly significantly increased the mRNA level and protein expression of OPN5 in the hypothalamus of long-day photoperiod on d 35 (p < 0.05). The gene or protein expression patterns of GnRH, TRH, TSHβ, DIO2, THRβ, Vasoactive Intestinal peptide(IP), and PRL were positively correlated with OPN5, whereas the gene expression patterns of GnIH and DI O 3 were negatively correlated with OPN5. The results revealed that OPN5 mediated the effect of light on follicular development through the TSH-DIO2/DIO3 pathway, the expression of OPN5 increased with light duration and improved the efficiency of the HPG axis to promote follicular development in mountain ducks.
Both hypothalamic neurotransmitters and serum steroid hormones are impacted by photoperiod and have effects on physiology and seasonal reproductive. However, the relationship between circulating gonadal steroids and hypothalamic neurotransmitters underlying different photoperiod is still unclear. To further understand the crosstalk of neurotransmitters and steroids in seasonal reproduction, metabolic changes of 27 neurotransmitters concentrated in hypothalamus tissues and 42 steroids hormones in serum were assessed during two artificial photoperiodic programs. The results showed that photoperiod induce testicular atrophy and recrudescence. In L-to-S groups, significantly decreased levels of testosterone concentration were found in serum (P < 0.001) and increased 11-Dehydrocorticosterone (P < 0.05); Testosterone were almost undetectable at SD_14d. In addition, the hypothalamus exhibited significantly increased arginine and 4-aminobutyric acid (GABA) concentration and decreased serotonin and epinephrine content (P < 0.01 or P < 0.05). Accordingly, serum testosterone and androstenedione became detectable at LD_3d in the S-to-L group and were markedly increase at LD_7d. Furthermore, Serum androstenedione showed a significant increase with long light expose (P < 0.01). Additionally, the hypothalamus exhibited both significantly increased L.Tryptophan and phenylalanine concentration, as well as decreased L-glutamine and L-glutamine.acid content (P < 0.01 or P < 0.05). Serotonin metabolism showed significant differences between L-to-S group and S-to-L group. Furthermore, in the correlation analysis, serum testosterone had a positive correlation with 5-Hydroxyindole-3-acetic acid (5-HIAA), while Androstenedione was significantly negative with L.Tryptophan in L-to-S (P < 0.05). However, in S-to-L group, serum testosterone showed strong negative correlation with both serotonin and 5-HIAA (P < 0.05), but positive correlation with L.Tryptophan (P < 0.01), while Androstenedione was significantly negative correlation with both serotonin (P < 0.05) and L-Glutamine (P < 0.01). Photoperiod also had significant effects on the mRNA expression. We found significant differences in gene expression patterns of both serotonin signaling and steroid biosynthesis, while MAOB, NR5A1, and 3β-HSD showed an opposite tendency between two groups. Taken together, our results revealed that circulating gonadal steroids and hypothalamic neurotransmitters were significantly impact quail’s seasonal reproduction. Circulating gonadal steroids have different effects on neurotransmitter at different photoperiodism, which may coordinately influence the seasonal reproduction of quails.
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