Extended Photoperiod Facilitated the Restoration of the Expression of GH-IGF Axis Genes in Submerged Rainbow Trout (Oncorhynchus mykiss)

Abstract

Salmonids, classified as physostomous fish, maintain buoyancy by ingesting air to inflate their swim bladders. Long-term submergence has been shown to cause body imbalance and reduced growth performance in these fish. Previous studies have demonstrated that extended photoperiod can promote growth in salmonids. This study aimed to investigate the regulatory effects of prolonged lighting on the growth of submerged rainbow trout (Oncorhynchus mykiss) by examining the transcriptional expression of genes in the growth hormone (GH)-insulin-like growth factor (IGF) axis. Rainbow trout were individually reared in one of the six environments, defined by the combination of three photoperiods (0L:24D, 12L:12D, and 24L:0D) and two spatial rearing modes (routine and submerged), for 16 weeks. We compared the growth performance of rainbow trout in different environments and further analyzed the transcription profiles and correlations of GH-IGF axis genes in the brain, liver, and muscle. The findings of this study were as follows: growth performance of rainbow trout gradually increased with photoperiod duration. Specifically, final body weight (FBW) and specific growth rate (SGR) increased, while feed conversion ratio (FCR) decreased. Extended photoperiod partially mitigated the adverse effects of long-term submergence on rainbow trout growth. Under 24L:0D photoperiod conditions, growth performance (FBW, SGR, and FCR) in submerged and routine rainbow trout was more closely aligned compared to 0L:24D and 12L:12D photoperiod conditions. In response to variations in the photoperiod, GH-IGF axis genes of rainbow trout exhibited significant transcriptional differences, particularly between treatments with 0L:24D and 24L:0D light exposure. An extended photoperiod facilitated the restoration of the expression of GH-IGF axis genes in submerged rainbow trout towards routine levels, including the up-regulation of sst and sstr2 genes in the brain. Correlation analysis implied differentiation of physiological functions of ghr and igfbp paralogs. This study provided insights into the feasibility of enhancing the growth performance of submerged salmonids through photoperiod manipulation.

Keywords: GH-IGF axis; growth; photoperiod; submerged rainbow trout.

Figure 1

Comparative analysis of growth parameters of rainbow trout in various environments. (A) Final body weight (FBW) (n = 36). (B) Specific growth rate (SGR) (n = 3). (C) Feed conversion ratio (FCR) (n = 3). (D) Survival rate (SR) (n = 3). The percentages represent the ratios of growth parameters of rainbow trout between submerged and routine modes under the same photoperiod. Data are expressed as means ± standard deviation. Different uppercase letters indicate statistically significant differences between modes under the same photoperiod, while different lowercase letters indicate statistically significant differences among photoperiods under the same mode, p < 0.05. “ns” indicates no significant differences between groups.

Figure 2

Transcriptional profiles of brain GH-IGF axis genes in various environments. (A–C) The heatmap (A), principal component analysis (PCA) (B), and partial least squares discriminant analysis (PLS-DA) (C) of the brain GH-IGF axis genes under different photoperiods in routine mode. (D–F) The heatmap (D), PCA (E), and PLS-DA (F) of the brain GH-IGF axis genes under different photoperiods in submerged mode. (G–I) The heatmap (G), PCA (H), and PLS-DA (I) of the brain GH-IGF axis genes in interactive environments of photoperiod and mode. R0, 0L:24D photoperiod with routine mode; R12, 12L:12D photoperiod with routine mode; R24, 24L:0D photoperiod with routine mode; S0, 0L:24D photoperiod with submerged mode; S12, 12L:12D photoperiod with submerged mode; S24, 24L:0D photoperiod with submerged mode.

Figure 3

Transcriptional profiles of liver GH-IGF axis genes in various environments. (A–C) The heatmap (A), principal component analysis (PCA) (B), and partial least squares discriminant analysis (PLS-DA) (C) of liver GH-IGF axis genes under different photoperiods in routine mode. (D–F) The heatmap (D), PCA (E), and PLS-DA (F) of liver GH-IGF axis genes under different photoperiods in submerged mode. (G–I) The heatmap (G), PCA (H), and PLS-DA (I) of liver GH-IGF axis genes in interactive environments of photoperiod and mode. R0, 0L:24D photoperiod with routine mode; R12, 12L:12D photoperiod with routine mode; R24, 24L:0D photoperiod with routine mode; S0, 0L:24D photoperiod with submerged mode; S12, 12L:12D photoperiod with submerged mode; S24, 24L:0D photoperiod with submerged mode.

Figure 4

Transcriptional profiles of muscle GH-IGF axis genes in various environments. (A–C) The heatmap (A), principal component analysis (PCA) (B), and partial least squares discriminant analysis (PLS-DA) (C) of muscle GH-IGF axis genes under different photoperiods in routine mode. (D–F) The heatmap (D), PCA (E), and PLS-DA (F) of muscle GH-IGF axis genes under different photoperiods in submerged mode. (G–I) The heatmap (G), PCA (H), and PLS-DA (I) of muscle GH-IGF axis genes in interactive environments of photoperiod and mode. R0, 0L:24D photoperiod with routine mode; R12, 12L:12D photoperiod with routine mode; R24, 24L:0D photoperiod with routine mode; S0, 0L:24D photoperiod with submerged mode; S12, 12L:12D photoperiod with submerged mode; S24, 24L:0D photoperiod with submerged mode.

Figure 5

Correlation analysis of GH-IGF axis genes in the brain, liver, and muscle. (A–E) Heatmap of correlations among GH-IGF axis genes (A) and Pearson correlation coefficients of two genes (B–E) in the brain. (F–J) Heatmap of correlations among GH-IGF axis genes (F) and Pearson correlation coefficients of two genes (G–J) in the liver. (K–O) Heatmap of correlations among GH-IGF axis genes (K) and Pearson correlation coefficients of two genes (L–O) in the muscle.

Figure 6

Schematic representation of the experimental procedure. (Left) The trout were subjected to a series of acclimation steps prior to the experiment: (I) Freshwater environment. (II) Seawater domestication. (III) Seawater environment. (Middle) Experimental design. Six groups were set up with triplicates: 0L:24D photoperiod with routine mode (R0), 12L:12D photoperiod with routine mode (R12), 24L:0D photoperiod with routine mode (R24), 0L:24D photoperiod with submerged mode (S0), 12L:12D photoperiod with submerged mode (S12), and 24L:0D photoperiod with submerged mode (S24), respectively. (Right) Brain, liver, and dorsal muscle tissues were dissected for the analysis of the GH-IGF axis genes.