Transcriptomics and metabolomics reveal the regulation of reproductive performance and egg quality of blotched snakehead Channa maculata broodstock induced by a high protein diet

To evaluate the effects of dietary protein on reproductive performance, egg quality and larval health of the blotched snakehead Channa maculata, three groups were designed: a high protein group (HP) with 48% protein content, a low protein group (LP) with 44% protein content, and a control group (C)...

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Main Authors: Shuzhan Fei, Mi Ou, Haiyang Liu, Xincheng Zhang, Qing Luo, Kaibin Li, Kunci Chen, Baixiang Chen, Jian Zhao
Format: Article
Language:English
Published: Elsevier 2024-02-01
Series:Aquaculture Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2352513423004416
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author Shuzhan Fei
Mi Ou
Haiyang Liu
Xincheng Zhang
Qing Luo
Kaibin Li
Kunci Chen
Baixiang Chen
Jian Zhao
author_facet Shuzhan Fei
Mi Ou
Haiyang Liu
Xincheng Zhang
Qing Luo
Kaibin Li
Kunci Chen
Baixiang Chen
Jian Zhao
author_sort Shuzhan Fei
collection DOAJ
description To evaluate the effects of dietary protein on reproductive performance, egg quality and larval health of the blotched snakehead Channa maculata, three groups were designed: a high protein group (HP) with 48% protein content, a low protein group (LP) with 44% protein content, and a control group (C) fed with commercial feed containing 40% protein. The results demonstrated that the HP diet significantly enhanced maternal absolute fecundity, egg size and offspring health; however, it had no impact on fertilization rate and hatching rate. The maternal plasma levels of 11-ketotestosterone, 17β-estradiol, and vitellogenin in the HP group were found to be significantly higher compared to those in the C group. Plasma SOD activity and T-AOC capacity in the HP group were significantly higher than those in the C group, while MDA content showed an opposite trend. The trend of T-AOC in 7 days post-hatching larvae exhibited a consistent pattern with that observed in the maternal. Metabolomics and transcriptomics results indirectly indicated that the differences in reproductive and egg quality of the broodstock were associated with the regulation of arachidonic acid metabolism, steroid hormone biosynthesis, cholesterol metabolism, glycerophospholipid metabolism, and glycerolipid metabolism. The expression levels of star, zp3, foxo3, tgf-β, ghr, igf, cyp17a1, and cyp19a1 genes associated with reproduction and were significantly upregulated in the HP group. By depleting the abundance of metabolites in key pathway such as the pentose phosphate pathway, glycolysis/gluconeogenesis, nicotinate and nicotinamide metabolism, vitamin B6 metabolism within the ovary, there is an elevation in arachidonic acid metabolite abundance, thereby facilitating ovarian maturation and regulating egg quality. In conclusion, the high protein diet may affect the reproductive process and egg quality by inducing an upregulation of TGF-beta signaling pathway and ovarian steroidogenesis and arachidonic acid metabolism, leading to increased plasma cholesterol levels and enhanced steroid hormone synthesis.
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spelling doaj.art-ce9645551be7409c8bf8c27d6a00bdb22023-12-29T04:45:34ZengElsevierAquaculture Reports2352-51342024-02-0134101902Transcriptomics and metabolomics reveal the regulation of reproductive performance and egg quality of blotched snakehead Channa maculata broodstock induced by a high protein dietShuzhan Fei0Mi Ou1Haiyang Liu2Xincheng Zhang3Qing Luo4Kaibin Li5Kunci Chen6Baixiang Chen7Jian Zhao8Key Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, Guangdong 510380, PR ChinaKey Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, Guangdong 510380, PR ChinaKey Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, Guangdong 510380, PR ChinaKey Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, Guangdong 510380, PR ChinaKey Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, Guangdong 510380, PR ChinaKey Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, Guangdong 510380, PR ChinaKey Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, Guangdong 510380, PR ChinaFoshan Nanhai BaiRong Improved Aquatic Seed Co., Ltd, Foshan,Guangdong 528216, ChinaKey Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou, Guangdong 510380, PR China; Corresponding author.To evaluate the effects of dietary protein on reproductive performance, egg quality and larval health of the blotched snakehead Channa maculata, three groups were designed: a high protein group (HP) with 48% protein content, a low protein group (LP) with 44% protein content, and a control group (C) fed with commercial feed containing 40% protein. The results demonstrated that the HP diet significantly enhanced maternal absolute fecundity, egg size and offspring health; however, it had no impact on fertilization rate and hatching rate. The maternal plasma levels of 11-ketotestosterone, 17β-estradiol, and vitellogenin in the HP group were found to be significantly higher compared to those in the C group. Plasma SOD activity and T-AOC capacity in the HP group were significantly higher than those in the C group, while MDA content showed an opposite trend. The trend of T-AOC in 7 days post-hatching larvae exhibited a consistent pattern with that observed in the maternal. Metabolomics and transcriptomics results indirectly indicated that the differences in reproductive and egg quality of the broodstock were associated with the regulation of arachidonic acid metabolism, steroid hormone biosynthesis, cholesterol metabolism, glycerophospholipid metabolism, and glycerolipid metabolism. The expression levels of star, zp3, foxo3, tgf-β, ghr, igf, cyp17a1, and cyp19a1 genes associated with reproduction and were significantly upregulated in the HP group. By depleting the abundance of metabolites in key pathway such as the pentose phosphate pathway, glycolysis/gluconeogenesis, nicotinate and nicotinamide metabolism, vitamin B6 metabolism within the ovary, there is an elevation in arachidonic acid metabolite abundance, thereby facilitating ovarian maturation and regulating egg quality. In conclusion, the high protein diet may affect the reproductive process and egg quality by inducing an upregulation of TGF-beta signaling pathway and ovarian steroidogenesis and arachidonic acid metabolism, leading to increased plasma cholesterol levels and enhanced steroid hormone synthesis.http://www.sciencedirect.com/science/article/pii/S2352513423004416Blotched snakeheadDietary proteinEgg qualitySex steroid hormoneReproductive performance
spellingShingle Shuzhan Fei
Mi Ou
Haiyang Liu
Xincheng Zhang
Qing Luo
Kaibin Li
Kunci Chen
Baixiang Chen
Jian Zhao
Transcriptomics and metabolomics reveal the regulation of reproductive performance and egg quality of blotched snakehead Channa maculata broodstock induced by a high protein diet
Aquaculture Reports
Blotched snakehead
Dietary protein
Egg quality
Sex steroid hormone
Reproductive performance
title Transcriptomics and metabolomics reveal the regulation of reproductive performance and egg quality of blotched snakehead Channa maculata broodstock induced by a high protein diet
title_full Transcriptomics and metabolomics reveal the regulation of reproductive performance and egg quality of blotched snakehead Channa maculata broodstock induced by a high protein diet
title_fullStr Transcriptomics and metabolomics reveal the regulation of reproductive performance and egg quality of blotched snakehead Channa maculata broodstock induced by a high protein diet
title_full_unstemmed Transcriptomics and metabolomics reveal the regulation of reproductive performance and egg quality of blotched snakehead Channa maculata broodstock induced by a high protein diet
title_short Transcriptomics and metabolomics reveal the regulation of reproductive performance and egg quality of blotched snakehead Channa maculata broodstock induced by a high protein diet
title_sort transcriptomics and metabolomics reveal the regulation of reproductive performance and egg quality of blotched snakehead channa maculata broodstock induced by a high protein diet
topic Blotched snakehead
Dietary protein
Egg quality
Sex steroid hormone
Reproductive performance
url http://www.sciencedirect.com/science/article/pii/S2352513423004416
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