Liver Transcriptomic Analysis of the Effects of Dietary Fish Oil Revealed a Regulated Expression Pattern of Genes in Adult Female Spotted Scat (Scatophagus argus)

Despite the significance of n-3 long-chain polyunsaturated fatty acid (n-3 LC-PUFA) in fish oil in promoting the maturation of female broodstocks, the detailed mechanism of the effect on the expression of hepatic reproduction-related genes is still unclear. In this study, transcriptome sequencing wa...

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Main Authors: Tuo Wang, Dongneng Jiang, Hongjuan Shi, Umar Farouk Mustapha, Siping Deng, Zhilong Liu, Wanxin Li, Huapu Chen, Chunhua Zhu, Guangli Li
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-11-01
Series:Frontiers in Marine Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmars.2021.784845/full
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author Tuo Wang
Dongneng Jiang
Hongjuan Shi
Umar Farouk Mustapha
Siping Deng
Zhilong Liu
Wanxin Li
Huapu Chen
Chunhua Zhu
Chunhua Zhu
Guangli Li
author_facet Tuo Wang
Dongneng Jiang
Hongjuan Shi
Umar Farouk Mustapha
Siping Deng
Zhilong Liu
Wanxin Li
Huapu Chen
Chunhua Zhu
Chunhua Zhu
Guangli Li
author_sort Tuo Wang
collection DOAJ
description Despite the significance of n-3 long-chain polyunsaturated fatty acid (n-3 LC-PUFA) in fish oil in promoting the maturation of female broodstocks, the detailed mechanism of the effect on the expression of hepatic reproduction-related genes is still unclear. In this study, transcriptome sequencing was used to analyze the effect of the higher dietary n-3 LC-PUFA level on gene expression in the liver of adult females spotted scat. Two-year-old female spotted scat (average weight, 242.83 ± 50.90 g) were fed with diets containing 8% fish oil (FO) or 8% soybean oil (SO) for 40 days. The fatty acid profile in the serum, liver, and ovary was analyzed, and high proportions of n-3 LC-PUFA were observed in the FO group. The final average fish body weight and gonadosomatic index were similar between the FO and SO groups. The serum vitellogenin (Vtg) and hepatosomatic index (HSI) of the FO group were significantly higher and lower than that of the SO group, respectively. Comparatively, the liver transcriptome analysis showed 497 upregulated and 267 downregulated genes in the FO group. Among them, the expression levels of three estrogen-regulated genes (i.e., Vtga, Vtgb, and Zp4) were significantly higher in the FO than in the SO group. This expression pattern could be related to the upregulation of Hsd17b7 (the key gene for the synthesis of liver steroid hormone) and the downregulation of the Hsp90 (the estrogen receptor chaperone). The expression levels of Foxo1a and Lep, which are involved in the lipid metabolism, decreased significantly in the FO group, which may be related to the lower level of HSI in the FO group. The genes related to liver LC-PUFA absorption and transport, Fabp2 and Mfsd2ab, were significantly upregulated in the FO group, indicating that fish actively adapt to high-fish-oil diets. In brief, high-fish-oil diets can influence the expression of genes related to liver n-3 LC-PUFA metabolism and reproduction, inhibit the accumulation of liver fat, and promote the liver health and gonad development. This study will contribute to clarifying the mechanism of dietary n-3 LC-PUFA on promoting reproductive development in teleost fish.
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spelling doaj.art-ee28a4848cab42fa92ccc1e1ee26d4882022-12-22T04:10:22ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452021-11-01810.3389/fmars.2021.784845784845Liver Transcriptomic Analysis of the Effects of Dietary Fish Oil Revealed a Regulated Expression Pattern of Genes in Adult Female Spotted Scat (Scatophagus argus)Tuo Wang0Dongneng Jiang1Hongjuan Shi2Umar Farouk Mustapha3Siping Deng4Zhilong Liu5Wanxin Li6Huapu Chen7Chunhua Zhu8Chunhua Zhu9Guangli Li10Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Fisheries College, Guangdong Ocean University, Zhanjiang, ChinaGuangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Fisheries College, Guangdong Ocean University, Zhanjiang, ChinaGuangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Fisheries College, Guangdong Ocean University, Zhanjiang, ChinaGuangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Fisheries College, Guangdong Ocean University, Zhanjiang, ChinaGuangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Fisheries College, Guangdong Ocean University, Zhanjiang, ChinaGuangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Fisheries College, Guangdong Ocean University, Zhanjiang, ChinaGuangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Fisheries College, Guangdong Ocean University, Zhanjiang, ChinaGuangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Fisheries College, Guangdong Ocean University, Zhanjiang, ChinaGuangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Fisheries College, Guangdong Ocean University, Zhanjiang, ChinaSouthern Marine Science and Engineering Guangdong Laboratory, Zhanjiang, ChinaGuangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Fisheries College, Guangdong Ocean University, Zhanjiang, ChinaDespite the significance of n-3 long-chain polyunsaturated fatty acid (n-3 LC-PUFA) in fish oil in promoting the maturation of female broodstocks, the detailed mechanism of the effect on the expression of hepatic reproduction-related genes is still unclear. In this study, transcriptome sequencing was used to analyze the effect of the higher dietary n-3 LC-PUFA level on gene expression in the liver of adult females spotted scat. Two-year-old female spotted scat (average weight, 242.83 ± 50.90 g) were fed with diets containing 8% fish oil (FO) or 8% soybean oil (SO) for 40 days. The fatty acid profile in the serum, liver, and ovary was analyzed, and high proportions of n-3 LC-PUFA were observed in the FO group. The final average fish body weight and gonadosomatic index were similar between the FO and SO groups. The serum vitellogenin (Vtg) and hepatosomatic index (HSI) of the FO group were significantly higher and lower than that of the SO group, respectively. Comparatively, the liver transcriptome analysis showed 497 upregulated and 267 downregulated genes in the FO group. Among them, the expression levels of three estrogen-regulated genes (i.e., Vtga, Vtgb, and Zp4) were significantly higher in the FO than in the SO group. This expression pattern could be related to the upregulation of Hsd17b7 (the key gene for the synthesis of liver steroid hormone) and the downregulation of the Hsp90 (the estrogen receptor chaperone). The expression levels of Foxo1a and Lep, which are involved in the lipid metabolism, decreased significantly in the FO group, which may be related to the lower level of HSI in the FO group. The genes related to liver LC-PUFA absorption and transport, Fabp2 and Mfsd2ab, were significantly upregulated in the FO group, indicating that fish actively adapt to high-fish-oil diets. In brief, high-fish-oil diets can influence the expression of genes related to liver n-3 LC-PUFA metabolism and reproduction, inhibit the accumulation of liver fat, and promote the liver health and gonad development. This study will contribute to clarifying the mechanism of dietary n-3 LC-PUFA on promoting reproductive development in teleost fish.https://www.frontiersin.org/articles/10.3389/fmars.2021.784845/fullspotted scatfemale broodstockfish oillivertranscriptomereproduction
spellingShingle Tuo Wang
Dongneng Jiang
Hongjuan Shi
Umar Farouk Mustapha
Siping Deng
Zhilong Liu
Wanxin Li
Huapu Chen
Chunhua Zhu
Chunhua Zhu
Guangli Li
Liver Transcriptomic Analysis of the Effects of Dietary Fish Oil Revealed a Regulated Expression Pattern of Genes in Adult Female Spotted Scat (Scatophagus argus)
Frontiers in Marine Science
spotted scat
female broodstock
fish oil
liver
transcriptome
reproduction
title Liver Transcriptomic Analysis of the Effects of Dietary Fish Oil Revealed a Regulated Expression Pattern of Genes in Adult Female Spotted Scat (Scatophagus argus)
title_full Liver Transcriptomic Analysis of the Effects of Dietary Fish Oil Revealed a Regulated Expression Pattern of Genes in Adult Female Spotted Scat (Scatophagus argus)
title_fullStr Liver Transcriptomic Analysis of the Effects of Dietary Fish Oil Revealed a Regulated Expression Pattern of Genes in Adult Female Spotted Scat (Scatophagus argus)
title_full_unstemmed Liver Transcriptomic Analysis of the Effects of Dietary Fish Oil Revealed a Regulated Expression Pattern of Genes in Adult Female Spotted Scat (Scatophagus argus)
title_short Liver Transcriptomic Analysis of the Effects of Dietary Fish Oil Revealed a Regulated Expression Pattern of Genes in Adult Female Spotted Scat (Scatophagus argus)
title_sort liver transcriptomic analysis of the effects of dietary fish oil revealed a regulated expression pattern of genes in adult female spotted scat scatophagus argus
topic spotted scat
female broodstock
fish oil
liver
transcriptome
reproduction
url https://www.frontiersin.org/articles/10.3389/fmars.2021.784845/full
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