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Zhang J, Wang QH, Miao BB, Wu RX, Li QQ, Tang BG, Liang ZB, Niu SF. Liver transcriptome analysis reveal the metabolic and apoptotic responses of Trachinotus ovatus under acute cold stress. FISH & SHELLFISH IMMUNOLOGY 2024; 148:109476. [PMID: 38447780 DOI: 10.1016/j.fsi.2024.109476] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 12/13/2023] [Revised: 02/07/2024] [Accepted: 03/03/2024] [Indexed: 03/08/2024]
Abstract
Trachinotus ovatus is an economically important fish and has been recommended as a high-quality aquaculture fish breed for the high-quality development of sea ranches in the South China Sea. However, T. ovatus shows intolerance to low temperature, greatly limiting the extension of farming scale, reducing production efficiency in winter, and increasing farming risks. In this study, liver transcriptome analysis was investigated in T. ovatus under acute low temperature conditions (20 and 15 °C) using RNA sequencing (RNA-Seq) technology. Inter-groups differential expression analysis and trend analysis screened 1219 DEGs and four significant profiles (profiles 0, 3, 4, and 7), respectively. GO enrichment analysis showed that these DEGs were mainly related to metabolic process and cell growth and death process. KEGG enrichment analysis found that DEGs were mainly associated with lipid metabolism, carbohydrate metabolism, and cell growth and death, such as gluconeogenesis, glycolysis, fatty acid oxidation, cholesterol biosynthesis, p53 signaling pathway, cell cycle arrest, and apoptotic cell death. Moreover, protein-protein interaction networks identified two hub genes (FOS and JUNB) and some important genes related to metabolic process and cell growth and death process, that corresponding to enrichment analysis. Overall, gluconeogenesis, lipid mobilization, and fatty acid oxidation in metabolic process and cell cycle arrest and apoptotic cell death in cell growth and death process were enhanced, while glycolysis, liver glycogen synthesis and cholesterol biosynthesis in metabolic process were inhibited. The enhancement or attenuatment of metabolic process and cell growth and death process is conducive to maintain energy balance, normal fluidity of cell membrane, normal physiological functions of liver cell, enhancing the tolerance of T. ovatus to cold stress. These results suggested that metabolic process and cell growth and death process play important roles in response to acute cold stress in the liver of T. ovatus. Gene expreesion level analysis showed that acute cold stress at 15 °C was identified as a critical temperature point for T. ovatus in term of cellular metabolism alteration and apoptosis inducement, and rewarming intervention should be timely implemented above 15 °C. Our study can provide theoretical support for breeding cold-tolerant cultivars of T. ovatus, which is contributed to high-quality productions fish production.
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Affiliation(s)
- Jing Zhang
- College of Fisheries, Guangdong Ocean University, Zhanjiang, 524088, China; Southern Marine Science and Engineering Guangdong Laboratory, Zhanjiang, 524025, China
| | - Qing-Hua Wang
- College of Fisheries, Guangdong Ocean University, Zhanjiang, 524088, China
| | - Ben-Ben Miao
- College of Fisheries, Guangdong Ocean University, Zhanjiang, 524088, China
| | - Ren-Xie Wu
- College of Fisheries, Guangdong Ocean University, Zhanjiang, 524088, China; Southern Marine Science and Engineering Guangdong Laboratory, Zhanjiang, 524025, China
| | - Qian-Qian Li
- College of Fisheries, Guangdong Ocean University, Zhanjiang, 524088, China
| | - Bao-Gui Tang
- College of Fisheries, Guangdong Ocean University, Zhanjiang, 524088, China; Southern Marine Science and Engineering Guangdong Laboratory, Zhanjiang, 524025, China
| | - Zhen-Bang Liang
- College of Fisheries, Guangdong Ocean University, Zhanjiang, 524088, China
| | - Su-Fang Niu
- College of Fisheries, Guangdong Ocean University, Zhanjiang, 524088, China; Southern Marine Science and Engineering Guangdong Laboratory, Zhanjiang, 524025, China.
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Xiao W, Chen B, Wang J, Zou Z, Wang C, Li D, Zhu J, Yu J, Yang H. Integration of mRNA and miRNA Profiling Reveals Heterosis in Oreochromis niloticus × O. aureus Hybrid Tilapia. Animals (Basel) 2022; 12:640. [PMID: 35268207 PMCID: PMC8909811 DOI: 10.3390/ani12050640] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/15/2022] [Revised: 02/28/2022] [Accepted: 03/01/2022] [Indexed: 02/08/2023] Open
Abstract
Heterosis is a widespread biological phenomenon in fishes, in which hybrids have superior traits to parents. However, the underlying molecular basis for heterosis remains uncertain. Heterosis in growth and survival rates is apparent in hybrid tilapia (Oreochromis niloticus ♀ × O. aureus ♂). Comparisons of growth and hematological biochemical characteristics and mRNA and miRNA transcriptional analyses were performed in hybrid and parents tilapia stocks to investigate the underlying molecular basis for heterosis. Growth characteristics and hematological glucose and cholesterol parameters were significantly improved in hybrids. Of 3097 differentially expressed genes (DEGs) and 120 differentially expressed miRNAs (DEMs) identified among three stocks (O. niloticus, O. aureus, and hybrids), 1598 DEGs and 62 DEMs were non-additively expressed in hybrids. Both expression level dominance and overdominance patterns occurred for DEGs and DEMs, indicating that dominance and overdominance models are widespread in the transcriptional and post-transcriptional regulation of genes involved in growth, metabolism, immunity, and antioxidant capacity in hybrid tilapia. Moreover, potential negative regulation networks between DEMs and predicted target DEGs revealed that most DEGs from miRNA-mRNA pairs are up-regulated. Dominance and overdominance models in levels of transcriptome and miRNAome facilitate the integration of advantageous parental alleles into hybrids, contributing to heterosis of growth and improved survival. The present study provides new insights into molecular heterosis in hybrid tilapia, advancing our understanding of the complex mechanisms involved in this phenomenon in aquatic animals.
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Affiliation(s)
- Wei Xiao
- Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture, National Demonstration Center for Experimental Fisheries Science Education, Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University, Shanghai 201306, China; (W.X.); (J.W.)
- Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi 214081, China; (B.C.); (Z.Z.); (D.L.); (J.Z.); (J.Y.)
| | - Binglin Chen
- Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi 214081, China; (B.C.); (Z.Z.); (D.L.); (J.Z.); (J.Y.)
| | - Jun Wang
- Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture, National Demonstration Center for Experimental Fisheries Science Education, Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University, Shanghai 201306, China; (W.X.); (J.W.)
| | - Zhiying Zou
- Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi 214081, China; (B.C.); (Z.Z.); (D.L.); (J.Z.); (J.Y.)
| | - Chenghui Wang
- Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture, National Demonstration Center for Experimental Fisheries Science Education, Shanghai Engineering Research Center of Aquaculture, Shanghai Ocean University, Shanghai 201306, China; (W.X.); (J.W.)
| | - Dayu Li
- Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi 214081, China; (B.C.); (Z.Z.); (D.L.); (J.Z.); (J.Y.)
| | - Jinglin Zhu
- Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi 214081, China; (B.C.); (Z.Z.); (D.L.); (J.Z.); (J.Y.)
| | - Jie Yu
- Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi 214081, China; (B.C.); (Z.Z.); (D.L.); (J.Z.); (J.Y.)
| | - Hong Yang
- Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi 214081, China; (B.C.); (Z.Z.); (D.L.); (J.Z.); (J.Y.)
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Shi H, Ru X, Pan S, Jiang D, Huang Y, Zhu C, Li G. Transcriptomic analysis of pituitary in female and male spotted scat (Scatophagus argus) after 17β-estradiol injection. COMPARATIVE BIOCHEMISTRY AND PHYSIOLOGY. PART D, GENOMICS & PROTEOMICS 2021; 41:100949. [PMID: 34942522 DOI: 10.1016/j.cbd.2021.100949] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 07/25/2021] [Revised: 12/01/2021] [Accepted: 12/02/2021] [Indexed: 02/07/2023]
Abstract
Spotted scat (Scatophagus argus) is a popular species of marine fish cultured in China. It shows normal sexual growth dimorphism. Female spotted scat grows quicker and bigger than males. Growth and reproduction are the most important traits in aquaculture. In vertebrates, the pituitary gland occupies an important position in the growth and reproduction axis. Estrogen is involved in regulating growth and reproduction in the pituitary gland in an endocrine fashion. Transcriptome sequencing of the pituitary was performed in female and male fish at 6 h after 17β-estradiol injection (4.0 μg E2/g body weight, BW). Compared with the pituitary of female and male groups, 144 and 64 genes [|log2(fold change)| ≥ 1.0 and false discovery rate (FDR) < 0.05] were significantly differentially expressed in E2-injected females and males, respectively (p < 0.05). Of these, 59 and 48 were up-regulated, and 85 and 16 were down-regulated. According to the Kyoto Encyclopedia of Genes and Genomes (KEGG) and Gene Ontology (GO) pathway analyses, DEGs were involved in signal pathways, such as growth, reproduction, oocyte meiosis and steroid biosynthesis. Of these, estrogen affected the expression of some sex steroid synthesis and receptor genes in the pituitary gland through feedback, such as hsd17b7, pgr and cyp19a1b, regulating the reproductive activities. Besides, some growth-related genes, such as gap43, junbb, mstn2 and insm1a responded to estrogen. E2 might affect the expression level of gh mRNA by regulating the expression levels of growth-related genes. Our results provide a theoretical basis for studying the molecular mechanism of growth and reproduction regulation at the pituitary level of spotted scat responded to E2.
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Affiliation(s)
- Hongjuan Shi
- Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Fisheries College, Guangdong Ocean University, Zhanjiang 524088, China
| | - Xiaoying Ru
- Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Fisheries College, Guangdong Ocean University, Zhanjiang 524088, China; Southern Marine Science and Engineering Guangdong Laboratory-Zhanjiang, Zhanjiang 524088, China
| | - Shuhui Pan
- Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Fisheries College, Guangdong Ocean University, Zhanjiang 524088, China
| | - Dongneng Jiang
- Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Fisheries College, Guangdong Ocean University, Zhanjiang 524088, China
| | - Yang Huang
- Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Fisheries College, Guangdong Ocean University, Zhanjiang 524088, China
| | - Chunhua Zhu
- Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Fisheries College, Guangdong Ocean University, Zhanjiang 524088, China
| | - Guangli Li
- Guangdong Research Center on Reproductive Control and Breeding Technology of Indigenous Valuable Fish Species, Fisheries College, Guangdong Ocean University, Zhanjiang 524088, China.
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Wang Y, Wang H, Hu L, Chen L. Leptin Gene Protects Against Cold Stress in Antarctic Toothfish. Front Physiol 2021; 12:740806. [PMID: 34975517 PMCID: PMC8715755 DOI: 10.3389/fphys.2021.740806] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/13/2021] [Accepted: 10/19/2021] [Indexed: 11/13/2022] Open
Abstract
Leptin is a cytokine-like peptide, predominantly biosynthesized in adipose tissue, which plays an important role in regulating food intake, energy balance and reproduction in mammals. However, how it may have been modified to enable life in the chronic cold is unclear. Here, we identified a leptin-a gene (lepa) in the cold-adapted and neutrally buoyant Antarctic toothfish Dissostichus mawsoni that encodes a polypeptide carrying four α-helices and two cysteine residues forming in-chain disulfide bonds, structures shared by most vertebrate leptins. Quantitative RT-PCR confirmed that mRNA levels of the leptin-a gene of D. mawsoni (DM-lepa) were highest in muscle, followed by kidney and liver; detection levels were low in the gill, brain, intestine, and ovary tissues. Compared with leptin-a genes of fishes living in warmer waters, DM-lepa underwent rapid evolution and was subjected to positive selection. Over-expression of DM-lepa in the zebrafish cell line ZFL resulted in signal accumulation in the cytoplasm and significantly increased cell proliferation both at the normal culture temperature and under cold treatment. DM-lepa over-expression also reduced apoptosis under low-temperature stress and activated the STAT3 signaling pathway, in turn upregulating the anti-apoptotic proteins bcl2l1, bcl2a, myca and mdm2 while downregulating the pro-apoptotic baxa, p53 and caspase-3. These results demonstrate that DM-lepa, through STAT3 signaling, plays a protective role in cold stress by preventing apoptotic damage. Our study reveals a new role of lepa in polar fish.
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Affiliation(s)
- Ying Wang
- International Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, China
- Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, China
- Shanghai Collaborative Innovation for Aquatic Animal Genetics and Breeding, Shanghai Ocean University, Shanghai, China
| | - Huamin Wang
- International Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, China
- Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, China
- Shanghai Collaborative Innovation for Aquatic Animal Genetics and Breeding, Shanghai Ocean University, Shanghai, China
| | - Linghong Hu
- International Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, China
- Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, China
- Shanghai Collaborative Innovation for Aquatic Animal Genetics and Breeding, Shanghai Ocean University, Shanghai, China
| | - Liangbiao Chen
- International Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, China
- Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, China
- Shanghai Collaborative Innovation for Aquatic Animal Genetics and Breeding, Shanghai Ocean University, Shanghai, China
- *Correspondence: Liangbiao Chen,
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