Application of transcriptome analysis to investigate the effects of long-term low temperature stress on liver function in the tiger puffer (Takifugu rubripes)

The tiger puffer (Takifugu rubripes) is an important economic fish species in northern China. However, it is a warm-temperature species, and low winter temperatures can result in high mortality in aquaculture. Understanding the mechanisms of cold resistance in tiger puffers will thus provide critica...

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Main Authors: Zhifeng Liu, Liguang Zhu, Xinan Wang, Shiying Liu, Aijun Ma, Haowen Chang, Zhibin Sun, Fei Xu, Haichi Zhao
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-11-01
Series:Frontiers in Marine Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmars.2022.1069711/full
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author Zhifeng Liu
Zhifeng Liu
Liguang Zhu
Liguang Zhu
Liguang Zhu
Xinan Wang
Xinan Wang
Shiying Liu
Shiying Liu
Aijun Ma
Aijun Ma
Haowen Chang
Haowen Chang
Haowen Chang
Zhibin Sun
Zhibin Sun
Fei Xu
Fei Xu
Haichi Zhao
Haichi Zhao
Haichi Zhao
author_facet Zhifeng Liu
Zhifeng Liu
Liguang Zhu
Liguang Zhu
Liguang Zhu
Xinan Wang
Xinan Wang
Shiying Liu
Shiying Liu
Aijun Ma
Aijun Ma
Haowen Chang
Haowen Chang
Haowen Chang
Zhibin Sun
Zhibin Sun
Fei Xu
Fei Xu
Haichi Zhao
Haichi Zhao
Haichi Zhao
author_sort Zhifeng Liu
collection DOAJ
description The tiger puffer (Takifugu rubripes) is an important economic fish species in northern China. However, it is a warm-temperature species, and low winter temperatures can result in high mortality in aquaculture. Understanding the mechanisms of cold resistance in tiger puffers will thus provide critical information to help cope with winter cold. In this study, we performed transcriptome analysis of livers from puffer fish kept at different temperatures (18°C, 13°C, and 8°C) to identify the key pathways and genes involved in the response to low-temperature stress. We also detected serum levels of proteases, arginine, and proline to obtain further information on the response to cold adaption. Totals of 51, 942, and 195 differentially expressed genes were identified in the 18°C vs 13°C, 18°C vs 8°C, and 13°C vs 8°C groups, respectively. Pathway analysis showed that significantly enriched pathways were mainly related to digestion, metabolism, and environmental adaptation. Most genes in the pathways related to digestion and metabolism were down-regulated, while most genes in the pathways related to environmental adaptation were up-regulated. Serum levels of proteases were significantly lower in the low-temperature groups (13°C and 8°C) compared with the control group (18°C), while arginine and proline levels were significantly higher in the 8°C group compared with the other two groups. These results suggest that low temperature caused digestive and metabolic disorders, as well as adaptive changes to low temperature in tiger puffers. On this premise, we found that some up-regulated genes in the pancreatic secretion pathway, arginine and proline metabolism pathway, and circadian rhythm pathway played important roles in the survival, growth, and development of tiger puffers under low-temperature stress. The accumulation of arginine and proline can maintain metabolism and circulation and resist cold stress. The circadian rhythm is closely related to digestion and metabolism, which is an adaptive change and plays a positive role in the resistance to low temperature. The results of this study provide new insights and a theoretical basis for the study of cold tolerance in tiger puffers.
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spelling doaj.art-a0c83a2d113a4ed6a14c21d14fe0206b2022-12-22T02:44:39ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452022-11-01910.3389/fmars.2022.10697111069711Application of transcriptome analysis to investigate the effects of long-term low temperature stress on liver function in the tiger puffer (Takifugu rubripes)Zhifeng Liu0Zhifeng Liu1Liguang Zhu2Liguang Zhu3Liguang Zhu4Xinan Wang5Xinan Wang6Shiying Liu7Shiying Liu8Aijun Ma9Aijun Ma10Haowen Chang11Haowen Chang12Haowen Chang13Zhibin Sun14Zhibin Sun15Fei Xu16Fei Xu17Haichi Zhao18Haichi Zhao19Haichi Zhao20Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, ChinaLaboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, ChinaYellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, ChinaLaboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, ChinaCollege of Fisheries and Life Science, Dalian Ocean University, Dalian, ChinaYellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, ChinaLaboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, ChinaYellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, ChinaLaboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, ChinaYellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, ChinaLaboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, ChinaYellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, ChinaLaboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, ChinaCollege of Fisheries and Life Science, Shanghai Ocean University, Ministry of Education, Shanghai, ChinaYellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, ChinaLaboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, ChinaYellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, ChinaLaboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, ChinaYellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, ChinaLaboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, ChinaCollege of Fisheries and Life Science, Shanghai Ocean University, Ministry of Education, Shanghai, ChinaThe tiger puffer (Takifugu rubripes) is an important economic fish species in northern China. However, it is a warm-temperature species, and low winter temperatures can result in high mortality in aquaculture. Understanding the mechanisms of cold resistance in tiger puffers will thus provide critical information to help cope with winter cold. In this study, we performed transcriptome analysis of livers from puffer fish kept at different temperatures (18°C, 13°C, and 8°C) to identify the key pathways and genes involved in the response to low-temperature stress. We also detected serum levels of proteases, arginine, and proline to obtain further information on the response to cold adaption. Totals of 51, 942, and 195 differentially expressed genes were identified in the 18°C vs 13°C, 18°C vs 8°C, and 13°C vs 8°C groups, respectively. Pathway analysis showed that significantly enriched pathways were mainly related to digestion, metabolism, and environmental adaptation. Most genes in the pathways related to digestion and metabolism were down-regulated, while most genes in the pathways related to environmental adaptation were up-regulated. Serum levels of proteases were significantly lower in the low-temperature groups (13°C and 8°C) compared with the control group (18°C), while arginine and proline levels were significantly higher in the 8°C group compared with the other two groups. These results suggest that low temperature caused digestive and metabolic disorders, as well as adaptive changes to low temperature in tiger puffers. On this premise, we found that some up-regulated genes in the pancreatic secretion pathway, arginine and proline metabolism pathway, and circadian rhythm pathway played important roles in the survival, growth, and development of tiger puffers under low-temperature stress. The accumulation of arginine and proline can maintain metabolism and circulation and resist cold stress. The circadian rhythm is closely related to digestion and metabolism, which is an adaptive change and plays a positive role in the resistance to low temperature. The results of this study provide new insights and a theoretical basis for the study of cold tolerance in tiger puffers.https://www.frontiersin.org/articles/10.3389/fmars.2022.1069711/fullTakifugu rubripeslow temperaturelivertranscriptomeqPCR
spellingShingle Zhifeng Liu
Zhifeng Liu
Liguang Zhu
Liguang Zhu
Liguang Zhu
Xinan Wang
Xinan Wang
Shiying Liu
Shiying Liu
Aijun Ma
Aijun Ma
Haowen Chang
Haowen Chang
Haowen Chang
Zhibin Sun
Zhibin Sun
Fei Xu
Fei Xu
Haichi Zhao
Haichi Zhao
Haichi Zhao
Application of transcriptome analysis to investigate the effects of long-term low temperature stress on liver function in the tiger puffer (Takifugu rubripes)
Frontiers in Marine Science
Takifugu rubripes
low temperature
liver
transcriptome
qPCR
title Application of transcriptome analysis to investigate the effects of long-term low temperature stress on liver function in the tiger puffer (Takifugu rubripes)
title_full Application of transcriptome analysis to investigate the effects of long-term low temperature stress on liver function in the tiger puffer (Takifugu rubripes)
title_fullStr Application of transcriptome analysis to investigate the effects of long-term low temperature stress on liver function in the tiger puffer (Takifugu rubripes)
title_full_unstemmed Application of transcriptome analysis to investigate the effects of long-term low temperature stress on liver function in the tiger puffer (Takifugu rubripes)
title_short Application of transcriptome analysis to investigate the effects of long-term low temperature stress on liver function in the tiger puffer (Takifugu rubripes)
title_sort application of transcriptome analysis to investigate the effects of long term low temperature stress on liver function in the tiger puffer takifugu rubripes
topic Takifugu rubripes
low temperature
liver
transcriptome
qPCR
url https://www.frontiersin.org/articles/10.3389/fmars.2022.1069711/full
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