Transcriptomic Insights into Dual Temperature–Salinity Stress Response in “Shuike No. 1”, a Pioneering Rainbow Trout Strain Bred in China

Global warming poses a significant threat to aquaculture, particularly for cold-water species like rainbow trout (<i>Oncorhynchus mykiss</i>). Understanding the molecular mechanisms underlying stress responses is crucial for developing resilient strains. This study investigates the dual...

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Main Authors: Xiaojun Liu, Gaochao Wang, Tianqing Huang, Enhui Liu, Wei Gu, Peng Fan, Kaibo Ge, Datian Li, Yunchao Sun, Gefeng Xu
Format: Article
Language:English
Published: MDPI AG 2025-01-01
Series:Biology
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Online Access:https://www.mdpi.com/2079-7737/14/1/49
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author Xiaojun Liu
Gaochao Wang
Tianqing Huang
Enhui Liu
Wei Gu
Peng Fan
Kaibo Ge
Datian Li
Yunchao Sun
Gefeng Xu
author_facet Xiaojun Liu
Gaochao Wang
Tianqing Huang
Enhui Liu
Wei Gu
Peng Fan
Kaibo Ge
Datian Li
Yunchao Sun
Gefeng Xu
author_sort Xiaojun Liu
collection DOAJ
description Global warming poses a significant threat to aquaculture, particularly for cold-water species like rainbow trout (<i>Oncorhynchus mykiss</i>). Understanding the molecular mechanisms underlying stress responses is crucial for developing resilient strains. This study investigates the dual stress of salinity and temperature response of “Shuike No. 1” (SK), a pioneering commercially bred rainbow trout strain in China, using RNA-sequencing of gill, intestine, and liver tissues from fish exposed to four treatment combinations: freshwater at 16 °C, freshwater at 25 °C, saltwater (30‰) at 16 °C, and saltwater at 25 °C. Differential gene expression analysis identified a substantial number of DEGs, with the liver showing the most pronounced response and a clear synergistic effect observed under combined high-temperature and salinity stress. Weighted gene co-expression network analysis (WGCNA) revealed stress-responsive gene modules and identified hub genes, primarily associated with gene expression, endoplasmic reticulum (ER) function, disease immunity, energy metabolism, and substance transport. Key hub genes included <i>klf9</i>, <i>fkbp5a</i>, <i>fkbp5b</i>, <i>ef2</i>, <i>cirbp</i>, <i>atp1b1</i>, <i>atp1b2</i>, <i>foxi3b</i>, <i>smoc1</i>, and <i>arf1</i>. Functional enrichment analysis confirmed the prominent role of ER stress, particularly the pathway “protein processing in the endoplasmic reticulum.” Our results reveal complex, tissue-specific responses to dual stress, with high temperature exerting a stronger influence than salinity. These findings provide valuable insights into the molecular mechanisms underpinning dual stress responses in SK, informing future breeding programs for enhanced resilience in the face of climate change.
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spelling doaj-art-a686a0e138ae49f5bdb7ca73110946e72025-01-24T13:23:26ZengMDPI AGBiology2079-77372025-01-011414910.3390/biology14010049Transcriptomic Insights into Dual Temperature–Salinity Stress Response in “Shuike No. 1”, a Pioneering Rainbow Trout Strain Bred in ChinaXiaojun Liu0Gaochao Wang1Tianqing Huang2Enhui Liu3Wei Gu4Peng Fan5Kaibo Ge6Datian Li7Yunchao Sun8Gefeng Xu9Heilongjiang River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Harbin 150070, ChinaHeilongjiang River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Harbin 150070, ChinaHeilongjiang River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Harbin 150070, ChinaHeilongjiang River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Harbin 150070, ChinaHeilongjiang River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Harbin 150070, ChinaHeilongjiang River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Harbin 150070, ChinaHeilongjiang River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Harbin 150070, ChinaHeilongjiang River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Harbin 150070, ChinaHeilongjiang River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Harbin 150070, ChinaHeilongjiang River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Harbin 150070, ChinaGlobal warming poses a significant threat to aquaculture, particularly for cold-water species like rainbow trout (<i>Oncorhynchus mykiss</i>). Understanding the molecular mechanisms underlying stress responses is crucial for developing resilient strains. This study investigates the dual stress of salinity and temperature response of “Shuike No. 1” (SK), a pioneering commercially bred rainbow trout strain in China, using RNA-sequencing of gill, intestine, and liver tissues from fish exposed to four treatment combinations: freshwater at 16 °C, freshwater at 25 °C, saltwater (30‰) at 16 °C, and saltwater at 25 °C. Differential gene expression analysis identified a substantial number of DEGs, with the liver showing the most pronounced response and a clear synergistic effect observed under combined high-temperature and salinity stress. Weighted gene co-expression network analysis (WGCNA) revealed stress-responsive gene modules and identified hub genes, primarily associated with gene expression, endoplasmic reticulum (ER) function, disease immunity, energy metabolism, and substance transport. Key hub genes included <i>klf9</i>, <i>fkbp5a</i>, <i>fkbp5b</i>, <i>ef2</i>, <i>cirbp</i>, <i>atp1b1</i>, <i>atp1b2</i>, <i>foxi3b</i>, <i>smoc1</i>, and <i>arf1</i>. Functional enrichment analysis confirmed the prominent role of ER stress, particularly the pathway “protein processing in the endoplasmic reticulum.” Our results reveal complex, tissue-specific responses to dual stress, with high temperature exerting a stronger influence than salinity. These findings provide valuable insights into the molecular mechanisms underpinning dual stress responses in SK, informing future breeding programs for enhanced resilience in the face of climate change.https://www.mdpi.com/2079-7737/14/1/49rainbow troutsalinity stresstemperature stressRNA-seqWGCNA
spellingShingle Xiaojun Liu
Gaochao Wang
Tianqing Huang
Enhui Liu
Wei Gu
Peng Fan
Kaibo Ge
Datian Li
Yunchao Sun
Gefeng Xu
Transcriptomic Insights into Dual Temperature–Salinity Stress Response in “Shuike No. 1”, a Pioneering Rainbow Trout Strain Bred in China
Biology
rainbow trout
salinity stress
temperature stress
RNA-seq
WGCNA
title Transcriptomic Insights into Dual Temperature–Salinity Stress Response in “Shuike No. 1”, a Pioneering Rainbow Trout Strain Bred in China
title_full Transcriptomic Insights into Dual Temperature–Salinity Stress Response in “Shuike No. 1”, a Pioneering Rainbow Trout Strain Bred in China
title_fullStr Transcriptomic Insights into Dual Temperature–Salinity Stress Response in “Shuike No. 1”, a Pioneering Rainbow Trout Strain Bred in China
title_full_unstemmed Transcriptomic Insights into Dual Temperature–Salinity Stress Response in “Shuike No. 1”, a Pioneering Rainbow Trout Strain Bred in China
title_short Transcriptomic Insights into Dual Temperature–Salinity Stress Response in “Shuike No. 1”, a Pioneering Rainbow Trout Strain Bred in China
title_sort transcriptomic insights into dual temperature salinity stress response in shuike no 1 a pioneering rainbow trout strain bred in china
topic rainbow trout
salinity stress
temperature stress
RNA-seq
WGCNA
url https://www.mdpi.com/2079-7737/14/1/49
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