Comparative Transcriptome Analyses Provide New Insights into the Evolution of Divergent Thermal Resistance in Two Eel Gobies

Adaptation to thermal conditions in tidal mudflats always involves tolerating frequent fluctuations and often extreme environmental temperatures. Regulation of gene expression plays a fundamental role in the evolution of these thermal adaptations. To identify the key gene regulatory networks associa...

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Main Authors: Jing Liu, Tianwei Liu, Yantao Liu, Yuzhen Wang, Liqin Liu, Li Gong, Bingjian Liu, Zhenming Lü
Format: Article
Language:English
Published: MDPI AG 2023-12-01
Series:Current Issues in Molecular Biology
Subjects:
Online Access:https://www.mdpi.com/1467-3045/46/1/12
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author Jing Liu
Tianwei Liu
Yantao Liu
Yuzhen Wang
Liqin Liu
Li Gong
Bingjian Liu
Zhenming Lü
author_facet Jing Liu
Tianwei Liu
Yantao Liu
Yuzhen Wang
Liqin Liu
Li Gong
Bingjian Liu
Zhenming Lü
author_sort Jing Liu
collection DOAJ
description Adaptation to thermal conditions in tidal mudflats always involves tolerating frequent fluctuations and often extreme environmental temperatures. Regulation of gene expression plays a fundamental role in the evolution of these thermal adaptations. To identify the key gene regulatory networks associated with the thermal adaptation, we investigated the capability of cold tolerance, as well as the transcriptomic changes under cold stress in two mudflat inhabitants (<i>Odontamblyopus lacepedii</i> and <i>O. rebecca</i>) with contrasting latitude affinity. Our results revealed a remarkable divergent capacity of cold tolerance (CT<sub>min</sub>: 0.61 °C vs. 9.57 °C) between the two gobies. Analysis of transcriptomic changes under cold stress unveiled 193 differentially expressed genes exhibiting similar expression profiles across all tissues and species, including several classic metabolic and circadian rhythm molecules such as <i>ACOD</i> and <i>CIART</i> that may represent the core cold response machinery in eel gobies. Meanwhile, some genes show a unique expression spectrum in the more cold-tolerant <i>O. lacepedii</i> suggesting their roles in the enhanced cold tolerance and hence the extreme thermal adaptations. In addition, a weighted gene co-expression network analysis (WGCNA) revealed a subset of metabolic hub genes including <i>MYH11</i> and <i>LIPT2</i> showing distinct down-regulation in <i>O. lacepedii</i> when exposed to cold stress which highlights the role of reduced energy consumption in the enhanced cold tolerance of eel gobies. These findings not only provide new insights into how mudflat teleosts could cope with cold stress and their potential evolutionary strategies for adapting to their thermal environment, but also have important implications for sound management and conservation of their fishery resources in a scenario of global climate warming in the marine realm.
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spelling doaj.art-d77224d0d2fe4c9fb508893eb5f20e702024-01-26T15:50:26ZengMDPI AGCurrent Issues in Molecular Biology1467-30371467-30452023-12-0146115317010.3390/cimb46010012Comparative Transcriptome Analyses Provide New Insights into the Evolution of Divergent Thermal Resistance in Two Eel GobiesJing Liu0Tianwei Liu1Yantao Liu2Yuzhen Wang3Liqin Liu4Li Gong5Bingjian Liu6Zhenming Lü7National Engineering Laboratory of Marine Germplasm Resources Exploration and Utilization, College of Marine Sciences and Technology, Zhejiang Ocean University, Zhoushan 316022, ChinaNational Engineering Laboratory of Marine Germplasm Resources Exploration and Utilization, College of Marine Sciences and Technology, Zhejiang Ocean University, Zhoushan 316022, ChinaNational Engineering Laboratory of Marine Germplasm Resources Exploration and Utilization, College of Marine Sciences and Technology, Zhejiang Ocean University, Zhoushan 316022, ChinaNational Engineering Research Center for Facilitated Marine Aquaculture, Zhejiang Ocean University, Zhoushan 316022, ChinaNational Engineering Laboratory of Marine Germplasm Resources Exploration and Utilization, College of Marine Sciences and Technology, Zhejiang Ocean University, Zhoushan 316022, ChinaNational Engineering Laboratory of Marine Germplasm Resources Exploration and Utilization, College of Marine Sciences and Technology, Zhejiang Ocean University, Zhoushan 316022, ChinaNational Engineering Laboratory of Marine Germplasm Resources Exploration and Utilization, College of Marine Sciences and Technology, Zhejiang Ocean University, Zhoushan 316022, ChinaNational Engineering Laboratory of Marine Germplasm Resources Exploration and Utilization, College of Marine Sciences and Technology, Zhejiang Ocean University, Zhoushan 316022, ChinaAdaptation to thermal conditions in tidal mudflats always involves tolerating frequent fluctuations and often extreme environmental temperatures. Regulation of gene expression plays a fundamental role in the evolution of these thermal adaptations. To identify the key gene regulatory networks associated with the thermal adaptation, we investigated the capability of cold tolerance, as well as the transcriptomic changes under cold stress in two mudflat inhabitants (<i>Odontamblyopus lacepedii</i> and <i>O. rebecca</i>) with contrasting latitude affinity. Our results revealed a remarkable divergent capacity of cold tolerance (CT<sub>min</sub>: 0.61 °C vs. 9.57 °C) between the two gobies. Analysis of transcriptomic changes under cold stress unveiled 193 differentially expressed genes exhibiting similar expression profiles across all tissues and species, including several classic metabolic and circadian rhythm molecules such as <i>ACOD</i> and <i>CIART</i> that may represent the core cold response machinery in eel gobies. Meanwhile, some genes show a unique expression spectrum in the more cold-tolerant <i>O. lacepedii</i> suggesting their roles in the enhanced cold tolerance and hence the extreme thermal adaptations. In addition, a weighted gene co-expression network analysis (WGCNA) revealed a subset of metabolic hub genes including <i>MYH11</i> and <i>LIPT2</i> showing distinct down-regulation in <i>O. lacepedii</i> when exposed to cold stress which highlights the role of reduced energy consumption in the enhanced cold tolerance of eel gobies. These findings not only provide new insights into how mudflat teleosts could cope with cold stress and their potential evolutionary strategies for adapting to their thermal environment, but also have important implications for sound management and conservation of their fishery resources in a scenario of global climate warming in the marine realm.https://www.mdpi.com/1467-3045/46/1/12comparative transcriptomicsthermal adaptationgenetic mechanismseel goby
spellingShingle Jing Liu
Tianwei Liu
Yantao Liu
Yuzhen Wang
Liqin Liu
Li Gong
Bingjian Liu
Zhenming Lü
Comparative Transcriptome Analyses Provide New Insights into the Evolution of Divergent Thermal Resistance in Two Eel Gobies
Current Issues in Molecular Biology
comparative transcriptomics
thermal adaptation
genetic mechanisms
eel goby
title Comparative Transcriptome Analyses Provide New Insights into the Evolution of Divergent Thermal Resistance in Two Eel Gobies
title_full Comparative Transcriptome Analyses Provide New Insights into the Evolution of Divergent Thermal Resistance in Two Eel Gobies
title_fullStr Comparative Transcriptome Analyses Provide New Insights into the Evolution of Divergent Thermal Resistance in Two Eel Gobies
title_full_unstemmed Comparative Transcriptome Analyses Provide New Insights into the Evolution of Divergent Thermal Resistance in Two Eel Gobies
title_short Comparative Transcriptome Analyses Provide New Insights into the Evolution of Divergent Thermal Resistance in Two Eel Gobies
title_sort comparative transcriptome analyses provide new insights into the evolution of divergent thermal resistance in two eel gobies
topic comparative transcriptomics
thermal adaptation
genetic mechanisms
eel goby
url https://www.mdpi.com/1467-3045/46/1/12
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