Differences in gene expression between high and low tolerance rainbow trout (Oncorhynchus mykiss) to acute thermal stress.

Understanding the mechanisms that underlie the adaptive response of ectotherms to rising temperatures is key to mitigate the effects of climate change. We assessed the molecular and physiological processes that differentiate between rainbow trout (Oncorhynchus mykiss) with high and low tolerance to...

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Main Authors: Leah A Turner, Anne A Easton, Moira M Ferguson, Roy G Danzmann
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0312694
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author Leah A Turner
Anne A Easton
Moira M Ferguson
Roy G Danzmann
author_facet Leah A Turner
Anne A Easton
Moira M Ferguson
Roy G Danzmann
author_sort Leah A Turner
collection DOAJ
description Understanding the mechanisms that underlie the adaptive response of ectotherms to rising temperatures is key to mitigate the effects of climate change. We assessed the molecular and physiological processes that differentiate between rainbow trout (Oncorhynchus mykiss) with high and low tolerance to acute thermal stress. To achieve our goal, we used a critical thermal maximum trial in two strains of rainbow trout to elicit loss of equilibrium responses to identify high and low tolerance fish. We then compared the hepatic transcriptome profiles of high and low tolerance fish relative to untreated controls common to both strains to uncover patterns of differential gene expression and to gain a broad perspective on the interacting gene pathways and functional processes involved. We observed some of the classic responses to increased temperature (e.g., induction of heat shock proteins) but these responses were not the defining factors that differentiated high and low tolerance fish. Instead, high tolerance fish appeared to suppress growth-related functions, enhance certain autophagy components, better regulate neurodegenerative processes, and enhance stress-related protein synthesis, specifically spliceosomal complex activities, mRNA regulation, and protein processing through post-translational processes, relative to low tolerance fish. In contrast, low tolerance fish had higher transcript diversity and demonstrated elevated developmental, cytoskeletal, and morphogenic, as well as lipid and carbohydrate metabolic processes, relative to high tolerance fish. Our results suggest that high tolerance fish engaged in processes that supported the prevention of further damage by enhancing repair pathways, whereas low tolerance fish were more focused on replacing damaged cells and their structures.
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spelling doaj-art-8170d6d6b28d4a0789873281ece4e1aa2025-01-17T05:31:34ZengPublic Library of Science (PLoS)PLoS ONE1932-62032025-01-01201e031269410.1371/journal.pone.0312694Differences in gene expression between high and low tolerance rainbow trout (Oncorhynchus mykiss) to acute thermal stress.Leah A TurnerAnne A EastonMoira M FergusonRoy G DanzmannUnderstanding the mechanisms that underlie the adaptive response of ectotherms to rising temperatures is key to mitigate the effects of climate change. We assessed the molecular and physiological processes that differentiate between rainbow trout (Oncorhynchus mykiss) with high and low tolerance to acute thermal stress. To achieve our goal, we used a critical thermal maximum trial in two strains of rainbow trout to elicit loss of equilibrium responses to identify high and low tolerance fish. We then compared the hepatic transcriptome profiles of high and low tolerance fish relative to untreated controls common to both strains to uncover patterns of differential gene expression and to gain a broad perspective on the interacting gene pathways and functional processes involved. We observed some of the classic responses to increased temperature (e.g., induction of heat shock proteins) but these responses were not the defining factors that differentiated high and low tolerance fish. Instead, high tolerance fish appeared to suppress growth-related functions, enhance certain autophagy components, better regulate neurodegenerative processes, and enhance stress-related protein synthesis, specifically spliceosomal complex activities, mRNA regulation, and protein processing through post-translational processes, relative to low tolerance fish. In contrast, low tolerance fish had higher transcript diversity and demonstrated elevated developmental, cytoskeletal, and morphogenic, as well as lipid and carbohydrate metabolic processes, relative to high tolerance fish. Our results suggest that high tolerance fish engaged in processes that supported the prevention of further damage by enhancing repair pathways, whereas low tolerance fish were more focused on replacing damaged cells and their structures.https://doi.org/10.1371/journal.pone.0312694
spellingShingle Leah A Turner
Anne A Easton
Moira M Ferguson
Roy G Danzmann
Differences in gene expression between high and low tolerance rainbow trout (Oncorhynchus mykiss) to acute thermal stress.
PLoS ONE
title Differences in gene expression between high and low tolerance rainbow trout (Oncorhynchus mykiss) to acute thermal stress.
title_full Differences in gene expression between high and low tolerance rainbow trout (Oncorhynchus mykiss) to acute thermal stress.
title_fullStr Differences in gene expression between high and low tolerance rainbow trout (Oncorhynchus mykiss) to acute thermal stress.
title_full_unstemmed Differences in gene expression between high and low tolerance rainbow trout (Oncorhynchus mykiss) to acute thermal stress.
title_short Differences in gene expression between high and low tolerance rainbow trout (Oncorhynchus mykiss) to acute thermal stress.
title_sort differences in gene expression between high and low tolerance rainbow trout oncorhynchus mykiss to acute thermal stress
url https://doi.org/10.1371/journal.pone.0312694
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