Tissue-specific temperature dependence of RNA editing levels in zebrafish

Abstract Background RNA editing by adenosine deaminase acting on RNA (ADAR) occurs in all metazoans and fulfils several functions. Here, we examined effects of acclimation temperature (27 °C, 18 °C,13 °C) on editing patterns in six tissues of zebrafish (Danio rerio). Results Sites and total amounts...

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Main Authors: Wenhao Li, Mengdi Bu, Ruiqin Hu, Shouwen Jiang, Liangbiao Chen, George N. Somero
Format: Article
Language:English
Published: BMC 2023-11-01
Series:BMC Biology
Subjects:
Online Access:https://doi.org/10.1186/s12915-023-01738-4
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author Wenhao Li
Mengdi Bu
Ruiqin Hu
Shouwen Jiang
Liangbiao Chen
George N. Somero
author_facet Wenhao Li
Mengdi Bu
Ruiqin Hu
Shouwen Jiang
Liangbiao Chen
George N. Somero
author_sort Wenhao Li
collection DOAJ
description Abstract Background RNA editing by adenosine deaminase acting on RNA (ADAR) occurs in all metazoans and fulfils several functions. Here, we examined effects of acclimation temperature (27 °C, 18 °C,13 °C) on editing patterns in six tissues of zebrafish (Danio rerio). Results Sites and total amounts of editing differed among tissues. Brain showed the highest levels, followed by gill and skin. In these highly edited tissues, decreases in temperatures led to large increases in total amounts of editing and changes in specific edited sites. Gene ontology analysis showed both similarities (e.g., endoplasmic reticulum stress response) and differences in editing among tissues. The majority of edited sites were in transcripts of transposable elements and the 3′UTR regions of protein coding genes. By experimental validation, translation efficiency was directly related to extent of editing of the 3′UTR region of an mRNA. Conclusions RNA editing increases 3′UTR polymorphism and affects efficiency of translation. Such editing may lead to temperature-adaptive changes in the proteome through altering relative amounts of synthesis of different proteins.
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spelling doaj.art-cd156ed7576b4112b5383934ea59f91d2023-11-26T14:14:33ZengBMCBMC Biology1741-70072023-11-0121111610.1186/s12915-023-01738-4Tissue-specific temperature dependence of RNA editing levels in zebrafishWenhao Li0Mengdi Bu1Ruiqin Hu2Shouwen Jiang3Liangbiao Chen4George N. Somero5Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, College of Fisheries and Life Sciences, Shanghai Ocean UniversityKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, College of Fisheries and Life Sciences, Shanghai Ocean UniversityKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, College of Fisheries and Life Sciences, Shanghai Ocean UniversityKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, College of Fisheries and Life Sciences, Shanghai Ocean UniversityKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, College of Fisheries and Life Sciences, Shanghai Ocean UniversityDepartment of Biology, Hopkins Marine Station, Stanford UniversityAbstract Background RNA editing by adenosine deaminase acting on RNA (ADAR) occurs in all metazoans and fulfils several functions. Here, we examined effects of acclimation temperature (27 °C, 18 °C,13 °C) on editing patterns in six tissues of zebrafish (Danio rerio). Results Sites and total amounts of editing differed among tissues. Brain showed the highest levels, followed by gill and skin. In these highly edited tissues, decreases in temperatures led to large increases in total amounts of editing and changes in specific edited sites. Gene ontology analysis showed both similarities (e.g., endoplasmic reticulum stress response) and differences in editing among tissues. The majority of edited sites were in transcripts of transposable elements and the 3′UTR regions of protein coding genes. By experimental validation, translation efficiency was directly related to extent of editing of the 3′UTR region of an mRNA. Conclusions RNA editing increases 3′UTR polymorphism and affects efficiency of translation. Such editing may lead to temperature-adaptive changes in the proteome through altering relative amounts of synthesis of different proteins.https://doi.org/10.1186/s12915-023-01738-4AcclimationAdenosine deaminase acting on RNA (ADAR)Corresponding statesRNARNA editingTemperature
spellingShingle Wenhao Li
Mengdi Bu
Ruiqin Hu
Shouwen Jiang
Liangbiao Chen
George N. Somero
Tissue-specific temperature dependence of RNA editing levels in zebrafish
BMC Biology
Acclimation
Adenosine deaminase acting on RNA (ADAR)
Corresponding states
RNA
RNA editing
Temperature
title Tissue-specific temperature dependence of RNA editing levels in zebrafish
title_full Tissue-specific temperature dependence of RNA editing levels in zebrafish
title_fullStr Tissue-specific temperature dependence of RNA editing levels in zebrafish
title_full_unstemmed Tissue-specific temperature dependence of RNA editing levels in zebrafish
title_short Tissue-specific temperature dependence of RNA editing levels in zebrafish
title_sort tissue specific temperature dependence of rna editing levels in zebrafish
topic Acclimation
Adenosine deaminase acting on RNA (ADAR)
Corresponding states
RNA
RNA editing
Temperature
url https://doi.org/10.1186/s12915-023-01738-4
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AT ruiqinhu tissuespecifictemperaturedependenceofrnaeditinglevelsinzebrafish
AT shouwenjiang tissuespecifictemperaturedependenceofrnaeditinglevelsinzebrafish
AT liangbiaochen tissuespecifictemperaturedependenceofrnaeditinglevelsinzebrafish
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