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The ability to induce heat shock transcription factor-regulated genes in response to lethal heat stress is associated with thermotolerance in tomato cultivars

Heat stress is a severe challenge for plant production, and the use of thermotolerant cultivars is critical to ensure stable production in high-temperature-prone environments. However, the selection of thermotolerant cultivars is difficult due to the complex nature of heat stress and the time and sp...

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Autores principales: Mizoi, Junya, Todaka, Daisuke, Imatomi, Tomohiro, Kidokoro, Satoshi, Sakurai, Tetsuya, Kodaira, Ken-Suke, Takayama, Hidehito, Shinozaki, Kazuo, Yamaguchi-Shinozaki, Kazuko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10585066/
https://www.ncbi.nlm.nih.gov/pubmed/37868310
http://dx.doi.org/10.3389/fpls.2023.1269964
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author Mizoi, Junya
Todaka, Daisuke
Imatomi, Tomohiro
Kidokoro, Satoshi
Sakurai, Tetsuya
Kodaira, Ken-Suke
Takayama, Hidehito
Shinozaki, Kazuo
Yamaguchi-Shinozaki, Kazuko
author_facet Mizoi, Junya
Todaka, Daisuke
Imatomi, Tomohiro
Kidokoro, Satoshi
Sakurai, Tetsuya
Kodaira, Ken-Suke
Takayama, Hidehito
Shinozaki, Kazuo
Yamaguchi-Shinozaki, Kazuko
author_sort Mizoi, Junya
collection PubMed
description Heat stress is a severe challenge for plant production, and the use of thermotolerant cultivars is critical to ensure stable production in high-temperature-prone environments. However, the selection of thermotolerant cultivars is difficult due to the complex nature of heat stress and the time and space needed for evaluation. In this study, we characterized genome-wide differences in gene expression between thermotolerant and thermosensitive tomato cultivars and examined the possibility of selecting gene expression markers to estimate thermotolerance among different tomato cultivars. We selected one thermotolerant and one thermosensitive cultivar based on physiological evaluations and compared heat-responsive gene expression in these cultivars under stepwise heat stress and acute heat shock conditions. Transcriptomic analyses reveled that two heat-inducible gene expression pathways, controlled by the heat shock element (HSE) and the evening element (EE), respectively, presented different responses depending on heat stress conditions. HSE-regulated gene expression was induced under both conditions, while EE-regulated gene expression was only induced under gradual heat stress conditions in both cultivars. Furthermore, HSE-regulated genes showed higher expression in the thermotolerant cultivar than the sensitive cultivar under acute heat shock conditions. Then, candidate expression biomarker genes were selected based on the transcriptome data, and the usefulness of these candidate genes was validated in five cultivars. This study shows that the thermotolerance of tomato is correlated with its ability to maintain the heat shock response (HSR) under acute severe heat shock conditions. Furthermore, it raises the possibility that the robustness of the HSR under severe heat stress can be used as an indicator to evaluate the thermotolerance of crop cultivars.
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spelling pubmed-105850662023-10-20 The ability to induce heat shock transcription factor-regulated genes in response to lethal heat stress is associated with thermotolerance in tomato cultivars Mizoi, Junya Todaka, Daisuke Imatomi, Tomohiro Kidokoro, Satoshi Sakurai, Tetsuya Kodaira, Ken-Suke Takayama, Hidehito Shinozaki, Kazuo Yamaguchi-Shinozaki, Kazuko Front Plant Sci Plant Science Heat stress is a severe challenge for plant production, and the use of thermotolerant cultivars is critical to ensure stable production in high-temperature-prone environments. However, the selection of thermotolerant cultivars is difficult due to the complex nature of heat stress and the time and space needed for evaluation. In this study, we characterized genome-wide differences in gene expression between thermotolerant and thermosensitive tomato cultivars and examined the possibility of selecting gene expression markers to estimate thermotolerance among different tomato cultivars. We selected one thermotolerant and one thermosensitive cultivar based on physiological evaluations and compared heat-responsive gene expression in these cultivars under stepwise heat stress and acute heat shock conditions. Transcriptomic analyses reveled that two heat-inducible gene expression pathways, controlled by the heat shock element (HSE) and the evening element (EE), respectively, presented different responses depending on heat stress conditions. HSE-regulated gene expression was induced under both conditions, while EE-regulated gene expression was only induced under gradual heat stress conditions in both cultivars. Furthermore, HSE-regulated genes showed higher expression in the thermotolerant cultivar than the sensitive cultivar under acute heat shock conditions. Then, candidate expression biomarker genes were selected based on the transcriptome data, and the usefulness of these candidate genes was validated in five cultivars. This study shows that the thermotolerance of tomato is correlated with its ability to maintain the heat shock response (HSR) under acute severe heat shock conditions. Furthermore, it raises the possibility that the robustness of the HSR under severe heat stress can be used as an indicator to evaluate the thermotolerance of crop cultivars. Frontiers Media S.A. 2023-10-05 /pmc/articles/PMC10585066/ /pubmed/37868310 http://dx.doi.org/10.3389/fpls.2023.1269964 Text en Copyright © 2023 Mizoi, Todaka, Imatomi, Kidokoro, Sakurai, Kodaira, Takayama, Shinozaki and Yamaguchi-Shinozaki https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Mizoi, Junya
Todaka, Daisuke
Imatomi, Tomohiro
Kidokoro, Satoshi
Sakurai, Tetsuya
Kodaira, Ken-Suke
Takayama, Hidehito
Shinozaki, Kazuo
Yamaguchi-Shinozaki, Kazuko
The ability to induce heat shock transcription factor-regulated genes in response to lethal heat stress is associated with thermotolerance in tomato cultivars
title The ability to induce heat shock transcription factor-regulated genes in response to lethal heat stress is associated with thermotolerance in tomato cultivars
title_full The ability to induce heat shock transcription factor-regulated genes in response to lethal heat stress is associated with thermotolerance in tomato cultivars
title_fullStr The ability to induce heat shock transcription factor-regulated genes in response to lethal heat stress is associated with thermotolerance in tomato cultivars
title_full_unstemmed The ability to induce heat shock transcription factor-regulated genes in response to lethal heat stress is associated with thermotolerance in tomato cultivars
title_short The ability to induce heat shock transcription factor-regulated genes in response to lethal heat stress is associated with thermotolerance in tomato cultivars
title_sort ability to induce heat shock transcription factor-regulated genes in response to lethal heat stress is associated with thermotolerance in tomato cultivars
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10585066/
https://www.ncbi.nlm.nih.gov/pubmed/37868310
http://dx.doi.org/10.3389/fpls.2023.1269964
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