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

Junya Mizoi; Daisuke Todaka; Tomohiro Imatomi; Satoshi Kidokoro; Tetsuya Sakurai; Ken-Suke Kodaira; Hidehito Takayama; Kazuo Shinozaki; Kazuko Yamaguchi-Shinozaki

doi:10.3389/fpls.2023.1269964

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

Front Plant Sci. 2023 Oct 5:14:1269964. doi: 10.3389/fpls.2023.1269964. eCollection 2023.

Authors

Affiliations

¹ Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan.
² RIKEN Center for Sustainable Resource Science, Yokohama, Japan.
³ Interdisciplinary Science Unit, Multidisciplinary Science Cluster, Research and Education Faculty, Kochi University, Nankoku, Japan.
⁴ The KAITEKI Institute, Inc., Tokyo, Japan.
⁵ Gene Discovery Research Group, RIKEN Center for Sustainable Resource Science, Tsukuba, Japan.
⁶ Institute for Advanced Research, Nagoya University, Nagoya, Japan.
⁷ Research Institute for Agricultural and Life Sciences, Tokyo University of Agriculture, Tokyo, Japan.

Abstract

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.

Keywords: Solanum lycopersicum; cultivars; expression biomarker; heat shock response; heat stress; thermotolerance; transcriptome.

Grants and funding

The authors declare financial support was received for the research, authorship, and/or publication of this article. This work was conducted with financial support from JSPS KAKENHI Grant Number 20K06700 (to JM), and Funding from Nagoya University, Institute for Advanced Research (to KS).