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Ethanol induces heat tolerance in plants by stimulating unfolded protein response

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Ethanol priming induces heat stress tolerance by the stimulation of unfolded protein response.

Abstract

Global warming increases the risk of heat stress-related yield losses in agricultural crops. Chemical priming, using safe agents, that can flexibly activate adaptive regulatory responses to adverse conditions, is a complementary approach to genetic improvement for stress adaptation. In the present study, we demonstrated that pretreatment of Arabidopsis with a low concentration of ethanol enhances heat tolerance without suppressing plant growth. We also demonstrated that ethanol pretreatment improved leaf growth in lettuce (Lactuca sativa L.) plants grown in the field conditions under high temperatures. Transcriptome analysis revealed a set of genes that were up-regulated in ethanol-pretreated plants, relative to water-pretreated controls. Binding Protein 3 (BIP3), an endoplasmic reticulum (ER)-stress marker chaperone gene, was among the identified up-regulated genes. The expression levels of BIP3 were confirmed by RT-qPCR. Root-uptake of ethanol was metabolized to organic acids, nucleic acids, amines and other molecules, followed by an increase in putrescine content, which substantially promoted unfolded protein response (UPR) signaling and high-temperature acclimation. We also showed that inhibition of polyamine production and UPR signaling negated the heat stress tolerance induced by ethanol pretreatment. These findings collectively indicate that ethanol priming activates UPR signaling via putrescine accumulation, leading to enhanced heat stress tolerance. The information gained from this study will be useful for establishing ethanol-mediated chemical priming strategies that can be used to help maintain crop production under heat stress conditions.

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Acknowledgements

The method of Arabidopsis cultivation in MS liquid medium was advised by Dr. Takatoshi Kiba at Nagoya University. We thank Imato Takeuchi from Kihara Institute for Biological Research, Yokohama City University for the technical assistance of field experiments. We also thank Prof. Nozomu Koizumi at Osaka Prefecture University, for providing the mutant seeds (SALK_050203). We thank Journal Doctors (http://www.journaldoctors.com/about.html) for editing a draft of this manuscript.

Funding

This work was supported by grants from RIKEN, Japan (to MS), such as RIKEN–AIST Joint Research Fund (Full research), Core Research for Evolutionary Science and Technology (JPMJCR13B4 to MS) and A-STEP (JPMJTM19BS to MS) of the Japan Science and Technology Agency (JST), and Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan (Innovative Areas 18H04791 and 18H04705 to MS).

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Contributions

The heat stress experiments of ethanol-treated plants and transcriptome analysis were performed by AM, YS, KM, ST, MT, KK, JI and MS. NMR analysis was performed by KB, YT and JK. GC/MS analysis was performed by KB, MK and MK. The manuscript was written by AM, DT and MS. The total experiments of this study were designed by AM and MS.

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Correspondence to Motoaki Seki.

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The authors have not disclosed any competing interest.

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Matsui, A., Todaka, D., Tanaka, M. et al. Ethanol induces heat tolerance in plants by stimulating unfolded protein response. Plant Mol Biol 110, 131–145 (2022). https://doi.org/10.1007/s11103-022-01291-8

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  • DOI: https://doi.org/10.1007/s11103-022-01291-8

Keywords

  • Chemical priming
  • Ethanol
  • Heat stress tolerance
  • Polyamine
  • Unfolded protein response