Ethanol-Mediated Novel Survival Strategy against Drought Stress in Plants

Author:

Bashir Khurram12ORCID,Todaka Daisuke1,Rasheed Sultana1,Matsui Akihiro13,Ahmad Zarnab12,Sako Kaori14ORCID,Utsumi Yoshinori1ORCID,Vu Anh Thu1,Tanaka Maho13ORCID,Takahashi Satoshi13,Ishida Junko13,Tsuboi Yuuri5,Watanabe Shunsuke67ORCID,Kanno Yuri6,Ando Eigo89ORCID,Shin Kwang-Chul8,Seito Makoto10,Motegi Hinata110,Sato Muneo1112,Li Rui12,Kikuchi Saya13,Fujita Miki1113,Kusano Miyako1415,Kobayashi Makoto14,Habu Yoshiki1516,Nagano Atsushi J1718ORCID,Kawaura Kanako10,Kikuchi Jun51920ORCID,Saito Kazuki14,Hirai Masami Yokota112012ORCID,Seo Mitsunori6,Shinozaki Kazuo13,Kinoshita Toshinori821ORCID,Seki Motoaki1310ORCID

Affiliation:

1. Plant Genomic Network Research Team, RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho , Tsurumi-ku, Yokohama, Kanagawa, 230-0045 Japan

2. Department of Life Sciences, SBA School of Science and Engineering, Lahore University of Management Sciences , DHA Phase 5, Lahore 54792, Pakistan

3. Plant Epigenome Regulation Laboratory, RIKEN Cluster for Pioneering Research , 2-1 Hirosawa, Wako, Saitama, 351-0198 Japan

4. Department of Advanced Bioscience, Faculty of Agriculture, Kindai University, 3327-204 Nakamachi , Nara, 631-8505, Japan

5. Environmental Metabolic Analysis Research Team, RIKEN Center for Sustainable Resource Science , 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa, 230-0045 Japan

6. Dormancy and Adaptation Research Unit, RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi-ku , Yokohama, Kanagawa, 230-0045, Japan

7. IPSiM, University of Montpellier, CNRS, INRAE , Institut Agro, Montpellier 34060, France

8. Division of Biological Sciences, Graduate School of Science, Nagoya University , Chikusa, Nagoya, 464-8602 Japan

9. Department of Biological Sciences, School of Science, The University of Tokyo, 7-3-1 Hongo , Bunkyo-ku, Tokyo, 113-0033, Japan

10. Kihara Institute for Biological Research, Yokohama City University , 641-12 Maiokacho, Totsuka Ward, Yokohama, Kanagawa, 244-0813 Japan

11. Mass Spectrometry and Microscopy Unit, RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi-ku , Yokohama, Kanagawa, 230-0045 Japan

12. Metabolic Systems Research Team, RIKEN Center for Sustainable Resource Science , 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa, 230-0045 Japan

13. Gene Discovery Research Group, RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho , Tsurumi-ku, Yokohama, Kanagawa, 230-0045 Japan

14. Metabolomics Research Group, RIKEN Center for Sustainable Resource Science , 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045 Japan

15. Graduate School of Life and Environmental Science, University of Tsukuba , 1-1-1 Tennodai, Tsukuba, Ibaraki, 305-8572 Japan

16. Institute of Agrobiological Sciences, National Agriculture and Food Research Organization , 2-1-2 Kannondai, Tsukuba, Ibaraki, 305-8602 Japan

17. Faculty of Agriculture, Ryukoku University, Yokotani 1-5, Seta Oe-cho , Otsu, Shiga, 520-2914, Japan

18. Institute for Advanced Biosciences, Keio University , Tsuruoka, Yamagata, 997-0017 Japan

19. Graduate School of Medical Life Science, Yokohama City University, 1-7-22 Suehiro-cho, Tsurumi-ku , Yokohama, Kanagawa, 230-0045 Japan

20. Department of Applied Biosciences, Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya , Aichi, 464-8601 Japan

21. Institute of Transformative Bio-Molecules (WPI-ITbM) , Nagoya University, Chikusa, Nagoya, Aichi, 464-8601 Japan

Abstract

Abstract Water scarcity is a serious agricultural problem causing significant losses to crop yield and product quality. The development of technologies to mitigate the damage caused by drought stress is essential for ensuring a sustainable food supply for the increasing global population. We herein report that the exogenous application of ethanol, an inexpensive and environmentally friendly chemical, significantly enhances drought tolerance in Arabidopsis thaliana, rice and wheat. The transcriptomic analyses of ethanol-treated plants revealed the upregulation of genes related to sucrose and starch metabolism, phenylpropanoids and glucosinolate biosynthesis, while metabolomic analysis showed an increased accumulation of sugars, glucosinolates and drought-tolerance-related amino acids. The phenotyping analysis indicated that drought-induced water loss was delayed in the ethanol-treated plants. Furthermore, ethanol treatment induced stomatal closure, resulting in decreased transpiration rate and increased leaf water contents under drought stress conditions. The ethanol treatment did not enhance drought tolerance in the mutant of ABI1, a negative regulator of abscisic acid (ABA) signaling in Arabidopsis, indicating that ABA signaling contributes to ethanol-mediated drought tolerance. The nuclear magnetic resonance analysis using 13C-labeled ethanol indicated that gluconeogenesis is involved in the accumulation of sugars. The ethanol treatment did not enhance the drought tolerance in the aldehyde dehydrogenase (aldh) triple mutant (aldh2b4/aldh2b7/aldh2c4). These results show that ABA signaling and acetic acid biosynthesis are involved in ethanol-mediated drought tolerance and that chemical priming through ethanol application regulates sugar accumulation and gluconeogenesis, leading to enhanced drought tolerance and sustained plant growth. These findings highlight a new survival strategy for increasing crop production under water-limited conditions.

Funder

Core Research for Evolutional Science and Technology

RIKEN-AIST Joint Research Fund

Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology

A-STEP, JST

Publisher

Oxford University Press (OUP)

Subject

Cell Biology,Plant Science,Physiology,General Medicine

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