Abstract

Water deficit caused by global climate changes seriously endangers the survival of organisms and crop productivity, and increases environmental deterioration1,2. Plants' resistance to drought involves global reprogramming of transcription, cellular metabolism, hormone signalling and chromatin modification3,​4,​5,​6,​7,​8. However, how these regulatory responses are coordinated via the various pathways, and the underlying mechanisms, are largely unknown. Herein, we report an essential drought-responsive network in which plants trigger a dynamic metabolic flux conversion from glycolysis into acetate synthesis to stimulate the jasmonate (JA) signalling pathway to confer drought tolerance. In Arabidopsis, the ON/OFF switching of this whole network is directly dependent on histone deacetylase HDA6. In addition, exogenous acetic acid promotes de novo JA synthesis and enrichment of histone H4 acetylation, which influences the priming of the JA signalling pathway for plant drought tolerance. This novel acetate function is evolutionarily conserved as a survival strategy against environmental changes in plants. Furthermore, the external application of acetic acid successfully enhanced the drought tolerance in Arabidopsis, rapeseed, maize, rice and wheat plants. Our findings highlight a radically new survival strategy that exploits an epigenetic switch of metabolic flux conversion and hormone signalling by which plants adapt to drought.

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Acknowledgements

We thank C. Pikaard for the hda6 mutant seeds and T. Hirayama for the ein2-5 mutant seeds. This work was supported by RIKEN; the Japan Science and Technology Agency (JST), Core Research for Evolutionary Science and Technology (CREST) (grant no. JPMJCR13B4) to M.S.; and Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology, Japan, (Innovative Areas 23119522 and 25119724 to M.S.; Innovative Areas 24113523 and (C) 24570065 to J.M.K.). JST, PRESTO 15665950 to K.T. A.D. was supported by a Japan Society for the promotion of Science (JSPS) Invitation Fellowship for Research in Japan (L10551) and by a Royal Society International Joint Project (JP091348, to A.D and M.S).

Author information

Author notes

    • Jong-Myong Kim
    •  & Taiko Kim To

    These authors contributed equally to this work.

Affiliations

  1. Plant Genomic Network Research Team, RIKEN Centre for Sustainable Resource Science (CSRS), 1-7-22 Suehiro, Tsurumi, Yokohama 230-0045, Japan

    • Jong-Myong Kim
    • , Akihiro Matsui
    • , Khurram Bashir
    • , Sultana Rasheed
    • , Marina Ando
    • , Junko Ishida
    • , Taeko Morosawa
    • , Maho Tanaka
    • , Chieko Torii
    •  & Motoaki Seki
  2. CREST, Japan Science and Technology Agency, 4-1-8 Honcho, Kawaguchi, Saitama 332-0012, Japan

    • Jong-Myong Kim
    •  & Motoaki Seki
  3. Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan

    • Taiko Kim To
  4. Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1, Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan

    • Keitaro Tanoi
    •  & Natsuko I. Kobayashi
  5. PRESTO, Japan Science and Technology Agency, 4-1-8 Honcho, Kawaguchi, Saitama 332-0012, Japan

    • Keitaro Tanoi
  6. Metabolic Engineering Laboratory, Department of Bioinformatic Engineering, Graduate School of Information Science and Technology, Osaka University, 1-5, Yamadaoka, Suita, Osaka 565-0871, Japan

    • Fumio Matsuda
  7. Metabolomics Research Group, RIKEN CSRS, 1-7-22 Suehiro, Tsurumi, Yokohama 230-0045, Japan

    • Fumio Matsuda
    • , Miyako Kusano
    •  & Kazuki Saito
  8. Plant Physiology Research Unit, Division of Plant and Microbial Sciences, Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, 2-1-2 Kannondai, Tsukuba, Ibaraki 305-8602, Japan

    • Yoshiki Habu
  9. Breeding Strategies Research Unit, Division of Basic Research, Institute of Crop Science, National Agriculture and Food Research Organization, 2-1-2 Kannondai, Tsukuba, Ibaraki 305-8602, Japan

    • Daisuke Ogawa
  10. Department of Applied Biological Science, Graduate School of Science and Technology, Tokyo University of Science, Noda, Chiba 278-8510, Japan

    • Takuya Sakamoto
    •  & Sachihiro Matsunaga
  11. Kihara Institute for Biological Research, Yokohama City University, 641-12 Maioka, Totsuka, Yokohama 244-0813, Japan

    • Marina Ando
    • , Hiroko Takeda
    • , Kanako Kawaura
    • , Yasunari Ogihara
    •  & Motoaki Seki
  12. Graduate School of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8572, Japan

    • Miyako Kusano
  13. Metabolome Informatics Research Team, RIKEN CSRS, 1-7-22 Suehiro, Tsurumi, Yokohama 230-0045, Japan

    • Atsushi Fukushima
  14. Laboratory for Integrative Genomics, RIKEN Centre for Integrative Medical Sciences, 1-7-22 Suehiro, Tsurumi, Yokohama 230-0045, Japan

    • Takaho A. Endo
  15. Gene Discovery Research Group, RIKEN CSRS, 1-7-22 Suehiro, Tsurumi, Yokohama 230-0045, Japan

    • Takashi Kuromori
    •  & Kazuo Shinozaki
  16. Plant Productivity System Research Group, RIKEN CSRS, 1-7-22 Suehiro, Tsurumi, Yokohama 230-0045, Japan

    • Yumiko Takebayashi
    •  & Hitoshi Sakakibara
  17. Graduate School of Pharmaceutical Sciences, Chiba University, 1-8-1 Inohana, Chuo-ku, Chiba 260-8675, Japan

    • Kazuki Saito
  18. School of Biological Sciences, Plant Molecular Sciences, Centre for Systems and Synthetic Biology, Royal Holloway University of London, Egham TW20 0EX, UK

    • Alessandra Devoto

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Contributions

J.M.K., T.K.T., and M.S. conceived the project. J.M.K., and T.K.T. designed the experiments. J.M.K. and T.K.T. carried out all drought stress and growth tests in Arabidopsis. J.M.K. performed the ChIP assay. T.K.T. and J.I. performed the qRT–PCR and RT–PCR expression analyses. J.M.K., K.T. and N.I.K. performed the radioactive incorporation assay. F.M. measured the acetic acid concentration by GC–MS. M.K., A.F. and K.S. carried out the metabolomic analyses. Y.T. and H.S. measured the phytohormone levels. J.I., M.T. and T.M. supported the microarray analyses. A.M. analysed the microarray data. S.M. and T.S. measured the xylem sap pH. J.M.K., D.O. and Y.H. carried out the drought stress test in rice and maize. J.M.K., M.A., H.T., K.K. and Y.O. carried out the drought stress test in wheat and rapeseed. T.A.E carried out data analysis for ChIP-seq. C.T. supported the management of plants and seeds. J.M.K., T.K.T. and A.D. identified the link with JA and conceived the experiments using mutants of the jasmonate signalling pathway genes. J.M.K., M.A., S.R. and K.B. analysed the transgenic plants expressing PDC1 and ALDH2B7. T.K., K.S. and A.D. supplied the pdc1, aldh2b7 and coi1-16B mutant seeds, respectively. J.M.K., T.K.T., A.D. and M.S. wrote, reviewed and edited the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Jong-Myong Kim or Motoaki Seki.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    Supplementary Figures 1–17, Supplementary Table 4 and 8.

Excel files

  1. 1.

    Supplementary Table 1

    Expression profiles of 248 genes whose expressions were higher in hda6 than in wild-type plants under drought stress conditions.

  2. 2.

    Supplementary Table 2

    Expression changes in glycolysis and acetate fermentation pathway genes under drought treatment in wild-type plants and hda6 mutants.

  3. 3.

    Supplementary Table 3

    Drought-induced, highly expressed 357 genes in wild-type Arabidopsis plants pretreated with acetic acid.

  4. 4.

    Supplementary Table 5

    Metabolite profiles of Arabidopsis plants exposed to acetate treatment.

  5. 5.

    Supplementary Table 6

    Expression profiles of 3,914 genes with histone H4 acetylation enriched by acetic acid treatment during acetic acid and drought treatments.

  6. 6.

    Supplementary Table 7

    List of histone modifier gene mutants used in this study.