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Acetate-mediated novel survival strategy against drought in plants

An Erratum to this article was published on 17 July 2017

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 modification38. 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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Figure 1: HDA6 correlates with the activation of the acetate biosynthetic pathway, which is essential for plant drought tolerance.
Figure 2: HDA6 directly regulates acetate biosynthetic pathway genes, PDC1 and ALDH2B7.
Figure 3: Acetic acid promotes jasmonate signalling and histone acetylation.
Figure 4: Proposed mechanism for acetic acid-induced drought tolerance and its evolutionary conservation.

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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

Authors and Affiliations

Authors

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.

Corresponding authors

Correspondence to Jong-Myong Kim or Motoaki Seki.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Figures 1–17, Supplementary Table 4 and 8. (PDF 20829 kb)

Supplementary Table 1

Expression profiles of 248 genes whose expressions were higher in hda6 than in wild-type plants under drought stress conditions. (XLS 171 kb)

Supplementary Table 2

Expression changes in glycolysis and acetate fermentation pathway genes under drought treatment in wild-type plants and hda6 mutants. (XLSX 27 kb)

Supplementary Table 3

Drought-induced, highly expressed 357 genes in wild-type Arabidopsis plants pretreated with acetic acid. (XLS 189 kb)

Supplementary Table 5

Metabolite profiles of Arabidopsis plants exposed to acetate treatment. (XLSX 21 kb)

Supplementary Table 6

Expression profiles of 3,914 genes with histone H4 acetylation enriched by acetic acid treatment during acetic acid and drought treatments. (XLSX 3209 kb)

Supplementary Table 7

List of histone modifier gene mutants used in this study. (XLSX 12 kb)

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Kim, JM., To, T., Matsui, A. et al. Acetate-mediated novel survival strategy against drought in plants. Nature Plants 3, 17097 (2017). https://doi.org/10.1038/nplants.2017.97

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