Letter

NLR locus-mediated trade-off between abiotic and biotic stress adaptation in Arabidopsis

  • Nature Plants 3, Article number: 17072 (2017)
  • doi:10.1038/nplants.2017.72
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Abstract

Osmotic stress caused by drought, salt or cold decreases plant fitness. Acquired stress tolerance defines the ability of plants to withstand stress following an initial exposure1. We found previously that acquired osmotolerance after salt stress is widespread among Arabidopsis thaliana accessions2. Here, we identify ACQOS as the locus responsible for ACQUIRED OSMOTOLERANCE. Of its five haplotypes, only plants carrying group 1 ACQOS are impaired in acquired osmotolerance. ACQOS is identical to VICTR, encoding a nucleotide-binding leucine-rich repeat (NLR) protein3. In the absence of osmotic stress, group 1 ACQOS contributes to bacterial resistance. In its presence, ACQOS causes detrimental autoimmunity, thereby reducing osmotolerance. Analysis of natural variation at the ACQOS locus suggests that functional and non-functional ACQOS alleles are being maintained due to a trade-off between biotic and abiotic stress adaptation. Thus, polymorphism in certain plant NLR genes might be influenced by competing environmental stresses.

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Acknowledgements

We thank M. von Reth of the Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, for technical assistance. We gratefully acknowledge K. Urano of RIKEN CSRS for providing seed. The Arabidopsis accessions used in this study are maintained and provided by the RIKEN BRC through the National Bio-Resource Project of the MEXT, Japan. This work was supported by JSPS KAKENHI grant numbers JP25119722 (to T. Taji), JP15K07845 (to T. Taji), JP14J07115 (to H.A.), JP26291062 and 16H01469 (to Y. Saijo), Strategic Young Researcher Overseas Visits Program for Accelerating Brain Circulation of JSPS (no. S2306 to T. Taji), JST PRESTO (JPMJPR13B6 to Y. Saijo) and a Deutsche Forschungsgemeinschaft CRC 680 grant (to J.E.P and R.A.).

Author information

Author notes

    • Hirotaka Ariga
    • , Owen Hoekenga
    • , Alexander E. Lipka
    • , Michael A. Gore
    •  & Yuriko Kobayashi

    Present addresses: Division of Plant Sciences, Institute of Agrobiological Science, NARO, Ibaraki 305-8602, Japan (H.A.); Cayuga Genetics Consulting Group LLC, Ithaca, New York 14850, USA (O.H.); Department of Crop Sciences, University of Illinois, Urbana, Illinois 61801, USA (A.E.L); Plant Breeding and Genetics Section, School of Integrative Plant Science, Cornell University, Ithaca, New York 14853, USA (M.A.G.); Faculty of Applied Biological Sciences, Gifu University, Gifu 501-1193, Japan (Y.K.)

    • Taku Katori
    • , Takashi Tsuchimatsu
    •  & Taishi Hirase

    These authors contributed equally to this work.

Affiliations

  1. Department of Bioscience, Tokyo University of Agriculture, Tokyo 156-8502, Japan

    • Hirotaka Ariga
    • , Taku Katori
    • , Yoichi Sakata
    • , Takahisa Hayashi
    •  & Teruaki Taji
  2. Department of Biology, Chiba University, Chiba 263-8522, Japan

    • Takashi Tsuchimatsu
  3. Graduate School of Biological Sciences, Nara Institute for Science and Technology, Ikoma 630-0192, Japan

    • Taishi Hirase
    • , Yuri Tajima
    •  & Yusuke Saijo
  4. Department of Plant-Microbe Interactions, Max-Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany

    • Jane E. Parker
  5. Department of Plant Biology, University of Barcelona, 08028 Barcelona, Spain

    • Rubén Alcázar
  6. Department of Plant Breeding and Genetics, Max-Planck Institute for Plant Breeding Research D-50829 Cologne, Germany

    • Maarten Koornneef
  7. United States Department of Agriculture, Agricultural Research Service (USDA-ARS), Ithaca, 14853 New York, USA

    • Owen Hoekenga
    •  & Alexander E. Lipka
  8. United States Department of Agriculture, Agricultural Research Service (USDA-ARS), Maricopa, Arizona 85138, USA

    • Michael A. Gore
  9. Plant Productivity Systems Research Group, RIKEN Centre for Sustainable Resource Science, Kanagawa 230-0045, Japan

    • Hitoshi Sakakibara
    •  & Mikiko Kojima
  10. RIKEN BioResource Center, Ibaraki, 305-0074 Japan

    • Yuriko Kobayashi
    • , Satoshi Iuchi
    •  & Masatomo Kobayashi
  11. Gene Discovery Research Group, RIKEN Center for Sustainable Resource Science, Kanagawa 230-0045, Japan

    • Kazuo Shinozaki
  12. JST PRESTO, Ikoma 630-0192, Japan

    • Yusuke Saijo

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Contributions

H.A. and T. Taji initiated, conceived and coordinated the project; H.A., identified ACQOS locus and characterized plants altered with the ACQOS locus; T.K., generated NIL plants; T. Tsuchimatsu performed population genetic analyses; T. Tsuchimatsu, O.H., A.E.L., Y. Kobayashi and M.A.G. performed GWAS; T. Hirase, Y.T. and Y. Saijo designed and performed defence-related assays; H.S. and M.K. determined SA and ABA contents; S.I. and M.K. provided A. thaliana accession seeds and their markers; J.E.P., R.A., M.K., K.S., T. Hayashi, Y. Sakata and Y. Saijo supervised the project; T. Taji and Y. Saijo wrote the manuscript with assistance from T. Tsuchimatsu, J.E.P., R.A., M.K., K.S. and Y. Sakata.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Teruaki Taji.

Supplementary information

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    Supplementary Information

    Supplementary Figures 1–17, Supplementary Tables 1–6.