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

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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Figure 1: Identification of the ACQOS locus.
Figure 2: Haplotype diversity and functional evolution of the ACQOS locus.
Figure 3: Contribution of ACQOS to immune responses and pathogen resistance after MAMP treatment.

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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.).

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Authors and Affiliations

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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.

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Correspondence to Teruaki Taji.

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The authors declare no competing financial interests.

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Supplementary Figures 1–17, Supplementary Tables 1–6. (PDF 52481 kb)

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Ariga, H., Katori, T., Tsuchimatsu, T. et al. NLR locus-mediated trade-off between abiotic and biotic stress adaptation in Arabidopsis. Nature Plants 3, 17072 (2017). https://doi.org/10.1038/nplants.2017.72

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