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


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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

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.


  1. 1

    Sung, D. Y., Kaplan, F., Lee, K. J. & Guy, C. L. Acquired tolerance to temperature extremes. Trends Plant Sci. 8, 179–187 (2003).

    CAS  PubMed  Google Scholar 

  2. 2

    Katori, T. et al. Dissecting the genetic control of natural variation in salt tolerance of Arabidopsis thaliana accessions. J. Exp. Bot. 61, 1125–1138 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  3. 3

    Kim, T. H. et al. Natural variation in small molecule-induced TIR-NB-LRR signaling induces root growth arrest via EDS1- and PAD4-complexed R protein VICTR in Arabidopsis. Plant Cell 24, 5177–5192 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  4. 4

    Weigel, D. Natural variation in Arabidopsis: from molecular genetics to ecological genomics. Plant Physiol. 158, 2–22 (2012).

    CAS  PubMed  Google Scholar 

  5. 5

    Mitchell-Olds, T. & Schmitt, J. Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis. Nature 441, 947–952 (2006).

    CAS  PubMed  Google Scholar 

  6. 6

    Kim, T. H. et al. Chemical genetics reveals negative regulation of abscisic acid signaling by a plant immune response pathway. Curr. Biol. 21, 990–997 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. 7

    Maekawa, T., Kufer, T. A. & Schulze-Lefert, P. NLR functions in plant and animal immune systems: so far and yet so close. Nat. Immunol. 12, 817–826 (2011).

    CAS  PubMed  Google Scholar 

  8. 8

    Shao, Z. Q. et al. Large-scale analyses of angiosperm nucleotide-binding site-leucine-rich repeat genes reveal three anciently diverged classes with distinct evolutionary patterns. Plant Physiol. 170, 2095–2109 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. 9

    Nordborg, M. et al. The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol. 3, e196 (2005).

    PubMed  PubMed Central  Google Scholar 

  10. 10

    Shirano, Y., Kachroo, P., Shah, J. & Klessig, D. F. A gain-of-function mutation in an Arabidopsis Toll Interleukin1 receptor-nucleotide binding site-leucine-rich repeat type R gene triggers defense responses and results in enhanced disease resistance. Plant Cell 14, 3149–3162 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. 11

    Cui, H. et al. A core function of EDS1 with PAD4 is to protect the salicylic acid defense sector in Arabidopsis immunity. New Phytol. 213, 1802–1817 (2017).

    CAS  PubMed  Google Scholar 

  12. 12

    Zhang, Y., Goritschnig, S., Dong, X. & Li, X. A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1-1, constitutive 1. Plant Cell 15, 2636–2646 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. 13

    Yasuda, M. et al. Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. Plant Cell 20, 1678–1692 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. 14

    Alcázar, R. & Parker, J. E. The impact of temperature on balancing immune responsiveness and growth in Arabidopsis. Trends Plant Sci. 16, 666–675 (2011).

    PubMed  Google Scholar 

  15. 15

    Shirasu, K. The HSP90-SGT1 chaperone complex for NLR immune sensors. Annu. Rev. Plant Biol. 60, 139–164 (2009).

    CAS  PubMed  Google Scholar 

  16. 16

    Huang, X., Li, J., Bao, F., Zhang, X. & Yang, S. A gain-of-function mutation in the Arabidopsis disease resistance gene RPP4 confers sensitivity to low temperature. Plant Physiol. 154, 796–809 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. 17

    Yang, H. et al. A mutant CHS3 protein with TIR-NB-LRR-LIM domains modulates growth, cell death and freezing tolerance in a temperature-dependent manner in Arabidopsis. Plant J. 63, 283–296 (2010).

    CAS  PubMed  Google Scholar 

  18. 18

    Léon-Kloosterziel, K. M. et al. Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci. Plant J. 10, 655–661 (1996).

    PubMed  Google Scholar 

  19. 19

    Urano, K. et al. Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics. Plant J. 57, 1065–1078 (2009).

    CAS  PubMed  Google Scholar 

  20. 20

    Leung, J. et al. Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264, 1448–1452 (1994).

    CAS  PubMed  Google Scholar 

  21. 21

    Meyer, K., Leube, M. P. & Grill, E. A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264, 1452–1455 (1994).

    CAS  PubMed  Google Scholar 

  22. 22

    Bostock, R. M., Pye, M. F. & Roubtsova, T. V. Predisposition in plant disease: exploiting the nexus in abiotic and biotic stress perception and response. Annu. Rev. Phytopathol. 52, 517–549 (2014).

    CAS  PubMed  Google Scholar 

  23. 23

    Ahmad, S. et al. Genetic dissection of basal defence responsiveness in accessions of Arabidopsis thaliana. Plant Cell Environ. 34, 1191–1206 (2011).

    CAS  PubMed  Google Scholar 

  24. 24

    Boller, T. & Felix, G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60, 379–406 (2009).

    CAS  PubMed  Google Scholar 

  25. 25

    Vetter, M. M. et al. Flagellin perception varies quantitatively in Arabidopsis thaliana and its relatives. Mol. Biol. Evol. 29, 1655–1667 (2012).

    CAS  PubMed  Google Scholar 

  26. 26

    Jeworutzki, E. et al. Early signaling through the Arabidopsis pattern recognition receptors FLS2 and EFR involves Ca-associated opening of plasma membrane anion channels. Plant J. 62, 367–378 (2010).

    CAS  PubMed  Google Scholar 

  27. 27

    Sun, Y. et al. Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 342, 624–628 (2013).

    CAS  PubMed  Google Scholar 

  28. 28

    Zipfel, C. et al. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428, 764–767 (2004).

    CAS  PubMed  Google Scholar 

  29. 29

    Bartsch, M. et al. Salicylic acid-independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the nudix hydrolase NUDT7. Plant Cell 18, 1038–1051 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. 30

    Reuber, T. L. et al. Correlation of defense gene induction defects with powdery mildew susceptibility in Arabidopsis enhanced disease susceptibility mutants. Plant J. 16, 473–485 (1988).

    Google Scholar 

  31. 31

    Horton, M. W. et al. Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel. Nat. Genet. 44, 212–216 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. 32

    Atwell, S. et al. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465, 627–631 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. 33

    Seren, U. et al. GWAPP: A Web application for genome-wide association mapping in Arabidopsis. Plant Cell 24, 4793–4805 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. 34

    Hellens, R. P., Edwards, E. A., Leyland, N. R., Bean, S. & Mullineaux, P. M. Pgreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 42, 819–832 (2000).

    CAS  PubMed  Google Scholar 

  35. 35

    Jefferson, R. A., Kavanagh, T. A. & Bevan, M. W. GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901–3907 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. 36

    Librado, P. & Rozas, J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452 (2009).

    CAS  PubMed  Google Scholar 

  37. 37

    Tamura, K. et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. 38

    Darling, A. E., Mau, B. & Perna, N. T. Progressivemauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 5, e11147 (2010).

    PubMed  PubMed Central  Google Scholar 

  39. 39

    Kojima, M. & Sakakibara, H. Highly sensitive high-throughput profiling of six phytohormones using MS-probe modification and liquid chromatography-tandem mass spectrometry. Methods Mol. Biol. 918, 151–164 (2012).

    CAS  PubMed  Google Scholar 

  40. 40

    Lu, X. et al. Uncoupling of sustained MAMP receptor signaling from early outputs in an Arabidopsis endoplasmic reticulum glucosidase II allele. Proc. Natl Acad. Sci. USA 106, 22522–7 (2009).

    CAS  PubMed  Google Scholar 

  41. 41

    Yamada, K., Saijo, Y., Nakagami, H. & Takano, Y. Regulation of sugar transporter activity for antibacterial defense in Arabidopsis. Science 354, 1427–1430 (2016).

    CAS  PubMed  Google Scholar 

  42. 42

    Cao, H., Bowling, S. A., Gordon, A. S. & Dong, X. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6, 1583–1592 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. 43

    Wildermuth, M. C., Dewdney, J., Wu, G. & Ausubel, F. M. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414, 562–565 (2001).

    CAS  PubMed  Google Scholar 

  44. 44

    Rogers, E. E. & Ausubel, F. M. Arabidopsis enhanced disease susceptibility mutants exhibit enhanced susceptibility to several bacterial pathogens and alterations in PR-1 gene expression. Plant Cell 9, 305–316 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references


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




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.

Corresponding author

Correspondence to Teruaki Taji.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

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

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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).

Download citation

Further reading


Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing