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Is localized acquired resistance the mechanism for effector-triggered disease resistance in plants?

Abstract

Plant nucleotide-binding leucine-rich repeat receptors (NLRs) are intracellular immune receptors that are activated by their direct or indirect interactions with virulence effectors. NLR activation triggers a strong immune response and consequent disease resistance. However, the NLR-driven immune response can be targeted by virulence effectors. It is thus unclear how immune activation can occur concomitantly with virulence effector suppression of immunity. Recent observations suggest that the activation of effector-triggered immunity does not sustain defence gene expression in tissues in contact with the hemi-biotrophic pathogen Pseudomonas syringae pv. tomato. Instead, strong defence was observed on the border of the infection area. This response is reminiscent of localized acquired resistance (LAR). LAR is a strong defence response occurring in a ~2 mm area around cells in contact with the pathogen and probably serves to prevent the spread of pathogens. Here we propose that effector-triggered immunity is essentially a quarantining mechanism to prevent systemic pathogen spread and disease, and that the induction of LAR is a key component of this mechanism.

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Fig. 1: ETI does not restore defence gene expression that has been suppressed by virulence effectors.
Fig. 2: ETI does not inhibit pathogen growth locally but limits pathogen propagation.
Fig. 3: Does ETI induce LAR to prevent systemic pathogen spread?.

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References

  1. Jones, J. D. G., Vance, R. E. & Dangl, J. L. Intracellular innate immune surveillance devices in plants and animals. Science 354, aaf6395 (2016).

    Article  PubMed  Google Scholar 

  2. Jones, J. D. G. & Dangl, J. L. The plant immune system. Nature 444, 323–329 (2006).

    Article  CAS  PubMed  Google Scholar 

  3. Laflamme, B. et al. The pan-genome effector-triggered immunity landscape of a host–pathogen interaction. Science 367, 763–768 (2020).

    Article  CAS  PubMed  Google Scholar 

  4. Van de Weyer, A. L. et al. A species-wide inventory of NLR genes and alleles in Arabidopsis thaliana. Cell 178, 1260–1272.e14 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  5. Huang, S. et al. Identification and receptor mechanism of TIR-catalyzed small molecules in plant immunity. Science 377, eabq3297 (2022).

    Article  CAS  PubMed  Google Scholar 

  6. Wan, L. et al. TIR domains of plant immune receptors are NAD+-cleaving enzymes that promote cell death. Science 365, 799–803 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Yu, D. et al. TIR domains of plant immune receptors are 2′,3′-cAMP/cGMP synthetases mediating cell death. Cell 185, 2370–2386.e18 (2022).

    Article  CAS  PubMed  Google Scholar 

  8. Essuman, K., Milbrandt, J., Dangl, J. L. & Nishimura, M. T. Shared TIR enzymatic functions regulate cell death and immunity across the tree of life. Science 377, eabo0001 (2022).

    Article  CAS  PubMed  Google Scholar 

  9. Jia, A. et al. TIR-catalyzed ADP-ribosylation reactions produce signaling molecules for plant immunity. Science 377, eabq8180 (2022).

    Article  CAS  PubMed  Google Scholar 

  10. Jacob, P. et al. Plant ‘helper’ immune receptors are Ca2+-permeable nonselective cation channels. Science 373, 420–425 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Bi, G. et al. The ZAR1 resistosome is a calcium-permeable channel triggering plant immune signaling. Cell 184, 3528–3541.e12 (2021).

    Article  CAS  PubMed  Google Scholar 

  12. Förderer, A. et al. A wheat resistosome defines common principles of immune receptor channels. Nature 610, 532–539 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Köster, P., DeFalco, T. A. & Zipfel, C. Ca2+ signals in plant immunity. EMBO J. 41, e110741 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Jacob, P. et al. Broader functions of TIR domains in Arabidopsis immunity. Proc. Natl Acad. Sci. USA 120, e2220921120 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Tian, H. et al. Activation of TIR signalling boosts pattern-triggered immunity. Nature 598, 500–503 (2021).

    Article  CAS  PubMed  Google Scholar 

  16. Ngou, B. P. M., Ahn, H. K., Ding, P. & Jones, J. D. G. Mutual potentiation of plant immunity by cell-surface and intracellular receptors. Nature 592, 110–115 (2021).

    Article  CAS  PubMed  Google Scholar 

  17. Yuan, M. et al. Pattern-recognition receptors are required for NLR-mediated plant immunity. Nature 592, 105–109 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Pruitt, R. N. et al. The EDS1–PAD4–ADR1 node mediates Arabidopsis pattern-triggered immunity. Nature https://doi.org/10.1038/s41586-021-03829-0 (2021).

  19. Tena, G. PTI and ETI are one. Nat. Plants 7, 1527 (2021).

    Article  PubMed  Google Scholar 

  20. Wei, H. L., Zhang, W. & Collmer, A. Modular study of the type III effector repertoire in Pseudomonas syringae pv. tomato DC3000 reveals a matrix of effector interplay in pathogenesis. Cell Rep. 23, 1630–1638 (2018).

    Article  CAS  PubMed  Google Scholar 

  21. Guo, M., Tian, F., Wamboldt, Y. & Alfano, J. R. The majority of the type III effector inventory of Pseudomonas syringae pv. tomato DC3000 can suppress plant immunity. Mol. Plant. Microbe Interact. 22, 1069–1080 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Ruiz-Bedoya, T., Wang, P. W., Desveaux, D. & Guttman, D. S. Cooperative virulence via the collective action of secreted pathogen effectors. Nat. Microbiol. 8, 640–650 (2023).

    Article  CAS  PubMed  Google Scholar 

  23. Ross, A. F. Localized acquired resistance to plant virus infection in hypersensitive hosts. Virology 14, 329–339 (1961).

    Article  CAS  PubMed  Google Scholar 

  24. Bomblies, K. et al. Autoimmune response as a mechanism for a Dobzhansky–Muller-type incompatibility syndrome in plants. PLoS Biol. 5, e236 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  25. Calvo-Baltanás, V., Wang, J. & Chae, E. Hybrid incompatibility of the plant immune system: an opposite force to heterosis equilibrating hybrid performances. Front. Plant Sci. 11, 2308 (2021).

    Article  Google Scholar 

  26. Saile, S. C. et al. Two unequally redundant ‘helper’ immune receptor families mediate Arabidopsis thaliana intracellular ‘sensor’ immune receptor functions. PLoS Biol. 18, e3000783 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  28. Kim, N. H., Jacob, P. & Dangl, J. L. Con-Ca2+-tenating plant immune responses via calcium-permeable cation channels. N. Phytol. 234, 813–818 (2022).

    Article  CAS  Google Scholar 

  29. Mcdowell, J. M. et al. Downy mildew (Peronospora parasitica) resistance genes in Arabidopsis vary in functional requirements for NDR1, EDS1, NPR1 and salicylic acid accumulation. Plant J. 22, 523–529 (2000).

    Article  CAS  PubMed  Google Scholar 

  30. Lapin, D. et al. A coevolved EDS1–SAG101–NRG1 module mediates cell death signaling by TIR-domain immune receptors. Plant Cell 31, 2430 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Castel, B. et al. Diverse NLR immune receptors activate defence via the RPW8–NLR NRG1. N. Phytol. 222, 966–980 (2019).

    Article  CAS  Google Scholar 

  32. Wu, Z. et al. Differential regulation of TNL-mediated immune signaling by redundant helper CNLs. N. Phytol. 222, 938–953 (2019).

    Article  CAS  Google Scholar 

  33. Rufián, J. S. et al. Confocal microscopy reveals in planta dynamic interactions between pathogenic, avirulent and non‐pathogenic Pseudomonas syringae strains. Mol. Plant Pathol. 19, 537–551 (2018).

    Article  PubMed  Google Scholar 

  34. Alvarez, M. E. et al. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92, 773–784 (1998).

    Article  CAS  PubMed  Google Scholar 

  35. Costet, L. et al. Relationship between localized acquired resistance (LAR) and the hypersensitive response (HR): HR is necessary for LAR to occur and salicylic acid is not sufficient to trigger LAR. Mol. Plant Microbe Interact. 12, 655–662 (1999).

    Article  CAS  Google Scholar 

  36. Dorey, S. et al. Spatial and temporal induction of cell death, defense genes, and accumulation of salicylic acid in tobacco leaves reacting hypersensitively to a fungal glycoprotein elicitor. Mol. Plant Microbe Interact. 10, 646–655 (1997).

    Article  CAS  Google Scholar 

  37. Ross, A. F. Systemic acquired resistance induced by localized virus infections in plants. Virology 14, 340–358 (1961).

    Article  CAS  PubMed  Google Scholar 

  38. Betsuyaku, S. et al. Salicylic acid and jasmonic acid pathways are activated in spatially different domains around the infection site during effector-triggered immunity in Arabidopsis thaliana. Plant Cell Physiol. 59, 8–16 (2018).

    Article  CAS  PubMed  Google Scholar 

  39. Ghareeb, H. et al. Quantitative hormone signaling output analyses of Arabidopsis thaliana interactions with virulent and avirulent Hyaloperonospora arabidopsidis isolates at single-cell resolution. Front. Plant Sci. 11, 1737 (2020).

    Article  Google Scholar 

  40. Samac’, D. A. & Shah, D. M. Developmental and pathogen-induced activation of the Arabidopsis acidic chitinase promoter. Plant Cell 3, 1063–1072 (1991).

    Article  PubMed  Google Scholar 

  41. Roberts, M., Tang, S., Stallmann, A., Dangl, J. L. & Bonardi, V. Genetic requirements for signaling from an autoactive plant NB-LRR intracellular innate immune receptor. PLoS Genet. 9, e1003465 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Bonardi, V. et al. Expanded functions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors. Proc. Natl Acad. Sci. USA 108, 16463–16468 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Jabs, T., Dietrich, R. A. & Dangl, J. L. Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273, 1853–1856 (1996).

    Article  CAS  PubMed  Google Scholar 

  44. Hander, T. et al. Damage on plants activates Ca2+-dependent metacaspases for release of immunomodulatory peptides. Science 363, eaar7486 (2019).

    Article  CAS  PubMed  Google Scholar 

  45. Zhu, J. et al. Single-cell profiling of Arabidopsis leaves to Pseudomonas syringae infection. Cell Rep. 42, 112676 (2023).

    Article  CAS  PubMed  Google Scholar 

  46. Salguero-Linares, J. et al. Robust transcriptional indicators of immune cell death revealed by spatiotemporal transcriptome analyses. Mol. Plant 15, 1059–1075 (2022).

    Article  CAS  PubMed  Google Scholar 

  47. Delannoy, E. et al. Cell specialization and coordination in Arabidopsis leaves upon pathogenic attack revealed by scRNA-seq. Preprint at bioRxiv https://doi.org/10.1101/2023.03.02.530814 (2023).

  48. Liu, X. et al. Dynamic decomposition of transcriptome responses during plant effector-triggered immunity revealed conserved responses in two distinct cell populations. Preprint at bioRxiv https://doi.org/10.1101/2022.12.30.522333 (2022).

  49. Nobori, T. et al. Time-resolved single-cell and spatial gene regulatory atlas of plants under pathogen attack. Preprint at bioRxiv https://doi.org/10.1101/2023.04.10.536170 (2023).

  50. Misas-Villamil, J. C., Kolodziejek, I. & Van Der Hoorn, R. A. L. Pseudomonas syringae colonizes distant tissues in Nicotiana benthamiana through xylem vessels. Plant J. 67, 774–782 (2011).

    Article  CAS  PubMed  Google Scholar 

  51. Liu, Y., Schiff, M., Marathe, R. & Dinesh-Kumar, S. P. Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. Plant J. 30, 415–429 (2002).

    Article  CAS  PubMed  Google Scholar 

  52. Lepiniec, L. et al. Genetics and biochemistry of seed flavonoids. Annu. Rev. Plant Biol. 57, 405–430 (2006).

    Article  CAS  PubMed  Google Scholar 

  53. Wright, K. M. et al. Analysis of the N gene hypersensitive response induced by a fluorescently tagged tobacco mosaic virus. Plant Physiol. 123, 1375 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Baebler, Š. et al. Salicylic acid is an indispensable component of the Ny-1 resistance-gene-mediated response against potato virus Y infection in potato. J. Exp. Bot. 65, 1095–1109 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Chandra-Shekara, A. C. et al. Signaling requirements and role of salicylic acid in HRT- and rrt-mediated resistance to turnip crinkle virus in Arabidopsis. Plant J. 40, 647–659 (2004).

    Article  CAS  PubMed  Google Scholar 

  56. Sánchez, G. et al. Salicylic acid is involved in the Nb-mediated defense responses to potato virus X in Solanum tuberosum. Mol. Plant. Microbe Interact. 23, 394–405 (2010).

    Article  PubMed  Google Scholar 

  57. Torres, M. A., Jones, J. D. G. & Dangl, J. L. Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat. Genet. 37, 1130–1134 (2005).

    Article  CAS  PubMed  Google Scholar 

  58. Torres, M. A., Dangl, J. L. & Jones, J. D. G. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl Acad. Sci. USA 99, 517–522 (2002).

    Article  CAS  PubMed  Google Scholar 

  59. Torres, M. A., Jones, J. D. G. & Dangl, J. L. Reactive oxygen species signaling in response to pathogens. Plant Physiol. 141, 373–378 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Miller, G. et al. The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal. 2, ra45 (2009).

    Article  PubMed  Google Scholar 

  61. Bendahmane, A., Kanyuka, K. & Baulcombe, D. C. The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell 11, 781–791 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Gross, P., Julius, C., Schmelzer, E. & Hahlbrock, K. Translocation of cytoplasm and nucleus to fungal penetration sites is associated with depolymerization of microtubules and defence gene activation in infected, cultured parsley cells. EMBO J. 12, 1735–1744 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Li, L. & Weigel, D. One hundred years of hybrid necrosis: hybrid autoimmunity as a window into the mechanisms and evolution of plant–pathogen interactions. Annu. Rev. Phytopathol. 59, 213–237 (2021).

    Article  CAS  PubMed  Google Scholar 

  64. Barragan, A. C. et al. A truncated singleton NLR causes hybrid necrosis in Arabidopsis thaliana. Mol. Biol. Evol. 38, 557–574 (2021).

    Article  CAS  PubMed  Google Scholar 

  65. Cheng, Y. T. et al. Stability of plant immune-receptor resistance proteins is controlled by SKP1-CULLIN1-F-box (SCF)-mediated protein degradation. Proc. Natl Acad. Sci. USA 108, 14694–14699 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Zavaliev, R., Mohan, R., Chen, T. & Dong, X. Formation of NPR1 condensates promotes cell survival during the plant immune response. Cell 182, 1093–1108.e18 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank T. Nobori, J. G. Ellis, G. L. Coaker and T. Nuernberger for constructive critical reading of the manuscript and members of the Dangl lab for useful discussions. This research was supported by the National Science Foundation (grant no. IOS-1758400 to J.L.D.) and the Howard Hughes Medical Institute (HHMI). J.L.D. is an HHMI Investigator. This article is subject to HHMI’s Open Access to Publications policy. HHMI lab heads have previously granted a non-exclusive CC BY 4.0 licence to the public and a sublicensable licence to HHMI in their research articles. Pursuant to those licences, the author-accepted manuscript of this article can be made freely available under a CC BY4.0 licence immediately upon publication.

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P.J. conceptualized the project, wrote the original draft, reviewed and edited the manuscript, and conducted the formal analysis. J.H. conducted the investigation. J.L.D. conceptualized the project, reviewed and edited the manuscript, acquired the funding and supervised the project.

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Correspondence to Jeffery L. Dangl.

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Jacob, P., Hige, J. & Dangl, J.L. Is localized acquired resistance the mechanism for effector-triggered disease resistance in plants?. Nat. Plants 9, 1184–1190 (2023). https://doi.org/10.1038/s41477-023-01466-1

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