Is localized acquired resistance the mechanism for effector

Nature Plants (2023)Cite this article

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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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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

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

Article CAS PubMed Google Scholar

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

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

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

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

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

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

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

Article CAS PubMed Google Scholar

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

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

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

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

Article PubMed PubMed Central Google Scholar

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

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

Article CAS PubMed Google Scholar

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

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

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).

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

Article PubMed Google Scholar

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

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

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

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

Article CAS PubMed Google Scholar

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

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

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

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

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

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

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

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

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

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

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

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

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

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

Article CAS PubMed Google Scholar

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

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

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

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

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

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

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

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

Article CAS PubMed Google Scholar

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

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).

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).

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).

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

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

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

Article CAS PubMed Google Scholar

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

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

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

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

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

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

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

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

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

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

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

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

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

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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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.

Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA

Pierre Jacob, Junko Hige & Jeffery L. Dangl

Howard Hughes Medical Institute, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA

Pierre Jacob, Junko Hige & Jeffery L. Dangl

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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.

Correspondence to Jeffery L. Dangl.

The authors declare no competing interests.

Nature Plants thanks Matthieu Joosten and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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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 (2023). https://doi.org/10.1038/s41477-023-01466-1

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Received: 30 January 2023

Accepted: 23 June 2023

Published: 03 August 2023

DOI: https://doi.org/10.1038/s41477-023-01466-1

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