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NOD-like receptor-mediated plant immunity: from structure to cell death

Nature Reviews Immunology volume 21, pages 305–318 (2021)Cite this article

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Abstract

Animal and plant immune systems use intracellular nucleotide-binding oligomerization domain (NOD)-like receptors (NLRs) to detect pathogens, resulting in the activation of immune responses that are often associated with localized host cell death. Whereas vertebrate NLRs detect evolutionarily conserved molecular patterns and have undergone comparatively little copy number expansion, plant NLRs detect virulence factors that have often diversified in plant pathogen populations, and thus plant NLRs have been subject to parallel diversification. Plant NLRs sense the presence of virulence factors with enzymatic virulence activity often indirectly through their modification of host target proteins. By contrast, phytopathogenic virulence factors without enzymatic activity are usually recognized by NLRs directly by their structure. Structural and biochemical analyses have shown that both indirect and direct recognition of plant pathogens trigger the oligomerization of plant NLRs into active complexes. Assembly into three-layered ring-like structures has emerged as a common principle of NLR activation in plants and animals, but with distinct amino-terminal domains initiating different signalling pathways. Collectively, these analyses point to host cell membranes as a convergence point for activated plant NLRs and the disruption of cellular ion homeostasis as a possible major factor in NLR-triggered cell death signalling.

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Fig. 1: Modes of plant NLR-mediated non-self recognition across pathogen lineages.
Fig. 2: Co-evolutionary arms race between plant NLRs and pathogen effectors.
Fig. 3: Schematic representation of ZAR1 resistosome formation.
Fig. 4: Comparison between the ZAR1 coiled-coil (CC) domain and the four-helix bundles of CC and HeLo-like domain structures from plants and vertebrates.
Fig. 5: The predicted pore formed by ZAR1 coiled-coil (CC) domains is markedly different in size from that formed by gasdermin.
Fig. 6: Schematic summary of the current model describing plant immunity mediated by TIR-type NLRs.
Fig. 7: Schematic summary of signalling pathways presumed to be involved in NLR-mediated membrane perturbation.

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Acknowledgements

This work was supported by the Max Planck Society (P.S.-L.), the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) in the Collaborative Research Centre Grant 1403 (P.S.-L.) and under Germany’s Excellence Strategy — EXC-Number 2048/1 — project 390686111 (P.S.-L.), the Novo Nordisk Foundation grant NNF19OC0056457 (R.P.) and the Daimler und Benz Foundation (I.M.L.S.).

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Authors and Affiliations

  1. Department of Plant-Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany

    Isabel M. L. Saur & Paul Schulze-Lefert

  2. Unit of Plant Molecular Cell Biology, Institute for Biology I, RWTH Aachen University, Aachen, Germany

    Ralph Panstruga

  3. Cluster of Excellence on Plant Sciences, Cologne, Germany

    Paul Schulze-Lefert

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  1. Isabel M. L. Saur
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The authors contributed equally to all aspects of the article.

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Correspondence to Paul Schulze-Lefert.

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Nature Reviews Immunology thanks J. D. G. Jones, B. Kobe, D. Mackey and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Related links

Protein Data Bank: https://www.rcsb.org/

Glossary

Microbe-associated molecular patterns

(MAMPs). Epitopes that are often conserved among a class of microorganisms and recognized by animal and plant immune receptors.

Damage-associated molecular patterns

Host molecules produced and released on cellular insults, including cell wall damage, and perceived by host receptor proteins to activate or amplify host immune responses.

Haustoria

Specialized pathogen structures that invaginate the plasma membrane of individual host cells to promote pathogen virulence, supposedly via effector delivery and nutrient uptake.

Accessions

Groups of related plant material from one species and collected at one time from a specific location.

Necroptotic cell death

Caspase-independent form of programmed cell death in vertebrates.

Apoptosome

A protein complex formed during the process of apoptosis and composed of cytochrome c, APAF1 and deoxyadenosine triphosphate.

Inflammasome

A protein complex responsible for sensing pathogens, the activation of inflammatory responses and the initiation of a form of programmed cell death known as pyroptosis.

Pyroptosis

A form of programmed cell death involving cell lysis through the formation of membrane pores and subsequent release of cellular contents.

Toll-like receptors

Mammalian transmembrane immune receptors incorporating an amino-terminal Toll/interleukin-1 receptor domain.

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Saur, I.M.L., Panstruga, R. & Schulze-Lefert, P. NOD-like receptor-mediated plant immunity: from structure to cell death. Nat Rev Immunol 21, 305–318 (2021). https://doi.org/10.1038/s41577-020-00473-z

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