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  • Review Article
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How do plants achieve immunity? Defence without specialized immune cells

Key Points

  • Unlike vertebrates, plants do not have an adaptive immune system. Nonetheless, plants can launch specific, self-tolerant immune responses and establish immune memory.

  • To promote virulence, pathogens inject effector molecules that target conserved immune signalling hubs into the plant cell. In response, plants have evolved resistance (R) proteins that detect effector-induced perturbations in these hubs, providing the potential to specifically recognize a large number of pathogens with similar infection strategies through a smaller number of R proteins.

  • Intraspecific and interspecific plant crosses suggest that autoimmunity can arise from self-reacting R proteins, illustrating the threat of uncontrolled R protein activity. Dynamic transcriptional and post-transcriptional regulation of R protein levels is thought to minimize the risk of autoimmunity in plants.

  • Pathogen-infected tissues generate a mobile immune signal consisting of multiple proteins as well as lipid-derived and hormone-like molecules. These signal molecules are transported to systemic tissues, where they induce systemic acquired resistance (SAR). SAR is associated with the systemic reprogramming of thousands of genes to prioritize immune responses over routine cellular requirements.

  • Epigenetic modifications and site-specific chromatin remodelling seem to provide a long-lasting memory of pathogen attack. They are also hypothesized to induce genome rearrangements in specific loci, which can be transmitted to subsequent generations.

Abstract

Vertebrates have evolved a sophisticated adaptive immune system that relies on an almost infinite diversity of antigen receptors that are clonally expressed by specialized immune cells that roam the circulatory system. These immune cells provide vertebrates with extraordinary antigen-specific immune capacity and memory, while minimizing self-reactivity. Plants, however, lack specialized mobile immune cells. Instead, every plant cell is thought to be capable of launching an effective immune response. So how do plants achieve specific, self-tolerant immunity and establish immune memory? Recent developments point towards a multilayered plant innate immune system comprised of self-surveillance, systemic signalling and chromosomal changes that together establish effective immunity.

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Figure 1: The guard model: surveillance of the host immune regulator RIN4 by the R proteins RPM1 and RPS2.
Figure 2: Autoimmunity in necrotic hybrids might be caused by a mismatching of R proteins and the targets of pathogen effectors that they guard.
Figure 3: Translocation of mobile immune signals induces systemic immunity and immune memory.

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Acknowledgements

We thank F. M. Ausubel for critically reading the manuscript and providing insightful suggestions, and we apologize to colleagues whose work we did not cite owing to space limitations. This work was supported by grants from The Royal Society (Uf090321) to S.H.S. and from the US National Institutes of Health (R01 GM069594-07) and the National Science Foundation (IOS-0929226, IOS-0744602) to X.D.

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Glossary

Phytopathogens

Microbial organisms that are specialized in attacking plant hosts. They use a variety of infection strategies, ranging from feeding on live plant cells to destroying plants cells to feed on their contents.

Callose

Following pathogen infection, this polysaccharide is produced by plant cells and deposited near the site of attempted penetration to reinforce the cell wall.

Convergent evolution

A process by which organisms from different lineages independently evolve similar traits that help them to adapt to their environment.

Pattern-triggered immunity

A basal type of immunity conferred by the recognition of conserved microorganism-associated molecular patterns by specific transmembrane receptors that protect hosts against non-specialized pathogens.

Effector molecules

Pathogen-produced proteins that are injected into the host cell, where they suppress the function of host immune regulators to promote pathogen virulence.

Effector-triggered immunity

A type of immunity triggered by resistance (R) proteins that sense perturbations of host signalling hubs caused by pathogen-produced effector molecules. Effector-triggered immunity frequently culminates in programmed cell death of the infected cell.

Hypersensitive response

A plant immune response that occurs locally to isolate and prevent the growth of pathogens or insects whose life cycles depend on live host cells. This response is triggered when the presence of a pathogen effector is detected by a host resistance (R) protein and is characterized by the rapid death of cells at the infection site.

Programmed cell death

Unlike cell senescence, this is an active form of cell death that occurs through a regulated process during normal development and has a physiological function.

Systemic acquired resistance

A long-lasting, broad-spectrum immune response that is induced throughout the entire plant following attempted local infection.

NLR proteins

(Nucleotide-binding oligomerization domain (NOD)- and leucine-rich repeat (LRR)-containing proteins). A group of intracellular immune receptors that have a structure that closely resembles that of resistance (R) proteins in plants. In contrast to R proteins, NLRs in mammals detect microorganism-associated molecular patterns rather than pathogen effectors.

Metacaspases

Arginine- and lysine-specific proteases that are related to animal caspases. Metacaspases are found in plants, fungi and protists, where they have an essential role in programmed cell death responses.

Hybrid necrosis

A post-zygotic incompatibility resulting from intraspecific or interspecific crosses that is typified by severe tissue necrosis, stunting and auto-activation of immune responses.

Phloem

The plant vascular tissue, which transports organic nutrients (such as sugars) from photosynthetic 'source' tissues to nutrient-consuming 'sink' tissues throughout the entire plant.

Apoplastic

Localized to the free diffusional space outside the plasma membrane of plant cells.

Redox state

A term that can be used narrowly to describe the ratio of interconvertible oxidized and reduced forms of a specific redox couple (such as NAD+–NADH), but that can also be used broadly to describe the cellular redox environment, which is determined by the states of all of the redox couples combined.

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Spoel, S., Dong, X. How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol 12, 89–100 (2012). https://doi.org/10.1038/nri3141

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