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Plant immunity: towards an integrated view of plant–pathogen interactions

Nature Reviews Genetics volume 11, pages 539–548 (2010)Cite this article

Subjects

Key Points

  • Plant immunity depends on cell-autonomous events that are related to animal innate immunity, but plants have a greatly expanded recognition repertoire to compensate for their lack of an adaptive immune system. Ongoing research is revealing the recognition capacity of the plant immune system and concurrent studies on pathogen biology are beginning to unravel how these organisms manipulate host immunity to cause disease.

  • Plants have evolved two strategies to detect pathogens. On the external face of the host cell, conserved microbial elicitors called pathogen-associated molecular patterns (PAMPs) are recognized by receptor proteins called pattern recognition receptors (PRRs); stimulation of PRRs leads to PAMP-triggered immunity (PTI). The second class of perception involves recognition by intracellular receptors of pathogen virulence molecules called effectors; this recognition induces effector-triggered immunity (ETI).

  • PTI is generally effective against non-adapted pathogens in a phenomenon called non-host resistance, whereas ETI is active against adapted pathogens. However, these relationships are not exclusive and depend on the elicitor molecules present in each infection.

  • Successful pathogens are able to suppress PTI responses and thereby multiply and cause disease. They achieve suppression through the deployment of 'effector' proteins. Plant receptor proteins can recognize pathogen effectors either by direct physical association or indirectly through an accessory protein.

  • Our understanding of effector proteins and their host targets is at an early stage. Sophisticated biochemical screens for host protein targets that interact with the diverse suites of pathogen effectors is likely to lead to the identification of important components of host defence mechanisms, and teach us more about host immune pathways and pathogenicity strategies.

  • It is crucially important for the deployment of existing and novel resistance genes in agriculture that we advance our knowledge of plant–pathogen molecular co-evolution.

Abstract

Plants are engaged in a continuous co-evolutionary struggle for dominance with their pathogens. The outcomes of these interactions are of particular importance to human activities, as they can have dramatic effects on agricultural systems. The recent convergence of molecular studies of plant immunity and pathogen infection strategies is revealing an integrated picture of the plant–pathogen interaction from the perspective of both organisms. Plants have an amazing capacity to recognize pathogens through strategies involving both conserved and variable pathogen elicitors, and pathogens manipulate the defence response through secretion of virulence effector molecules. These insights suggest novel biotechnological approaches to crop protection.

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Figure 1: The principles of plant immunity.
Figure 2: Formation of active pattern recognition receptor complexes.
Figure 3: Models of direct and indirect recognition.

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Acknowledgements

We apologize to those authors whose workcouldnotbecited owing to space limitations. J.P.R. is an Australian Research Council Future Fellow. Work in P.N.D.'s laboratory is funded by the Australian Research Council, the US National Institutes of Health and the Grains Research and Development Corporation. We thank J. Ellis and B. Staskawicz for helpful discussions.

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Authors and Affiliations

  1. Division of Plant Industry, Commonwealth Scientific and Industrial Research Organisation (CSIRO), GPO BOX 1600, Canberra, 2601, Australian Capital Territory, Australia

    Peter N. Dodds

  2. Research School of Biology, Australian National University, RN Robertson Building, Biology Place, Acton, 0200, Australian Capital Territory, Australia

    John P. Rathjen

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Glossary

Elicitors

Molecules that induce ('elicit') an immune defence response. In the context of this Review, this term is used to refer to both pathogen-associated molecular patterns (PAMPs) and effectors.

Pathogen-associated molecular patterns

Any of a number of conserved, usually structural, molecules common to pathogen organisms.

Pattern recognition receptors

Plasma membrane-localized receptors that recognize the presence of pathogen-associated molecular patterns (PAMPs) in the extracellular environment.

PAMP-triggered immunity

The plant defence response elicited by pathogen-associated molecular pattern (PAMP) recognition.

Effectors

Proteins secreted by pathogens into host cells to enhance infection. Many of these function to suppress PAMP-triggered immunity responses.

Effector-triggered immunity

The plant defence response elicited by effector recognition.

Biotrophic

Biotrophic pathogens propagate in living plant tissue and generally do not cause necrosis as a result of infection. They use various means, such as haustoria production, to extract nutrients from host cells.

Necrotrophic

Necrotrophic pathogens actively induce necrosis in infected tissues, often through the production of toxins, and obtain nutrients from the dead host tissue.

Type-III secretion system

A syringe-like structure produced by many plant and animal pathogen bacteria that allows direct secretion of effector proteins from the bacterial cytoplasm into host cells.

Haustoria

(sing. haustorium.) Specialized structures produced by some fungal and oomycete pathogens. Haustoria extend through the plant cell wall and expand in the host cell. They remain surrounded by a host-derived membrane and hence are topologically extracellular and separated from the host cytoplasm.

Hemibiotrophic

Hemibiotrophic pathogens incorporate aspects of both biotrophic and necrotrophic infection strategies. Often this involves an initial biotrophic infection phase during which the pathogen spreads in host tissue, followed by a necrotrophic phase during which host cell death is induced.

NB-LRR proteins

A class of intracellular receptor proteins containing nucleotide-binding (NB) and leucine-rich repeat (LRR) domains that recognize specific pathogen effectors.

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Dodds, P., Rathjen, J. Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet 11, 539–548 (2010). https://doi.org/10.1038/nrg2812

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