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Bacterial elicitation and evasion of plant innate immunity

Key Points

  • An overview of the various mechanisms of bacterial pathogenesis is presented, with a focus on bacterial proteins, protein-secretion systems and small molecules that modulate plant biology.

  • The mechanisms by which plant pathogen recognition receptors (PRRs) recognize bacterial pathogen-associated molecular patterns (PAMPS) are discussed. Latest developments in this field are examined with an emphasis on the flagellin–FLS2 and elongation factor Tu (EF-Tu)–EFR (EF-Tu receptor) systems.

  • PRR-mediated defences represent a significant obstacle for plant pathogens. However, type III effectors that function to suppress PRR-mediated basal defences have been discovered. These effectors have been shown to limit cell wall-based defences and expression of defence-associated genes.

  • Plants probably evolved resistance (R) proteins to recognize the presence of bacterial effectors that suppress PRR-mediated defences. R proteins elicit a strong hypersensitive response that provides immunity to the host plant. Mechanisms of effector–R protein recognition are discussed in the context of current models.

  • In response to plant R proteins, it seems that pathogens have evolved an alternative set of effectors that suppress R-protein-mediated defences. The mechanisms by which effectors suppress R-protein-mediated defences are examined.

  • Current research establishes that resistance to bacterial pathogens is regulated by both PRR- and R-protein-mediated recognition. The outcome of each interaction is dependent on at least four factors: the complement of PAMPS and effectors in the pathogen, and the PRR and R proteins in the host.

Abstract

Recent research on plant responses to bacterial attack has identified extracellular and intracellular host receptors that recognize conserved pathogen-associated molecular patterns and more specialized virulence proteins, respectively. These findings have shed light on our understanding of the molecular mechanisms by which bacteria elicit host defences and how pathogens have evolved to evade or suppress these defences.

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Figure 1: Disease symptoms caused by some bacterial pathogens of plants and representative virulence mechanisms used by these pathogens.
Figure 2: Model depicting the activation of PRR-mediated basal defences and their suppression by type III effectors.
Figure 3: Suppression of R-protein-mediated defences by type III effectors.
Figure 4: Factors that influence the outcome of plant–bacteria interactions.

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Acknowledgements

We thank Tracy Rosebrock and Ann Taylor for critical reading of the manuscript. We are grateful to Tom Burr, Amy Charkowski, and Paul Frey for providing photographs for Figure 1. Research in our laboratory is supported by the National Science Foundation, National Institutes of Health, United States Department of Agriculture-National Research Initiative, Binational Agriculture Research Fund, Binational Science Foundation and the Triad Foundation.

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Glossary

Stomate

A natural opening on leaves and stems. Stomata can open and close to ensure efficient exchange of gases and moisture in the apoplast.

Apoplast

The intercellular space in the plant tissue, including the cell wall, that is outside the plasma membrane, through which nutrients and water can freely diffuse.

Xylem

A network of cells in the vascular system of a plant that moves water and minerals.

Virulence

Increases in the rate of growth and final population size, or enhanced disease symptoms, that promote the spread of the pathogen through the plant or in nature.

Type III secretion system

A bacterial membrane-spanning protein complex, extended by a pilus. This complex functions like a syringe to inject bacterial proteins into the host cell cytoplasm.

Effector

A bacterial protein that is translocated by the type III secretion system into the plant cell cytoplasm.

Pathogen-associated molecular patterns

(PAMPs). Bacterial molecules that have an important role in the microbial lifestyle, and that contain a conserved feature that is recognized by a pathogen recognition receptor (PRR).

Pathogen recognition receptor

(PRR). A host receptor, such as FLS2 or EFR, that can detect the presence of pathogens by recognizing conserved pathogen molecules (such as PAMPs).

Basal defence

Plant defence that occurs early in the host–pathogen interaction in response to the perception by plant pattern recognition receptors (PRRs) of extracellular pathogen-associated molecular patterns (PAMPs).

Biotrophy

A period of colonization during which a microorganism relies on living host tissue to grow.

Hormone

A signal molecule that is produced at specific locations and at low concentrations. Hormones can be transported throughout the plant and regulate biological processes.

Arabidopsis

A plant of the mustard family that is used as a model organism in plant molecular biology.

Callose

A polysaccharide that is a common plant cell wall constituent and that is deposited near infection sites in structures known as papillae. Callose deposition is associated with basal defences and is believed to limit pathogen virulence.

Resistance (R) protein

A plant protein that recognizes, either directly or indirectly, a specific pathogen avirulence protein (often a type III effector) to activate plant immunity.

Gene-for-gene model of disease resistance

A model for plant immunity in which plant resistance genes are only effective if a specific avirulence gene is expressed by the pathogen.

Avirulence (Avr) protein

A pathogen protein that elicits plant immunity in plants that express a specific resistance protein. Avr proteins are often type III effector proteins.

Hypersensitive response

(HR). A defence that is often associated with resistance (R)-protein-mediated immunity. During the HR, the plant initiates programmed cell death in cells that surround the pathogen to inhibit pathogen spreading.

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Abramovitch, R., Anderson, J. & Martin, G. Bacterial elicitation and evasion of plant innate immunity. Nat Rev Mol Cell Biol 7, 601–611 (2006). https://doi.org/10.1038/nrm1984

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