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Evasion of plant immunity by microbial pathogens

Abstract

Plant pathogenic viruses, bacteria, fungi and oomycetes cause destructive diseases in natural habitats and agricultural settings, thereby threatening plant biodiversity and global food security. The capability of plants to sense and respond to microbial infection determines the outcome of plant–microorganism interactions. Host-adapted microbial pathogens exploit various infection strategies to evade or counter plant immunity and eventually establish a replicative niche. Evasion of plant immunity through dampening host recognition or the subsequent immune signalling and defence execution is a crucial infection strategy used by different microbial pathogens to cause diseases, underpinning a substantial obstacle for efficient deployment of host genetic resistance genes for sustainable disease control. In this Review, we discuss current knowledge of the varied strategies microbial pathogens use to evade the complicated network of plant immunity for successful infection. In addition, we discuss how to exploit this knowledge to engineer crop resistance.

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Fig. 1: Stepwise activation of plant innate immunity.
Fig. 2: Microbial pathogens possess multiple mechanisms to evade plant PRR-mediated recognition.
Fig. 3: Microbial evasion of host NLR receptor-mediated recognition.
Fig. 4: Manipulation of plant immune signalling.
Fig. 5: Manipulation of plant immune output.

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Acknowledgements

The authors apologize to colleagues whose studies were not cited owing to space limitations. They thank X. Tao, S. Dong, Z. Ma, Y. Xia, J. Huang, G. Sun and J. Wu for helpful suggestions, and D. Lv, M. Zeng and Y. Xu for help in designing the draft figures. Yan Wang and Yuanchao Wang are supported by China National Natural Science Foundation grants 31721004, 32020103012 and 31872927 and the grant for Distinguished Young Scholars of Jiangsu Province BK20190027. R.N.P. and T.N. are supported by Deutsche Forschungsgemeinschaft grant Nu70/16-1.

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Yan Wang and R.N.P. researched data for the article. Yuanchao Wang, Yan Wang, R.N.P. and T.N. contributed to the discussion of content, wrote the article, and reviewed and edited the article.

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Correspondence to Yuanchao Wang.

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Glossary

Disease triangle

A paradigm describing the interactions among the three casual factors (the environment, the host and pathogens) governing plant disease. Plant disease occurs only when pathogenic microorganisms encounter susceptible plants under favourable environmental conditions.

Microbe-associated molecular patterns

(MAMPs). Structurally conserved microorganism-derived signature molecules, including peptides, carbohydrates or fatty acids, that are detected by surface-localized host cell receptors to activate plant defence.

Apoplast

The extracellular matrix outside plant plasma membranes, including cell walls and the intercellular space.

Helper NLRs

(hNLRs). NOD-like receptors (NLRs) that act as regulatory nodes controlling immune signalling downstream of sensor NLRs.

Sensor NLRs

NOD-like receptors (NLRs) that bind to or perceive effectors directly or indirectly by monitoring modifications in host targets.

Epistatic effectors

Microbial effectors that are genetically suppressive with regard to the activity or expression of other effectors.

Guardees

Plant proteins that are targeted by microbial effectors and are monitored by plant immune receptors.

Decoys

Mimic proteins in plants or microbial pathogens that are dispensable for microbial virulence in the absence of the cognate effectors or immune receptors.

Biotrophic pathogens

Pathogens that survive only in living plant cells without killing hosts during infection. Pathogens of this type often cannot be extensively cultured in vitro.

Necrotrophic pathogens

Pathogens that kill host cells and feed on dead or dying tissues throughout the life cycle.

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Wang, Y., Pruitt, R.N., Nürnberger, T. et al. Evasion of plant immunity by microbial pathogens. Nat Rev Microbiol 20, 449–464 (2022). https://doi.org/10.1038/s41579-022-00710-3

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