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  • Review Article
  • Published:

On the front line: structural insights into plant–pathogen interactions

Nature Reviews Microbiology volume 11, pages 761–776 (2013)Cite this article

Subjects

Key Points

  • Structural biology studies of proteins involved in plant pathogen–host interactions are crucial to understanding the molecular mechanisms of both pathogen virulence and host defence.

  • Plant pathogens and their hosts deploy molecules to the extracellular space (apoplast), and the structures of these molecules have revealed a relationship with membrane-damaging toxins and a mechanism for how plant receptors recognize microbial signatures.

  • Plant pathogens translocate effector proteins into host cells, and many suppress host immune defences. Structural studies of these effectors have showed how trans-kingdom protein–protein interactions have evolved to target immune regulators and have defined folds that have homology to proteins with known catalytic activities that were not apparent from protein sequence.

  • Protein structure analysis of both bacterial and oomycete effectors has identified conserved repeat folds both within and between certain effectors, which suggests evolution of protein function from a core, stable protein scaffold, probably through duplication and diversification.

  • Oligomerization of intracellular plant immune receptors (nucleotide-binding and Leu-rich repeat-containing (NB-LRR) proteins) is increasingly recognized as being important to trigger signalling in response to pathogens. Structures of the amino-terminal domains of both coiled-coil (CC) and Toll and interleukin-1 receptor (TLR) classes of NB-LRRs have shown how these regions can mediate dimerization.

Abstract

Over the past decade, considerable advances have been made in understanding the molecular mechanisms that underpin the arms race between plant pathogens and their hosts. Alongside genomic, bioinformatic, proteomic, biochemical and cell biological analyses of plant–pathogen interactions, three-dimensional structural studies of virulence proteins deployed by pathogens to promote infection, in some cases complexed with their plant cell targets, have uncovered key insights into the functions of these molecules. Structural information on plant immune receptors, which regulate the response to pathogen attack, is also starting to emerge. Structural studies of bacterial plant pathogen–host systems have been leading the way, but studies of filamentous plant pathogens are gathering pace. In this Review, we summarize the key developments in the structural biology of plant pathogen–host interactions.

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Figure 1: Overview of some of the molecular players in plant–pathogen interactions.
Figure 2: Structural basis of the interaction between Pseudomonas syringae T3SEs AvrPtoB and AvrPto and immune kinases.
Figure 3: Structural homology between bacterial effectors and conserved enzymes suggests protein function.
Figure 4: Crystal structures of RXLR effector proteins.
Figure 5: Dimerization in the amino-terminal domains of NB-LRR proteins.

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Acknowledgements

The authors thank S. Schornack and C. Zipfel for comments during the preparation of this manuscript. L.W. acknowledges support from Federation of the European Biochemical Societies (long-term fellowship) and the Biotechnology and Biological Sciences Research Council (BBSRC; grant BB/K009176/1). Work in the M.J.B. laboratory, relevant to the areas discussed, is funded by the BBSRC (grants BB/J004553/1 and BB/I019557/1), the European Research Council (proposal 294608), the John Innes Foundation and the Gatsby Charitable Foundation.

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  1. Lennart Wirthmueller and Abbas Maqbool: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Biological Chemistry, John Innes Centre, Norwich Research Park, Norwich, NR4 7UH, UK

    Lennart Wirthmueller, Abbas Maqbool & Mark J. Banfield

  2. The Sainsbury Laboratory, Norwich Research Park, Norwich, NR4 7UH, UK

    Lennart Wirthmueller

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FURTHER INFORMATION

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Glossary

Apoplastic effectors

Effectors that are secreted into and act in the apoplast, a tissue-level compartment outside the plant plasma membrane that includes the cell wall.

Cytoplasmic effectors

Effectors that are secreted and translocated across the plant plasma membrane into the host cytoplasm, where they can target different subcellular compartments.

Necrotrophic

An organism that kills host cells before invasion and gains nutrients from the dead plant tissue.

Hemibiotrophic

An organism that feeds on living tissues for a period and then switches to necrotrophic colonization of dead tissues.

Obligate biotrophic

An organism that can only complete its life cycle on living plant tissue; such organisms actively prevent host cell death and feed on living plant tissue.

Hypersensitive response

(HR). A specific form of programmed cell death, often induced by effector-triggered immunity and correlated with accumulation of antimicrobial compounds and systemic acquired resistance.

Pathovars

Pathogenic variants within a species that are defined by a characteristic host range and/or tissue specificity.

E3 ligases

Enzymes required to attach the molecular tag ubiquitin to proteins. This tag modifies protein function or targets the protein for proteosomal degradation.

Salicylic acid

Also known as salicylate, this is a central plant hormone signal that induces local and systemic defence responses in plants, collectively known as systemic acquired resistance.

Ethylene

A gaseous, unsaturated hydrocarbon that acts as a plant hormone to promote growth and development and as an inhibiting stress factor.

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Wirthmueller, L., Maqbool, A. & Banfield, M. On the front line: structural insights into plant–pathogen interactions. Nat Rev Microbiol 11, 761–776 (2013). https://doi.org/10.1038/nrmicro3118

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