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  • Review Article
  • Published:

Filamentous plant pathogen effectors in action

Nature Reviews Microbiology volume 11, pages 800–814 (2013)Cite this article

Subjects

Key Points

  • The use of live-cell fluorescence imaging as eukaryotic filamentous pathogens invade living plant cells has generated a detailed picture of the focused secretory 'warfare' that occurs between plants and potential pathogens, beginning even before the pathogen breaches the host surface.

  • Fungi and oomycete pathogens use diverse biotrophic strategies to invade living plant cells, but they all secrete a considerable range of effector proteins, including apoplastic effectors that remain in the plant extracellular space and cytoplasmic effectors that move across the plant plasma membrane into plant cells.

  • Effector secretion seems to be precisely controlled in time and space, as waves of effectors are secreted at different invasion stages and effector secretion is targeted to specific locations. Some effectors are secreted through appressorium pores before penetration and others are secreted into specialized compartments at the biotrophic interface inside plant cells.

  • After delivery into plant cells, cytoplasmic effectors target diverse cellular locations and some even move into uninvaded plant cells, presumably to prepare these before invasion. Many effectors function to defeat the plant's defences, but most host targets of effectors are unknown.

  • At least one fungal pathogen has evolved distinct secretion systems to target effectors to the plant's extracellular and cytoplasmic compartments. Multivesicular bodies and exosomes have been implicated in the secretion of defence components by plants and in the secretion of virulence factors by fungi.

Abstract

Live-cell imaging assisted by fluorescent markers has been fundamental to understanding the focused secretory 'warfare' that occurs between plants and biotrophic pathogens that feed on living plant cells. Pathogens succeed through the spatiotemporal deployment of a remarkably diverse range of effector proteins to control plant defences and cellular processes. Some effectors can be secreted by appressoria even before host penetration, many enter living plant cells where they target diverse subcellular compartments and others move into neighbouring cells to prepare them before invasion. This Review summarizes the latest advances in our understanding of the cell biology of biotrophic interactions between plants and their eukaryotic filamentous pathogens based on in planta analyses of effectors.

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Figure 1: Biotrophic strategies and identified secreted effectors for diverse pathogens.
Figure 2: Structure and secretion dynamics at the biotrophic interface.
Figure 3: Focal effector secretion in melanized appressoria.
Figure 4: Effector secretion and accumulation during live cell invasions.
Figure 5: Pathogen-dependent and pathogen-independent effector translocation assays.

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Acknowledgements

The authors apologize to authors whose work could not be cited as a result of space limitations. They thank M. Dalby for technical support and P. Dodds and M. Yi for comments and discussions. Their research was supported by grants from the National Research Initiative Competitive Grants Program (Grants 2008-35600-18809 and 2010-65108-20538) from the United States Department of Agriculture (USDA) National Institute of Food and Agriculture. They acknowledge support from the Centre of Biomedical Research Excellence (COBRE) Confocal Microfluorometry and Microscopy Core at Kansas State University (KSU), USA, funded by College of Veterinary Medicine, KSU (CVM-KSU) and US National Institutes of Health (NIH) Grant P20 RR-017686. This is contribution no.14-012-J from the Kansas Agricultural Experiment Station.

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Authors and Affiliations

  1. Department of Plant Pathology, 4024 Throckmorton Plant Sciences Center

    Martha C. Giraldo & Barbara Valent

  2. Kansas State University, Manhattan, 66506–5502, KS, USA

    Martha C. Giraldo & Barbara Valent

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  1. Martha C. Giraldo
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Correspondence to Barbara Valent.

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PowerPoint slides

Glossary

Biotrophic

A biotrophic organism feeds and completes its life cycle on living plant tissue and lacks a necrotrophic phase of killing host cells before feeding.

Hemibiotrophic

A hemibiotropic organism feeds on living tissues for a period of time and then switches to necrotrophic colonization of dead tissues.

Apoplast

Plant extracellular space; a tissue-level compartment outside the plasma membrane that includes the cell walls and xylem vessels, through which water and solutes freely diffuse.

Effectors

Pathogen molecules that modify host cell structure, metabolism and function. They often interfere with signal pathways, either those required for host invasion or those that trigger host resistance.

Avirulence effectors

(AVR effectors). Effectors that are recognized by a corresponding plant resistance (R) protein, triggering the hypersensitive response and rendering pathogen strains expressing these effectors unable to infect (known as avirulent toward) host genotypes expressing the R protein.

Apoplastic effectors

Effectors that are secreted into and function in the plant extracellular space.

Cytoplasmic effectors

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

Necrotrophic

An organism that kills host cells before invasion and gains nutrition from the dead cells.

Extrahaustorial matrix

(EHMx). A substance that resides between the pathogen cell wall and the surrounding extrahaustorial membrane. Called the extrainvasive hyphal matrix when it surrounds invasive hyphae.

Neckband

An undefined structure that seals the interface between host and pathogen plasma membranes; sometimes observed as an electron-dense ring around haustorial necks by electron microscopy.

Papilla

Cell wall apposition at a site of attempted penetration; contains callose, phenolic compounds, lignin, reactive oxygen species, proteins and even membranes and exosomes; it is thought to function as a physical barrier to penetration.

Multivesicular bodies

(MVBs). Membrane-bound vesicles associated with late endosomes.

Exosomes

Intact vesicles that are secreted when multivesicular bodies fuse with the plasma membrane; suggested as an alternative route for secretion of virulence and pathogenicity factors into the host.

Appressorium pore

A cell wall-less region of the appressorium adjacent to the plant cuticle that also lacks the melanin layer, which results in fungal plasma membrane in direct contact with the cuticle; it is sealed against the cuticle by a 'pore ring' that surrounds the perimeter of the pore.

Tonoplast

The vacuolar membrane in a plant cell.

Plasmolysis

Shrinkage of the protoplast away from the plant cell wall as a result of the loss of water through osmosis.

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Giraldo, M., Valent, B. Filamentous plant pathogen effectors in action. Nat Rev Microbiol 11, 800–814 (2013). https://doi.org/10.1038/nrmicro3119

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