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Ustilago maydis effectors and their impact on virulence

Key Points

  • Ustilago maydis is a member of the smut fungi (phylum Basidiomycota) that infect maize. This group of plant pathogens is characterized by their biotrophic lifestyle and narrow host range.

  • The establishment of a biotrophic, compatible interaction between U. maydis and maize depends on the secretion of specialized fungal proteins termed effectors.

  • A large proportion of these effectors are completely novel, as they do not contain any annotated domains, and most of them are species-specific or lineage-specific.

  • Many of the novel effector genes are arranged in gene clusters, which arose through gene duplications and represent genomic islands with accelerated evolution. Many of these clusters are important for virulence.

  • Effector genes that markedly contribute to virulence are conserved among the smut fungi.

  • For a few effectors their mode of action has been elucidated. They counteract defence responses, re-route metabolic pathways and stimulate plant cell division.

  • The expression of effector genes is regulated by a hierarchical network of transcription factors and is coupled to sexual development and spore formation. The plant signals that induce the expression of effector genes are largely unknown.

Abstract

Biotrophic fungal plant pathogens establish an intimate relationship with their host to support the infection process. Central to this strategy is the secretion of a range of protein effectors that enable the pathogen to evade plant immune defences and modulate host metabolism to meet its needs. In this Review, using the smut fungus Ustilago maydis as an example, we discuss new insights into the effector repertoire of smut fungi that have been gained from comparative genomics and discuss the molecular mechanisms by which U. maydis effectors change processes in the plant host. Finally, we examine how the expression of effector genes and effector secretion are coordinated with fungal development in the host.

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Figure 1: The life cycle of Ustilago maydis.
Figure 2: Effector repertoire of Ustilago maydis and related smut fungi.
Figure 3: Functionally characterized effectors of Ustilago maydis.
Figure 4: The regulatory network that controls effector gene expression and secretion.

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Acknowledgements

The authors thank R. Rösser for providing the photograph that depicts a field example of a maize cob infected with Ustilago maydis and S. Winterberg for carrying out infections using U. maydis effector mutant strains and providing photographs. The authors apologize to colleagues whose original work could not be cited owing to space limitations. Research in the author's laboratories was supported by grants from the Deutsche Forschungsgemeinschaft (DFG) in the frame of the collaborative research center SFB593, through the LOEWE program SYNMIKRO of the state of Hesse, and through the Max Planck Society.

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Glossary

Effectors

Secreted pathogen proteins that function either inside host cells or at the interface between host and pathogen. Effectors are used to suppress host defences or tune host metabolism to support the infection process.

Smut fungi

Biotrophic basidiomycete plant pathogens of the order Ustilaginales that undergo sexual reproduction only during the infection of a host plant. They produce dark pigmented spores that look similar to coal dust or 'smut' when released into the environment.

Biotrophic

In a biotrophic interaction, plant pathogens establish a compatible interaction with their hosts, during which the plant stays fully alive, provides nutrients to the pathogen and enables the pathogen to complete its life cycle.

Anthocyanin

A red plant pigment that is synthesized through the phenylpropanoid pathway and protects cells from high-light damage, acts as an antioxidant or is an attractant for pollinators.

Appressoria

Specialized cells that develop at the hyphal tips of many fungal plant pathogens that are used to infect host plants either by mechanical pressure or with the help of the localized secretion of plant cell wall-degrading or loosening enzymes.

Clamp

A hook-like structure formed by the dikaryotic hyphal tip cells of basidiomycete fungi that assures the correct segregation of the two different nuclei and the maintenance of the dikaryotic state in growing hyphae.

Secretome

The totality of all proteins of a species that are predicted to be, or shown to be, secreted into the extracellular space.

Cystatin

A member of a family of conserved proteins that act as cysteine protease inhibitors.

Reactive oxygen species

(ROS). Chemically reactive chemical species that contain oxygen and have important roles in the development of, and defence responses in, plants.

Apoplast

The compartment outside the plant plasma membrane that is formed by the continuum of the cell walls of adjacent cells and the extracellular spaces, through which water and solutes can diffuse.

Shikimate pathway

A metabolic route for the biosynthesis of the aromatic amino acids phenylalanine, tyrosine and tryptophan.

Guard cells

Specialized epidermal cells that surround the stomatal pore and enable it to open and close.

Plasmodesmata

Microscopic channels that traverse the cell walls of plant cells and enable transport and communication between them.

Non-host resistance

A term that defines the broad-spectrum resistance of a particular plant species against all isolates of a pathogen that can cause disease in other plant species.

Retrograde signalling

In the context used, it refers to the propensity of early endosomes to deliver signals from the growing hyphal tip back to the nucleus.

Early endosomes

Distinct membrane-bound endocytic organelles that constitute a central compartment in the endocytic pathway; in filamentous fungi early endosomes move along microtubuli, and this process supports hyphal growth

WOPR protein

Proteins of the WOPR family constitute a class of fungal-specific transcriptional regulators that bind to DNA through their amino-terminal WOPR box.

Teliospores

Diploid resting spores that can survive extended periods of time under harsh environmental conditions.

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Lanver, D., Tollot, M., Schweizer, G. et al. Ustilago maydis effectors and their impact on virulence. Nat Rev Microbiol 15, 409–421 (2017). https://doi.org/10.1038/nrmicro.2017.33

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