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Extracellular niche establishment by plant pathogens

Nature Reviews Microbiology (2024)Cite this article

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Abstract

The plant extracellular space, referred to as the apoplast, is inhabited by a variety of microorganisms. Reflecting the crucial nature of this compartment, both plants and microorganisms seek to control, exploit and respond to its composition. Upon sensing the apoplastic environment, pathogens activate virulence programmes, including the delivery of effectors with well-established roles in suppressing plant immunity. We posit that another key and foundational role of effectors is niche establishment — specifically, the manipulation of plant physiological processes to enrich the apoplast in water and nutritive metabolites. Facets of plant immunity counteract niche establishment by restricting water, nutrients and signals for virulence activation. The complex competition to control and, in the case of pathogens, exploit the apoplast provides remarkable insights into the nature of virulence, host susceptibility, host defence and, ultimately, the origin of phytopathogenesis. This novel framework focuses on the ecology of a microbial niche and highlights areas of future research on plant–microorganism interactions.

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Fig. 1: A model for a feedforward loop supporting pathogenic niche establishment.
Fig. 2: Microbial strategies leading to niche establishment.
Fig. 3: Opposing forces of effector-triggered susceptibility and plant immunity determine niche quality.

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Acknowledgements

Research in the Moffett laboratory is supported by funding from the Natural Sciences and Engineering Research Council (NSERC) of Canada, from the Fonds de Recherche Québécois — Nature et Technologies, and C.R-L. is supported by an NSERC doctoral fellowship. Support for the Mackey laboratory is provided by the National Science Foundation (Division of Integrative Organismal Systems, grant no. 1953509). The authors are grateful to members of the research group of Sebastian Schornack (Sainsbury Laboratory, University of Cambridge) for suggestions to improve the visual models.

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  1. These authors contributed equally: Charles Roussin-Léveillée, David Mackey.

Authors and Affiliations

  1. Centre SÈVE, Département de Biologie, Université de Sherbrooke, Sherbrooke, Québec, Canada

    Charles Roussin-Léveillée & Peter Moffett

  2. Department of Horticulture and Crop Science, The Ohio State University, Columbus, OH, USA

    David Mackey, Gayani Ekanayake & Reid Gohmann

  3. Department of Molecular Genetics, The Ohio State University, Columbus, OH, USA

    David Mackey

  4. Center for Applied Plant Sciences, The Ohio State University, Columbus, OH, USA

    David Mackey

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Contributions

C.R.-L. and D.M. contributed equally to the conceptualization, research and writing of this manuscript. C.R.-L. and D.M. drafted the figures. R.G., G.E. and P.M. contributed to the research and to writing and reviewing of this manuscript. All authors reviewed and/or edited the manuscript before submission.

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Correspondence to David Mackey or Peter Moffett.

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Roussin-Léveillée, C., Mackey, D., Ekanayake, G. et al. Extracellular niche establishment by plant pathogens. Nat Rev Microbiol (2024). https://doi.org/10.1038/s41579-023-00999-8

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