Extracellular niche establishment by plant pathogens

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. In this Review, Roussin-Léveillée, Mackey and colleagues examine microorganism interaction with and manipulation of the plant apoplast. Effector-driven extracellular niche establishment is conceptualized as foundational to plant pathogenesis and frames the discussion of the complex interplay between pathogen virulence, host immunity and the physiological dynamics shaping plant–microorganism interactions.