Subversion of plant endomembrane trafficking by a Plasmodiophora brassicae effector PbALE that recruits membrane components at the host–pathogen interface to aid in colonization

Abstract

Summary Plasmodiophora brassicae , an intracellular biotrophic protist that causes clubroot in crucifers, extensively alters the host endomembrane system for colonization. However, the molecular mechanisms and functions of effectors to achieve this remain poorly understood. Using fluorescent and transmission electron microscopy of P. brassicae ‐infected Arabidopsis, we show that host endomembranes and organelles become closely associated with P. brassicae secondary plasmodial structures and are subsequently phagocytosed by the pathogen. PbALE is a secreted endomembrane‐targeting effector that binds a range of phospholipids. Overexpression of the effector results in plants with glossy leaves that progressively become chlorotic. Fluorescent protein‐tagged PbALE is observed in large condensates that cluster with plant organelles, disrupting endocytic recycling of plant membrane receptors and immune regulatory proteins, thereby impairing penetration resistance to nonadapted barley powdery mildew infection. PbALE's association with the P. brassicae plasmodial surface and the extrahaustorial membrane during adaptive powdery mildew infection, along with the recruitment of PI(4,5)P 2 to these membrane contacts, supports a model in which the effector nucleates lipid‐rich compartments and enriches organelles at the host‐pathogen interface. Our findings reveal a lipid‐binding effector that remodels host endomembranes, disrupts immune trafficking, and aids pathogen colonization, offering insights into strategies for durable disease resistance.