Vacuolar sorting receptors coordinate lytic vacuolar and autophagic transport for plant effector-triggered immunity

Abstract

Vacuolar sorting receptors (VSRs) are involved in sorting soluble vacuolar proteins during normal plant growth and development, but their role in plant stress responses remains largely unexplored. Here we report that a subgroup of the Arabidopsis thaliana VSR genes are transcriptionally induced during infection with avirulent Pseudomonas syringae strains, leading to higher VSR protein accumulation. We demonstrate that the pathogen-responsive VSR1, VSR5, VSR6 and VSR7 genes function redundantly in sorting vacuolar death-related enzymes induced during bacterial infection. Moreover, VSRs are required for fusion of the tonoplast with the plasma membrane and the subsequent release of vacuolar contents into the apoplast, where bacterial pathogens reside. Indeed, dysfunction of this subgroup of VSRs blocks hypersensitive cell death and leads to stronger disease symptoms and higher bacterial loads, revealing their essential role in defence against avirulent bacterial infection. Intriguingly, their disruption also leads to defects in autophagy, impairing autophagosome-mediated degradation of bacterial effector proteins. Collectively, our results show that VSR1, VSR5, VSR6 and VSR7 are key regulators of plant effector-triggered immunity (ETI) by orchestrating receptor-mediated vacuolar sorting of immunity-related proteins, tonoplast to plasma membrane fusion, and autophagic degradation of effector proteins.