Plant targets for Pseudomonas syringae type III effectors: virulence targets or guarded decoys?

Abstract

The phytopathogenic bacterium Pseudomonas syringae can suppress both pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) and effector-triggered immunity (ETI) by the injection of type III effector (T3E) proteins into host cells. T3Es achieve immune suppression using a variety of strategies including interference with immune receptor signaling, blocking RNA pathways and vesicle trafficking, and altering organelle function. T3Es can be recognized indirectly by resistance proteins monitoring specific T3E targets resulting in ETI. It is presently unclear whether the monitored targets represent bona fide virulence targets or guarded decoys. Extensive overlap between PTI and ETI signaling suggests that T3Es may suppress both pathways through common targets and by possessing multiple activities.

Figure 1. The site of action of Pseudomonas syringae T3Es

P. syringae injects type III effectors (T3Es) (red text) into the host cell using a type III secretion system (T3SS). P. syringae PAMPs are recognized by the plant using PAMP RLKs such as FLS2 (light blue) leading to PAMP-triggered immunity (PTI). PTI includes MAP kinase and calcium-dependant protein kinases (CDPKs) signaling leading to the production of reactive oxygen species (ROS) by NADPH oxidases (grey box); accumulation of hormones such as salicylic acid (SA); and alterations in immunity-related transcription and cell wall defenses. T3Es suppress PTI at the level of the PAMP receptor complexes with AvrPto and AvrPtoB targeting the PAMP RLKs themselves including FLS2 and its co-receptor BAK1 (dark blue), while the T3E AvrPphB cleaves the PAMP RLK-associated kinase BIK1 (pink hexagon). HopF2 and HopAI1 inactivate the MAPK cascade by ADP-ribosylating MAP kinase kinases (MAPKK) and dephosphorylating MAP kinases (MAPK), respectively. The T3E HopM1 induces the degradation of the ARF-GEF MIN7 interfering with vesicle trafficking. The T3E HopU1 ADP-ribosylates RNA-binding proteins such as GRP7, likely inhibiting RNA translation. T3Es also target organelles with HopG1 targeting the mitochondria and HopI1 the chloroplasts where it activates Hsp70 and suppresses SA production. The R protein RPS2 (green) recognizes the cleavage of RIN4 by the T3E AvrRpt2 but the T3E HopF2, which ADP-ribosylates RIN4, can prevent this recognition. The R protein RPM1 (turquoise) recognizes hyperphosphorylation of RIN4 induced by the T3Es AvrB and AvrRpm1. AvrB also interacts with RAR1 and MAP kinase 4 (MPK4) that form a complex with RIN4. T3E recognition by R proteins leads to effector-triggered immunity (ETI) that largely overlaps with PTI. See text for additional details.