Phytopathogen type III effector weaponry and their plant targets

Abstract

Phytopathogenic bacteria suppress plant innate immunity and promote pathogenesis by injecting proteins called type III effectors into plant cells using a type III protein secretion system. These type III effectors use at least three strategies to alter host responses. One strategy is to alter host protein turnover, either by direct cleavage or by modulating ubiquitination and targeting the 26S proteasome. Another strategy involves alteration of RNA metabolism by transcriptional activation or ADP-ribosylation of RNA-binding proteins. A third major strategy is to inhibit the kinases involved in plant defence signaling, either by the removal of phosphates or by direct inhibition. The wide array of strategies that bacterial pathogens employ to suppress innate immunity suggest that circumvention of innate immunity is crucial for bacterial pathogenicity of plants.

Fig. 1. Plant targets and activities of type III effectors from phytobacterial pathogens

Bacterial plant pathogens inject many different type III effectors (T3Es) into plant cells via the type III secretion system. The activities of T3Es can be recognized by plant resistance (R) proteins inducing effector-triggered immunity (ETI). The R protein RPM1 causes ETI by recognizing the phosphorylation (P) of RIN4 by the T3Es AvrRpm1 and AvrB, while RPS2 causes ETI upon the cleavage of RIN4 by the T3E AvrRpt2. The T3E AvrPphB degrades the PBS1 kinase inducing RPS5-dependent ETI. The R protein Prf recognizes the interaction of the Pto kinase with AvrPto or AvrPtoB eliciting ETI, however, AvrPtoB ubiquinates (Ub) the Fen kinase targeting it for degradation and preventing recognition by Prf. Plants can also use receptor kinases such as EFR or FLS2 to detect pathogen-associated molecular patterns (PAMPs). This leads to PAMP-triggered immunity (PTI), which like ETI, induces innate immune responses. AvrPto inhibits the kinase activity of Pto, FLS2, and EFR. The HopAI1 T3E is a phosphothreonine lyase that suppresses MAPKs. The HopAO1 T3E is a protein tyrosine phosphatase whose target is unknown. The HopU1 T3E is a mono-ADP-ribosyltransferase that modifies GRP7 glycine-rich RNA-binding protein and likely prevents it from binding RNA. The HopM1 T3E causes the ubiquination and degradation via the 26S proteasome of AtMIN7, which may be involved in vesicle trafficking. The GALA T3Es contain F-box domains and can interact with plant ASK proteins (part of an SCF-type E3 ubiquitin ligase complex). GALAs are predicted to change the ubiquitination status of host proteins. The T3Es XopD and AvrXv4, which function in different locations in the plant cell, are isopeptidases that remove SUMO (Su) from host proteins. The chloroplast localized, J domain-containing T3E HopI1, suppresses salicylic acid (SA) production and may associate with Hsp70. T3Es AvrBs3, PthXo6/7 and HsvG/B bind to specific promoters in the nucleus inducing the transcription of genes favoring pathogenesis. Broken lines indicate plant responses and solid lines T3E activities.