A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity

Abstract

Many bacterial pathogens of plants and animals use a type III secretion system to deliver diverse virulence-associated 'effector' proteins into the host cell. The mechanisms by which these effectors act are mostly unknown; however, they often promote disease by suppressing host immunity. One type III effector, AvrPtoB, expressed by the plant pathogen Pseudomonas syringae pv. tomato, has a carboxy-terminal domain that is an E3 ubiquitin ligase. Deletion of this domain allows an amino-terminal region of AvrPtoB (AvrPtoB(1-387)) to be detected by certain tomato varieties leading to immunity-associated programmed cell death. Here we show that a host kinase, Fen, physically interacts with AvrPtoB(1-387 )and is responsible for activating the plant immune response. The AvrPtoB E3 ligase specifically ubiquitinates Fen and promotes its degradation in a proteasome-dependent manner. This degradation leads to disease susceptibility in Fen-expressing tomato lines. Various wild species of tomato were found to exhibit immunity in response to AvrPtoB(1-387 )and not to full-length AvrPtoB. Thus, by acquiring an E3 ligase domain, AvrPtoB has thwarted a highly conserved host resistance mechanism.

Crystal Structure of the Complex between Pseudomonas Effector AvrPtoB and the Tomato Pto Kinase Reveals Both a Shared and a Unique Interface Compared with AvrPto-Pto

“…The observation that the F173A in AvrPtoB affects both virulence and avirulence activities suggests that the virulence target of AvrPtoB 1-307 might be a Pto-related protein, or at least a protein kinase. Indeed, AvrPtoB appears to preferentially interact with kinases for both its avirulence and virulence activities (Rosebrock et al, 2007;Gö hre et al, 2008;Shan et al, 2008).…”

“…A longer N-terminal region, AvrPtoB 1-387 (but not AvrPtoB 1-307 ), is able to suppress certain PTI responses in Arabidopsis (He et al, 2006) by directly interacting with BAK1 (Shan et al, 2008). The same AvrPtoB fragment was recently shown to interact with Fen, activating Prf-dependent resistance to Pst (Rosebrock et al, 2007). A C-terminal domain of AvrPtoB has evolved to be an E3 ubiquitin ligase that targets Fen for degradation in a proteasome-dependent manner, disrupting Fen-mediated resistance Janjusevic et al, 2006;Rosebrock et al, 2007).…”

“…The same AvrPtoB fragment was recently shown to interact with Fen, activating Prf-dependent resistance to Pst (Rosebrock et al, 2007). A C-terminal domain of AvrPtoB has evolved to be an E3 ubiquitin ligase that targets Fen for degradation in a proteasome-dependent manner, disrupting Fen-mediated resistance Janjusevic et al, 2006;Rosebrock et al, 2007). Elimination of Fen allows the PTI-suppressing ability of AvrPtoB 1-387 to function.…”

Effector Biology of Plant-Associated Organisms: Concepts and Perspectives

“…Many pathogen effectors are extraordinary examples of biological innovation; they include some of the most remarkable proteins known to function inside plant cells. Among such remarkable effectors, we highlight the transcription activator-like (TAL) effectors of Xanthomonas bacteria, modular proteins that bind specific plant promoter elements to activate plant gene transcription (Boch et al 2009); the bacterial effectors AvrPtoB and coronatine, which mimic plant E3 ubiquitin ligases (Janjusevic et al 2006;Rosebrock et al 2007) and the hormone Figure 1. The concept of effectors in plant immunity.…”

Pseudomonas syringae type III effector HopAF1 suppresses plant immunity by targeting methionine recycling to block ethylene induction

“…T3Es commonly contain sequences addressing specific eukaryotic subcellular localizations (10,11) and enzymatic activities (12)(13)(14)(15)(16)(17) that disrupt and/or suppress PTI. Known targets of T3Es include plasma membrane-localized receptor complexes (13,(18)(19)(20)(21)(22)(23), downstream MAPK cascades (24,25), the stability of defenserelated transcripts (26), phytoalexin biosynthesis (27), and vesicle trafficking (28).…”