The Pseudomonas syringae effector HopF2 suppresses Arabidopsis immunity by targeting BAK1

Abstract

Summary Pseudomonas syringae delivers a plethora of effector proteins into host cells to sabotage immune responses and modulate physiology to favor infection. We have previously shown that P. syringae pv. tomato DC3000 effector HopF2 suppresses Arabidopsis innate immunity triggered by multiple microbe-associated molecular patterns (MAMP) at the plasma membrane. We show here that HopF2 possesses distinct mechanisms in the suppression of two branches of MAMP-activated MAP kinase (MPK) cascades. Besides blocking MKK5 (MPK kinase 5) activation in the MEKK1/MEKKs-MKK4/5-MPK3/6 cascade, HopF2 targets additional component(s) upstream of MEKK1 in the MEKK1-MKK1/2-MPK4 cascade and plasma membrane-localized receptor-like cytoplasmic kinase BIK1 and its homologs. We further show that HopF2 directly targets BAK1, a plasma membrane-localized receptor-like kinase involved in multiple MAMP signaling. The interaction between BAK1 and HopF2 or two other P. syringae effectors AvrPto and AvrPtoB, was confirmed in vivo and in vitro. Consistent with BAK1 as a physiological target of AvrPto, AvrPtoB and HopF2, the strong growth defects or lethality associated with ectopic expression of these effectors in wild-type Arabidopsis transgenic plants were largely alleviated in bak1 mutant plants. Thus, our results provide genetic evidence to further support that BAK1 is a physiological target of AvrPto, AvrPtoB and HopF2. Identification of BAK1 as an additional target of HopF2 virulence not only explains HopF2 suppression of multiple MAMP signaling at the plasma membrane, but also supports the notion that pathogen virulence effectors act through multiple targets in host cells.

An Overdose of the Arabidopsis Coreceptor BRASSINOSTEROID INSENSITIVE1-ASSOCIATED RECEPTOR KINASE1 or Its Ectodomain Causes Autoimmunity in a SUPPRESSOR OF BIR1-1-Dependent Manner

“…Recent observations reinforce the idea that the integrity or activity of multimeric SERK-BIR complexes is guarded by R proteins (Gao et al, 2009;Wang et al, 2011;Halter et al, 2014a). In line with this hypothesis, several microbial effectors have been identified that target BAK1 to defeat plant immunity (Shan et al, 2008;Cheng et al, 2011;Zhou et al, 2014). The constitutive immunity observed in Arabidopsis after BAK1 overexpression shares some common characteristics with the ETI responses (Jones and Dangl, 2006;Tsuda et al, 2013), like the prolonged MAPK activation and the presence of cell death (Figs.…”

Intervention of Phytohormone Pathways by Pathogen Effectors

“…AvrPtoB is known to interact with the BAK1 kinase domain, inhibiting its ability to bind with FLS2/EFR (ELONGATION FACTOR) and elicit PTI, while the mechanism of how AvrPto interferes with BAK1-FLS2 remains unclear (Shan et al, 2008;Cheng et al, 2011). More recently, BAK1 has also been identified as one of the targets of HopF2 (Table 1), another type III effector from P. syringae (Zhou et al, 2014). Xoo2875, a type III effector from the bacterial pathogen X. o. pv oryzae also interacts with OsBAK1 to inhibit innate immunity as well as BR signaling.…”

“…Effector-mediated manipulation of host hormone biology to promote plant growth may benefit pathogens by reducing resources available for the plant to mount an effective defense response De Bruyne et al, 2014;Huot et al, 2014). Furthermore, the versatility of pathogen effectors is evidenced by the demonstration that a single effector can interfere with multiple host targets (Cui et al, 2010;Lindeberg et al, 2012;Raffaele and Rivas, 2013;Zhou et al, 2014). A more complete understanding of the complex interactions of phytohormone signaling networks triggered by pathogen effectors may require the adoption of systems biology approaches (Kim et al, 2014;Naseem et al, 2014).…”

Bacterial AvrRpt2-Like Cysteine Proteases Block Activation of the Arabidopsis Mitogen-Activated Protein Kinases, MPK4 and MPK11

“…Several pathogen effectors target either MAPK cascade components directly or upstream signaling components to suppress defense signaling. Among the latter, the P. syringae effectors AvrPto, AvrPtoB, and HopF2 target PAMP receptor complex components to block PTI signaling (Göhre et al, 2008;Shan et al, 2008;Xiang et al, 2008;Gimenez-Ibanez et al, 2009;Zhou et al, 2014). In addition, HopF2 ADP ribosylates MKK5 (and possibly other MKKs), thereby blocking phosphorylation activity and interfering with immune signaling (Wang et al, 2010).…”