Two Pseudomonas syringae Type III Effectors Inhibit RIN4-Regulated Basal Defense in Arabidopsis

Kim, Min Gab; Cunha, Luis da; McFall, Aidan J.; Belkhadir, Youssef; DebRoy, Sruti; Dangl, Jeffrey L.; Mackey, David

doi:10.1016/j.cell.2005.03.025

Cited by 422 publications

(382 citation statements)

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“…Taken together, we propose that by changing the relative concentration of the RIN4-NDR1 interaction, modulation of the activation status of RPS2 in the absence of bacterial pathogen occurs as a result of shifting the balance of RIN4 from RPS2 to NDR1 and vice versa. While much work remains to be done to fully understand the stoichiometry of the protein-protein interactions associated with resistance signaling in plant defense, the association of RIN4 with multiple protein components required for resistance signaling lends itself to the possibility that RIN4 may exert its activity as a molecular switch by regulating various proteins involved in a number of effector-mediated and basal defense responses (Kim et al, 2005b).…”

Section: Discussionmentioning

confidence: 99%

NDR1 Interaction with RIN4 Mediates the Differential Activation of Multiple Disease Resistance Pathways in Arabidopsis

2006

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Recognition of pathogens by plants involves the coordinated efforts of molecular chaperones, disease resistance (R) proteins, and components of disease resistance signaling pathways. Characterization of events associated with pathogen perception in Arabidopsis thaliana has advanced understanding of molecular genetic mechanisms associated with disease resistance and protein interactions critical for the activation of resistance signaling. Regulation of R protein-mediated signaling in response to the bacterial pathogen Pseudomonas syringae in Arabidopsis involves the physical association of at least two R proteins with the negative regulator RPM1 INTERACTING PROTEIN4 (RIN4). While the RIN4-RPS2 (for RESISTANCE TO P. SYRINGAE2) and RIN4-RPM1 (for RESISTANCE TO P. SYRINGAE PV MACULICOLA1) signaling pathways exhibit differential mechanisms of activation in terms of effector action, the requirement for NON-RACE-SPECIFIC DISEASE RESISTANCE1 (NDR1) is shared. Using a yeast two-hybrid screen, followed by a series of coimmunoprecipitation experiments, we demonstrate that the RIN4-NDR1 interaction occurs on the cytoplasmically localized N-terminal portion of NDR1 and that this interaction is required for the activation of resistance signaling following infection by P. syringae expressing the Cys protease Type III effector protein AvrRpt2. We demonstrate that like RPS2 and RPM1, NDR1 also associates with RIN4 in planta. We suggest that this interaction serves to further regulate activation of disease resistance signaling following recognition of P. syringae DC3000-AvrRpt2 by Arabidopsis.

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Section: Discussionmentioning

confidence: 99%

NDR1 Interaction with RIN4 Mediates the Differential Activation of Multiple Disease Resistance Pathways in Arabidopsis

2006

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“…The significantly enhanced growth of both virulent (Pst and Psm) and nonpathogenic (hrcC) P. syringae strains on cds2-1D in comparison to wild-type Col-0 indicates an ABA effect on suppression of the nonspecific basal resistance against bacterial infection, which is consistent with the observation that suppression of Pst growth by treatment with bacterial MAMP (flg22 peptide) was attenuated in the cds2-D mutant. Previous studies showed that treatment of Arabidopsis plants with flg22 peptide or the nonpathogenic hrcC strain of Pst may lead to callose-associated cell wall modification (Gó mez-Gó mez et al, 1999; Hauck et al, 2003), and this extracellular defense response is suppressed by wild-type pathogenic bacteria or overexpression in planta of bacterial TTSS effectors (Hauck et al, 2003;Kim et al, 2005). Recent data showed that wild-type Pst enhances callose deposition in Arabidopsis mutants impaired in ABA biosynthesis or signaling, and exogenous ABA suppresses flg22 peptide induced callose deposition in wild-type Arabidopsis seedlings (de Torres-Zabala et al, 2007Clay et al, 2009), indicating a negative role of ABA in activation of callose deposition.…”

Section: Aba Modulation Of Plant Disease Resistance Mechanismsmentioning

confidence: 99%

Abscisic Acid Has a Key Role in Modulating Diverse Plant-Pathogen Interactions

et al. 2009

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We isolated an activation-tagged Arabidopsis (Arabidopsis thaliana) line, constitutive disease susceptibility2-1D (cds2-1D), that showed enhanced bacterial growth when challenged with various Pseudomonas syringae strains. Systemic acquired resistance and systemic PATHOGENESIS-RELATED GENE1 induction were also compromised in cds2-1D. The T-DNA insertion adjacent to NINE-CIS-EPOXYCAROTENOID DIOXYGENASE5 (NCED5), one of six genes encoding the abscisic acid (ABA) biosynthetic enzyme NCED, caused a massive increase in transcript level and enhanced ABA levels .2-fold. Overexpression of NCED genes recreated the enhanced disease susceptibility phenotype. NCED2, NCED3, and NCED5 were induced, and ABA accumulated strongly following compatible P. syringae infection. The ABA biosynthetic mutant aba3-1 showed reduced susceptibility to virulent P. syringae, and ABA, whether through exogenous application or endogenous accumulation in response to mild water stress, resulted in increased bacterial growth following challenge with virulent P. syringae, indicating that ABA suppresses resistance to P. syringae. Likewise ABA accumulation also compromised resistance to the biotrophic oomycete Hyaloperonospora arabidopsis, whereas resistance to the fungus Alternaria brassicicola was enhanced in cds2-1D plants and compromised in aba3-1 plants, indicating that ABA promotes resistance to this necrotroph. Comparison of the accumulation of salicylic acid and jasmonic acid in the wild type, cds2-1D, and aba3-1 plants challenged with P. syringae showed that ABA promotes jasmonic acid accumulation and exhibits a complex antagonistic relationship with salicylic acid. Our findings provide genetic evidence that the abiotic stress signal ABA also has profound roles in modulating diverse plantpathogen interactions mediated at least in part by cross talk with the jasmonic acid and salicylic acid biotic stress signal pathways.

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“…The rin4 rps2 mutant also exhibits enhanced resistance to virulent bacteria (Belkhadir et al, 2004;Kim et al, 2005b). Therefore, we next challenged the 35S-GmRIN4b rin4 rps2 and 35S-GmRIN4a rin4 rps2 transgenic plants with a virulent strain (DC3000) of P. syringae.…”

Section: Gmrin4b Complements the Arabidopsis Rin4 Mutationmentioning

confidence: 99%

“…The RIN4 protein also mediates basal defense in Arabidopsis (Kim et al, 2005b). Therefore, we next tested basal resistance in S 4a and S 4b plants to virulent (vir) strains of P. syringae pv glycinea race 4 and the oomycete P. sojae.…”

Section: Gmrin4a and Gmrin4b Mediate Basal Resistance In Soybeanmentioning

confidence: 99%

“…This led to the suggestion that R proteins monitor the presence of Avr proteins by "guarding" other host proteins targeted by the pathogen effector (Van der Biezen and Jones, 1998;Innes, 2004;Jones and Dangl, 2006). Avr proteins enhance pathogen virulence in genetic backgrounds lacking cognate R proteins by targeting components of the host basal defense machinery, including "guardee" proteins (Chang et al, 2000;Guttman and Greenberg, 2001;Chen et al, 2004, Kim et al, 2005bOng and Innes, 2006;van Esse et al, 2007;Shan et al, 2008;Xiang et al, 2008). However, some Avr proteins were found to also target host proteins that do not contribute to the virulence function of the effector (Shang et al, 2006;Shabab et al, 2008;Zhou and Chai, 2008;Zipfel and Rathjen, 2008).…”

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confidence: 99%

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RPG1-B-Derived Resistance to AvrB-Expressing Pseudomonas syringae Requires RIN4-Like Proteins in Soybean

Selote

Kachroo

2010

Plant Physiology

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Soybean (Glycine max) RPG1-B (for resistance to Pseudomonas syringae pv glycinea) mediates species-specific resistance to P. syringae expressing the avirulence protein AvrB, similar to the nonorthologous RPM1 in Arabidopsis (Arabidopsis thaliana). RPM1-derived signaling is presumably induced upon AvrB-derived modification of the RPM1-interacting protein, RIN4 (for RPM1-interacting 4). We show that, similar to RPM1, RPG1-B does not directly interact with AvrB but associates with RIN4-like proteins from soybean. Unlike Arabidopsis, soybean contains at least four RIN4-like proteins (GmRIN4a to GmRIN4d). GmRIN4b, but not GmRIN4a, complements the Arabidopsis rin4 mutation. Both GmRIN4a and GmRIN4b bind AvrB, but only GmRIN4b binds RPG1-B. Silencing either GmRIN4a or GmRIN4b abrogates RPG1-B-derived resistance to P. syringae expressing AvrB. Binding studies show that GmRIN4b interacts with GmRIN4a as well as with two other AvrB/RPG1-B-interacting isoforms, GmRIN4c and GmRIN4d. The lack of functional redundancy among GmRIN4a and GmRIN4b and their abilities to interact with each other suggest that the two proteins might function as a heteromeric complex in mediating RPG1-B-derived resistance. Silencing GmRIN4a or GmRIN4b in rpg1-b plants enhances basal resistance to virulent strains of P. syringae and the oomycete Phytophthora sojae. Interestingly, GmRIN4a- or GmRIN4b-silenced rpg1-b plants respond differently to AvrB-expressing bacteria. Although both GmRIN4a and GmRIN4b function to monitor AvrB in the presence of RPG1-B, GmRIN4a, but not GmRIN4b, negatively regulates AvrB virulence activity in the absence of RPG1-B.

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Two Pseudomonas syringae Type III Effectors Inhibit RIN4-Regulated Basal Defense in Arabidopsis

Cited by 422 publications

References 55 publications

NDR1 Interaction with RIN4 Mediates the Differential Activation of Multiple Disease Resistance Pathways in Arabidopsis

NDR1 Interaction with RIN4 Mediates the Differential Activation of Multiple Disease Resistance Pathways in Arabidopsis

Abscisic Acid Has a Key Role in Modulating Diverse Plant-Pathogen Interactions

RPG1-B-Derived Resistance to AvrB-Expressing Pseudomonas syringae Requires RIN4-Like Proteins in Soybean

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