Direct Interaction between the Tobacco Mosaic Virus Helicase Domain and the ATP-bound Resistance Protein, N Factor during the Hypersensitive Response in Tobacco Plants

Ueda, Hirokazu; Yamaguchi, Yube; Sano, Hiroshi

doi:10.1007/s11103-005-5817-8

Cited by 154 publications

(122 citation statements)

References 52 publications

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“…Direct R-Avr interaction has been detected for seven R proteins: Pi-ta (Jia et al, 2000), RRS1-R (Deslandes et al, 2003), N (Ueda et al, 2006), L5/L6 (Dodds et al, 2006), M (Catanzariti et al, 2010), RPP1 (Krasileva et al, 2010;Chou et al, 2011), and Pik/km/kp/ks/kh (Kanzaki et al, 2012). For some of them, it also has been demonstrated that physical interaction is required for resistance, validating the direct recognition model.…”

Section: Introductionsupporting

confidence: 59%

The Rice Resistance Protein Pair RGA4/RGA5 Recognizes the Magnaporthe oryzae Effectors AVR-Pia and AVR1-CO39 by Direct Binding

et al. 2013

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Resistance (R) proteins recognize pathogen avirulence (Avr) proteins by direct or indirect binding and are multidomain proteins generally carrying a nucleotide binding (NB) and a leucine-rich repeat (LRR) domain. Two NB-LRR protein-coding genes from rice (Oryza sativa), RGA4 and RGA5, were found to be required for the recognition of the Magnaporthe oryzae effector AVR1-CO39. RGA4 and RGA5 also mediate recognition of the unrelated M. oryzae effector AVR-Pia, indicating that the corresponding R proteins possess dual recognition specificity. For RGA5, two alternative transcripts, RGA5-A and RGA5-B, were identified. Genetic analysis showed that only RGA5-A confers resistance, while RGA5-B is inactive. Yeast two-hybrid, coimmunoprecipitation, and fluorescence resonance energy transfer-fluorescence lifetime imaging experiments revealed direct binding of AVR-Pia and AVR1-CO39 to RGA5-A, providing evidence for the recognition of multiple Avr proteins by direct binding to a single R protein. Direct binding seems to be required for resistance as an inactive AVR-Pia allele did not bind RGA5-A. A small Avr interaction domain with homology to the Avr recognition domain in the rice R protein Pik-1 was identified in the C terminus of RGA5-A. This reveals a mode of Avr protein recognition through direct binding to a novel, non-LRR interaction domain.

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Section: Introductionsupporting

confidence: 59%

The Rice Resistance Protein Pair RGA4/RGA5 Recognizes the Magnaporthe oryzae Effectors AVR-Pia and AVR1-CO39 by Direct Binding

et al. 2013

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“…This ligand-receptor model was supported by the fact that some Avr gene products are small and colocalize with R gene products, most of which encode receptor-like proteins carrying Leu-rich repeats (LRRs). Indeed, direct binding of a few R-Avr combinations was found, consistent with a receptor-ligand mode of action (e.g., Jia et al, 2000;Deslandes et al, 2003;Dodds et al, 2006;Ueda et al, 2006). However, for a number of R-Avr combinations, physical interactions have not been observed, and perception is thought to be indirect.…”

mentioning

confidence: 76%

From Guard to Decoy: A New Model for Perception of Plant Pathogen Effectors

2008

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The Guard Model for disease resistance postulates that plant resistance proteins act by monitoring (guarding) the target of their corresponding pathogen effector. We posit, however, that guarded effector targets are evolutionarily unstable in plant populations polymorphic for resistance (R) genes. Depending on the absence or presence of the R gene, guarded effector targets are subject to opposing selection forces (1) to evade manipulation by effectors (weaker interaction) and (2) to improve perception of effectors (stronger interaction). Duplication of the effector target gene or independent evolution of a target mimic could relax evolutionary constraints and result in a decoy that would be solely involved in effector perception. There is growing support for this Decoy Model from four diverse cases of effector perception involving Pto, Bs3, RCR3, and RIN4. We discuss the differences between the Guard and Decoy Models and their variants, hypothesize how decoys might have evolved, and suggest ways to challenge the Decoy Model.

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“…Work on animal NBS-containing proteins and recent work on the I-2 and N proteins of tomato and tobacco has indicated that ATP binding state may play a key role in NBS-LRR protein activation (13,14,22,23). In the I-2 protein, amino acid substitutions that reduce ATP hydrolysis, but not ATP binding, cause constitutive activation of I-2, whereas substitutions that inhibit ATP binding eliminate signaling (14).…”

Section: Pbs1mentioning

confidence: 99%

Indirect activation of a plant nucleotide binding site–leucine-rich repeat protein by a bacterial protease

Ade

DeYoung

Golstein

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

375

404

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Nucleotide binding site-leucine-rich repeat (NBS-LRR) proteins mediate pathogen recognition in both mammals and plants. The molecular mechanisms by which pathogen molecules activate NBS-LRR proteins are poorly understood. Here we show that RPS5, a NBS-LRR protein from Arabidopsis, is activated by AvrPphB, a bacterial protease, via an indirect mechanism. When transiently expressed in Nicotiana benthamiana leaves, full-length RPS5 protein triggered programmed cell death, but only when coexpressed with AvrPphB and a second Arabidopsis protein, PBS1, which is a specific substrate of AvrPphB. Using coimmunoprecipitation analysis, we found that PBS1 is in a complex with the N-terminal coiled coil (CC) domain of RPS5 before exposure to AvrPphB. Deletion of the RPS5 LRR domain caused RPS5 to constitutively activate programmed cell death, even in the absence of AvrPphB and PBS1, and this activation depended on both the CC and NBS domains. The LRR and CC domains both coimmunoprecipitate with the NBS domain but not with each other. Thus, the LRR domain appears to function in part to inhibit RPS5 signaling, and cleavage of PBS1 by AvrPphB appears to release RPS5 from this inhibition. An amino acid substitution in the NBS site of RPS5 that is known to inhibit ATP binding in other NBS-LRR proteins blocked activation of RPS5, whereas a substitution thought to inhibit ATP hydrolysis constitutively activated RPS5. Combined, these data suggest that ATP versus ADP binding functions as a molecular switch that is flipped by cleavage of PBS1.B oth plants and animals employ nucleotide binding siteleucine-rich repeat (NBS-LRR) proteins to mediate detection of pathogen molecules (1). There appear to be at least two distinct mechanisms by which NBS-LRR proteins detect pathogens: either by binding pathogen-derived molecules directly or by sensing the modification of host proteins by pathogen-derived molecules (2). It is presently unclear how either mechanism causes activation of signaling by NBS-LRR proteins. We have been investigating these processes by using the plant NBS-LRR protein RPS5, which mediates detection of the protease AvrPphB from the bacterial pathogen Pseudomonas syringae (3-6).In plants, NBS-LRR proteins were first identified as the products of classically defined disease-resistance genes (R genes) (7-9), which are genes that confer resistance to infection by specific pathogen strains. R gene-mediated resistance is typically manifested by activation of a programmed cell death response referred to as the hypersensitive response (HR) that is localized to the site of pathogen ingress (10). In the last decade, R genes have been cloned from a large range of plant species, with the majority being found to encode NBS-LRR proteins (11). Plant NBS-LRR proteins can be subdivided into two broad categories defined by the presence of a Toll-interleukin receptor (TIR) domain or a non-TIR domain, most often a coiled-coil (CC) domain, at the amino terminus. The function of the CC and TIR domains in pathogen perception and signaling is un...

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Direct Interaction between the Tobacco Mosaic Virus Helicase Domain and the ATP-bound Resistance Protein, N Factor during the Hypersensitive Response in Tobacco Plants

Cited by 154 publications

References 52 publications

The Rice Resistance Protein Pair RGA4/RGA5 Recognizes the Magnaporthe oryzae Effectors AVR-Pia and AVR1-CO39 by Direct Binding

The Rice Resistance Protein Pair RGA4/RGA5 Recognizes the Magnaporthe oryzae Effectors AVR-Pia and AVR1-CO39 by Direct Binding

From Guard to Decoy: A New Model for Perception of Plant Pathogen Effectors

Indirect activation of a plant nucleotide binding site–leucine-rich repeat protein by a bacterial protease

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