Specific Targeting of the<i>Arabidopsis</i>Resistance Protein RPW8.2 to the Interfacial Membrane Encasing the Fungal Haustorium Renders Broad-Spectrum Resistance to Powdery Mildew

Wang, Wenming; Wen, Ying-Qiang; Berkey, Robert; Xiao, Shaobo

doi:10.1105/tpc.109.067587

Cited by 174 publications

(218 citation statements)

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“…To identify additional amino acid substitutions likely responsible for the pronounced SHL and fungus-induced massive HR cell death phenotype of the Bg-1 accession (Orgil et al, 2007;Wang et al, 2009), we constructed RPW8.2 mutants carrying multiple-site substitutions (Table 1) by overlapping PCR using a fragment from R82 Bg-1 that contains the desired mutations and an overlapping fragment(s) from R82 Ms-0 for the rest. While T1 lines transgenic for R82 H19Q/S45T/V50I/Q52K/E59K showed phenotypes similar to those of the R82 Ms-0 wild-type control lines, adding T64S and F56L to this mutant construct resulted in enhanced SHL and HR in the T1 lines comparable to that seen in T1 plants transgenic for R82 T64S (Table 1).…”

Section: Resultsmentioning

confidence: 99%

“…One defense is the hypersensitive response (HR), which is rapid production of reactive oxygen species (e.g., hydrogen peroxide [H 2 O 2 ]), and subsequent collapse of the invaded cell (Xiao et al, 2001(Xiao et al, , 2003. Another defense strategy is the encasement of the haustorium complex by a cell wall-like structure, which conceivably constrains the haustorium while keeping the host cell alive (Meyer et al, 2009;Wang et al, 2009;Wen et al, 2011). The callosic haustorial encasement is similar to the papilla in structure and may be extended from the papilla by rim growth (Meyer et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

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A Comprehensive Mutational Analysis of the Arabidopsis Resistance Protein RPW8.2 Reveals Key Amino Acids for Defense Activation and Protein Targeting

et al. 2013

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The Arabidopsis thaliana RESISTANCE TO POWDERY MILDEW8.2 (RPW8.2) protein is specifically targeted to the extrahaustorial membrane (EHM) encasing the haustorium, or fungal feeding structure, where RPW8.2 activates broad-spectrum resistance against powdery mildew pathogens. How RPW8.2 activates defenses at a precise subcellular locale is not known. Here, we report a comprehensive mutational analysis in which more than 100 RPW8.2 mutants were functionally evaluated for their defense and trafficking properties. We show that three amino acid residues (i.e., threonine-64, valine-68, and aspartic acid-116) are critical for RPW8.2-mediated cell death and resistance to powdery mildew (Golovinomyces cichoracearum UCSC1). Also, we reveal that two arginine (R)-or lysine (K)-enriched short motifs (i.e., R/K-R/K-x-R/K) make up the likely core EHM-targeting signals, which, together with the N-terminal transmembrane domain, define a minimal sequence of 60 amino acids that is necessary and sufficient for EHM localization. In addition, some RPW8.2 mutants localize to the nucleus and/or to a potentially novel membrane that wraps around plastids or plastid-derived stromules. Results from this study not only reveal critical amino acid elements in RPW8.2 that enable haustorium-targeted trafficking and defense, but also provide evidence for the existence of a specific, EHM-oriented membrane trafficking pathway in leaf epidermal cells invaded by powdery mildew.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

A Comprehensive Mutational Analysis of the Arabidopsis Resistance Protein RPW8.2 Reveals Key Amino Acids for Defense Activation and Protein Targeting

et al. 2013

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“…hordei (Bgh; Miklis et al, 2007). The localization of RPW8.2 to the membrane surrounding the powdery mildew fungal haustorium is inhibited by the overexpression of Arabidopsis ADF6 but not by the overexpression of ADF5 (Wang et al, 2009). The mutant adf4 shows increased susceptibility to the bacterial pathogen Pseudomonas syringae pv tomato (Pst) DC3000 avirulent strain carrying AvrPphB but not to virulent Pst or avirulent Pst DC3000 carrying AvrRpt2 or AvrB (Tian et al, 2009;Porter et al, 2012).…”

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confidence: 99%

Nuclear Function of Subclass I Actin-Depolymerizing Factor Contributes to Susceptibility in Arabidopsis to an Adapted Powdery Mildew Fungus

2016

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Actin-depolymerizing factors (ADFs) are conserved proteins that function in regulating the structure and dynamics of actin microfilaments in eukaryotes. In this study, we present evidence that Arabidopsis (Arabidopsis thaliana) subclass I ADFs, particularly ADF4, functions as a susceptibility factor for an adapted powdery mildew fungus. The null mutant of ADF4 significantly increased resistance against the adapted powdery mildew fungus Golovinomyces orontii. The degree of resistance was further enhanced in transgenic plants in which the expression of all subclass I ADFs (i.e. ADF1-ADF4) was suppressed. Microscopic observations revealed that the enhanced resistance of adf4 and ADF1-4 knockdown plants (ADF1-4Ri) was associated with the accumulation of hydrogen peroxide and cell death specific to G. orontii-infected cells. The increased resistance and accumulation of hydrogen peroxide in ADF1-4Ri were suppressed by the introduction of mutations in the salicylic acid-and jasmonic acid-signaling pathways but not by a mutation in the ethylene-signaling pathway. Quantification by microscopic images detected an increase in the level of actin microfilament bundling in ADF1-4Ri but not in adf4 at early G. orontii infection time points. Interestingly, complementation analysis revealed that nuclear localization of ADF4 was crucial for susceptibility to G. orontii. Based on its G. orontii-infected-cell-specific phenotype, we suggest that subclass I ADFs are susceptibility factors that function in a direct interaction between the host plant and the powdery mildew fungus.Powdery mildew is an obligate biotrophic fungal pathogen that infects approximately 10,000 plant species, including crops, vegetables, and ornamental plants, thus causing extensive economic losses worldwide (Takamatsu, 2004). In an effort to understand the plant response to powdery mildew fungal infection and the mechanism of plant-powdery mildew fungus interactions, many mutants of host plants, particularly the model plant Arabidopsis (Arabidopsis thaliana), have been identified and analyzed.Genes for which loss causes increased resistance to a pathogen could encode factors involved in the suppression of plant immunity or susceptibility factors that function in support of the pathogenic infection. Previously identified Arabidopsis genes, the loss of whose expression causes enhanced resistance against adapted powdery mildew fungi, include POWDERY MILDEW RESISTANT1 (PMR1)

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“…Earlier studies demonstrated the hydrogenperoxide accumulates in response to biotrophic pathogen invasion (Wang et al, 2009). Therefore, we tested the location of the increased H 2 O 2 in wild type non-transgenic plants in response to O. neolycopersici.…”

Section: Resultsmentioning

confidence: 99%

“…Earlier results showed that biotrophic fungus infection induce hydrogen-peroxide accumulation at the site of infection (Wang et al, 2009). Observation of infected wildtype non transgenic plants lead to recognize, the increased H 2 O 2 is constricted around the developed haustorium, in the extrahaustorial matrix.…”

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confidence: 99%

Regulation of the JUB1 stress-related transcription factor in Arabidopsis thaliana in response to biotrophic fungus Oidium neolycopersici

Tóth

Kiss

2015

Columella

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Biotic stresses influence fitness of the plants and may decrease their productivity. Especially biotrophic fungi govern complex regulation of host metabolism to fulfill their nutritional needs, while the plant tries to avoid this fungal activity. The defense system of the plant may involve transcription of stress-dependent genes, activation of signaling pathways or production of antimicrobial compounds. The responsible signal molecule in biotrophic pathogen-host interaction was found to be mostly the salicylic acid (SA). We studied here, whether the salicylic acid (SA) is required for the induction of a stress-related transcription factor JUB1 by the biotrophic fungus of tomato Oidium neolycopersici or not. To prove the regulation of JUB1, we isolated the upstream region of the gene and transcriptionally fused to gus reporter gene. This promoter::reporter fusion was then transferred into wild type and two salicylic acid insensitive mutants of Arabidopsis thaliana (nim1-1 and nahG). The transgenic plants were infected by powdery mildew (PM) O. neolycopersici. We found an obvious increase of reporter gene expression in all three lines mostly at the area, where the pathogen was contacted to the plants. Based on the result, the stress-dependent JUB1 transcription factor is probably not influenced by the SA mutations of nim1-1 and nahG. However, the induction appeared along with hydrogen-peroxide development, which suggests that this gene regulation in response to powdery mildew is probably regulated via H 2 O 2 and not by SA signaling.

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Specific Targeting of theArabidopsisResistance Protein RPW8.2 to the Interfacial Membrane Encasing the Fungal Haustorium Renders Broad-Spectrum Resistance to Powdery Mildew

Cited by 174 publications

References 66 publications

A Comprehensive Mutational Analysis of the Arabidopsis Resistance Protein RPW8.2 Reveals Key Amino Acids for Defense Activation and Protein Targeting

A Comprehensive Mutational Analysis of the Arabidopsis Resistance Protein RPW8.2 Reveals Key Amino Acids for Defense Activation and Protein Targeting

Nuclear Function of Subclass I Actin-Depolymerizing Factor Contributes to Susceptibility in Arabidopsis to an Adapted Powdery Mildew Fungus

Regulation of the JUB1 stress-related transcription factor in Arabidopsis thaliana in response to biotrophic fungus Oidium neolycopersici

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