The atypical resistance gene, <i>RPW8</i>, recruits components of basal defence for powdery mildew resistance in Arabidopsis

Xiao, Shaobo; Çaliş, Özer; Patrick, Elaine; Zhang, Guangmin; Charoenwattana, Piyavadee; Muskett, Paul; Parker, Jane E.; Turner, John G.

doi:10.1111/j.1365-313x.2005.02356.x

Cited by 157 publications

(203 citation statements)

References 73 publications

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“…In addition, edr1 mutants display enhanced growth inhibition and spontaneous cell death in response to drought (Tang et al, 2005b), and enhanced cell death mediated by the RPW8 powdery mildew resistance gene (Xiao et al, 2005). All of these phenotypes, except for ethyleneinduced senescence, can be suppressed by mutations in the SA signaling pathway (sid2, npr1, pad4, and eds1; Frye et al, 2001;Tang et al, 2005b;Xiao et al, 2005). However, edr1 mutant plants do not show constitutive expression of SA-inducible genes when grown under optimal conditions (Frye and Innes, 1998), thus it has been unclear why loss of EDR1 function leads to these various phenotypes.…”

Section: Discussionmentioning

confidence: 99%

Powdery Mildew Resistance Conferred by Loss of the ENHANCED DISEASE RESISTANCE1 Protein Kinase Is Suppressed by a Missense Mutation in KEEP ON GOING, a Regulator of Abscisic Acid Signaling

et al. 2008

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Loss-of-function mutations in the Arabidopsis (Arabidopsis thaliana) ENHANCED DISEASE RESISTANCE1 (EDR1) gene confer enhanced resistance to infection by powdery mildew (Golovinomyces cichoracearum). EDR1 encodes a protein kinase, but its substrates and the pathways regulated by EDR1 are unknown. To identify components of the EDR1 signal transduction pathway(s), we conducted a forward genetic screen for mutations that suppressed edr1-mediated disease resistance. Genetic mapping and cloning of one of these suppressor mutations revealed a recessive missense mutation in the KEEP ON GOING gene (KEG; At5g13530), which we designated keg-4. KEG encodes a multidomain protein that includes a RING E3 ligase domain, a kinase domain, ankyrin repeats, and HERC2-like repeats. The KEG protein has previously been shown to have ubiquitin ligase activity and to negatively regulate protein levels of the transcription factor ABCISIC ACID INSENSITIVE5. KEG mRNA levels were found to be 3-fold higher in edr1 mutant plants compared to wild type. Loss-of-function mutations in KEG are seedling lethal and are hypersensitive to glucose and abscisic acid (ABA). The keg-4 mutation, in contrast, conferred resistance to 6% glucose and suppressed edr1-mediated hypersensitivity to ABA, suggesting that the keg-4 mutation suppresses ABA signaling by altering KEG function. Several ABA-responsive genes were found to be further up-regulated in the edr1 mutant following ABA treatment, and this up-regulation was suppressed by the keg-4 mutation. We conclude that edr1-mediated resistance to powdery mildew is mediated, in part, by enhanced ABA signaling.

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Section: Discussionmentioning

confidence: 99%

Powdery Mildew Resistance Conferred by Loss of the ENHANCED DISEASE RESISTANCE1 Protein Kinase Is Suppressed by a Missense Mutation in KEEP ON GOING, a Regulator of Abscisic Acid Signaling

et al. 2008

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“…The newly obtained accessions were tested with E. cichoracearum UCSC1 three times using the method previously described (Xiao et al 2003(Xiao et al , 2005. Among the 51 accessions surveyed, there was a range of disease reaction (DR) phenotypes from very resistant to very susceptible.…”

Section: Methodsmentioning

confidence: 99%

“…How powdery mildew pathogens cause disease and how RPW8 detects the pathogens and induces resistance in A. thaliana are not clear. However, RPW8 appears to activate defense through a conserved signaling pathway that is also utilized by a subset of NBS-LRR R genes (Xiao et al 2003(Xiao et al , 2005. Our previous evolutionary analysis indicated that the origin of the RPW8 locus is relatively young, probably after the separation of Arabidopsis from the Brassica lineages and that RPW8.1 and RPW8.2 evolved from an HR3-like progenitor gene by duplication and functional diversification (Xiao et al 2004).…”

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confidence: 99%

Intraspecific Genetic Variations, Fitness Cost and Benefit of RPW8, A Disease Resistance Locus in Arabidopsis thaliana

et al. 2007

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The RPW8 locus of Arabidopsis thaliana confers broad-spectrum resistance to powdery mildew pathogens. In many A. thaliana accessions, this locus contains two homologous genes, RPW8.1 and RPW8.2. In some susceptible accessions, however, these two genes are replaced by HR4, a homolog of RPW8.1. Here, we show that RPW8.2 from A. lyrata conferred powdery mildew resistance in A. thaliana, suggesting that RPW8.2 might have gained the resistance function before the speciation of A. thaliana and A. lyrata. To investigate how RPW8 has been maintained in A. thaliana, we examined the nucleotide sequence polymorphisms in RPW8 from 51 A. thaliana accessions, related disease reaction phenotypes to the evolutionary history of RPW8.1 and RPW8.2, and identified mutations that confer phenotypic variations. The average nucleotide diversities were high at RPW8.1 and RPW8.2, showing no sign of selective sweep. Moreover, we found that expression of RPW8 incurs fitness benefits and costs on A. thaliana in the presence and absence of the pathogens, respectively. Our results suggest that polymorphisms at the RPW8 locus in A. thaliana may have been maintained by complex selective forces, including those from the fitness benefits and costs both associated with RPW8.

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“…G. cichoracearum UCSC1 causes powdery mildew disease on some Brassicaceae and Cucurbitaceae species (Adam et al, 1999;Braun et al, 2002), and can establish either incompatible or compatible interactions with different Arabidopsis accessions (Adam and Somerville, 1996). Resistance against different Golovinomyces species is mediated by monogenic traits (Xiao et al, 1997(Xiao et al, , 2001Adam et al, 1999) such as that conferred by the RPW8 locus, which encodes a small novel protein conferring resistance against a wide range of powdery mildews (Xiao et al, 2001(Xiao et al, , 2005. In contrast, the conditions promoting compatibility have been less well characterized.…”

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confidence: 99%

Genome-Wide Expression Profiling Arabidopsis at the Stage ofGolovinomyces cichoracearumHaustorium Formation

et al. 2008

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(T.S., K.D.)Compatibility between plants and obligate biotrophic fungi requires fungal mechanisms for efficiently obtaining nutrients and counteracting plant defenses under conditions that are expected to induce changes in the host transcriptome. A key step in the proliferation of biotrophic fungi is haustorium differentiation. Here we analyzed global gene expression patterns in Arabidopsis thaliana leaves during the formation of haustoria by Golovinomyces cichoracearum. At this time, the endogenous levels of salicylic acid (SA) and jasmonic acid (JA) were found to be enhanced. The responses of wild-type, npr1-1, and jar1-1 plants were used to categorize the sensitivity of gene expression changes to NPR1 and JAR1, which are components of the SA and JA signaling pathways, respectively. We found that the infection process was the major source of variation, with 70 genes identified as having similarly altered expression patterns regardless of plant genotype. In addition, principal component analysis (PCA) identified genes responding both to infection and to lack of functional JAR1 (17 genes) or NPR1 (18 genes), indicating that the JA and SA signaling pathways function as secondary sources of variation. Participation of these genes in the SA or JA pathways had not been described previously. We found that some of these genes may be sensitive to the balance between the SA and JA pathways, representing novel markers for the elucidation of cross-talk points between these signaling cascades. Conserved putative regulatory motifs were found in the promoter regions of each subset of genes. Collectively, our results indicate that gene expression changes in response to infection by obligate biotrophic fungi may support fungal nutrition by promoting alterations in host metabolism. In addition, these studies provide novel markers for the characterization of defense pathways and susceptibility features under this infection condition.

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The atypical resistance gene, RPW8, recruits components of basal defence for powdery mildew resistance in Arabidopsis

Cited by 157 publications

References 73 publications

Powdery Mildew Resistance Conferred by Loss of the ENHANCED DISEASE RESISTANCE1 Protein Kinase Is Suppressed by a Missense Mutation in KEEP ON GOING, a Regulator of Abscisic Acid Signaling

Powdery Mildew Resistance Conferred by Loss of the ENHANCED DISEASE RESISTANCE1 Protein Kinase Is Suppressed by a Missense Mutation in KEEP ON GOING, a Regulator of Abscisic Acid Signaling

Intraspecific Genetic Variations, Fitness Cost and Benefit of RPW8, A Disease Resistance Locus in Arabidopsis thaliana

Genome-Wide Expression Profiling Arabidopsis at the Stage ofGolovinomyces cichoracearumHaustorium Formation

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