DspA/E, a Type III Effector Essential for <i>Erwinia amylovora</i> Pathogenicity and Growth In Planta, Induces Cell Death in Host Apple and Nonhost Tobacco Plants

Boureau, Tristan; ElMaarouf-Bouteau, Hayat; Garnier, Amélie; Brisset, Marie-Noëlle; Perino, C.; Pucheu, Igor; Barny, Marie‐Anne

doi:10.1094/mpmi-19-0016

Cited by 86 publications

(85 citation statements)

References 52 publications

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“…The comparison of this core effector set to the proteomes of three other plant pathogens from the subgroup of ␥-proteobacteria revealed that an ortholog of one of them, an AvrE/DspA family member (RSp1281), can be found in all these species. This ubiquitous TTSS effector has been shown to be critical for pathogenicity in Erwinia amylovora and Pseudomonas syringae (4,11).…”

Section: Vol 189 2007mentioning

confidence: 99%

Genomic Structure and Phylogeny of the Plant Pathogen Ralstonia solanacearum Inferred from Gene Distribution Analysis

et al. 2007

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In the present study, we investigated the gene distribution among strains of the highly polymorphic plant pathogenic ␤-proteobacterium Ralstonia solanacearum, paying particular attention to the status of known or candidate pathogenicity genes. Based on the use of comparative genomic hybridization on a pangenomic microarray for the GMI1000 reference strain, we have defined the conditions that allowed comparison of the repertoires of genes among a collection of 18 strains that are representative of the biodiversity of the R. solanacearum species. This identified a list of 2,690 core genes present in all tested strains. As a corollary, a list of 2,338 variable genes within the R. solanacearum species has been defined. The hierarchical clustering based on the distribution of variable genes is fully consistent with the phylotype classification that was previously defined from the nucleotide sequence analysis of four genes. The presence of numerous pathogenicity-related genes in the core genome indicates that R. solanacearum is an ancestral pathogen. The results establish the long coevolution of the two replicons that constitute the bacterial genome. We also demonstrate the clustering of variable genes in genomic islands. Most genomic islands are included in regions with an alternative codon usage, suggesting that they originate from acquisition of foreign genes through lateral gene transfers. Other genomic islands correspond to genes that have the same base composition as core genes, suggesting that they either might be ancestral genes lost by deletion in certain strains or might originate from horizontal gene transfers.

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Section: Vol 189 2007mentioning

confidence: 99%

Genomic Structure and Phylogeny of the Plant Pathogen Ralstonia solanacearum Inferred from Gene Distribution Analysis

et al. 2007

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“…Among these effectors, DspA/E has emerged as an indispensable T3-secreted protein that suppresses the host basal defences (DebRoy et al, 2004) and causes cell death in both host and non-host plants (Boureau et al, 2006;Oh et al, 2007), thus enabling and promoting disease. DspA/E is a large (198 kDa) protein that belongs to the AvrE family of effectors and may have multiple functional domains on account of its size (Bogdanove et al, 1998;Gaudriault et al, 1997).…”

Section: Introductionmentioning

confidence: 99%

Secretion and translocation signals and DspB/F-binding domains in the type III effector DspA/E of Erwinia amylovora

Carpenter

Hayes

et al. 2010

Microbiology

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DspA/E is a type III effector of Erwinia amylovora, the bacterial pathogen that causes fire blight disease in roseaceous plants. This effector is indispensable for disease development, and it is translocated into plant cells. A DspA/E-specific chaperone, DspB/F, is necessary for DspA/E secretion and possibly for its translocation. In this work, DspB/F-binding sites and secretion and translocation signals in the DspA/E protein were determined. Based on yeast two-hybrid assays, DspB/F was found to bind DspA/E within the first 210 amino acids of the protein. Surprisingly, both DspB/F and OrfA, the putative chaperone of Eop1, also interacted with the C-terminal 1059 amino acids of DspA/E; this suggests another chaperone-binding site. Secretion and translocation assays using serial N-terminal lengths of DspA/E fused with the active form of AvrRpt2 revealed that at least the first 109 amino acids, including the first N-terminal chaperone-binding motif and DspB/F, were required for efficient translocation of DspA/E, although the first 35 amino acids were sufficient for its secretion and the presence of DspB/F was not required. These results indicate that secretion and translocation signals are present in the N terminus of DspA/E, and that at least one DspB/F-binding motif is required for efficient translocation into plant cells.

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“…Many AvrE family T3Es, including WtsE, have been shown to elicit water-soaked disease symptoms in susceptible host plants and to promote the growth and survival of the bacteria in planta (Bogdanove et al, 1998;Badel et al, 2006;Boureau et al, 2006;Ham et al, 2009). Basal defense, as assessed by callose deposition, was suppressed by DspA/E of E. amylovora in apple and AvrE of P. syringae and WtsE of Pnss in Arabidopsis (DebRoy et al, 2004;Ham et al, 2008).…”

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Perturbation of Maize Phenylpropanoid Metabolism by an AvrE Family Type III Effector fromPantoea stewartii

et al. 2015

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Republic of Korea (S.-M.P., M.G.K.)AvrE family type III effector proteins share the ability to suppress host defenses, induce disease-associated cell death, and promote bacterial growth. However, despite widespread contributions to numerous bacterial diseases in agriculturally important plants, the mode of action of these effectors remains largely unknown. WtsE is an AvrE family member required for the ability of Pantoea stewartii ssp. stewartii (Pnss) to proliferate efficiently and cause wilt and leaf blight symptoms in maize (Zea mays) plants. Notably, when WtsE is delivered by a heterologous system into the leaf cells of susceptible maize seedlings, it alone produces water-soaked disease symptoms reminiscent of those produced by Pnss. Thus, WtsE is a pathogenicity and virulence factor in maize, and an Escherichia coli heterologous delivery system can be used to study the activity of WtsE in isolation from other factors produced by Pnss. Transcriptional profiling of maize revealed the effects of WtsE, including induction of genes involved in secondary metabolism and suppression of genes involved in photosynthesis. Targeted metabolite quantification revealed that WtsE perturbs maize metabolism, including the induction of coumaroyl tyramine. The ability of mutant WtsE derivatives to elicit transcriptional and metabolic changes in susceptible maize seedlings correlated with their ability to promote disease. Furthermore, chemical inhibitors that block metabolic flux into the phenylpropanoid pathways targeted by WtsE also disrupted the pathogenicity and virulence activity of WtsE. While numerous metabolites produced downstream of the shikimate pathway are known to promote plant defense, our results indicate that misregulated induction of phenylpropanoid metabolism also can be used to promote pathogen virulence.

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DspA/E, a Type III Effector Essential for Erwinia amylovora Pathogenicity and Growth In Planta, Induces Cell Death in Host Apple and Nonhost Tobacco Plants

Cited by 86 publications

References 52 publications

Genomic Structure and Phylogeny of the Plant Pathogen Ralstonia solanacearum Inferred from Gene Distribution Analysis

Genomic Structure and Phylogeny of the Plant Pathogen Ralstonia solanacearum Inferred from Gene Distribution Analysis

Secretion and translocation signals and DspB/F-binding domains in the type III effector DspA/E of Erwinia amylovora

Perturbation of Maize Phenylpropanoid Metabolism by an AvrE Family Type III Effector fromPantoea stewartii

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