scholarly journals The Majority of the Type III Effector Inventory of Pseudomonas syringae pv. tomato DC3000 Can Suppress Plant Immunity

2009 ◽  
Vol 22 (9) ◽  
pp. 1069-1080 ◽  
Author(s):  
Ming Guo ◽  
Fang Tian ◽  
Yashitola Wamboldt ◽  
James R. Alfano
Keyword(s):  
Pseudomonas Syringae ◽  
Plant Immunity ◽  
In Planta ◽  
Tomato Dc3000 ◽  
Type Iii Effector ◽  
Type Iii Effectors ◽  
Type Iii ◽  
Molecular Pattern ◽  
Effector Triggered Immunity ◽  
Type Iii Protein Secretion

The Pseudomonas syringae type III protein secretion system (T3SS) and the type III effectors it injects into plant cells are required for plant pathogenicity and the ability to elicit a hypersensitive response (HR). The HR is a programmed cell death that is associated with effector-triggered immunity (ETI). A primary function of P. syringae type III effectors appears to be the suppression of ETI and pathogen-associated molecular pattern–triggered immunity (PTI), which is induced by conserved molecules on microorganisms. We reported that seven type III effectors from P. syringae pv. tomato DC3000 were capable of suppressing an HR induced by P. fluorescens(pHIR11) and have now tested 35 DC3000 type III effectors in this assay, finding that the majority of them can suppress the HR induced by HopA1. One newly identified type III effector with particularly strong HR suppression activity was HopS2. We used the pHIR11 derivative pLN1965, which lacks hopA1, in related assays and found that a subset of the type III effectors that suppressed HopA1-induced ETI also suppressed an ETI response induced by AvrRpm1 in Arabidopsis thaliana. A. thaliana plants expressing either HopAO1 or HopF2, two type III effectors that suppressed the HopA1-induced HR, were reduced in the flagellin-induced PTI response as well as PTI induced by other PAMPs and allowed enhanced in planta growth of P. syringae. Collectively, our results suggest that the majority of DC3000 type III effectors can suppress plant immunity. Additionally, the construct pLN1965 will likely be a useful tool in determining whether other type III effectors or effectors from other types of pathogens can suppress either ETI, PTI, or both.

scholarly journals Metaeffector interactions modulate the type III effector-triggered immunity load of Pseudomonas syringae

2021 ◽  
Author(s):  
Alexandre Martel ◽  
Bradley Laflamme ◽  
Clare Breit-McNally ◽  
Darrell Desveaux ◽  
David S Guttman
Keyword(s):  
Arabidopsis Thaliana ◽  
Pseudomonas Syringae ◽  
Plant Pathogen ◽  
Species Complex ◽  
Plant Immunity ◽  
Prior Work ◽  
Tomato Dc3000 ◽  
Type Iii ◽  
Effector Triggered Immunity ◽  
Bacterial Plant Pathogen

The bacterial plant pathogen Pseudomonas syringae requires type III secreted effectors (T3SEs) for pathogenesis. However, a major facet of plant immunity entails the recognition of a subset of P. syringae's T3SEs by intracellular host receptors in a process called Effector-Triggered Immunity (ETI). Prior work has shown that ETI-eliciting T3SEs are pervasive in the P. syringae species complex raising the question of how P. syringae mitigates its ETI load to become a successful pathogen. While pathogens can evade ETI by T3SE mutation, recombination, or loss, there is increasing evidence that effector-effector (a.k.a., metaeffector) interactions can suppress ETI. To study the ETI-suppression potential of P. syringae T3SE repertoires, we compared the ETI-elicitation profiles of two genetically divergent strains: P. syringae pv. tomato DC3000 (PtoDC3000) and P. syringae pv. maculicola ES4326 (PmaES4326), which are both virulent on Arabidopsis thaliana but harbour largely distinct effector repertoires. Of the 529 T3SE alleles screened on A. thaliana Col-0 from the P. syringae T3SE compendium (PsyTEC) [1], 69 alleles from 21 T3SE families elicited ETI in at least one of the two strain backgrounds, while 50 elicited ETI in both backgrounds, resulting in 19 differential ETI responses including two novel ETI-eliciting families: AvrPto1 and HopT1. Although most of these differences were quantitative, three ETI responses were completely absent in one of the pathogenic backgrounds. We performed ETI suppression screens to test if metaeffector interactions contributed to these ETI differences, and found that HopQ1a suppressed AvrPto1m-mediated ETI, while HopG1c and HopF1g suppressed HopT1b-mediated ETI. Overall, these results show that P. syringae strains leverage metaeffector interactions and ETI suppression to overcome the ETI load associated with their native T3SE repertoires.

scholarly journals Genome context influences evolutionary flexibility of nearly identical type III effectors in two phytopathogenic Pseudomonads

2021 ◽  
Author(s):  
David A Baltrus ◽  
Qian Feng ◽  
Brian H Kvitko
Keyword(s):  
Pseudomonas Syringae ◽  
Evolutionary Dynamics ◽  
Effector Proteins ◽  
In Planta ◽  
Genomic Context ◽  
Type Iii Effectors ◽  
Type Iii ◽  
Genome Context ◽  
The Impact ◽  
Multiple Type

Integrative Conjugative Elements (ICEs) are replicons that can insert and excise from chromosomal locations in a site specific manner, can conjugate across strains, and which often carry a variety of genes useful for bacterial growth and survival under specific conditions. Although ICEs have been identified and vetted within certain clades of the agricultural pathogen Pseudomonas syringae, the impact of ICE carriage and transfer across the entire P. syringae species complex remains underexplored. Here we identify and vet an ICE (PmaICE-DQ) from P. syringae pv. maculicola ES4326, a strain commonly used for laboratory virulence experiments, demonstrate that this element can excise and conjugate across strains, and contains loci encoding multiple type III effector proteins. Moreover, genome context suggests that another ICE (PmaICE-AOAB) is highly similar in comparison with and found immediately adjacent to PmaICE-DQ within the chromosome of strain ES4326, and also contains multiple type III effectors. Lastly, we present passage data from in planta experiments that suggests that genomic plasticity associated with ICEs may enable strains to more rapidly lose type III effectors that trigger R-gene mediated resistance in comparison to strains where nearly isogenic effectors are not present in ICEs. Taken together, our study sheds light on a set of ICE elements from P. syringae pv. maculicola ES4326 and highlights how genomic context may lead to different evolutionary dynamics for shared virulence genes between strains.

scholarly journals A Pseudomonas syringae pv. tomato DC3000 mutant lacking the type III effector HopQ1-1 is able to cause disease in the model plant Nicotiana benthamiana

2007 ◽  
Vol 51 (1) ◽  
pp. 32-46 ◽  
Author(s):  
Chia-Fong Wei ◽  
Brian H. Kvitko ◽  
Rena Shimizu ◽  
Emerson Crabill ◽  
James R. Alfano ◽  
...  
Keyword(s):  
Pseudomonas Syringae ◽  
Nicotiana Benthamiana ◽  
Tomato Dc3000 ◽  
Type Iii Effector ◽  
Model Plant ◽  
Type Iii

scholarly journals The awr Gene Family Encodes a Novel Class of Ralstonia solanacearum Type III Effectors Displaying Virulence and Avirulence Activities

2012 ◽  
Vol 25 (7) ◽  
pp. 941-953 ◽  
Author(s):  
Montserrat Solé ◽  
Crina Popa ◽  
Oriane Mith ◽  
Kee Hoon Sohn ◽  
Jonathan D. G. Jones ◽  
...  
Keyword(s):  
Gene Family ◽  
Pseudomonas Syringae ◽  
Ralstonia Solanacearum ◽  
Tomato Dc3000 ◽  
Type Iii Effectors ◽  
Type Iii ◽  
New Gene ◽  
Transient Overexpression ◽  
Effector Recognition

We present here the characterization of a new gene family, awr, found in all sequenced Ralstonia solanacearum strains and in other bacterial pathogens. We demonstrate that the five paralogues in strain GMI1000 encode type III-secreted effectors and that deletion of all awr genes severely impairs its capacity to multiply in natural host plants. Complementation studies show that the AWR (alanine-tryptophan-arginine tryad) effectors display some functional redundancy, although AWR2 is the major contributor to virulence. In contrast, the strain devoid of all awr genes (Δawr1-5) exhibits enhanced pathogenicity on Arabidopsis plants. A gain-of-function approach expressing AWR in Pseudomonas syringae pv. tomato DC3000 proves that this is likely due to effector recognition, because AWR5 and AWR4 restrict growth of this bacterium in Arabidopsis. Transient overexpression of AWR in nonhost tobacco species caused macroscopic cell death to varying extents, which, in the case of AWR5, shows characteristics of a typical hypersensitive response. Our work demonstrates that AWR, which show no similarity to any protein with known function, can specify either virulence or avirulence in the interaction of R. solanacearum with its plant hosts.

scholarly journals Pseudomonas syringae pv. tomato DC3000 CmaL (PSPTO4723), a DUF1330 Family Member, Is Needed To Produce l-allo-Isoleucine, a Precursor for the Phytotoxin Coronatine

2012 ◽  
Vol 195 (2) ◽  
pp. 287-296 ◽  
Author(s):  
Jay N. Worley ◽  
Alistair B. Russell ◽  
Aaron G. Wexler ◽  
Philip A. Bronstein ◽  
Brian H. Kvitko ◽  
...  
Keyword(s):  
Pseudomonas Syringae ◽  
Genomic Region ◽  
Tomato Dc3000 ◽  
Content Type ◽  
Type Iii Effectors ◽  
Type Iii ◽  
Coronafacic Acid ◽  
Feeding Experiments ◽  
Leaf Chlorosis

ABSTRACTPseudomonas syringaepv. tomato DC3000 produces the phytotoxin coronatine, a major determinant of the leaf chlorosis associated with DC3000 pathogenesis. The DC3000 PSPTO4723 (cmaL) gene is located in a genomic region encoding type III effectors; however, it promotes chlorosis in the model plantNicotiana benthamianain a manner independent of type III secretion. Coronatine is produced by the ligation of two moieties, coronafacic acid (CFA) and coronamic acid (CMA), which are produced by biosynthetic pathways encoded in separate operons. Cross-feeding experiments, performed inN. benthamianawithcfa,cma, andcmaLmutants, implicate CmaL in CMA production. Furthermore, analysis of bacterial supernatants under coronatine-inducing conditions revealed that mutants lacking either thecmaoperon orcmaLaccumulate CFA rather than coronatine, supporting a role for CmaL in the regulation or biosynthesis of CMA. CmaL does not appear to regulate CMA production, since the expression of proteins with known roles in CMA production is unaltered incmaLmutants. Rather, CmaL is needed for the first step in CMA synthesis, as evidenced by the fact that wild-type levels of coronatine production are restored to a ΔcmaLmutant when it is supplemented with 50 μg/mll-allo-isoleucine, the starting unit for CMA production.cmaLis found in all other sequencedP. syringaestrains with coronatine biosynthesis genes. This characterization of CmaL identifies a critical missing factor in coronatine production and provides a foundation for further investigation of a member of the widespread DUF1330 protein family.

scholarly journals Two Novel Type III-Secreted Proteins of Xanthomonas campestris pv. vesicatoria Are Encoded within the hrp Pathogenicity Island

2002 ◽  
Vol 184 (5) ◽  
pp. 1340-1348 ◽  
Author(s):  
Laurent Noël ◽  
Frank Thieme ◽  
Dirk Nennstiel ◽  
Ulla Bonas
Keyword(s):  
Gene Cluster ◽  
Pseudomonas Syringae ◽  
Xanthomonas Campestris ◽  
Pathogenicity Island ◽  
Effector Proteins ◽  
In Planta ◽  
Type Iii ◽  
Reverse Transcription Pcr ◽  
New Genes ◽  
Type Iii Protein Secretion

ABSTRACT The Hrp type III protein secretion system (TTSS) is essential for pathogenicity of gram-negative plant pathogen Xanthomonas campestris pv. vesicatoria. cDNA-amplified fragment length polymorphism and reverse transcription-PCR analyses identified new genes, regulated by key hrp regulator HrpG, in the regions flanking the hrp gene cluster. Sequence analysis revealed genes encoding HpaG, a predicted leucine-rich repeat-containing protein, the lysozyme-like HpaH protein, and XopA and XopD, which are similar in sequence to Hpa1 from Xanthomonas oryzae pv. oryzae and PsvA from Pseudomonas syringae, respectively. XopA and XopD (Xanthomonas outer proteins) are secreted by the Xanthomonas Hrp TTSS and thus represent putative effector proteins. Mutations in xopA, but not in xopD, resulted in reduced bacterial growth in planta and delayed plant reactions in susceptible and resistant host plants. Since the xopD promoter contains a putative hrp box, which is characteristic of hrpL-regulated genes in P. syringae and Erwinia spp., the gene was probably acquired by horizontal gene transfer. Interestingly, the regions flanking the hrp gene cluster also contain insertion sequences and genes for a putative transposase and a tRNAArg. These features suggest that the hrp gene cluster of X. campestris pv. vesicatoria is part of a pathogenicity island.

scholarly journals A Remorin from Nicotiana benthamiana Interacts with the Pseudomonas Type-III Effector Protein HopZ1a and is Phosphorylated by the Immune-Related Kinase PBS1

2019 ◽  
Vol 32 (9) ◽  
pp. 1229-1242 ◽  
Author(s):  
Philip Albers ◽  
Suayib Üstün ◽  
Katja Witzel ◽  
Max Kraner ◽  
Frederik Börnke
Keyword(s):  
Pseudomonas Syringae ◽  
Nicotiana Benthamiana ◽  
Effector Protein ◽  
Type Iii Effector ◽  
Defense Signaling ◽  
Type Iii ◽  
Target Membrane ◽  
Effector Triggered Immunity ◽  
Transient Overexpression

The plasma membrane (PM) is at the interface of plant–pathogen interactions and, thus, many bacterial type-III effector (T3E) proteins target membrane-associated processes to interfere with immunity. The Pseudomonas syringae T3E HopZ1a is a host cell PM-localized effector protein that has several immunity-associated host targets but also activates effector-triggered immunity in resistant backgrounds. Although HopZ1a has been shown to interfere with early defense signaling at the PM, no dedicated PM-associated HopZ1a target protein has been identified until now. Here, we show that HopZ1a interacts with the PM-associated remorin protein NbREM4 from Nicotiana benthamiana in several independent assays. NbREM4 relocalizes to membrane nanodomains after treatment with the bacterial elicitor flg22 and transient overexpression of NbREM4 in N. benthamiana induces the expression of a subset of defense-related genes. We can further show that NbREM4 interacts with the immune-related receptor-like cytoplasmic kinase avrPphB-susceptible 1 (PBS1) and is phosphorylated by PBS1 on several residues in vitro. Thus, we conclude that NbREM4 is associated with early defense signaling at the PM. The possible relevance of the HopZ1a–NbREM4 interaction for HopZ1a virulence and avirulence functions is discussed. [Formula: see text]Copyright © 2019 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license .

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