scholarly journals The Pseudomonas syringae Type III Effector HopAM1 Enhances Virulence on Water-Stressed Plants

2008 ◽  
Vol 21 (3) ◽  
pp. 361-370 ◽  
Author(s):  
Ajay K. Goel ◽  
Derek Lundberg ◽  
Miguel A. Torres ◽  
Ryan Matthews ◽  
Chiharu Akimoto-Tomiyama ◽  
...  
Keyword(s):  
Host Plant ◽  
Pseudomonas Syringae ◽  
Stomatal Closure ◽  
Defense Responses ◽  
Effector Proteins ◽  
Host Cells ◽  
Type Iii Effector ◽  
Type Iii Effectors ◽  
Type Iii ◽  
Conditional Expression

Pseudomonas syringae strains deliver diverse type III effector proteins into host cells, where they can act as virulence factors. Although the functions of the majority of type III effectors are unknown, several have been shown to interfere with plant basal defense mechanisms. Type III effectors also could contribute to bacterial virulence by enhancing nutrient uptake and pathogen adaptation to the environment of the host plant. We demonstrate that the type III effector HopAM1 (formerly known as AvrPpiB) enhances the virulence of a weak pathogen in plants that are grown under drought stress. This is the first report of a type III effector that aids pathogen adaptation to water availability in the host plant. Expression of HopAM1 makes transgenic Ws-0 Arabidopsis hypersensitive to abscisic acid (ABA) for stomatal closure and germination arrest. Conditional expression of HopAM1 in Arabidopsis also suppresses basal defenses. ABA responses overlap with defense responses and ABA has been shown to suppress defense against P. syringae pathogens. We propose that HopAM1 aids P. syringae virulence by manipulation of ABA responses that suppress defense responses. In addition, host ABA responses enhanced by type III delivery of HopAM1 protect developing bacterial colonies inside leaves from osmotic stress.

scholarly journals The HopZ Family of Pseudomonas syringae Type III Effectors Require Myristoylation for Virulence and Avirulence Functions in Arabidopsis thaliana

2008 ◽  
Vol 190 (8) ◽  
pp. 2880-2891 ◽  
Author(s):  
Jennifer D. Lewis ◽  
Wasan Abada ◽  
Wenbo Ma ◽  
David S. Guttman ◽  
Darrell Desveaux
Keyword(s):  
Arabidopsis Thaliana ◽  
Pseudomonas Syringae ◽  
Hypersensitive Response ◽  
Pathogenic Bacteria ◽  
Functional Characterization ◽  
Defense Responses ◽  
Effector Proteins ◽  
Type Iii Effectors ◽  
Type Iii ◽  
Virulence Protein

ABSTRACT Pseudomonas syringae utilizes the type III secretion system to translocate effector proteins into plant cells, where they can contribute to the pathogen's ability to infect and cause disease. Recognition of these effectors by resistance proteins induces defense responses that typically include a programmed cell death reaction called the hypersensitive response. The YopJ/HopZ family of type III effector proteins is a common family of effector proteins found in animal- and plant-pathogenic bacteria. The HopZ family in P. syringae includes HopZ1aPsyA2, HopZ1bPgyUnB647, HopZ1cPmaE54326, HopZ2Ppi895A and HopZ3PsyB728a. HopZ1a is predicted to be most similar to the ancestral hopZ allele and causes a hypersensitive response in multiple plant species, including Arabidopsis thaliana. Therefore, it has been proposed that host defense responses have driven the diversification of this effector family. In this study, we further characterized the hypersensitive response induced by HopZ1a and demonstrated that it is not dependent on known resistance genes. Further, we identified a novel virulence function for HopZ2 that requires the catalytic cysteine demonstrated to be required for protease activity. Sequence analysis of the HopZ family revealed the presence of a predicted myristoylation sequence in all members except HopZ3. We demonstrated that the myristoylation site is required for membrane localization of this effector family and contributes to the virulence and avirulence activities of HopZ2 and HopZ1a, respectively. This paper provides insight into the selective pressures driving virulence protein evolution by describing a detailed functional characterization of the diverse HopZ family of type III effectors with the model plant Arabidopsis.

scholarly journals Virulence in a Pseudomonas syringae Strain with a Small Repertoire of Predicted Effectors

2013 ◽  
Author(s):  
Kevin L Hockett ◽  
Marc T Nishimura ◽  
Erick Karlsrud ◽  
Kevin Dougherty ◽  
David A Baltrus
Keyword(s):  
Pseudomonas Syringae ◽  
Effector Proteins ◽  
Type Iii Effector ◽  
Type Iii Effectors ◽  
Virulence Proteins ◽  
E Coli ◽  
Type Iii ◽  
Catalytic Sites ◽  
New Type ◽  
Additional Support

stract Both type III effector proteins and non-ribosomal peptide toxins play important roles for Pseudomonas syringae pathogenicity in host plants, but whether and how these virulence pathways interact to promote infection remains unclear. Genomic evidence from one clade of P. syringae suggests a tradeoff between the total number of type III effector proteins and presence of syringomycin, syringopeptin, and syringolin A toxins. Here we report the complete genome sequence from P. syringae CC1557, which contains the lowest number of known type III effectors to date and has also acquired genes similar to sequences encoding syringomycin pathways from other strains. We demonstrate that this strain is pathogenic on Nicotiana benthamiana and that both the type III secretion system and a new type III effector family, hopBJ1, contribute to virulence. We further demonstrate that virulence activity of HopBJ1 is dependent on similar catalytic sites as the E. coli CNF1 toxin. Taken together, our results provide additional support for a negative correlation between type III effector repertoires and the potential to produce syringomycin-like toxins while also highlighting how genomic synteny and bioinformatics can be used to identify and characterize novel virulence proteins.

scholarly journals Pseudomonas syringae CC1557: A Highly Virulent Strain With an Unusually Small Type III Effector Repertoire That Includes a Novel Effector

2014 ◽  
Vol 27 (9) ◽  
pp. 923-932 ◽  
Author(s):  
Kevin L. Hockett ◽  
Marc T. Nishimura ◽  
Erick Karlsrud ◽  
Kevin Dougherty ◽  
David A. Baltrus
Keyword(s):  
Pseudomonas Syringae ◽  
Virulent Strain ◽  
Effector Proteins ◽  
Type Iii Effector ◽  
Type Iii Effectors ◽  
Virulence Proteins ◽  
Type Iii ◽  
New Type ◽  
Peptide Toxins ◽  
Additional Support

Both type III effector proteins and nonribosomal peptide toxins play important roles for Pseudomonas syringae pathogenicity in host plants, but whether and how these pathways interact to promote infection remains unclear. Genomic evidence from one clade of P. syringae suggests a tradeoff between the total number of type III effector proteins and presence of syringomycin, syringopeptin, and syringolin A toxins. Here, we report the complete genome sequence from P. syringae CC1557, which contains the lowest number of known type III effectors to date and has also acquired genes similar to sequences encoding syringomycin pathways from other strains. We demonstrate that this strain is pathogenic on Nicotiana benthamiana and that both the type III secretion system and a new type III effector, hopBJ1, contribute to pathogenicity. We further demonstrate that activity of HopBJ1 is dependent on residues structurally similar to the catalytic site of Escherichia coli CNF1 toxin. Taken together, our results provide additional support for a negative correlation between type III effector repertoires and the potential to produce syringomycin-like toxins while also highlighting how genomic synteny and bioinformatics can be used to identify and characterize novel virulence proteins.

scholarly journals Bioinformatics-Enabled Identification of the HrpL Regulon and Type III Secretion System Effector Proteins of Pseudomonas syringae pv. phaseolicola 1448A

2006 ◽  
Vol 19 (11) ◽  
pp. 1193-1206 ◽  
Author(s):  
Monica Vencato ◽  
Fang Tian ◽  
James R. Alfano ◽  
C. Robin Buell ◽  
Samuel Cartinhour ◽  
...  
Keyword(s):  
Pseudomonas Syringae ◽  
Type Iii Secretion ◽  
Type Iii Secretion System ◽  
Secretion System ◽  
Effector Proteins ◽  
Host Cells ◽  
Candidate Gene Approach ◽  
Type Iii Effectors ◽  
Type Iii ◽  
Genes Encoding

The ability of Pseudomonas syringae pv. phaseolicola to cause halo blight of bean is dependent on its ability to translocate effector proteins into host cells via the hypersensitive response and pathogenicity (Hrp) type III secretion system (T3SS). To identify genes encoding type III effectors and other potential virulence factors that are regulated by the HrpL alternative sigma factor, we used a hidden Markov model, weight matrix model, and type III targeting-associated patterns to search the genome of P. syringae pv. phaseolicola 1448A, which recently was sequenced to completion. We identified 44 high-probability putative Hrp promoters upstream of genes encoding the core T3SS machinery, 27 candidate effectors and related T3SS substrates, and 10 factors unrelated to the Hrp system. The expression of 13 of these candidate HrpL regulon genes was analyzed by real-time polymerase chain reaction, and all were found to be upregulated by HrpL. Six of the candidate type III effectors were assayed for T3SS-dependent translocation into plant cells using the Bordetella pertussis calmodulin-dependent adenylate cyclase (Cya) translocation reporter, and all were translocated. PSPPH1855 (ApbE-family protein) and PSPPH3759 (alcohol dehydrogenase) have no apparent T3SS-related function; however, they do have homologs in the model strain P. syringae pv. tomato DC3000 (PSPTO2105 and PSPTO0834, respectively) that are similarly upregulated by HrpL. Mutations were constructed in the DC3000 homologs and found to reduce bacterial growth in host Arabidopsis leaves. These results establish the utility of the bioinformatic or candidate gene approach to identifying effectors and other genes relevant to pathogenesis in P. syringae genomes.

scholarly journals The Xanthomonas type-III effector protein XopS stabilizes CaWRKY40a to regulate defense hormone responses and preinvasion immunity in pepper (Capsicum annuum)

2021 ◽  
Author(s):  
Margot Raffeiner ◽  
Suayib Üstün ◽  
Tiziana Guerra ◽  
Daniela Spinti ◽  
Maria Fitzner ◽  
...  
Keyword(s):  
Gene Expression ◽  
Xanthomonas Campestris ◽  
Stomatal Closure ◽  
Ectopic Expression ◽  
Defense Responses ◽  
Dependent Manner ◽  
Plant Tolerance ◽  
Defense Gene Expression ◽  
Type Iii Effector ◽  
Type Iii

A critical component of plant immunity against invading pathogens is the rapid transcriptional reprogramming of the attacked cell to minimize virulence. Many adapted plant bacterial pathogens use type III effector (T3E) proteins to interfere with plant defense responses, including the induction of immunity genes. The elucidation of effector function is essential to understanding bacterial pathogenesis. Here, we show that XopS, a T3E of Xanthomonas campestris pv. vesicatoria (Xcv), interacts with and inhibits the proteasomal degradation of the transcriptional regulator of defense gene expression WRKY40. Virus-induced gene silencing of WRKY40 in pepper enhanced plant tolerance towards Xcv infection, indicating it represses immunity. Stabilization of WRKY40 by XopS reduces the expression of its targets including salicylic acid (SA)-responsive genes and the jasmonic acid (JA) signaling repressor JAZ8. Xcv bacteria lacking XopS display significantly reduced virulence when surface inoculated onto susceptible pepper leaves. XopS delivery by Xcv, as well as ectopic expression of XopS in Arabidopsis or Nicotiana benthamiana prevented stomatal closure in response to bacteria and biotic elicitors in a WRKY40 dependent manner. This suggests that XopS interferes with preinvasion as well as with apoplastic defense by manipulating WRKY40 stability and gene expression eventually altering phytohormone crosstalk to promote pathogen proliferation.

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 Multiple Xanthomonas euvesicatoria Type III Effectors Inhibit flg22-Triggered Immunity

2016 ◽  
Vol 29 (8) ◽  
pp. 651-660 ◽  
Author(s):  
Georgy Popov ◽  
Malou Fraiture ◽  
Frederic Brunner ◽  
Guido Sessa
Keyword(s):  
Pseudomonas Syringae ◽  
Map Kinases ◽  
Molecular Mechanisms ◽  
Inducible Promoter ◽  
Effector Proteins ◽  
Host Cells ◽  
In Planta ◽  
Callose Deposition ◽  
Type Iii ◽  
Xanthomonas Euvesicatoria

Xanthomonas euvesicatoria is the causal agent of bacterial spot disease in pepper and tomato. X. euvesicatoria bacteria interfere with plant cellular processes by injecting effector proteins into host cells through the type III secretion (T3S) system. About 35 T3S effectors have been identified in X. euvesicatoria 85-10, and a few of them were implicated in suppression of pattern-triggered immunity (PTI). We used an Arabidopsis thaliana pathogen-free protoplast–based assay to identify X. euvesicatoria 85-10 effectors that interfere with PTI signaling induced by the bacterial peptide flg22. Of 33 tested effectors, 17 inhibited activation of a PTI-inducible promoter. Among them, nine effectors also interfered with activation of an abscisic acid–inducible promoter. However, effectors that inhibited flg22-induced signaling did not affect phosphorylation of mitogen-activated protein (MAP) kinases acting downstream of flg22 perception. Further investigation of selected effectors revealed that XopAJ, XopE2, and XopF2 inhibited activation of a PTI-inducible promoter by the bacterial peptide elf18 in Arabidopsis protoplasts and by flg22 in tomato protoplasts. The effectors XopF2, XopE2, XopAP, XopAE, XopH, and XopAJ inhibited flg22-induced callose deposition in planta and enhanced disease symptoms caused by attenuated Pseudomonas syringae bacteria. Finally, selected effectors were found to localize to various plant subcellular compartments. These results indicate that X. euvesicatoria bacteria utilize multiple T3S effectors to suppress flg22-induced signaling acting downstream or in parallel to MAP kinase cascades and suggest they act through different molecular mechanisms.

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.

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