The pan-genome effector-triggered immunity landscape of a host-pathogen interaction

Science ◽  
2020 ◽  
Vol 367 (6479) ◽  
pp. 763-768 ◽  
Author(s):  
Bradley Laflamme ◽  
Marcus M. Dillon ◽  
Alexandre Martel ◽  
Renan N. D. Almeida ◽  
Darrell Desveaux ◽  
...  
Keyword(s):  
Arabidopsis Thaliana ◽  
Pseudomonas Syringae ◽  
Systematic Study ◽  
Effector Proteins ◽  
Host Pathogen Interaction ◽  
Pan Genome ◽  
Immune Receptors ◽  
Pathogen Diversity ◽  
Genome Complexity ◽  
Effector Triggered Immunity

Effector-triggered immunity (ETI), induced by host immune receptors in response to microbial effectors, protects plants against virulent pathogens. However, a systematic study of ETI prevalence against species-wide pathogen diversity is lacking. We constructed the Pseudomonas syringae Type III Effector Compendium (PsyTEC) to reduce the pan-genome complexity of 5127 unique effector proteins, distributed among 70 families from 494 strains, to 529 representative alleles. We screened PsyTEC on the model plant Arabidopsis thaliana and identified 59 ETI-eliciting alleles (11.2%) from 19 families (27.1%), with orthologs distributed among 96.8% of P. syringae strains. We also identified two previously undescribed host immune receptors, including CAR1, which recognizes the conserved effectors AvrE and HopAA1, and found that 94.7% of strains harbor alleles predicted to be recognized by either CAR1 or ZAR1.

The small molecule Zaractin activates ZAR1-mediated immunity in Arabidopsis

2021 ◽  
Vol 118 (47) ◽  
pp. e2116570118
Author(s):  
Derek Seto ◽  
Madiha Khan ◽  
D. Patrick Bastedo ◽  
Alexandre Martel ◽  
Trinh Vo ◽  
...  
Keyword(s):  
Immune System ◽  
Pseudomonas Syringae ◽  
Small Molecule ◽  
Nucleotide Binding ◽  
Infection Process ◽  
Effector Proteins ◽  
Cellular Proteins ◽  
Leucine Rich Repeat ◽  
Effector Triggered Immunity ◽  
Immune Pathway

Pathogenic effector proteins use a variety of enzymatic activities to manipulate host cellular proteins and favor the infection process. However, these perturbations can be sensed by nucleotide-binding leucine-rich-repeat (NLR) proteins to activate effector-triggered immunity (ETI). Here we have identified a small molecule (Zaractin) that mimics the immune eliciting activity of the Pseudomonas syringae type III secreted effector (T3SE) HopF1r and show that both HopF1r and Zaractin activate the same NLR-mediated immune pathway in Arabidopsis. Our results demonstrate that the ETI-inducing action of pathogenic effectors can be harnessed to identify synthetic activators of the eukaryotic immune system.

scholarly journals The type III effector HopF2Pto targets Arabidopsis RIN4 protein to promote Pseudomonas syringae virulence

2010 ◽  
Vol 107 (5) ◽  
pp. 2349-2354 ◽  
Author(s):  
Mike Wilton ◽  
Rajagopal Subramaniam ◽  
James Elmore ◽  
Corinna Felsensteiner ◽  
Gitta Coaker ◽  
...  
Keyword(s):  
Pseudomonas Syringae ◽  
Plant Immunity ◽  
Effector Proteins ◽  
Type Iii ◽  
Pathogen Effector ◽  
Effector Triggered Immunity ◽  
Type Iii Secretion Effector ◽  
Virulence Target

Plant immunity can be induced by two major classes of pathogen-associated molecules. Pathogen- or microbe-associated molecular patterns (PAMPs or MAMPs) are conserved molecular components of microbes that serve as “non-self” features to induce PAMP-triggered immunity (PTI). Pathogen effector proteins used to promote virulence can also be recognized as “non-self” features or induce a “modified-self” state that can induce effector-triggered immunity (ETI). The Arabidopsis protein RIN4 plays an important role in both branches of plant immunity. Three unrelated type III secretion effector (TTSE) proteins from the phytopathogen Pseudomonas syringae, AvrRpm1, AvrRpt2, and AvrB, target RIN4, resulting in ETI that effectively restricts pathogen growth. However, no pathogenic advantage has been demonstrated for RIN4 manipulation by these TTSEs. Here, we show that the TTSE HopF2Pto also targets Arabidopsis RIN4. Transgenic plants conditionally expressing HopF2Pto were compromised for AvrRpt2-induced RIN4 modification and associated ETI. HopF2Pto interfered with AvrRpt2-induced RIN4 modification in vitro but not with AvrRpt2 activation, suggestive of RIN4 targeting by HopF2Pto. In support of this hypothesis, HopF2Pto interacted with RIN4 in vitro and in vivo. Unlike AvrRpm1, AvrRpt2, and AvrB, HopF2Pto did not induce ETI and instead promoted P. syringae growth in Arabidopsis. This virulence activity was not observed in plants genetically lacking RIN4. These data provide evidence that RIN4 is a major virulence target of HopF2Pto and that a pathogenic advantage can be conveyed by TTSEs that target RIN4.

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 Genome-wide analysis uncovers tomato leaf lncRNAs transcriptionally active upon Pseudomonas syringae pv. tomato challenge

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Hernan G. Rosli ◽  
Emilia Sirvent ◽  
Florencia N. Bekier ◽  
Romina N. Ramos ◽  
Marina A. Pombo
Keyword(s):  
Pseudomonas Syringae ◽  
Pathogenic Bacteria ◽  
Direct Detection ◽  
Effector Proteins ◽  
Surface Pattern ◽  
Large Set ◽  
Protein Coding ◽  
Genome Wide ◽  
Effector Triggered Immunity ◽  
Molecular Patterns

AbstractPlants rely on (in)direct detection of bacterial pathogens through plasma membrane-localized and intracellular receptor proteins. Surface pattern-recognition receptors (PRRs) participate in the detection of microbe-associated molecular patterns (MAMPs) and are required for the activation of pattern-triggered immunity (PTI). Pathogenic bacteria, such as Pseudomonas syringae pv. tomato (Pst) deploys ~ 30 effector proteins into the plant cell that contribute to pathogenicity. Resistant plants are capable of detecting the presence or activity of effectors and mount another response termed effector-triggered immunity (ETI). In order to investigate the involvement of tomato’s long non-coding RNAs (lncRNAs) in the immune response against Pst, we used RNA-seq data to predict and characterize those that are transcriptionally active in leaves challenged with a large set of treatments. Our prediction strategy was validated by sequence comparison with tomato lncRNAs described in previous works and by an alternative approach (RT-qPCR). Early PTI (30 min), late PTI (6 h) and ETI (6 h) differentially expressed (DE) lncRNAs were identified and used to perform a co-expression analysis including neighboring (± 100 kb) DE protein-coding genes. Some of the described networks could represent key regulatory mechanisms of photosynthesis, PRR abundance at the cell surface and mitigation of oxidative stress, associated to tomato-Pst pathosystem.

scholarly journals Focus on Activation, Regulation, and Evolution of MTI and ETI

2019 ◽  
Vol 32 (1) ◽  
pp. 5-5
Author(s):  
John M. McDowell
Keyword(s):  
Pseudomonas Syringae ◽  
Plant Disease Resistance ◽  
Protein Complexes ◽  
Plant Cells ◽  
Effector Proteins ◽  
Mitogen Activated Protein Kinase ◽  
Receptor Protein ◽  
Cell Infection ◽  
Mitogen Activated Protein ◽  
Effector Triggered Immunity

Plants perceive a variety of molecules produced by microbes, insects, and nematodes. These pathogen-derived components include so-called microbe-associated molecular patterns, or MAMPs, as well as effector proteins that are secreted to the exterior or interior of plant cells and these molecules can be recognized by receptor protein complexes on the exterior or interior of plant cells, thereby activating MAMP- or effector-triggered immunity (MTI or ETI, respectively). Because these processes are key components of plant disease resistance, they have been studied intensively. We are now in a golden age of ETI and MTI research, in which mechanistic and evolutionary understanding of both processes is emerging rapidly. Accordingly, in this Focus issue , we explore diverse aspects of MTI and ETI, with a unifying theme of integration at multiple levels. Additional content is available on the Focus on Activation, Regulation, and Evolution of MTI and ETI. Mitogen-Activated Protein Kinase Phosphatase 1 (MKP1) Negatively Regulates the Production of Reactive Oxygen Species During Arabidopsis Immune Responses Development of a Pseudomonas syringae–Arabidopsis Suspension Cell Infection System for Investigating Host Metabolite-Dependent Regulation of Type III Secretion and Pattern-Triggered Immunity Direct Regulation of the EFR-Dependent Immune Response by Arabidopsis TCP Transcription Factors Convergent Evolution of Effector Protease Recognition by Arabidopsis and Barley

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 HopA1 Effector from Pseudomonas syringae pv syringae Strain 61 Affects NMD Processes and Elicits Effector-Triggered Immunity

2021 ◽  
Vol 22 (14) ◽  
pp. 7440
Author(s):  
Shraddha K. Dahale ◽  
Daipayan Ghosh ◽  
Kishor D. Ingole ◽  
Anup Chugani ◽  
Sang Hee Kim ◽  
...  
Keyword(s):  
Pseudomonas Syringae ◽  
Disease Susceptibility ◽  
Null Mutant ◽  
In Planta ◽  
Host Range Expansion ◽  
Unique System ◽  
Effector Triggered Immunity ◽  
Transcriptomic Changes ◽  
Immune Detection

Pseudomonas syringae-secreted HopA1 effectors are important determinants in host range expansion and increased pathogenicity. Their recent acquisitions via horizontal gene transfer in several non-pathogenic Pseudomonas strains worldwide have caused alarming increase in their virulence capabilities. In Arabidopsis thaliana, RESISTANCE TO PSEUDOMONAS SYRINGAE 6 (RPS6) gene confers effector-triggered immunity (ETI) against HopA1pss derived from P. syringae pv. syringae strain 61. Surprisingly, a closely related HopA1pst from the tomato pathovar evades immune detection. These responsive differences in planta between the two HopA1s represents a unique system to study pathogen adaptation skills and host-jumps. However, molecular understanding of HopA1′s contribution to overall virulence remain undeciphered. Here, we show that immune-suppressive functions of HopA1pst are more potent than HopA1pss. In the resistance-compromised ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1) null-mutant, transcriptomic changes associated with HopA1pss-elicited ETI are still induced and carry resemblance to PAMP-triggered immunity (PTI) signatures. Enrichment of HopA1pss interactome identifies proteins with regulatory roles in post-transcriptional and translational processes. With our demonstration here that both HopA1 suppress reporter-gene translations in vitro imply that the above effector-associations with plant target carry inhibitory consequences. Overall, with our results here we unravel possible virulence role(s) of HopA1 in suppressing PTI and provide newer insights into its detection in resistant plants.

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