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

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.

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

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-22-9-1069 ◽

2009 ◽

Vol 22 (9) ◽

pp. 1069-1080 ◽

Cited By ~ 147

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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Gene Ontology annotation highlights shared and divergent pathogenic strategies of type III effector proteins deployed by the plant pathogen Pseudomonas syringae pv tomato DC3000 and animal pathogenic Escherichia coli strains

BMC Microbiology ◽

10.1186/1471-2180-9-s1-s4 ◽

2009 ◽

Vol 9 (Suppl 1) ◽

pp. S4 ◽

Cited By ~ 18

Author(s):

Magdalen Lindeberg ◽

Bryan S Biehl ◽

Jeremy D Glasner ◽

Nicole T Perna ◽

Alan Collmer ◽

...

Keyword(s):

Escherichia Coli ◽

Gene Ontology ◽

Pseudomonas Syringae ◽

Plant Pathogen ◽

Effector Proteins ◽

Gene Ontology Annotation ◽

Tomato Dc3000 ◽

Type Iii Effector ◽

Type Iii ◽

Pathogenic Escherichia Coli

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

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.0904739107 ◽

2010 ◽

Vol 107 (5) ◽

pp. 2349-2354 ◽

Cited By ~ 92

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.

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Pseudomonas syringae pv. tomato DC3000 Effector HopG1 is a multi-faceted protein that Triggers Necrotic Cell Death that is attenuated by the Nonhost Resistance 2B (AtNHR2B) Protein

10.1101/2021.11.02.466876 ◽

2021 ◽

Author(s):

Catalina Rodriguez-Puerto ◽

Rupak Chakraborty ◽

Raksha Singh ◽

Perla Rocha-Loyola ◽

Clemencia M. Rojas

Keyword(s):

Cell Death ◽

Plant Defense ◽

Pseudomonas Syringae ◽

Plant Immunity ◽

Defense Responses ◽

Necrotic Cell Death ◽

Plant Defense Responses ◽

Necrotic Cell ◽

Tomato Dc3000 ◽

Type Iii

The plant pathogenic bacterium Pseudomonas syringae pv. tomato DC3000 (Pst DC3000) has become a paradigm in plant-bacteria interactions due to its ability to cause disease in the model plant Arabidopsis thaliana. Pst DC3000 uses the type III secretion system to deliver type III secreted effectors (T3SEs) directly into the plant cytoplasm. Pst DC3000 T3SEs contribute to pathogenicity by suppressing plant defense responses and targeting plant’s physiological processes. Although the complete repertoire of effectors encoded in the Pst DC3000 genome have been identified, the specific function for most of them remains to be elucidated. The mitochondrial-localized T3E HopG1, suppresses plant defense responses and promotes the development of disease symptoms. Here, we show that HopG1 triggers necrotic cell death that enables the growth of non-adapted pathogens. We further showed that HopG1 interacts with the plant immunity-related protein AtNHR2B and that AtNHR2B attenuates HopG1- virulence functions.

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A Draft Genome Sequence of Pseudomonas syringae pv. tomato T1 Reveals a Type III Effector Repertoire Significantly Divergent from That of Pseudomonas syringae pv. tomato DC3000

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-22-1-0052 ◽

2009 ◽

Vol 22 (1) ◽

pp. 52-62 ◽

Cited By ~ 101

Author(s):

Nalvo F. Almeida ◽

Shuangchun Yan ◽

Magdalen Lindeberg ◽

David J. Studholme ◽

David J. Schneider ◽

...

Keyword(s):

Host Range ◽

Host Specificity ◽

Pseudomonas Syringae ◽

Genome Sequence ◽

Draft Genome ◽

Draft Genome Sequence ◽

Tomato Dc3000 ◽

Type Iii ◽

Host Range Determination ◽

Range Determination

Diverse gene products including phytotoxins, pathogen-associated molecular patterns, and type III secreted effectors influence interactions between Pseudomonas syringae strains and plants, with additional yet uncharacterized factors likely contributing as well. Of particular interest are those interactions governing pathogen-host specificity. Comparative genomics of closely related pathogens with different host specificity represents an excellent approach for identification of genes contributing to host-range determination. A draft genome sequence of Pseudomonas syringae pv. tomato T1, which is pathogenic on tomato but nonpathogenic on Arabidopsis thaliana, was obtained for this purpose and compared with the genome of the closely related A. thaliana and tomato model pathogen P. syringae pv. tomato DC3000. Although the overall genetic content of each of the two genomes appears to be highly similar, the repertoire of effectors was found to diverge significantly. Several P. syringae pv. tomato T1 effectors absent from strain DC3000 were confirmed to be translocated into plants, with the well-studied effector AvrRpt2 representing a likely candidate for host-range determination. However, the presence of avrRpt2 was not found sufficient to explain A. thaliana resistance to P. syringae pv. tomato T1, suggesting that other effectors and possibly type III secretion system–independent factors also play a role in this interaction.

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Expression of a RING-HC protein from rice improves resistance to Pseudomonas syringae pv. tomato DC3000 in transgenic Arabidopsis thaliana

Journal of Experimental Botany ◽

10.1093/jxb/erm272 ◽

2007 ◽

Vol 58 (15-16) ◽

pp. 4147-4159 ◽

Cited By ~ 27

Author(s):

M.-Y. Cheung ◽

N.-Y. Zeng ◽

S.-W. Tong ◽

F. Wing-Yen Li ◽

K.-J. Zhao ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Pseudomonas Syringae ◽

Transgenic Arabidopsis ◽

Tomato Dc3000 ◽

Transgenic Arabidopsis Thaliana

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Chitosan Oligosaccharide Induces Resistance to Pseudomonas syringae pv. tomato DC3000 in Arabidopsis thaliana by Activating Both Salicylic Acid– and Jasmonic Acid–Mediated Pathways

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-03-18-0071-r ◽

2018 ◽

Vol 31 (12) ◽

pp. 1271-1279 ◽

Cited By ~ 21

Author(s):

Xiaochen Jia ◽

Haihong Zeng ◽

Wenxia Wang ◽

Fuyun Zhang ◽

Heng Yin

Keyword(s):

Salicylic Acid ◽

Jasmonic Acid ◽

Induced Resistance ◽

Pseudomonas Syringae ◽

Plant Immunity ◽

Chitosan Oligosaccharide ◽

Induction Effect ◽

Tomato Dc3000 ◽

Expression Of Genes ◽

Underlying Mechanisms

Chitosan oligosaccharide (COS) is an effective plant immunity elicitor; however, its induction mechanism in plants is complex and needs further investigation. In this study, the Arabidopsis–Pseudomonas syringae pv. tomato DC3000 (hereafter called DC3000) interaction was used to investigate the induction effect and the underlying mechanisms of COS. COS is effective in inducing resistance to DC3000 in Arabidopsis, and our results demonstrate that treatment with COS 3 days before DC3000 inoculation provided the most effective resistance. Disease severity in jar1 (jasmonic acid [JA]-deficient mutant), NahG, and sid2 (salicylic acid [SA]-deficient mutants) suggest both the SA and JA pathways are required for the Arabidopsis response to DC3000. COS pretreatment induced resistance in wild type (WT), jar1, and also, although to a lesser degree, in NahG and sid2 plants, implying that the SA and JA pathways play redundant roles in COS-induced resistance to DC3000. In COS-pretreated plants, expression of genes related to the SA pathway (PR1, PR2, and PR5) and SA content increased in both WT and jar1. Moreover, expression of genes related to the JA pathway (PDF1.2 and VSP2) and JA content both increased in WT and NahG. In conclusion, COS induces resistance to DC3000 in Arabidopsis by activating both SA- and JA-mediated pathways, although SA and JA pathways play redundant roles in this COS-induced resistance.

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Identification of IAA-regulated genes in Pseudomonas syringae pv. tomato strain DC3000

Journal of Bacteriology ◽

10.1128/jb.00380-21 ◽

2021 ◽

Author(s):

Arnaud-Thierry Djami-Tchatchou ◽

Zipeng Alex Li ◽

Paul Stodghill ◽

Melanie J. Filiatrault ◽

Barbara N. Kunkel

Keyword(s):

Gene Expression ◽

Arabidopsis Thaliana ◽

Acetic Acid ◽

Stress Response ◽

Pseudomonas Syringae ◽

Plant Pathogen ◽

Type Iii Secretion ◽

Plant Hormone ◽

Indole 3 Acetic Acid ◽

Exogenous Iaa

The auxin indole-3-acetic acid (IAA) is a plant hormone that not only regulates plant growth and development but also plays important roles in plant-microbe interactions. We previously reported that IAA alters expression of several virulence-related genes in the plant pathogen Pseudomonas syringae pv. tomato strain DC3000 ( Pto DC3000). To learn more about the impact of IAA on regulation of Pto DC3000 gene expression we performed a global transcriptomic analysis of bacteria grown in culture, in the presence or absence of exogenous IAA. We observed that IAA repressed expression of genes involved in the Type III secretion (T3S) system and motility and promoted expression of several known and putative transcriptional regulators. Several of these regulators are orthologs of factors known to regulate stress responses and accordingly expression of several stress response-related genes was also upregulated by IAA. Similar trends in expression for several genes were also observed by RT-qPCR. Using an Arabidopsis thaliana auxin receptor mutant that accumulates elevated auxin, we found that many of the P. syringae genes regulated by IAA in vitro were also regulated by auxin in planta . Collectively the data indicate that IAA modulates many aspects of Pto DC3000 biology, presumably to promote both virulence and survival under stressful conditions, including those encountered in or on plant leaves. IMPORTANCE Indole-3-acetic acid (IAA), a form of the plant hormone auxin, is used by many plant-associated bacteria as a cue to sense the plant environment. Previously, we showed that IAA can promote disease in interactions between the plant pathogen Pseudomonas syringae strain Pto DC000 and one of its hosts, Arabidopsis thaliana . However, the mechanisms by which IAA impacts the biology of Pto DC3000 and promotes disease are not well understood. Here we demonstrate that IAA is a signal molecule that regulates gene expression in Pto DC3000. The presence of exogenous IAA affects expression of over 700 genes in the bacteria, including genes involved in Type III secretion and genes involved in stress response. This work offers insight into the roles of auxin promoting pathogenesis.

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