Behind the lines–actions of bacterial type III effector proteins in plant cells

Büttner, Daniela

doi:10.1093/femsre/fuw026

Cited by 243 publications

(265 citation statements)

References 349 publications

(550 reference statements)

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“…This review emphasizes the biological context in which T3Es operate, as much as the functions of the T3Es themselves, and is intended to be a complementary update to two previous reviews focusing on Pst DC3000 and its T3E repertoire (Lindeberg et al ., ; Xin and He, ). Other recent reviews provide more comprehensive coverage of the molecular activities of bacterial T3Es (Buttner, ; Macho, ; Toruno et al ., ).…”

Section: Introduction: the Utility Of A Disarmed Pathogen In Probingmentioning

confidence: 99%

Defining essential processes in plant pathogenesis with Pseudomonas syringae pv. tomato DC3000 disarmed polymutants and a subset of key type III effectors

Wei

Collmer

2018

Molecular Plant Pathology

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Pseudomonas syringae pv. tomato DC3000 and its derivatives cause disease in tomato, Arabidopsis and Nicotiana benthamiana. The primary virulence factors include a repertoire of 29 effector proteins injected into plant cells by the type III secretion system and the phytotoxin coronatine. The complete repertoire of effector genes and key coronatine biosynthesis genes have been progressively deleted and minimally reassembled to reconstitute basic pathogenic ability in N. benthamiana, and in Arabidopsis plants that have mutations in target genes that mimic effector actions. This approach and molecular studies of effector activities and plant immune system targets have highlighted a small subset of effectors that contribute to essential processes in pathogenesis. Most notably, HopM1 and AvrE1 redundantly promote an aqueous apoplastic environment, and AvrPtoB and AvrPto redundantly block early immune responses, two conditions that are sufficient for substantial bacterial growth in planta. In addition, disarmed DC3000 polymutants have been used to identify the individual effectors responsible for specific activities of the complete repertoire and to more effectively study effector domains, effector interplay and effector actions on host targets. Such work has revealed that AvrPtoB suppresses cell death elicitation in N. benthamiana that is triggered by another effector in the DC3000 repertoire, highlighting an important aspect of effector interplay in native repertoires. Disarmed DC3000 polymutants support the natural delivery of test effectors and infection readouts that more accurately reveal effector functions in key pathogenesis processes, and enable the identification of effectors with similar activities from a broad range of other pathogens that also defeat plants with cytoplasmic effectors.

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Section: Introduction: the Utility Of A Disarmed Pathogen In Probingmentioning

confidence: 99%

Defining essential processes in plant pathogenesis with Pseudomonas syringae pv. tomato DC3000 disarmed polymutants and a subset of key type III effectors

Wei

Collmer

2018

Molecular Plant Pathology

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“…However, irrespective of the host they infect, most pathogenic bacteria use the type III secretion system (T3SS) to take advantage of the host cells (He et al, 2004). The T3SS machinery is a filamentous supramolecular structure that provides a channel through which type III effector (T3E) proteins are secreted into the host cells to manipulate host defense responses against bacteria (Büttner, 2016). The first T3SS-associated filamentous structure was discovered in Pseudomonas syringae, a plant pathogen with a broad host range including several important crop species (Jin and He, 2001;Xin and He, 2013;Galán et al, 2014;Büttner, 2016).…”

Section: Introductionmentioning

confidence: 99%

“…The T3SS machinery is a filamentous supramolecular structure that provides a channel through which type III effector (T3E) proteins are secreted into the host cells to manipulate host defense responses against bacteria (Büttner, 2016). The first T3SS-associated filamentous structure was discovered in Pseudomonas syringae, a plant pathogen with a broad host range including several important crop species (Jin and He, 2001;Xin and He, 2013;Galán et al, 2014;Büttner, 2016). Our current understanding of detailed molecular and biochemical properties of the T3SS machinery come from studies of human pathogenic bacteria such as Salmonella and Yersinia (Galán et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…T3Es are important for the pathogenicity of the bacteria and they play an important role in suppressing the first line of plant defense responses (Xin and He, 2013;Büttner, 2016). Several studies have demonstrated that the effector proteins from pathogenic bacteria are targeted to specific subcellular compartments in cells, where they alter the physiological properties of the cell and suppress innate immunity (Alfano and Collmer, 2004;Kay and Bonas, 2009;Choi et al, 2013;Aung et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

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Spatiotemporal Monitoring of Pseudomonas syringae Effectors via Type III Secretion Using Split Fluorescent Protein Fragments

et al. 2017

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Pathogenic gram-negative bacteria cause serious diseases in animals and plants. These bacterial pathogens use the type III secretion system (T3SS) to deliver effector proteins into host cells; these effectors then localize to different subcellular compartments to attenuate immune responses by altering biological processes of the host cells. The fluorescent protein (FP)-based approach to monitor effectors secreted from bacteria into the host cells is not possible because the folded FP prevents effector delivery through the T3SS. Therefore, we optimized an improved variant of self-assembling split super-folder green fluorescent protein (sfGFP OPT ) system to investigate the spatiotemporal dynamics of effectors delivered through bacterial T3SS into plant cells. In this system, effectors are fused to 11th b-strand of super-folder GFP (sfGFP11), and when delivered into plant cells expressing sfGFP1-10 b-strand (sfGFP1-10 OPT ), the two proteins reconstitute GFP fluorescence. We generated a number of Arabidopsis thaliana transgenic lines expressing sfGFP1-10 OPT targeted to various subcellular compartments to facilitate localization of sfGFP11-tagged effectors delivered from bacteria. We demonstrate the efficacy of this system using Pseudomonas syringae effectors AvrB and AvrRps4 in Nicotiana benthamiana and transgenic Arabidopsis plants. The versatile split sfGFP OPT system described here will facilitate a better understanding of bacterial invasion strategies used to evade plant immune responses.

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“…Most Gram-negative plant-pathogenic bacteria express a conserved type III secretion system (T3SS) and translocate type III effector (T3E) proteins directly into the plant cell cytosol (Büttner and He, 2009). Here, T3Es manipulate plant cellular processes in various ways for the benefit of the bacteria, e.g., to suppress PTI (Büttner, 2016). On the other hand, plants can recognize T3Es via resistance (R) genes or proteins that in return initiate effector-triggered immunity, ETI (Khan et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Non-host Resistance Induced by the Xanthomonas Effector XopQ Is Widespread within the Genus Nicotiana and Functionally Depends on EDS1

et al. 2016

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Most Gram-negative plant pathogenic bacteria translocate effector proteins (T3Es) directly into plant cells via a conserved type III secretion system, which is essential for pathogenicity in susceptible plants. In resistant plants, recognition of some T3Es is mediated by corresponding resistance (R) genes or R proteins and induces effector triggered immunity (ETI) that often results in programmed cell death reactions. The identification of R genes and understanding their evolution/distribution bears great potential for the generation of resistant crop plants. We focus on T3Es from Xanthomonas campestris pv. vesicatoria (Xcv), the causal agent of bacterial spot disease on pepper and tomato plants. Here, 86 Solanaceae lines mainly of the genus Nicotiana were screened for phenotypical reactions after Agrobacterium tumefaciens-mediated transient expression of 21 different Xcv effectors to (i) identify new plant lines for T3E characterization, (ii) analyze conservation/evolution of putative R genes and (iii) identify promising plant lines as repertoire for R gene isolation. The effectors provoked different reactions on closely related plant lines indicative of a high variability and evolution rate of potential R genes. In some cases, putative R genes were conserved within a plant species but not within superordinate phylogenetical units. Interestingly, the effector XopQ was recognized by several Nicotiana spp. lines, and Xcv infection assays revealed that XopQ is a host range determinant in many Nicotiana species. Non-host resistance against Xcv and XopQ recognition in N. benthamiana required EDS1, strongly suggesting the presence of a TIR domain-containing XopQ-specific R protein in these plant lines. XopQ is a conserved effector among most xanthomonads, pointing out the XopQ-recognizing RxopQ as candidate for targeted crop improvement.

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Behind the lines–actions of bacterial type III effector proteins in plant cells

Cited by 243 publications

References 349 publications

Defining essential processes in plant pathogenesis with Pseudomonas syringae pv. tomato DC3000 disarmed polymutants and a subset of key type III effectors

Defining essential processes in plant pathogenesis with Pseudomonas syringae pv. tomato DC3000 disarmed polymutants and a subset of key type III effectors

Spatiotemporal Monitoring of Pseudomonas syringae Effectors via Type III Secretion Using Split Fluorescent Protein Fragments

Non-host Resistance Induced by the Xanthomonas Effector XopQ Is Widespread within the Genus Nicotiana and Functionally Depends on EDS1

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