Direct and Indirect Visualization of Bacterial Effector Delivery into Diverse Plant Cell Types during Infection

Henry, Elizabeth; Toruño, Tania Y.; Jauneau, Alain; Deslandes, Laurent; Coaker, Gitta

doi:10.1105/tpc.17.00027

Cited by 45 publications

(40 citation statements)

References 88 publications

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“…It has long been assumed that R. solanacearum injects effectors into the living xylem parenchyma cells that are connected to vessels by bordered pits. Recent work confirmed this by visualizing delivery of an R. solanacearum effector (PopP2) into living Arabidopsis cells surrounding the xylem in petioles (Henry et al ., ).…”

Section: Discussionmentioning

confidence: 97%

Metabolomics of tomato xylem sap during bacterial wilt reveals Ralstonia solanacearum produces abundant putrescine, a metabolite that accelerates wilt disease

Lowe‐Power

Hendrich

Roepenack‐Lahaye

et al. 2017

Environmental Microbiology

116

130

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Ralstonia solanacearum thrives in plant xylem vessels and causes bacterial wilt disease despite the low nutrient content of xylem sap. We found that R. solanacearum manipulates its host to increase nutrients in tomato xylem sap, enabling it to grow better in sap from infected plants than in sap from healthy plants. Untargeted GC/MS metabolomics identified 22 metabolites enriched in R. solanacearum-infected sap. Eight of these could serve as sole carbon or nitrogen sources for R. solanacearum. Putrescine, a polyamine that is not a sole carbon or nitrogen source for R. solanacearum, was enriched 76-fold to 37 µM in R. solanacearum-infected sap. R. solanacearum synthesized putrescine via a SpeC ornithine decarboxylase. A ΔspeC mutant required ≥ 15 µM exogenous putrescine to grow and could not grow alone in xylem even when plants were treated with putrescine. However, co-inoculation with wildtype rescued ΔspeC growth, indicating R. solanacearum produced and exported putrescine to xylem sap. Intriguingly, treating plants with putrescine before inoculation accelerated wilt symptom development and R. solanacearum growth and systemic spread. Xylem putrescine concentration was unchanged in putrescine-treated plants, so the exogenous putrescine likely accelerated disease indirectly by affecting host physiology. These results indicate that putrescine is a pathogen-produced virulence metabolite.

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Section: Discussionmentioning

confidence: 97%

Metabolomics of tomato xylem sap during bacterial wilt reveals Ralstonia solanacearum produces abundant putrescine, a metabolite that accelerates wilt disease

Lowe‐Power

Hendrich

Roepenack‐Lahaye

et al. 2017

Environmental Microbiology

116

130

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“… AvrPtoB (De Vries et al ., ; Gimenez‐Ibanez et al ., ; Henry et al ., ; Martin, ; Mathieu et al ., ; Rosebrock et al ., ; Shan et al ., ; Wei et al ., ).…”

Section: Defence Subversion and Other Processes Promoting Pathogenesiunclassified

“…AvrPto (Martin, 2012;Shan et al, 2008;Tang et al, 1996;Xiang et al, 2008). AvrPtoB (De Vries et al, 2006;Gimenez-Ibanez et al, 2009;Henry et al, 2017;Martin, 2012;Mathieu et al, 2014;Rosebrock et al, 2007;Shan et al, 2008;Wei et al, 2015). HopE1 (Guo et al, 2009(Guo et al, , 2016Jamir et al, 2004).…”

Section: Defence Subversion and Other Processes Promoting Pathogenesimentioning

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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“…Therefore, studies that monitor the dynamics of effectors that are delivered into host organelles directly by the pathogen are needed to understand the precise localization and role of these effectors in virulence. Recently, a split fluorescent protein-based assay has been described to detect the subcellular localization of effectors delivered directly by bacterial pathogens into host cells (Henry et al, 2017;Park et al, 2017). Using this assay, Pseudomonas effectors are fused to the 11 th b-strand of super-folder GFP (sfGFP11) and, when delivered into plant cells expressing the sfGFP 1-10 b-strand (sfGFP1-10), sfGFP is reconstituted in the cytosol or in target organelles and can be visualized by confocal microscopy (Park et al, 2017).…”

Section: Chloroplasts: Major Contributors To Plant Immunity and Key Tmentioning

confidence: 99%

Plant–microbe interactions: organelles and the cytoskeleton in action

et al. 2017

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Contents Summary1012I.Introduction1012II.The endomembrane system in plant–microbe interactions1013III.The cytoskeleton in plant–microbe interactions1017IV.Organelles in plant–microbe interactions1019V.Inter‐organellar communication in plant–microbe interactions1022VI.Conclusions and prospects1023Acknowledgements1024References1024 Summary Plants have evolved a multilayered immune system with well‐orchestrated defense strategies against pathogen attack. Multiple immune signaling pathways, coordinated by several subcellular compartments and interactions between these compartments, play important roles in a successful immune response. Pathogens use various strategies to either directly attack the plant's immune system or to indirectly manipulate the physiological status of the plant to inhibit an immune response. Microscopy‐based approaches have allowed the direct visualization of membrane trafficking events, cytoskeleton reorganization, subcellular dynamics and inter‐organellar communication during the immune response. Here, we discuss the contributions of organelles and the cytoskeleton to the plant's defense response against microbial pathogens, as well as the mechanisms used by pathogens to target these compartments to overcome the plant's defense barrier.

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Direct and Indirect Visualization of Bacterial Effector Delivery into Diverse Plant Cell Types during Infection

Cited by 45 publications

References 88 publications

Metabolomics of tomato xylem sap during bacterial wilt reveals Ralstonia solanacearum produces abundant putrescine, a metabolite that accelerates wilt disease

Metabolomics of tomato xylem sap during bacterial wilt reveals Ralstonia solanacearum produces abundant putrescine, a metabolite that accelerates wilt disease

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

Plant–microbe interactions: organelles and the cytoskeleton in action

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