Functional Analysis of Plant Defense Suppression and Activation by the <i>Xanthomonas</i> Core Type III Effector XopX

Stork, William; Kim, Jung‐Gun; Mudgett, Mary Beth

doi:10.1094/mpmi-09-14-0263-r

Cited by 33 publications

(37 citation statements)

References 86 publications

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“…Thus, it is possible this protein is associated with host cell membranes following secretion. Our observations for XopK are contrasted with the roles of AvrBs2 and XopX, which exhibit reduced virulence phenotypes, consistent with previous studies (Kearney and Staskawicz, 1990;Metz et al, 2005;Zhao et al, 2011;Sinha et al, 2013;Li et al, 2015b;Stork et al, 2015). Our results further illustrate that T3E mutants may impact certain aspects of host-pathogen interactions more than others.…”

Section: Discussionsupporting

confidence: 91%

“…AvrBs2 contains a glycerol phosphodiesterase domain that is required for its virulence functions in other Xanthomonas pathovars (Kearney and Staskawicz, 1990;Tai et al, 1999;Zhao et al, 2011;Li et al, 2015b). XopX is involved in suppressing pathogen-triggered immunity (Metz et al, 2005;Sinha et al, 2013;Stork et al, 2015). XopK was first identified in the rice pathogen Xanthomonas oryzae pv.…”

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confidence: 99%

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Quantitative, image-based phenotyping methods provide insight into spatial and temporal dimensions of plant disease

et al. 2016

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Plant disease symptoms exhibit complex spatial and temporal patterns that are challenging to quantify. Image-based phenotyping approaches enable multidimensional characterization of host-microbe interactions and are well suited to capture spatial and temporal data that are key to understanding disease progression. We applied image-based methods to investigate cassava bacterial blight, which is caused by the pathogen Xanthomonas axonopodis pv. manihotis (Xam). We generated Xam strains in which individual predicted type III effector (T3E) genes were mutated and applied multiple imaging approaches to investigate the role of these proteins in bacterial virulence. Specifically, we quantified bacterial populations, water-soaking disease symptoms, and pathogen spread from the site of inoculation over time for strains with mutations in avrBs2, xopX, and xopK as compared to wild-type Xam. ΔavrBs2 and ΔxopX both showed reduced growth in planta and delayed spread through the vasculature system of cassava. ΔavrBs2 exhibited reduced water-soaking symptoms at the site of inoculation. In contrast, ΔxopK exhibited enhanced induction of disease symptoms at the site of inoculation but reduced spread through the vasculature. Our results highlight the importance of adopting a multipronged approach to plant disease phenotyping to more fully understand the roles of T3Es in virulence. Finally, we demonstrate that the approaches used in this study can be extended to many host-microbe systems and increase the dimensions of phenotype that can be explored.

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Section: Discussionsupporting

confidence: 91%

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confidence: 99%

Quantitative, image-based phenotyping methods provide insight into spatial and temporal dimensions of plant disease

et al. 2016

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“…benthamiana . While the in planta expression level of the cell death inducer was not analyzed in the former characterization of XopQ (Teper et al ., ), this was regularly tested, e.g., studying cell death suppression by XopB (Schulze et al ., ) and XopX (Stork et al ., ).…”

Section: Discussionmentioning

confidence: 97%

Dissecting virulence function from recognition: cell death suppression in Nicotiana benthamiana by XopQ/HopQ1‐family effectors relies on EDS1‐dependent immunity

Adlung

Bonas

2017

The Plant Journal

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Many Gram-negative plant pathogenic bacteria express effector proteins of the XopQ/HopQ1 family which are translocated into plant cells via the type III secretion system during infection. In Nicotiana benthamiana, recognition of XopQ/HopQ1 proteins induces an effector-triggered immunity (ETI) reaction which is not associated with strong cell death but renders plants immune against Pseudomonas syringae and Xanthomonas campestris pv. vesicatoria strains. Additionally, XopQ suppresses cell death in N. benthamiana when transiently co-expressed with cell death inducers. Here, we show that representative XopQ/HopQ1 proteins are recognized similarly, likely by a single resistance protein of the TIR-NB-LRR class. Extensive analysis of XopQ derivatives indicates the recognition of structural features. We performed Agrobacterium-mediated protein expression experiments in wild-type and EDS1-deficient (eds1) N. benthamiana leaves, not recognizing XopQ/HopQ1. XopQ recognition limits multiplication of Agrobacterium and attenuates levels of transiently expressed proteins. Remarkably, XopQ fails to suppress cell death reactions induced by different effectors in eds1 plants. We conclude that XopQ-mediated cell death suppression in N. benthamiana is due to the attenuation of Agrobacterium-mediated protein expression rather than the cause of the genuine XopQ virulence activity. Thus, our study expands our understanding of XopQ recognition and function, and also challenges the commonly used co-expression assays for elucidation of in planta effector activities, at least under conditions of ETI induction.

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“…Several Xcv T3Es induce cell death reactions in Nicotiana spp., presumably as a result of ETI upon T3E recognition. For example, transient expression of XopJ (Thieme et al, 2007), XopE1 (Thieme et al, 2007), XopL (Singer et al, 2013), XopX (Metz et al, 2005; Stork et al, 2015), AvrRxv, and AvrBsT (Schulze et al, 2012) induces severe cell death reactions in N. benthamiana , whereas expression of XopG induces cell death in N. tabacum (Schulze et al, 2012). …”

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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Functional Analysis of Plant Defense Suppression and Activation by the Xanthomonas Core Type III Effector XopX

Cited by 33 publications

References 86 publications

Quantitative, image-based phenotyping methods provide insight into spatial and temporal dimensions of plant disease

Quantitative, image-based phenotyping methods provide insight into spatial and temporal dimensions of plant disease

Dissecting virulence function from recognition: cell death suppression in Nicotiana benthamiana by XopQ/HopQ1‐family effectors relies on EDS1‐dependent immunity

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

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