skip to main content
Explore Scholarly Publications and Datasets in the NSF-PAR

  • NSF Public Access
  • Search Results
  • Accepted Manuscript: The Pseudomonas syringae type III effector HopG1 triggers necrotic cell death that is attenuated by AtNHR2B

This content will become publicly available on December 1, 2023

Title: The Pseudomonas syringae type III effector HopG1 triggers necrotic cell death that is attenuated by AtNHR2B
Abstract The plant pathogenic bacterium Pseudomonas syringae pv. tomato DC3000 ( Pst DC3000) has become a paradigm to investigate 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. Among those effectors, 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 adapted and non-adapted pathogens. We further showed that HopG1 interacts with the plant immunity-related protein AtNHR2B and that AtNHR2B attenuates HopG1- virulence functions. These results highlight the importance of HopG1 as a multi-faceted protein and uncover its interplay with AtNHR2B.
Authors:
; ; ; ;
Award ID(s):
1842970
Publication Date:
NSF-PAR ID:
10404169
Journal Name:
Scientific Reports
Volume:
12
Issue:
1
ISSN:
2045-2322
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; ; ( , Plant Physiology)
    Abstract

    Basic helix–loop–helix (bHLH) transcription factors constitute a superfamily in eukaryotes, but their roles in plant immunity remain largely uncharacterized. We found that the transcript abundance in tomato (Solanum lycopersicum) leaves of one bHLH transcription factor-encoding gene, negative regulator of resistance to DC3000 1 (Nrd1), increased significantly after treatment with the immunity-inducing flgII-28 peptide. Plants carrying a loss-of-function mutation in Nrd1 (Δnrd1) showed enhanced resistance to Pseudomonas syringae pv. tomato (Pst) DC3000 although early pattern-triggered immunity responses, such as generation of reactive oxygen species and activation of mitogen-activated protein kinases after treatment with flagellin-derived flg22 and flgII-28 peptides, were unaltered compared to wild-type plants. RNA-sequencing (RNA-seq) analysis identified a gene, Arabinogalactan protein 1 (Agp1), whose expression is strongly suppressed in an Nrd1-dependent manner. Agp1 encodes an arabinogalactan protein, and overexpression of the Agp1 gene in Nicotiana benthamiana led to ∼10-fold less Pst growth compared to the control. These results suggest that the Nrd1 protein promotes tomato susceptibility to Pst by suppressing the defense gene Agp1. RNA-seq also revealed that the loss of Nrd1 function has no effect on the transcript abundance of immunity-associated genes, including AvrPtoB tomato-interacting 9 (Bti9), Cold-shock protein receptor (Core), Flagellin sensing 2 (Fls2), Flagellin sensing (Fls3),more »and Wall-associated kinase 1 (Wak1) upon Pst inoculation, suggesting that the enhanced immunity observed in the Δnrd1 mutants is due to the activation of key PRR signaling components as well as the loss of Nrd1-regulated suppression of Agp1.

    « less
  2. ; ; ( , Scientific Reports)
    Abstract The plant apoplast has a crucial role in photosynthesis and respiration due to its vital function in gas exchange and transpiration. The apoplast is also a dynamic environment that participates in many ion and nutrient transport processes via plasma membrane-localized proteins. Furthermore, diverse microbes colonize the plant apoplast, including the hemibiotrophic bacterial pathogen, Pseudomonas syringae pv. tomato ( Pto ) strain DC3000. Pto DC3000 initiates pathogenesis upon moving through stomata into the apoplast and then proliferating to high levels. Here we developed a centrifugation-based method to isolate and quantify the apoplast fluid in Arabidopsis leaves, without significantly damaging the tissue. We applied the simple apoplast extraction method to demonstrate that the Pto DC3000 type III bacterial effectors AvrE1 and HopM1 induce hydration of the Arabidopsis apoplast in advance of macroscopic water-soaking, disruption of host cell integrity, and disease progression. Finally, we demonstrate the utility of the apoplast extraction method for isolation of bacteria proliferating in the apoplast.
  3. ; ; ; ; ; ; ; ( , The EMBO Journal)
    Abstract

    Phytosulfokine (PSK) is a plant pentapeptide hormone that fulfills a wide range of functions. Although PSK has frequently been reported to function in the inverse regulation of growth and defense in response to (hemi)biotrophic pathogens, the mechanisms involved remain largely unknown. Using the tomato (Solanum lycopersicum) andPseudomonas syringaepv.tomato(Pst) DC3000 pathogen system, we present compelling evidence that the PSK receptor PSKR1 interacts with the calcium‐dependent protein kinase CPK28, which in turn phosphorylates the key enzyme of nitrogen assimilation glutamine synthetase GS2 at two sites (Serine‐334 and Serine‐360). GS2 phosphorylation at S334 specifically regulates plant defense, whereas S360 regulates growth, uncoupling the PSK‐induced effects on defense responses and growth regulation. The discovery of these sites will inform breeding strategies designed to optimize the growth‐defense balance in a compatible manner.

  4. ; ; ; ; ; ; ; ; ; ; et al ( , Nature Communications)
    Abstract

    Agrobacterium-mediated plant transformation (AMT) is the basis of modern-day plant biotechnology. One major drawback of this technology is the recalcitrance of many plant species/varieties toAgrobacteriuminfection, most likely caused by elicitation of plant defense responses. Here, we develop a strategy to increase AMT by engineeringAgrobacterium tumefaciensto express a type III secretion system (T3SS) fromPseudomonas syringaeand individually deliver theP. syringaeeffectors AvrPto, AvrPtoB, or HopAO1 to suppress host defense responses. Using the engineeredAgrobacterium, we demonstrate increase in AMT of wheat, alfalfa and switchgrass by ~250%–400%. We also show that engineeredA. tumefaciensexpressing a T3SS can deliver a plant protein, histone H2A-1, to enhance AMT. This strategy is of great significance to both basic research and agricultural biotechnology for transient and stable transformation of recalcitrant plant species/varieties and to deliver proteins into plant cells in a non-transgenic manner.

  5. ; ; ( , Plant Physiology)
    Abstract Plants contain many nucleotide-binding leucine-rich repeat (NLR) proteins that are postulated to function as intracellular immune receptors but do not yet have an identified function during plant-pathogen interactions. SUPPRESSOR OF NPR1-1, CONSTITUTIVE 1 (SNC1) one such NLR protein of the Toll-interleukin 1 receptor (TIR) type despite its well characterized gain-of-function activity and its involvement in autoimmunity in Arabidopsis (Arabidopsis thaliana). Here, we investigated the role of SNC1 in natural plant-pathogen interactions and genetically tested the importance of the enzymatic activities of its TIR domain for its function. The SNC1 loss-of-function mutants were more susceptible to avirulent bacterial pathogen strains of Pseudomonas syringae containing specific effectors, especially under constant light growth condition. The mutants also had reduced defense gene expression induction and hypersensitive responses upon infection by avirulent pathogens under constant light growth condition. In addition, genetic and biochemical studies supported that the TIR enzymatic activity of SNC1 is required for its gain-of-function activity. In sum, our study uncovers a role of SNC1 as an amplifier of plant defense responses during natural plant-pathogen interactions and indicates its use of enzymatic activity and intermolecular interactions for triggering autoimmune responses.
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email