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1.
Proc Natl Acad Sci U S A ; 118(47)2021 11 23.
Article in English | MEDLINE | ID: mdl-34799454

ABSTRACT

Pathogenic effector proteins use a variety of enzymatic activities to manipulate host cellular proteins and favor the infection process. However, these perturbations can be sensed by nucleotide-binding leucine-rich-repeat (NLR) proteins to activate effector-triggered immunity (ETI). Here we have identified a small molecule (Zaractin) that mimics the immune eliciting activity of the Pseudomonas syringae type III secreted effector (T3SE) HopF1r and show that both HopF1r and Zaractin activate the same NLR-mediated immune pathway in Arabidopsis Our results demonstrate that the ETI-inducing action of pathogenic effectors can be harnessed to identify synthetic activators of the eukaryotic immune system.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/drug effects , Carrier Proteins/metabolism , Plant Immunity/drug effects , Small Molecule Libraries/pharmacology , Arabidopsis/microbiology , Bacterial Proteins/metabolism , NLR Proteins/metabolism , Plant Diseases/microbiology , Protein Binding/drug effects , Pseudomonas syringae/pathogenicity
2.
PLoS Pathog ; 15(7): e1007900, 2019 07.
Article in English | MEDLINE | ID: mdl-31269090

ABSTRACT

The Pseudomonas syringae acetyltransferase HopZ1a is delivered into host cells by the type III secretion system to promote bacterial growth. However, in the model plant host Arabidopsis thaliana, HopZ1a activity results in an effector-triggered immune response (ETI) that limits bacterial proliferation. HopZ1a-triggered immunity requires the nucleotide-binding, leucine-rich repeat domain (NLR) protein, ZAR1, and the pseudokinase, ZED1. Here we demonstrate that HopZ1a can acetylate members of a family of 'receptor-like cytoplasmic kinases' (RLCK family VII; also known as PBS1-like kinases, or PBLs) and promote their interaction with ZED1 and ZAR1 to form a ZAR1-ZED1-PBL ternary complex. Interactions between ZED1 and PBL kinases are determined by the pseudokinase features of ZED1, and mutants designed to restore ZED1 kinase motifs can (1) bind to PBLs, (2) recruit ZAR1, and (3) trigger ZAR1-dependent immunity in planta, all independently of HopZ1a. A ZED1 mutant that mimics acetylation by HopZ1a also triggers immunity in planta, providing evidence that effector-induced perturbations of ZED1 also activate ZAR1. Overall, our results suggest that interactions between these two RLCK families are promoted by perturbations of structural features that distinguish active from inactive kinase domain conformations. We propose that effector-induced interactions between ZED1/ZRK pseudokinases (RLCK family XII) and PBL kinases (RLCK family VII) provide a sensitive mechanism for detecting perturbations of either kinase family to activate ZAR1-mediated ETI.


Subject(s)
Arabidopsis Proteins/immunology , Arabidopsis Proteins/metabolism , Arabidopsis/immunology , Arabidopsis/metabolism , Phosphotransferases/immunology , Phosphotransferases/metabolism , Plant Immunity , Acetylation , Arabidopsis/genetics , Arabidopsis Proteins/chemistry , Arabidopsis Proteins/genetics , Bacterial Proteins/chemistry , Bacterial Proteins/metabolism , Carrier Proteins/chemistry , Carrier Proteins/immunology , Carrier Proteins/metabolism , Host Microbial Interactions/genetics , Host Microbial Interactions/immunology , Models, Immunological , Mutation , Phosphotransferases/genetics , Protein Interaction Domains and Motifs , Protein Kinases/chemistry , Protein Kinases/metabolism , Pseudomonas syringae/immunology , Pseudomonas syringae/metabolism , Pseudomonas syringae/pathogenicity
3.
Plant J ; 93(4): 651-663, 2018 02.
Article in English | MEDLINE | ID: mdl-29160935

ABSTRACT

Phytopathogens translocate effector proteins into plant cells where they sabotage the host cellular machinery to promote infection. An individual pathogen can translocate numerous distinct effectors during the infection process to target an array of host macromolecules (proteins, metabolites, DNA, etc.) and manipulate them using a variety of enzymatic activities. In this review, we have surveyed the literature for effector targets and curated them to convey the range of functions carried out by phytopathogenic proteins inside host cells. In particular, we have curated the locations of effector targets, as well as their biological and molecular functions and compared these properties across diverse phytopathogens. This analysis validates previous observations about effector functions (e.g. immunosuppression), and also highlights some interesting features regarding effector specificity as well as functional diversification of phytopathogen virulence strategies.


Subject(s)
Bacteria/pathogenicity , Host-Pathogen Interactions , Oomycetes/pathogenicity , Plant Diseases/microbiology , Plants/microbiology , Bacteria/metabolism , Oomycetes/metabolism , Plant Diseases/immunology , Plant Immunity , Plants/immunology
5.
Front Plant Sci ; 11: 1290, 2020.
Article in English | MEDLINE | ID: mdl-32983191

ABSTRACT

The Arabidopsis nucleotide-binding leucine-rich repeat protein ZAR1 can recognize at least six distinct families of pathogenic effector proteins to mount an effector-triggered immune response. This remarkable immunodiversity appears to be conveyed by receptor-like cytoplasmic kinase (RLCK) complexes, which associate with ZAR1 to sense several effector-induced kinase perturbations. Here we show that the recently identified ZAR1-mediated immune responses against the HopX1, HopO1, and HopBA1 effector families of Pseudomonas syringae rely on an expanded diversity of RLCK sensors. We show that individual sensors can recognize distinct effector families, thereby contributing to the expanded surveillance potential of ZAR1 and supporting its role as a guardian of the plant kinome.

6.
Mol Plant Pathol ; 18(3): 457-468, 2017 04.
Article in English | MEDLINE | ID: mdl-27061875

ABSTRACT

Pseudomonas syringae is a bacterial phytopathogen that utilizes the type III secretion system to inject effector proteins into plant host cells. Pseudomonas syringae can infect a wide range of plant hosts, including agronomically important crops such as tomatoes and beans. The ability of P. syringae to infect such numerous hosts is caused, in part, by the diversity of effectors employed by this phytopathogen. Over 60 different effector families exist in P. syringae; one such family is HopF, which contains over 100 distinct alleles. Despite this diversity, research has focused on only two members of this family: HopF1 from P. syringae pathovar phaseolicola 1449B and HopF2 from P. syringae pathovar tomato DC3000. In this study, we review the research on HopF family members, including their host targets and molecular mechanisms of immunity suppression, and their enzymatic function. We also provide a phylogenetic analysis of this expanding effector family which provides a basis for a proposed nomenclature to guide future research. The extensive genetic diversity that exists within the HopF family presents a great opportunity to study how functional diversification on an effector family contributes to host specialization.


Subject(s)
Bacterial Proteins/metabolism , Bacterial Secretion Systems , Pseudomonas syringae/metabolism , Amino Acid Sequence , Bacterial Proteins/chemistry , Bacterial Secretion Systems/chemistry , Bacterial Secretion Systems/metabolism , Phylogeny
7.
Nat Plants ; 3: 17027, 2017 03 13.
Article in English | MEDLINE | ID: mdl-28288096

ABSTRACT

Nucleotide-binding domain and leucine-rich repeat domain-containing (NLR) proteins are sentinels of plant immunity that monitor host proteins for perturbations induced by pathogenic effector proteins. Here we show that the Arabidopsis ZAR1 NLR protein requires the ZRK3 kinase to recognize the Pseudomonas syringae type III effector (T3E) HopF2a. These results support the hypothesis that ZAR1 associates with an expanded ZRK protein family to broaden its effector recognition spectrum.


Subject(s)
Arabidopsis Proteins/genetics , Arabidopsis/genetics , Arabidopsis/immunology , Bacterial Proteins/genetics , Carrier Proteins/genetics , Plant Immunity , Protein Serine-Threonine Kinases/genetics , Pseudomonas syringae/physiology , Amino Acid Sequence , Arabidopsis Proteins/chemistry , Arabidopsis Proteins/immunology , Bacterial Proteins/metabolism , Carrier Proteins/chemistry , Carrier Proteins/immunology , NLR Proteins/chemistry , NLR Proteins/genetics , NLR Proteins/immunology , Protein Serine-Threonine Kinases/chemistry , Protein Serine-Threonine Kinases/immunology
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