scholarly journals The blast pathogen effector AVR-Pik binds and stabilizes rice heavy metal-associated (HMA) proteins to co-opt their function in immunity

2020 ◽  
Author(s):  
K. Oikawa ◽  
K. Fujisaki ◽  
M. Shimizu ◽  
T. Takeda ◽  
H. Saitoh ◽  
...  
Keyword(s):  
Heavy Metal ◽  
Susceptibility Gene ◽  
Leucine Rich Repeat ◽  
Nucleotide Binding Domain ◽  
Host Proteins ◽  
Immune Receptors ◽  
Pathogen Effectors ◽  
Pathogen Effector ◽  
Integrated Domains ◽  
Complex Architecture

AbstractPlant intracellular nucleotide-binding domain and leucine-rich repeat-containing (NLR) immune receptors have a complex architecture. They can include noncanonical integrated domains that are thought to have evolved from host targets of pathogen effectors to serve as pathogen baits. However, the functions of host proteins with similarity to NLR integrated domains and the extent to which they are targeted by pathogen effectors remain largely unknown. Here, we show that the blast fungus effector AVR-Pik binds a subset of related rice proteins containing a heavy metal-associated (HMA) domain, one of the domains that has repeatedly integrated into plant NLR immune receptors. We find that AVR-Pik binding stabilizes the rice HMA proteins OsHIPP19 and OsHIPP20. Knockout of OsHIPP20 causes enhanced disease resistance towards the blast pathogen, indicating that OsHIPP20 is a susceptibility gene (S-gene). We propose that AVR-Pik has evolved to bind HMA domain proteins and co-opt their function to suppress immunity. Yet this binding carries a trade-off, it triggers immunity in plants carrying NLR receptors with integrated HMA domains.

scholarly journals An unconventional NOI/RIN4 domain of a rice NLR protein binds host EXO70 protein to confer fungal immunity

2017 ◽  
Author(s):  
Koki Fujisaki ◽  
Yoshiko Abe ◽  
Eiko Kanzaki ◽  
Kazue Ito ◽  
Hiroe Utsushi ◽  
...  
Keyword(s):  
Host Protein ◽  
Current View ◽  
Nucleotide Binding Domain ◽  
Host Proteins ◽  
Core Motif ◽  
Pathogen Effectors ◽  
Pathogen Effector ◽  
Integrated Domains ◽  
Effector Recognition ◽  
Fungal Immunity

A subset of plant nucleotide-binding domain and leucine-rich repeat-containing (NLR) proteins carry extraneous integrated domains that have been proposed to mediate pathogen effector recognition. The current view is that these unconventional domains function by directly binding or serving as substrates for pathogen effectors, yet only a few domains have been functionally characterized to date. Here we report that the integrated NOI domain of the rice NLR protein Pii-2, together with its partner Pii-1, mediates immunity to the rice blast fungus Magnaporthe oryzae by indirect recognition of the AVR-Pii effector. We discovered that the Pii-2 NOI domain does not physically interact with the effector itself but instead binds the host protein OsExo70-F3, which is a target of AVR-Pii. We further identified mutations within the NOI core motif (PxFGxW) of Pii-2 that abolish both OsExo70-F3 binding and Pii-mediated resistance to M. oryzae expressing AVR-Pii. This led us to propose a novel conceptual model in which an NLR-integrated domain functions to detect host proteins targeted by pathogen effectors, in a framework that extends classical indirect recognition models.

scholarly journals Lessons in effector and NLR biology of plant-microbe systems

2017 ◽  
Author(s):  
Aleksandra Białas ◽  
Erin K. Zess ◽  
Juan Carlos De la Concepcion ◽  
Marina Franceschetti ◽  
Helen G. Pennington ◽  
...  
Keyword(s):  
Plant Physiology ◽  
Magnaporthe Oryzae ◽  
Rice Blast ◽  
Molecular Mechanisms ◽  
Rice Blast Fungus ◽  
Leucine Rich Repeat ◽  
Nucleotide Binding Domain ◽  
Immune Receptors ◽  
Microbe Interactions ◽  
Host Infection

A diversity of plant-associated organisms secrete effectors—proteins and metabolites that modulate plant physiology to favor host infection and colonization. However, effectors can also activate plant immune receptors, notably nucleotide-binding domain and leucine-rich repeat-containing (NLR) proteins, enabling plants to fight off invading organisms. This interplay between effectors, their host targets, and the matching immune receptors is shaped by intricate molecular mechanisms and exceptionally dynamic coevolution. In this article, we focus on three effectors, AVR-Pik, AVR-Pia, and AVR-Pii, from the rice blast fungus Magnaporthe oryzae (syn. Pyricularia oryzae), and their corresponding rice NLR immune receptors, Pik, Pia, and Pii, to highlight general concepts of plant-microbe interactions. We draw 12 lessons in effector and NLR biology that have emerged from studying these three little effectors and are broadly applicable to other plant-microbe systems.

scholarly journals Lessons in Effector and NLR Biology of Plant-Microbe Systems

2018 ◽  
Vol 31 (1) ◽  
pp. 34-45 ◽  
Author(s):  
Aleksandra Białas ◽  
Erin K. Zess ◽  
Juan Carlos De la Concepcion ◽  
Marina Franceschetti ◽  
Helen G. Pennington ◽  
...  
Keyword(s):  
Plant Physiology ◽  
Rice Blast ◽  
Molecular Mechanisms ◽  
Rice Blast Fungus ◽  
Leucine Rich Repeat ◽  
Repeat Region ◽  
Nucleotide Binding Domain ◽  
Immune Receptors ◽  
Microbe Interactions ◽  
Host Infection

A diversity of plant-associated organisms secrete effectors—proteins and metabolites that modulate plant physiology to favor host infection and colonization. However, effectors can also activate plant immune receptors, notably nucleotide-binding domain and leucine-rich repeat region (NLR)-containing proteins, enabling plants to fight off invading organisms. This interplay between effectors, their host targets, and the matching immune receptors is shaped by intricate molecular mechanisms and exceptionally dynamic coevolution. In this article, we focus on three effectors, AVR-Pik, AVR-Pia, and AVR-Pii, from the rice blast fungus Magnaporthe oryzae (syn. Pyricularia oryzae), and their corresponding rice NLR immune receptors, Pik, Pia, and Pii, to highlight general concepts of plant-microbe interactions. We draw 12 lessons in effector and NLR biology that have emerged from studying these three little effectors and are broadly applicable to other plant-microbe systems.

scholarly journals The potato NLR immune receptor R3a does not contain non-canonical integrated domains

2016 ◽  
Author(s):  
Artemis Giannakopoulou ◽  
Angela Chaparro-Garcia ◽  
Sophien Kamoun
Keyword(s):  
Late Blight ◽  
Unknown Function ◽  
False Positive ◽  
Domain Architecture ◽  
Leucine Rich Repeat ◽  
Plant Genomes ◽  
Pathogen Effectors ◽  
C Terminus ◽  
Domain Of Unknown Function ◽  
Integrated Domains

A recent study by Kroj et al. (New Phytologist, 2016) surveyed nucleotide binding-leucine rich repeat (NLR) proteins from plant genomes for the presence of extraneous integrated domains that may serve as decoys or sensors for pathogen effectors. They reported that a FAM75 domain of unknown function occurs near the C-terminus of the potato late blight NLR protein R3a. Here, we investigated in detail the domain architecture of the R3a protein, its potato paralog R3b, and their tomato ortholog I2. We conclude that the R3a, R3b, and I2 proteins do not carry additional domains besides the classic NLR modules, and that the FAM75 domain match is likely a false positive among computationally predicted NLR-integrated domains.

scholarly journals Dominant integration locus drives continuous diversification of plant immune receptors with exogenous domain fusions

2017 ◽  
Author(s):  
Paul C. Bailey ◽  
Christian Schudoma ◽  
William Jackson ◽  
Erin Baggs ◽  
Gulay Dagdas ◽  
...  
Keyword(s):  
Synthetic Receptors ◽  
Diverse Range ◽  
Ectopic Recombination ◽  
Immune Receptors ◽  
Pathogen Effectors ◽  
Plant Immune System ◽  
Fusion Site ◽  
Plant Genes ◽  
Integrated Domains ◽  
Domain Integration

AbstractBackgroundThe plant immune system is innate, encoded in the germline. Using it efficiently, plants are capable of recognizing a diverse range of rapidly evolving pathogens. A recently described phenomenon shows that plant immune receptors are able to recognize pathogen effectors through the acquisition of exogenous protein domains from other plant genes.ResultsWe showed that plant immune receptors with integrated domains are distributed unevenly across their phylogeny in grasses. Using phylogenetic analysis, we uncovered a major integration clade, whose members underwent repeated independent integration events producing diverse fusions. This clade is ancestral in grasses with members often found on syntenic chromosomes. Analyses of these fusion events revealed that homologous receptors can be fused to diverse domains. Furthermore, we discovered a 43 amino acids long motif that was associated with this dominant integration clade and was located immediately upstream of the fusion site. Sequence analysis revealed that DNA transposition and/or ectopic recombination are the most likely mechanisms of NLR-ID formation.ConclusionsThe identification of this subclass of plant immune receptors that is naturally adapted to new domain integration will inform biotechnological approaches for generating synthetic receptors with novel pathogen ‘baits’.

scholarly journals Structure of the activated ROQ1 resistosome directly recognizing the pathogen effector XopQ

Science ◽  
2020 ◽  
Vol 370 (6521) ◽  
pp. eabd9993 ◽  
Author(s):  
Raoul Martin ◽  
Tiancong Qi ◽  
Haibo Zhang ◽  
Furong Liu ◽  
Miles King ◽  
...  
Keyword(s):  
Active Site ◽  
Nicotiana Benthamiana ◽  
Interleukin 1 ◽  
Leucine Rich Repeat ◽  
Tir Domain ◽  
Pathogen Effectors ◽  
Cryo Electron Microscopy ◽  
Pathogen Effector ◽  
Tir Domains ◽  
Direct Recognition

Plants and animals detect pathogen infection using intracellular nucleotide-binding leucine-rich repeat receptors (NLRs) that directly or indirectly recognize pathogen effectors and activate an immune response. How effector sensing triggers NLR activation remains poorly understood. Here we describe the 3.8-angstrom-resolution cryo–electron microscopy structure of the activated ROQ1 (recognition of XopQ 1), an NLR native to Nicotiana benthamiana with a Toll-like interleukin-1 receptor (TIR) domain bound to the Xanthomonaseuvesicatoria effector XopQ (Xanthomonas outer protein Q). ROQ1 directly binds to both the predicted active site and surface residues of XopQ while forming a tetrameric resistosome that brings together the TIR domains for downstream immune signaling. Our results suggest a mechanism for the direct recognition of effectors by NLRs leading to the oligomerization-dependent activation of a plant resistosome and signaling by the TIR domain.

scholarly journals Structure of the activated Roq1 resistosome directly recognizing the pathogen effector XopQ

2020 ◽  
Author(s):  
Raoul Martin ◽  
Tiancong Qi ◽  
Haibo Zhang ◽  
Furong Liu ◽  
Miles King ◽  
...  
Keyword(s):  
Immune Response ◽  
Active Site ◽  
Interleukin 1 ◽  
Leucine Rich Repeat ◽  
Tir Domain ◽  
Pathogen Effectors ◽  
Cryo Electron Microscopy ◽  
Pathogen Effector ◽  
Tir Domains ◽  
Direct Recognition

AbstractPlants and animals detect pathogen infection via intracellular nucleotide-binding leucine-rich repeat receptors (NLRs) that directly or indirectly recognize pathogen effectors and activate an immune response. How effector sensing triggers NLR activation remains poorly understood. Here we describe the 3.8 Å resolution cryo-electron microscopy structure of the activated Roq1, an NLR native to Nicotiana benthamiana with a Toll-like interleukin-1 receptor (TIR) domain, bound to the Xanthomonas effector XopQ. Roq1 directly binds to both the predicted active site and surface residues of XopQ while forming a tetrameric resistosome that brings together the TIR domains for downstream immune signaling. Our results suggest a mechanism for the direct recognition of effectors by NLRs leading to the oligomerization-dependent activation of a plant resistosome and signaling by the TIR domain.One Sentence SummaryVisualization of an activated plant immune receptor that triggers the immune response upon pathogen recognition.

scholarly journals A genetically linked pair of NLR immune receptors show contrasting patterns of evolution

2021 ◽  
Author(s):  
Motoki Shimizu ◽  
Akiko Hirabuchi ◽  
Yu Sugihara ◽  
Akira Abe ◽  
Takumi Takeda ◽  
...  
Keyword(s):  
Magnaporthe Oryzae ◽  
Balancing Selection ◽  
Nucleotide Binding ◽  
Defense Responses ◽  
Blast Disease ◽  
Phylogenomic Analysis ◽  
Leucine Rich Repeat ◽  
Pathogen Effectors ◽  
Integrated Domains ◽  
Domain Integration

AbstractThroughout their evolution, plant nucleotide-binding leucine-rich-repeat receptors (NLRs) have acquired widely divergent unconventional integrated domains that enhance their ability to detect pathogen effectors. However, the functional dynamics that drive the evolution of NLRs with integrated domains (NLR-IDs) remain poorly understood. Here, we reconstructed the evolutionary history of an NLR locus prone to unconventional domain integration and experimentally tested hypotheses about the evolution of NLR-IDs. We show that the rice (Oryza sativa) NLR Pias recognizes the effector AVR-Pias of the blast fungal pathogen Magnaporthe oryzae. Pias consists of a functionally specialized NLR pair, the helper Pias-1 and the sensor Pias-2, and is allelic to the previously characterized Pia pair of NLRs: the helper RGA4 and the sensor RGA5. Remarkably, Pias-2 carries a C-terminal DUF761 domain at a similar position to the heavy metal–associated (HMA) domain of RGA5. Phylogenomic analysis showed that Pias-2/RGA5 sensor NLRs have undergone recurrent genomic recombination within the genus Oryza, resulting in up to six sequence-divergent domain integrations. Allelic NLRs with divergent functions have been maintained trans-species in different Oryza lineages to detect sequence-divergent pathogen effectors. By contrast, Pias-1 has retained its NLR helper activity throughout evolution and is capable of functioning together with the divergent sensor-NLR RGA5 to recognize AVR-Pia. These results suggest that opposite selective forces have driven the evolution of paired NLRs: highly dynamic domain integration events maintained by balancing selection for sensor NLRs, in sharp contrast to purifying selection and functional conservation of immune signaling for helper NLRs.Significance statementPlants have evolved sophisticated defense mechanisms to fend off pathogens. Plant nucleotide-binding leucine-rich repeat receptor (NLR) proteins play crucial roles in detecting pathogen molecules inside plant cells and mounting defense responses. Here, we identified the Pias gene from rice, which encodes the NLR pair Pias-1 “helper” and Pias-2 “sensor.” These proteins function together to detect the pathogen molecule AVR-Pias of Magnaporthe oryzae and defend against rice blast disease. Pias is allelic to the previously reported Pia gene. A comparison of Pias/Pia alleles among Oryza species showed that Pias/Pia helper is evolutionarily and functionally conserved, whereas Pias/Pia sensor shows highly dynamic evolution, with various host domains integrated into similar positions, allowing it to detect a wide variety of pathogen molecules.

scholarly journals Recognitional Specificity and Evolution in the Tomato–Cladosporium fulvum Pathosystem

2009 ◽  
Vol 22 (10) ◽  
pp. 1191-1202 ◽  
Author(s):  
B. B. H. Wulff ◽  
A. Chakrabarti ◽  
D. A. Jones
Keyword(s):  
Defense Mechanisms ◽  
Extracellular Proteins ◽  
Effector Proteins ◽  
Cladosporium Fulvum ◽  
Host Proteins ◽  
Pathogen Effectors ◽  
Passalora Fulva ◽  
Pathogen Effector ◽  
Mold Fungus ◽  
Avr Genes

The interactions between plants and many biotrophic or hemibiotrophic pathogens are controlled by receptor proteins in the host and effector proteins delivered by the pathogen. Pathogen effectors facilitate pathogen growth through the suppression of host defenses and the manipulation of host metabolism, but recognition of a pathogen-effector protein by a host receptor enables the host to activate a suite of defense mechanisms that limit pathogen growth. In the tomato (Lycopersicon esculentum syn. Solanum lycopersicum)–Cladosporium fulvum (leaf mold fungus syn. Passalora fulva) pathosystem, the host receptors are plasma membrane–anchored, leucine-rich repeat, receptor-like proteins encoded by an array of Cf genes conferring resistance to C. fulvum. The pathogen effectors are mostly small, secreted, cysteine-rich, but otherwise largely dissimilar, extracellular proteins encoded by an array of avirulence (Avr) genes, so called because of their ability to trigger resistance and limit pathogen growth when the corresponding Cf gene is present in tomato. A number of Cf and Avr genes have been isolated, and details of the complex molecular interplay between tomato Cf proteins and C. fulvum effector proteins are beginning to emerge. Each effector appears to have a different role; probably most bind or modify different host proteins, but at least one has a passive role masking the pathogen. It is, therefore, not surprising that each effector is probably detected in a distinct and specific manner, some by direct binding, others as complexes with host proteins, and others via their modification of host proteins. The two papers accompanying this review contribute further to our understanding of the molecular specificity underlying effector perception by Cf proteins. This review, therefore, focuses on our current understanding of recognitional specificity in the tomato–C. fulvum pathosystem and highlights some of the critical questions that remain to be addressed. It also addresses the evolutionary causes and consequences of this specificity.

scholarly journals Protein engineering expands the effector recognition profile of a rice NLR immune receptor

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Juan Carlos De la Concepcion ◽  
Marina Franceschetti ◽  
Dan MacLean ◽  
Ryohei Terauchi ◽  
Sophien Kamoun ◽  
...  
Keyword(s):  
Protein Engineering ◽  
Direct Interaction ◽  
Structural Basis ◽  
In Planta ◽  
Pathogen Effectors ◽  
Binding Interface ◽  
Pathogen Effector ◽  
Integrated Domains

Plant nucleotide binding, leucine-rich repeat (NLR) receptors detect pathogen effectors and initiate an immune response. Since their discovery, NLRs have been the focus of protein engineering to improve disease resistance. However, this approach has proven challenging, in part due to their narrow response specificity. Previously, we revealed the structural basis of pathogen recognition by the integrated heavy metal associated (HMA) domain of the rice NLR Pikp (Maqbool et al., 2015). Here, we used structure-guided engineering to expand the response profile of Pikp to variants of the rice blast pathogen effector AVR-Pik. A mutation located within an effector-binding interface of the integrated Pikp–HMA domain increased the binding affinity for AVR-Pik variants in vitro and in vivo. This translates to an expanded cell-death response to AVR-Pik variants previously unrecognized by Pikp in planta. The structures of the engineered Pikp–HMA in complex with AVR-Pik variants revealed the mechanism of expanded recognition. These results provide a proof-of-concept that protein engineering can improve the utility of plant NLR receptors where direct interaction between effectors and NLRs is established, particularly where this interaction occurs via integrated domains.

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