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Science: Glycosidase and glycan polymorphism control hydrolytic release of immunogenic flagellin peptides (2019)

Science: Glycosidase and glycan polymorphism control hydrolytic release of immunogenic flagellin peptides (2019) | Plants and Microbes | Scoop.it

INTRODUCTION

Immunogenic flagellin fragments are a signature of bacterial invasion in both plants and animals. Plants recognize flagellin fragments via flagellin sensitive 2 (FLS2), a model receptor kinase that is highly conserved among angiosperms. However, little is known about events upstream of flagellin perception by FLS2. The flagellin fragments recognized by FLS2 are buried in the flagellin polymer structure and require hydrolytic release before recognition can occur, yet the hydrolases releasing these elicitors remain to be identified. Uncovering their identity is a daunting task because the extracellular space of plants (the apoplast) contains hundreds of uncharacterized glycosidases and proteases.

RATIONALE

We reasoned that pathogenic bacteria would suppress plant hydrolases that are important for immunity. To identify suppressed hydrolases in the apoplast of infected plants, we applied activity-based protein profiling with the use of chemical probes that irreversibly label the active site of hydrolases. We applied this strategy to study the infection of the tobacco relative Nicotiana benthamiana with the bacterial pathogens Pseudomonas syringae pv. tabaci(Pta6605), P. syringae pv. syringae (PsyB728a), and a virulent mutant of P. syringae pv. tomato[PtoDC3000(ΔhQ)].

RESULTS

Glycosidase activity profiling of apoplastic fluids isolated from PtoDC3000(ΔhQ)-infected plants revealed that the activity of β-galactosidase 1 (BGAL1) is suppressed in the apoplast during infection. BGAL1 suppression is caused by a heat-stable, basic, small inhibitor molecule that is produced by the bacteria under the control of hrpR/S/L virulence regulators. Null mutants of N. benthamiana lacking BGAL1 generated by genome editing have substantially reduced apoplastic β-galactosidase activity and are more susceptible to PtoDC3000(ΔhQ), demonstrating that BGAL1 contributes to immunity. When investigating how BGAL1 functions in immunity, we discovered that treatment of PtoDC3000(ΔhQ) and Pta6605 bacteria with apoplastic fluids containing BGAL1 results in the release of an elicitor that triggers a burst of reactive oxygen species in leaf discs, a signature immune response in plants. The released elicitor is flagellin derived because the triggered immune response requires both the FLS2 receptor in the plant and the flagellin-encoding fliC gene in the bacteria. More precisely, treatment of purified flagella with apoplastic fluids containing BGAL1 facilitates the release of immunogenic peptides from flagellin.

The flagellin polymer of both PtoDC3000(ΔhQ) and Pta6605 is O-glycosylated with glycans consisting of several rhamnose residues and a terminal modified viosamine (mVio). Mutant Pta6605 bacteria carrying nonglycosylated flagellin, or carrying rhamnosylated flagellin lacking mVio, trigger the plant immune response when treated with apoplastic fluids, irrespective of BGAL1 presence, thus demonstrating that BGAL1 requires mVio for its function in immunity. Addition of a protease inhibitor cocktail to apoplastic fluids blocks the release of the flagellin elicitor from nonglycosylated flagellin, implicating apoplastic proteases in elicitor release acting downstream of BGAL1. Consistent with a specific role of BGAL1 in elicitor release, bgal1 null mutants of N. benthamiana show increased susceptibility only to bacterial strains carrying mVio. Treatment of PsyB728a with apoplastic fluids containing BGAL1 does not facilitate release of the flagellin elicitor because its flagellin carries a different glycan moiety lacking mVio, thus providing protection against recognition.

CONCLUSION

Glycosidase BGAL1 acts upstream of proteases in the apoplast of N. benthamiana to release immunogenic peptides from glycosylated flagellin, but only on glycosylated flagellin containing mVio. P. syringae strains use both BGAL1 inhibitors and glycan polymorphism to suppress BGAL1 function and escape recognition. Glycan polymorphism is common to bacterial pathogens, indicating a general role for flagellin glycans in evading recognition of bacterial pathogens by both plants and animals.

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Zenodo: Death switch: how resistosomes activate immunity (2019)

Zenodo: Death switch: how resistosomes activate immunity (2019) | Plants and Microbes | Scoop.it

Pathogen perception triggers a monomeric NLR plant immune receptor to form a pentameric wheel-like complex termed a resistosome, with the N-terminal ahelices forming a funnel-shaped structure that may perturb plasma membrane integrity to cause hypersensitive cell death.

 

Nucleotide-binding leucine-rich repeat (NLR) proteins are intracellular receptors that detect pathogen molecules and activate a robust immune response that includes the hypersensitive response (HR) cell death in plants. Although plant NLRs are known to oilgomerize through their N-terminal domains, such as the coiled coil (CC) domain, the molecular mechanisms that underpin plant NLR activation and the subsequent execution of HR cell death have remained largely unknown. In two recent paradigm-shifting Science papers, Wang et al. have advanced our understanding of both the structural and biochemical bases of NLR activation in plants, creating a new conceptual framework. They reconstituted both the inactive and active complexes of the CC-NLR protein HOPZ-ACTIVATED RESISTANCE1 (ZAR1) with its partner receptor-like cytoplasmic kinases (RLCKs) and used cryo-electron microscopy to show that activated ZAR1 forms a resistosome—a wheel-like pentamer that can switch conformation to expose a funnel-shaped structure formed by the very N-terminal ahelices (a1) of the CC domains. They propose a provocative model in which the five exposeda1 helices of the ZAR1 resistosome form a funnel-like structurethat triggers HR cell death by translocating into the plasma membrane and perturbing membrane integrity similar to pore-forming toxins.

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Science: Reconstitution and structure of a plant NLR resistosome conferring immunity (2019)

Science: Reconstitution and structure of a plant NLR resistosome conferring immunity (2019) | Plants and Microbes | Scoop.it

INTRODUCTION

Nucleotide-binding (NB), leucine-rich repeat (LRR) receptors (NLRs) mediate plant immunity by directly or indirectly sensing pathogen effector proteins delivered into plant cells. The activation of plant NLRs stops pathogen proliferation through the induction of a variety of defenses, including the hypersensitive response, a form of programmed cell death. In the small mustard plant Arabidopsis thaliana, the coiled-coil (CC)–NLR HOPZ-ACTIVATED RESISTANCE 1 (ZAR1) exists in a preformed complex with resistance-related kinase 1 (RKS1) to sense the uridylyltransferase effector AvrAC from the microbial pathogen Xanthomonas campestris pv. campestris (Xcc). AvrAC uridylates the PBS1-like protein 2 (PBL2) kinase to produce PBL2UMP, which is recruited to ZAR1-RKS1. As members of the adenosine triphosphatases associated with diverse cellular activities, NLRs are hypothesized to function through oligomerization. Evidence for this model is provided by studies of animal NLRs. However, whether plant NLRs oligomerize after activation into large protein complexes like NLR inflammasomes remains unknown. Furthermore, little is known about the biochemical functions of plant NLRs.

RATIONALE

In an accompanying paper, we show that the ZAR1-RKS1-PBL2UMP complex in the absence of deoxyadenosine triphosphate (dATP) or adenosine triphosphate (ATP) is in a primed state. Gel filtration and cryo–electron microscopy (cryo-EM) were used to investigate whether the primed complex oligomerizes in the presence of dATP or ATP. We verified the biological relevance of the oligomerized ZAR1-RKS1-PBL2UMP complex induced by dATP or ATP with biochemical, cell-based, and functional assays.

RESULTS

Gel filtration analysis showed that ZAR1-RKS1 and PBL2UMP formed a high-order oligomeric complex with a molecular mass of ~900 kDa in the presence of dATP or ATP. We termed the complex the ZAR1 resistosome. A cryo-EM structure of the ZAR1 resistosome determined at a resolution of 3.4 Å revealed that it formed a wheel-like pentamer, the assembly of which is mediated by ZAR1. All the structural domains of ZAR1, including the CC domain, NB domain (NBD), helical domain 1 (HD1), winged-helix domain (WHD), and LRR domain, are involved in the pentamerization of the ZAR1 resistosome, which is further stabilized by dATP. Mutagenesis analyses and functional studies indicate that the resistosome activates the defensive hypersensitive cell death response and contributes to resistance to Xcc.

The ZAR1 CC domain (ZAR1CC) contributes to the oligomerization of the ZAR1 resistosome by forming an α-helical barrel. ZAR1CC undergoes fold switching during ZAR1 activation, in addition to the structural remodeling of ZAR1WHD-ZAR1LRR relative to ZAR1NBD-ZAR1HD1. The very N-terminal α helix (α1) buried in the inactive ZAR1 becomes exposed in the ZAR1 resistosome. The five exposed α1 helices in the ZAR1 resistosome form a funnel-shaped structure projecting out of the wheel-defined plane. Biochemical and functional data showed that this structure is required for AvrAC-induced ZAR1 plasma membrane (PM) association, cell death, and resistance to Xcc. Simultaneous mutation of two negatively charged residues at its inner surface did not affect ZAR1 binding to the PM but did abolish cell death and disease resistance, suggesting that the ZAR1 resistosome function requires the inner surface of the funnel structure.

CONCLUSION

Our study revealed the oligomerization of ZAR1, a plant NLR protein; clarified its activation mechanism; and provided insights into its biochemical functions.

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Science: A pentangular plant inflammasome (2019)

Science: A pentangular plant inflammasome (2019) | Plants and Microbes | Scoop.it

Like animals, plants require, and have evolved, a robust innate immune system. Plants can detect and respond to pathogen-derived molecules (effectors) through cell surface receptors and intracellular receptors, typically encoded by disease resistance (R) genes. Analysis of plant genome sequences reveals hundreds of such nucleotide-binding, leucine-rich repeat (NLR) proteins encoded by putative R genes. How such NLR proteins function has long been a matter of speculation. On page 43 and 44 of this issue, Wang et al. (1) and Wang et al. (2), respectively, end much of the speculation by defining the mechanism of activation for at least one NLR, the Arabidopsis thaliana HOPZ-ACTIVATED RESISTANCE 1 (ZAR1) protein, which activates defense in response to several pathogenic bacterial effectors.

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bioRxiv: Structure-function analysis of ZAR1 immune receptor reveals key molecular interactions for activity (2019)

bioRxiv: Structure-function analysis of ZAR1 immune receptor reveals key molecular interactions for activity (2019) | Plants and Microbes | Scoop.it

NLR (Nucleotide-binding [NB] Leucine-rich repeat [LRR] Receptor) proteins are critical for inducing immune responses in response to pathogen proteins, and must be tightly regulated to prevent spurious activation in the absence of a pathogen. The ZAR1 NLR recognizes diverse effector proteins from Pseudomonas syringae, including HopZ1a, and Xanthomonas species. Receptor-like cytoplasmic kinases (RLCKs) such as ZED1, interact with ZAR1 and provide specificity for different effector proteins, such as HopZ1a. We previously developed a transient expression system in Nicotiana benthamiana, that allowed us to demonstrate ZAR1 function is conserved from the Brassicaceae to the Solanaceae. Here, we combined structural modeling of ZAR1, with molecular and functional assays in our transient system, to show that multiple intramolecular and intermolecular interactions regulate ZAR1 activity. We identified new determinants required for the formation of the ZARCC dimer and its activity. Lastly, we characterized new intramolecular interactions between ZAR1 subdomains that participate in keeping ZAR1 immune complexes inactive. This work identifies molecular constraints on immune receptor function and activation.

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Protein Data Bank: 6J5T - Reconstitution and structure of a plant NLR resistosome conferring immunity (2019)

Protein Data Bank: 6J5T - Reconstitution and structure of a plant NLR resistosome conferring immunity (2019) | Plants and Microbes | Scoop.it

This is stunning! Plants have inflammasomes! Structure of the Arabidopsis NLR immune receptor ZAR1 in complex with its guarded kinases RKS1 and PBL2. Paper appears to be in press.

 

Wang, J.Z., Hu, M.J., Wang, J., Qi, J.F., Han, Z.F., Wang, G.X., Qi, Y.J., Wang, H.W., Zhou, J.M., Chai, J.J. 2019. Reconstitution and structure of a plant NLR resistosome conferring immunity. Science --: --

 

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Annual Rev Phytopathol: Flax Rust Resistance Gene Specificity is Based on Direct Resistance-Avirulence Protein Interactions (2007)

Annual Rev Phytopathol: Flax Rust Resistance Gene Specificity is Based on Direct Resistance-Avirulence Protein Interactions (2007) | Plants and Microbes | Scoop.it

Genetic studies of the flax-flax rust interaction led to the formulation of the gene-for-gene hypothesis and identified resistance genes (R) in the host plant and pathogenicity genes, including avirulence (Avr) and inhibitor of avirulence genes (I), in the rust pathogen. R genes have now been cloned from four of the five loci in flax and all encode proteins of the Toll, Interleukin-1 receptor, R gene-nucleotide binding site-leucine-rich repeat (TIR-NBS-LRR) class. Avr genes have been cloned from four loci in flax rust and encode small secreted proteins with no between locus similarity and no close homologs in current data bases. It is postulated that Avr proteins enter the host cell, have virulence effector functions, and in resistant host genotypes, are recognized by direct and specific interaction with host R proteins, leading to activation of rust resistance defense responses. Direct interaction between R and Avr proteins is the basis of gene-for-gene specificity in the flax-flax rust system and both R and Avr genes have the signatures of diversifying selection, suggesting the existence of a coevolutionary arms race between the host plant and its obligate rust pathogen.

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The Plant Pathology Journal: The Current Situation and Future Impacts (2019)

The Plant Pathology Journal: The Current Situation and Future Impacts (2019) | Plants and Microbes | Scoop.it

Wheat blast occurred in Bangladesh for the first time in Asia in 2016. It is caused by a fungal pathogen, Magnaporthe oryzae Triticum (MoT) pathotype. In this review, we focused on the current status of the wheat blast in regard to host, pathogen, and environment. Despite the many efforts to control the disease, it expanded to neighboring regions including India, the world's second largest wheat producer. However, the disease occurrence has definitely decreased in quantity, because of many farmers chose to grow alternate crops according to the government’s directions. Bangladesh government planned to introduce blast resistant cultivars but knowledges about genetics of resistance is limited. The genome analyses of the pathogen population revealed that the isolates caused wheat blast in Bangladesh are genetically close to a South American lineage of Magnaporthe oryzae. Understanding the genomes of virulent strains would be important to find target resistance genes for wheat breeding. Although the drier winter weather in Bangladesh was not favorable for development of wheat blast before, recent global warming and climate change are posing an increasing risk of disease development. Bangladesh outbreak in 2016 was likely to be facilitated by an extraordinary warm and humid weather in the affected districts before the harvest season. Coordinated international collaboration and steady financial supports are needed to mitigate the fearsome wheat blast in South Asia before it becomes a catastrophe.

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Zenodo: NLR singletons, pairs and networks: evolution, assembly and regulation of the intracellular immunoreceptor circuitry of plants (2019)

Zenodo: NLR singletons, pairs and networks: evolution, assembly and regulation of the intracellular immunoreceptor circuitry of plants (2019) | Plants and Microbes | Scoop.it

NLRs are modular plant and animal proteins that are intracellular sensors of pathogen-associated molecules that trigger a potent broad-spectrum immune reaction known as the hypersensitive response. An emerging paradigm is that plant NLRs form immune signalling networks with varying degrees of complexity. NLRs may have evolved from multifunctional singleton receptors, which combine pathogen detection (sensor activity) and immune signalling (helper or executor activity) into a single protein, to functionally specialized interconnected receptor pairs and networks. In this article, we highlight some of the recent advances in plant NLR biology by discussing models of NLR evolution, NLR complex formation, and how NLR (mis)regulation modulates immunity and autoimmunity. Multidisciplinary approaches are required to dissect the evolution, assembly and regulation of the immune receptor circuitry of plants.

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Nature Biotech: Resistance gene cloning from a wild crop relative by sequence capture and association genetics (2019)

Nature Biotech: Resistance gene cloning from a wild crop relative by sequence capture and association genetics (2019) | Plants and Microbes | Scoop.it

Disease resistance (R) genes from wild relatives could be used to engineer broad-spectrum resistance in domesticated crops. We combined association genetics with R gene enrichment sequencing (AgRenSeq) to exploit pan-genome variation in wild diploid wheat and rapidly clone four stem rust resistance genes. AgRenSeq enables R gene cloning in any crop that has a diverse germplasm panel.


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Nature Ecology & Evolution: The global burden of pathogens and pests on major food crops (2019)

Nature Ecology & Evolution: The global burden of pathogens and pests on major food crops (2019) | Plants and Microbes | Scoop.it

Crop pathogens and pests reduce the yield and quality of agricultural production. They cause substantial economic losses and reduce food security at household, national and global levels. Quantitative, standardized information on crop losses is difficult to compile and compare across crops, agroecosystems and regions. Here, we report on an expert-based assessment of crop health, and provide numerical estimates of yield losses on an individual pathogen and pest basis for five major crops globally and in food security hotspots. Our results document losses associated with 137 pathogens and pests associated with wheat, rice, maize, potato and soybean worldwide. Our yield loss (range) estimates at a global level and per hotspot for wheat (21.5% (10.1–28.1%)), rice (30.0% (24.6–40.9%)), maize (22.5% (19.5–41.1%)), potato (17.2% (8.1–21.0%)) and soybean (21.4% (11.0–32.4%)) suggest that the highest losses are associated with food-deficit regions with fast-growing populations, and frequently with emerging or re-emerging pests and diseases. Our assessment highlights differences in impacts among crop pathogens and pests and among food security hotspots. This analysis contributes critical information to prioritize crop health management to improve the sustainability of agroecosystems in delivering services to societies.

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Molecular Plant Pathology: Pyricularia graminis‐tritici is not the correct species name for the wheat blast fungus: response to Ceresini et al. (2019)

Molecular Plant Pathology: Pyricularia graminis‐tritici is not the correct species name for the wheat blast fungus: response to Ceresini et al. (2019) | Plants and Microbes | Scoop.it

In a review article published in this issue of Molecular Plant Pathology, Ceresini et al. (2019) wrongly treat the wheat blast fungus as a new species, Pyricularia graminis‐tritici (Pygt), following the proposal of Castroagudin et al. (2016). Despite the host specificity implied by the name Pygt, the proposed species concept includes isolates that cause major disease epidemics on finger millet and turf grasses (Castroagudin et al., 2016, 2017). These authors also conclude, based on little evidence, that ‘the hypothesis of grass‐specific populations for the overall Pyricularia oryzae species complex is falsified’. In addition, they stress that the rice blast fungus, which they describe as P. oryzae, ‘may not provide a suitable model for understanding the biology of Pygt’. All of these conclusions are misinformed and have serious consequences. International quarantine regulations are needed to block the movement of this fearsome seed‐borne blast fungus through the trade of seed or grain. The Pygt designation magnifies the challenge by grouping the dangerous, highly aggressive wheat pathogens from South America and Bangladesh, which are readily distinguishable from other P. oryzae lineages, with non‐wheat pathogens that are already found worldwide and are not known to be virulent on wheat or rice. Careful biological analysis of wheat blast host–pathogen interactions has clearly shown that studies of other host‐adapted forms of the fungus are relevant to an understanding of wheat blast and the development of new methods for disease control. Here, we summarize the overwhelming evidence that supports the alternative, internationally recognized designation of Pyricularia oryzae (synonym Magnaporthe oryzae; Zhang et al., 2016) as a single species divided into host‐adapted lineages with limited primary host ranges. We also delineate the errors that led Ceresini et al. (2019) to their false conclusions. The same discussion applies to a second recently published review on the same topic (Ceresini et al., 2018).

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Resource: BRIGIT Vector Borne Disease of Plants (2019)

Resource: BRIGIT Vector Borne Disease of Plants (2019) | Plants and Microbes | Scoop.it

BRIGIT builds a collaborative capability to understand and prevent introduction of arthropod-borne plant pathogens to the UK and the challenges it poses to the UK flora.


Xylella fastidiosa has been described by the European Commission as “one of the most dangerous plant bacteria worldwide”.

 

This insect-transmitted bacterial plant pathogen infects >500 species including crops, ornamental plants, and trees. In Italy alone, over one million olive trees are dying from Xylella in a disease called Olive Quick Decline Syndrome. So far, Xylella has not been reported in the UK.

 

Infected plants can show leaf scorching and loss of leaves or fruit. Although these symptoms may not appear at first, infected plants will eventually die and currently there is no known cure for the disease.

 

Xylella is a bacterial pathogen, transmitted by insects that feed on the xylem, a plant tissue that transports water from roots to leaves in plants. These bugs include sharpshooters in the Americas and spittlebugs/froghoppers in Europe, including the UK. If Xylella-infected plants or carrier insects enter the UK, there is potential for the disease to spread to many plants through native insects or via transport of plants across the UK by humans, with consequences for commercial and amenity horticulture, forestry, crop production, woodlands and wider biodiversity, with economic, environmental and social impacts.

 

Despite this threat, very little is known about how the bacteria might spread in Northern European climates as most research on Xylella and its insect vectors has been based in warmer southern climates. Plants are imported into the UK every day and greater knowledge is required to prevent the further Xylella spread.

 

BRIGIT will develop new methods to detect the bacterium and develop understanding of factors that could contribute to Xylella entry and dispersal in the UK. The project interacts with stakeholders and policymakers to reduce the impacts of Xylella in the UK and mitigate the impacts of the pathogen.

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PNAS: Biosynthesis and secretion of the microbial sulfated peptide RaxX and binding to the rice XA21 immune receptor (2019)

PNAS: Biosynthesis and secretion of the microbial sulfated peptide RaxX and binding to the rice XA21 immune receptor (2019) | Plants and Microbes | Scoop.it

The rice immune receptor XA21 is activated by the sulfated microbial peptide required for activation of XA21-mediated immunity X (RaxX) produced by Xanthomonas oryzae pv. oryzae (Xoo). Mutational studies and targeted proteomics revealed that the RaxX precursor peptide (proRaxX) is processed and secreted by the protease/transporter RaxB, the function of which can be partially fulfilled by a noncognate peptidase-containing transporter component B (PctB). proRaxX is cleaved at a Gly–Gly motif, yielding a mature peptide that retains the necessary elements for RaxX function as an immunogen and host peptide hormone mimic. These results indicate that RaxX is a prokaryotic member of a previously unclassified and understudied group of eukaryotic tyrosine sulfated ribosomally synthesized, posttranslationally modified peptides (RiPPs). We further demonstrate that sulfated RaxX directly binds XA21 with high affinity. This work reveals a complete, previously uncharacterized biological process: bacterial RiPP biosynthesis, secretion, binding to a eukaryotic receptor, and triggering of a robust host immune response.

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YouTube: KamounLab ZAR1 Video (2019)

Commentary by @KamounLab on the structure and activation mechanism of NLR type plant immune receptor ZAR1 solved by teams of scientists led by Jijie Chai, Jian-Min Zhou and Hong-Wei Wang.

 

Check also the commentary by Adachi et al. https://zenodo.org/record/2628967

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Science: Ligand-triggered allosteric ADP release primes a plant NLR complex (2019)

Science: Ligand-triggered allosteric ADP release primes a plant NLR complex (2019) | Plants and Microbes | Scoop.it

INTRODUCTION

Nucleotide-binding (NB), leucine-rich repeat (LRR) receptor (NLR) proteins constitute a family of intracellular immune receptors in both animals and plants that detect the presence of pathogen molecules or host-derived signals. NLRs share a conserved tripartite domain structure with a conserved central NB and oligomerization domain (NOD), a C-terminal LRR domain, and a variable N-terminal domain. The NOD module can be further divided into an NB domain (NBD), a helical domain (HD1), and a winged-helix domain (WHD). In plants, direct or indirect recognition of pathogen effectors by NLRs induces numerous defenses, including programmed cell death called hypersensitive response, and restricts pathogens to the infection site. For instance, the coiled-coil (CC)–NLR HOPZ-ACTIVATED RESISTANCE 1 (ZAR1) of the small mustard plant Arabidopsis thaliana forms a preactivation complex with resistance-related kinase 1 (RKS1, a pseudokinase belonging to receptor-like cytoplasmic kinase subfamily XII-2) and recognizes the uridylyltransferase effector AvrAC from the pathogen Xanthomonas campestris pv. campestris that is responsible for the black rot disease of crucifiers. AvrAC uridylates a number of host protein kinases, including the PBS1-like protein 2 (PBL2) kinase. PBL2UMP, the version of the Arabidopsis protein uridylated by AvrAC, then acts as a ligand of the preformed ZAR1-RKS1 complex. NLRs are believed to function as a nucleotide [adenosine diphosphate (ADP) or adenosine triphosphate (ATP)]–operated molecular switch, with ADP- and ATP-bound forms corresponding to the “off” and “on” states, respectively, but the mechanism of how ADP is released from an NLR for exchange with ATP remains elusive. Structural elucidation of a full-length plant NLR protein and its recognition of modified self is lacking.

RATONALE

We reconstituted a ZAR1-RKS1 and a ZAR1-RKS1-PBL2UMP complex and determined their cryo–electron microscopy (cryo-EM) structures at resolutions of 3.7 and 4.3 Å, respectively. The structures were verified by biochemical, cell-based, and functional data. We determined how PBL2UMP affects the ADP-binding activity of the ZAR1-RKS1 complex by radiolabeled assays. Structural comparison of the ZAR1-RKS1 and ZAR1-RKS1-PBL2UMP complexes was used to probe the mechanism of PBL2UMP-induced ADP release from ZAR1, which was further validated by biochemical assays.

RESULTS

The cryo-EM structure of the ZAR1-RKS1 complex revealed that intramolecular interactions within ZAR1 maintain the NLR protein in an inactive state. The inactive state is further stabilized by an ADP. The LRR domain of ZAR1 (ZAR1LRR) is positioned differently from LRR domains of animal NLRs but functions similarly to sequester ZAR1 in a monomeric state. ZAR1CC appears to be kept in an inactive state via contacts with ZAR1LRR, ZAR1HD1, and ZAR1WHD. This contrasts with the flexible N-terminal domain of inactive apoptotic protease-activating factor 1 (Apaf-1). ZAR1LRR mediates interaction with RKS1 in the preformed ZAR1-RKS1 complex. The ZAR1-RKS1-PBL2UMP structure shows that RKS1 is exclusively responsible for the binding of PBL2UMP. The two uridylyl moieties of PBL2UMP interact with and consequently stabilize the activation segment of RKS1. Comparison of the two cryo-EM structures shows that the stabilized activation segment of RKS1 sterically clashes with the ADP-bound ZAR1NBD from the ZAR1-RKS1 complex, resulting in conformational changes in the NBD but not other domains of ZAR1: ZAR1NBD is rotated outward about 60° compared with that from the inactive ZAR1. Thus, PBL2UMP allosterically induces release of ADP from the ZAR1-RKS1-PBL2UMP complex. Indeed, radiolabeling assays showed that PBL2UMP, but not PBL2, reduced the ADP-binding activity of the ZAR1-RKS1 complex.

CONCLUSION

Our study revealed the mechanisms of PBL2UMP recognition by ZAR1-RKS1 and PBL2UMP-induced priming of ZAR1, providing a structural template for understanding NLR proteins.

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PNAS: Structural analysis of Phytophthora suppressor of RNA silencing 2 (PSR2) reveals a conserved modular fold contributing to virulence (2019)

PNAS: Structural analysis of Phytophthora suppressor of RNA silencing 2 (PSR2) reveals a conserved modular fold contributing to virulence (2019) | Plants and Microbes | Scoop.it

Phytophthora are eukaryotic pathogens that cause enormous losses in agriculture and forestry. Each Phytophthora species encodes hundreds of effector proteins that collectively have essential roles in manipulating host cellular processes and facilitating disease development. Here we report the crystal structure of the effector Phytophthorasuppressor of RNA silencing 2 (PSR2). PSR2 produced by the soybean pathogen Phytophthora sojae (PsPSR2) consists of seven tandem repeat units, including one W-Y motif and six L-W-Y motifs. Each L-W-Y motif forms a highly conserved fold consisting of five α-helices. Adjacent units are connected through stable, directional linkages between an internal loop at the C terminus of one unit and a hydrophobic pocket at the N terminus of the following unit. This unique concatenation results in an overall stick-like structure of PsPSR2. Genome-wide analyses reveal 293 effectors from five Phytophthora species that have the PsPSR2-like arrangement, that is, containing a W-Y motif as the “start” unit, various numbers of L-W-Y motifs as the “middle” units, and a degenerate L-W-Y as the “end” unit. Residues involved in the interunit interactions show significant conservation, suggesting that these effectors also use the conserved concatenation mechanism. Furthermore, functional analysis demonstrates differential contributions of individual units to the virulence activity of PsPSR2. These findings suggest that the L-W-Y fold is a basic structural and functional module that may serve as a “building block” to accelerate effector evolution in Phytophthora.

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bioRxiv: Perturbations of a Kinase-Pseudokinase Module Activate Plant Immunity (2019)

bioRxiv: Perturbations of a Kinase-Pseudokinase Module Activate Plant Immunity (2019) | Plants and Microbes | Scoop.it

The Pseudomonas syringae acetyltransferase HopZ1a is delivered directly 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 ZED1 pseudokinase. 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 immunity in planta, all independently of HopZ1a. 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 and activating ZAR1-mediated ETI.

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Zenodo: Open science to tackle a cereal killer on the run (2019)

Zenodo: Open science to tackle a cereal killer on the run (2019) | Plants and Microbes | Scoop.it

Outbreaks of emerging plant diseases and insect pests are increasing at an alarming rate threatening the food security needs of a booming world population. The role of plant pathologists in addressing these threats to plant health is critical. This report elaborates our personal experience with the appearance in Bangladesh of a destructive new fungal disease wheat blast. Here we recap our experience and stress the importance of open science platforms and crowdsourced community responses in tackling emerging plant diseases. Benefits of the open science approach include recruitment of multidisciplinary experts, application of cutting-edge methods and timely replication of data analyses to increase the robustness of the findings.

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Zenodo: Rmg8 confers resistance to the Bangladeshi lineage of the wheat blast fungus (2019)

Zenodo: Rmg8 confers resistance to the Bangladeshi lineage of the wheat blast fungus (2019) | Plants and Microbes | Scoop.it

First reported in South America, wheat blast, caused by the fungus Magnaporthe oryzae(Syn. Pyricularia oryzae), has recently spread to Bangladesh and is threatening neighboring South Asian countries. To date, only a few resistance genes have been identified to function against wheat blast. Whether these genes are effective against the Bangaldeshi lineage of the wheat blast fungus is unknown. Here, we found that a hexaploid common wheat line S-615 carrying the gene Rmg8is resistant to M. oryzaeBangladeshi isolate BTJP4-1 but susceptible to Brazilian isolate N06047. These findings are consistent with the observation that AvrRmg8, which encodes the avirulence effector protein recognized by Rmg8, is present in Bangladeshi isolates of the wheat blast fungus. These results indicate that Rmg8could contribute to breeding blast resistant wheat varieties adapted to South Asian conditions.

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PNAS: Intercellular cooperation in a fungal plant pathogen facilitates host colonization (2019)

PNAS: Intercellular cooperation in a fungal plant pathogen facilitates host colonization (2019) | Plants and Microbes | Scoop.it

Cooperation between specialized cells and organisms supports complex biological functions, from the colonization of unfavorable environments to the formation of organs and sociality. Some bacterial pathogens are known to rely on cooperation between individuals and species for efficient colonization of their host and the onset of disease. We examined the regulation of genes in cells from different parts of a fungal plant pathogen and found evidence for cooperation between these fungal cells. We further show that cooperation between fungal cells is particularly important for the efficient colonization of resistant plants. These findings establish cooperation as a mechanism supporting disease caused by fungal pathogens that should be taken into account in the design of disease management strategies.

Cooperation is associated with major transitions in evolution such as the emergence of multicellularity. It is central to the evolution of many complex traits in nature, including growth and virulence in pathogenic bacteria. Whether cells of multicellular parasites function cooperatively during infection remains, however, largely unknown. Here, we show that hyphal cells of the fungal pathogen Sclerotinia sclerotiorum reprogram toward division of labor to facilitate the colonization of host plants. Using global transcriptome sequencing, we reveal that gene expression patterns diverge markedly in cells at the center and apex of hyphae during Arabidopsis thaliana colonization compared with in vitro growth. We reconstructed a genome-scale metabolic model for S. sclerotiorum and used flux balance analysis to demonstrate metabolic heterogeneity supporting division of labor between hyphal cells. Accordingly, continuity between the central and apical compartments of invasive hyphae was required for optimal growth in planta . Using a multicell model of fungal hyphae, we show that this cooperative functioning enhances fungal growth predominantly during host colonization. Our work identifies cooperation in fungal hyphae as a mechanism emerging at the multicellular level to support host colonization and virulence.


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New Phytologist: Diverse NLR immune receptors activate defence via the RPW8‐NLR NRG1 (2018)

New Phytologist: Diverse NLR immune receptors activate defence via the RPW8‐NLR NRG1 (2018) | Plants and Microbes | Scoop.it

Most land‐plant genomes carry genes that encode RPW8‐NLR resistance (R) proteins. Angiosperms carry two RPW8‐NLR subclasses: ADR1 and NRG1. ADR1s act as ‘helper’ NLRs for multiple TIR‐ and CC‐NLR R proteins in Arabidopsis. In angiosperm families, NRG1 co‐occurs with TIR‐NLR Resistance (R) genes. We tested if NRG1 is required for signalling of multiple TIR‐NLRs.

Using CRISPR mutagenesis, we obtained an nrg1a‐nrg1b double mutant in two Arabidopsis accessions, and an nrg1 mutant in Nicotiana benthamiana.

 

These mutants are compromised in signalling of all TIR‐NLRs tested, including WRR4A, WRR4B, RPP1, RPP2, RPP4 and the pairs RRS1/RPS4, RRS1B/RPS4B, CHS1/SOC3 and CHS3/CSA1. In Arabidopsis, NRG1 is required for the hypersensitive cell‐death response (HR) and full oomycete resistance, but not for salicylic acid induction or bacterial resistance. By contrast, nrg1 loss‐of‐function does not compromise the CC‐NLR R proteins RPS5 and MLA. RPM1 and RPS2 (CC‐NLRs) function is slightly compromised in an nrg1mutant. Thus, NRG1 is required for full TIR‐NLR function and contributes to the signalling of some CC‐NLRs.

 

Some NRG1‐dependent R proteins also signal partially via the NRG1 sister clade, ADR1. We propose that some NLRs signal via NRG1 only, some via ADR1 only and some via both or neither.


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New Phytologist: Commentary: Convergence of cell‐surface and intracellular immune receptor signalling (2019)

New Phytologist: Commentary: Convergence of cell‐surface and intracellular immune receptor signalling (2019) | Plants and Microbes | Scoop.it

This article is a Commentary on Kadota et al., 221: 2160–2175.

 

Plant immune responses are initiated by recognition of pathogen invasion through immune receptors. The pathogen sensing system is mainly composed of two structurally different proteins that are located on different subcellular compartments. One is the plasma membrane‐localized pattern recognition receptors (PRRs) that detect pathogen‐associated molecular patterns (PAMPs) (Boutrot & Zipfel, 2017). PRRs perceive extracellular PAMPs to activate PAMP‐triggered immunity (PTI). In turn, adapted pathogens interfere with or modulate host signalling by virulence factors (called effectors) for successful infection. The other is intracellular nucleotide‐binding domain and leucine‐rich repeat proteins (NLRs) that recognize these effectors (Jones et al., 2016). Activation of an NLR induces a robust immune response called effector‐triggered immunity (ETI), which is often accompanied by hypersensitive response (HR) cell death. Animals encode both plasma membrane and intracellular immune receptors, which share similar structures with plant PRRs and NLRs for recognition of PAMPs; but plant and animal immune receptors evolved independently (Ronald & Beutler, 2010; Jones et al., 2016). Interestingly, although PRRs and NLRs are structurally different and localize in distinct subcellular compartments, they share substantial downstream signalling, such as Ca2+, mitogen‐activated protein kinase (MAPK), reactive oxygen species (ROS), and phytohormone signalling as well as massive transcriptional reprogramming (Peng et al., 2018). However, it is not known how PRRs and NLRs activate similar signalling outputs. In this issue of New Phytologist, Kadota et al. (2019, pp. 2160–2175) investigated protein phosphorylation dynamics upon NLR activation by phosphoproteomics. By comparing with previously published phosphoproteomics data for PTI, they discovered that phosphorylation occurred in the same residues of an NADPH oxidase, RESPIRATORY BURST OXIDASE HOMOLOGUE D (RBOHD), which is activated during both PTI and ETI. Thus, Kadota et al. (2019) precisely defined a signal convergent point between PRR and NLR signalling at the molecular level.


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bioRxiv: The Arabidopsis thaliana pan-NLRome (2019)

bioRxiv: The Arabidopsis thaliana pan-NLRome (2019) | Plants and Microbes | Scoop.it

Disease is both among the most important selection pressures in nature and among the main causes of yield loss in agriculture. In plants, resistance to disease is often conferred by Nucleotide-binding Leucine-rich Repeat (NLR) proteins. These proteins function as intracellular immune receptors that recognize pathogen proteins and their effects on the plant. Consistent with evolutionarily dynamic interactions between plants and pathogens, NLRs are known to be encoded by one of the most variable gene families in plants, but the true extent of intraspecific NLR diversity has been unclear. Here, we define the majority of the Arabidopsis thaliana species-wide 'NLRome'. From NLR sequence enrichment and long-read sequencing of 65 diverse A. thaliana accessions, we infer that the pan-NLRome saturates with approximately 40 accessions. Despite the high diversity of NLRs, half of the pan-NLRome is present in most accessions. We chart the architectural diversity of NLR proteins, identify novel architectures, and quantify the selective forces that act on specific NLRs, domains, and positions. Our study provides a blueprint for defining the pan-NLRome of plant species.

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bioRxiv: Cross-reactivity of a rice NLR immune receptor to distinct effectors from the blast pathogen leads to partial disease resistance (2019)

bioRxiv: Cross-reactivity of a rice NLR immune receptor to distinct effectors from the blast pathogen leads to partial disease resistance (2019) | Plants and Microbes | Scoop.it

Unconventional integrated domains in plant intracellular immune receptors (NLRs) can directly bind translocated pathogen effector proteins to initiate an immune response. The rice immune receptor pairs Pik-1/Pik-2 and RGA5/RGA4 both use integrated heavy metal-associated (HMA) domains to bind the Magnaporthe oryzae effectors AVR-Pik and AVR-Pia, respectively. These effectors both belong to the MAX effector family and share a core structural fold, despite being divergent in sequence. How integrated domains maintain specificity of recognition, even for structurally similar effectors, has implications for understanding plant immune receptor evolution and function. Here we show that the rice NLR pair Pikp-1/Pikp-2 triggers an immune response leading to partial disease resistance towards the mis-matched effector AVR-Pia in planta, and that the Pikp-HMA domain binds AVR-Pia in vitro. The HMA domain from another Pik-1 allele, Pikm, is unable to bind AVR-Pia, and does not trigger a response in plants. The crystal structure of Pikp-HMA bound to AVR-Pia reveals a different binding interface compared to AVR-Pik effectors, suggesting plasticity in integrated domain/effector interactions. This work shows how a single NLR can bait multiple pathogen effectors via an integrated domain, and may enable engineering immune receptors with extended disease resistance profiles.

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