Endocytosis: At the Crossroads of Pattern Recognition Immune Receptors and Pathogen Effectors

2013 ◽  
pp. 273-297 ◽  
Author(s):  
Silke Robatzek
Keyword(s):  
Pattern Recognition ◽  
Immune Receptors ◽  
Pathogen Effectors

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’.

Toxoplasma Mechanisms for Delivery of Proteins and Uptake of Nutrients Across the Host-Pathogen Interface

2020 ◽  
Vol 74 (1) ◽  
pp. 567-586 ◽  
Author(s):  
Yifan Wang ◽  
Lamba Omar Sangaré ◽  
Tatiana C. Paredes-Santos ◽  
Jeroen P. J. Saeij
Keyword(s):  
Pattern Recognition ◽  
Toxoplasma Gondii ◽  
Parasitophorous Vacuole ◽  
Protozoan Parasite ◽  
Intracellular Pathogens ◽  
Parasitophorous Vacuole Membrane ◽  
Vacuole Membrane ◽  
Pathogen Effectors ◽  
Host Pathogen ◽  
Uptake Of Nutrients

Many intracellular pathogens, including the protozoan parasite Toxoplasma gondii, live inside a vacuole that resides in the host cytosol. Vacuolar residence provides these pathogens with a defined niche for replication and protection from detection by host cytosolic pattern recognition receptors. However, the limiting membrane of the vacuole, which constitutes the host-pathogen interface, is also a barrier for pathogen effectors to reach the host cytosol and for the acquisition of host-derived nutrients. This review provides an update on the specialized secretion and trafficking systems used by Toxoplasma to overcome the barrier of the parasitophorous vacuole membrane and thereby allow the delivery of proteins into the host cell and the acquisition of host-derived nutrients.

scholarly journals Mai1 protein acts between host recognition of pathogen effectors and MAPK signaling

2019 ◽  
Author(s):  
Sarah R. Hind ◽  
Robyn Roberts ◽  
Kerry F. Pedley ◽  
Benjamin A. Diner ◽  
Matthew J. Szarzanowicz ◽  
...  
Keyword(s):  
Protein Kinase ◽  
Nicotiana Benthamiana ◽  
Kinase Domain ◽  
Mapk Signaling ◽  
Mitogen Activated Protein Kinase ◽  
Host Recognition ◽  
Mapk Phosphorylation ◽  
Immune Receptors ◽  
Pathogen Effectors ◽  
Mitogen Activated Protein

AbstractThe molecular mechanisms acting between host recognition of pathogen effectors by NOD-like receptor (NLR) proteins and mitogen-activated protein kinase (MAPK) signaling cascades are unknown. MAPKKKα (M3Kα) activates MAPK signaling leading to programmed cell death (PCD) associated with NLR-triggered immunity. We identified a tomato M3Kα-interacting protein, SlMai1, that has 80% amino acid identity with Arabidopsis brassinosteroid kinase 1 (AtBsk1). SlMai1 has a protein kinase domain and a C-terminal tetratricopeptide repeat domain which interacts with the kinase domain of M3Kα. Virus-induced gene silencing of Mai1 homologs in Nicotiana benthamiana increased susceptibility to Pseudomonas syringae and compromised PCD induced by four NLR proteins. PCD was restored by expression of a synthetic SlMai1 gene that resists silencing. Expression of AtBsk1 did not restore PCD in Mai1-silenced plants, suggesting SlMai1 is functionally divergent from AtBsk1. PCD caused by overexpression of M3Kα or MKK2 was unaffected by Mai1 silencing indicating Mai1 acts upstream of these proteins. Co-expression of Mai1 with M3Kα in leaves enhanced MAPK phosphorylation and accelerated PCD. These findings reveal Mai1 as a molecular link acting between host recognition of pathogens and MAPK signaling.Author SummaryPlants use intracellular immune receptors to detect and respond to specific effector proteins which pathogens translocate into the host cell as part of their infection process. Localized programmed cell death (PCD) involving a mitogen-activated protein kinase (MAPK) cascade is an important host response associated with effector-triggered immunity, although the molecular connections between immune receptors and MAPK signaling is unknown. The Mai1 protein was found to act downstream of multiple immune receptors in Nicotiana benthamiana and to physically interact with MAPKKKα. The Mai1-MAPKKKα interaction enhances MAPK phosphorylation, triggers PCD and promotes disease resistance.

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 Convergent and Divergent Signaling in PAMP-Triggered Immunity and Effector-Triggered Immunity

2018 ◽  
Vol 31 (4) ◽  
pp. 403-409 ◽  
Author(s):  
Yujun Peng ◽  
Rowan van Wersch ◽  
Yuelin Zhang
Keyword(s):  
Plasma Membrane ◽  
Mitogen Activated Protein Kinase ◽  
Defense Gene Expression ◽  
Kinase Activation ◽  
Immune Receptors ◽  
Pathogen Effectors ◽  
Molecular Events ◽  
Protein Kinase Activation ◽  
Mitogen Activated Protein ◽  
Effector Triggered Immunity

Plants use diverse immune receptors to sense pathogen attacks. Recognition of pathogen-associated molecular patterns (PAMPs) by pattern recognition receptors localized on the plasma membrane leads to PAMP-triggered immunity (PTI). Detection of pathogen effectors by intracellular or plasma membrane–localized immune receptors results in effector-triggered immunity (ETI). Despite the large variations in the magnitude and duration of immune responses triggered by different PAMPs or pathogen effectors during PTI and ETI, plasma membrane–localized immune receptors activate similar downstream molecular events such as mitogen-activated protein kinase activation, oxidative burst, ion influx, and increased biosynthesis of plant defense hormones, indicating that defense signals initiated at the plasma membrane converge at later points. On the other hand, activation of ETI by immune receptors localized to the nucleus appears to be more directly associated with transcriptional regulation of defense gene expression. Here, we review recent progress in signal transductions downstream of different groups of plant immune receptors, highlighting the converging and diverging molecular events.

scholarly journals Expanded functions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors

2011 ◽  
Vol 108 (39) ◽  
pp. 16463-16468 ◽  
Author(s):  
V. Bonardi ◽  
S. Tang ◽  
A. Stallmann ◽  
M. Roberts ◽  
K. Cherkis ◽  
...  
Keyword(s):  
Specific Recognition ◽  
Immune Receptors ◽  
Pathogen Effectors

scholarly journals The rice NLR pair Pikp-1/Pikp-2 initiates cell death through receptor cooperation rather than negative regulation

2020 ◽  
Author(s):  
Rafał Zdrzałek ◽  
Sophien Kamoun ◽  
Ryohei Terauchi ◽  
Hiromasa Saitoh ◽  
Mark J Banfield
Keyword(s):  
Cell Death ◽  
Negative Regulation ◽  
Sequence Motifs ◽  
Multidomain Proteins ◽  
In Planta ◽  
Effector Functions ◽  
Immune Receptors ◽  
Pathogen Effectors ◽  
Domain Truncation ◽  
Truncated Variants

AbstractPlant NLR immune receptors are multidomain proteins that can function as specialized sensor/helper pairs. Paired NLR immune receptors are generally thought to function via negative regulation, where one NLR represses the activity of the second and detection of pathogen effectors relieves this repression to initiate immunity. However, whether this mechanism is common to all NLR pairs is not known. Here, we show that the rice NLR pair Pikp-1/Pikp-2, which confers resistance to strains of the blast pathogen Magnaporthe oryzae (syn. Pyricularia oryzae) expressing the AVR-PikD effector, functions via receptor cooperation, with effector-triggered activation requiring both NLRs to trigger the immune response. To investigate the mechanism of Pikp-1/Pikp-2 activation, we expressed truncated variants of these proteins, and made mutations in previously identified NLR sequence motifs. We found that any domain truncation, in either Pikp-1 or Pikp-2, prevented cell death in the presence of AVR-PikD, revealing that all domains are required for activity. Further, expression of individual Pikp-1 or Pikp-2 domains did not result in cell death. Mutations in the conserved P-loop and MHD sequence motifs in both Pikp-1 and Pikp-2 prevented cell death activation, demonstrating that these motifs are required for the function of the two partner NLRs. Finally, we showed that Pikp-1 and Pikp-2 associate to form homo- and hetero-complexes in planta in the absence of AVR-PikD; on co-expression the effector binds to Pikp-1 generating a tripartite complex. Taken together, we provide evidence that Pikp-1 and Pikp-2 form a fine-tuned system that is activated by AVR-PikD via receptor cooperation rather than negative regulation.

scholarly journals Distinct modes of derepression of an Arabidopsis immune receptor complex by two different bacterial effectors

2018 ◽  
Vol 115 (41) ◽  
pp. 10218-10227 ◽  
Author(s):  
Yan Ma ◽  
Hailong Guo ◽  
Lanxi Hu ◽  
Paula Pons Martinez ◽  
Panagiotis N. Moschou ◽  
...  
Keyword(s):  
Wrky Transcription Factor ◽  
Leucine Rich Repeat ◽  
Wrky Domain ◽  
Inactive State ◽  
Immune Receptors ◽  
Pathogen Effectors ◽  
Effector Recognition ◽  
Bacterial Effectors ◽  
Colicin E9 ◽  
Domain 4

Plant intracellular nucleotide-binding leucine-rich repeat (NLR) immune receptors often function in pairs to detect pathogen effectors and activate defense. The Arabidopsis RRS1-R–RPS4 NLR pair recognizes the bacterial effectors AvrRps4 and PopP2 via an integrated WRKY transcription factor domain in RRS1-R that mimics the effector’s authentic targets. How the complex activates defense upon effector recognition is unknown. Deletion of the WRKY domain results in an RRS1 allele that triggers constitutive RPS4-dependent defense activation, suggesting that in the absence of effector, the WRKY domain contributes to maintaining the complex in an inactive state. We show the WRKY domain interacts with the adjacent domain 4, and that the inactive state of RRS1 is maintained by WRKY–domain 4 interactions before ligand detection. AvrRps4 interaction with the WRKY domain disrupts WRKY–domain 4 association, thus derepressing the complex. PopP2-triggered activation is less easily explained by such disruption and involves the longer C-terminal extension of RRS1-R. Furthermore, some mutations in RPS4 and RRS1 compromise PopP2 but not AvrRps4 recognition, suggesting that AvrRps4 and PopP2 derepress the complex differently. Consistent with this, a “reversibly closed” conformation of RRS1-R, engineered in a method exploiting the high affinity of colicin E9 and Im9 domains, reversibly loses AvrRps4, but not PopP2 responsiveness. Following RRS1 derepression, interactions between domain 4 and the RPS4 C-terminal domain likely contribute to activation. Simultaneous relief of autoinhibition and activation may contribute to defense activation in many immune receptors.

scholarly journals A coevolved EDS1-SAG101-NRG1 module mediates cell death signaling by TIR-domain immune receptors

2019 ◽  
Author(s):  
Dmitry Lapin ◽  
Viera Kovacova ◽  
Xinhua Sun ◽  
Joram Dongus ◽  
Deepak D. Bhandari ◽  
...  
Keyword(s):  
Cell Death ◽  
Coiled Coil ◽  
Rate Variation ◽  
Distinctive Features ◽  
Tir Domain ◽  
Immune Receptors ◽  
Pathogen Effectors ◽  
Cell Death Signaling ◽  
Basal Defense

AbstractPlant intracellular nucleotide-binding/leucine-rich repeat (NLR) immune receptors are activated by pathogen effectors to trigger host defenses and cell death. Toll-Interleukin1-receptor (TIR)-domain NLRs (TNLs) converge on the Enhanced Disease Susceptibility1 (EDS1) family of lipase-like proteins for all resistance outputs. In Arabidopsis TNL immunity,AtEDS1 heterodimers with Phytoalexin Deficient4 (AtPAD4) transcriptionally boost basal defense pathways.AtEDS1 uses the same surface to interact with PAD4-related Senescence-Associated Gene101 (AtSAG101), but the role ofAtEDS1-AtSAG101 heterodimers was unclear. We show thatAtEDS1-AtSAG101 function together withAtNRG1 coiled-coil domain helper NLRs as a coevolved TNL cell death signaling module.AtEDS1-AtSAG101-AtNRG1 cell death activity is transferable to the solanaceous species,Nicotiana benthamiana, and cannot be substituted byAtEDS1-AtPAD4 withAtNRG1 orAtEDS1-AtSAG101 with endogenousNbNRG1. Analysis of EDS1-family evolutionary rate variation and heterodimer structure-guided phenotyping ofAtEDS1 variants orAtPAD4-AtSAG101 chimeras identify closely aligned α-helical coil surfaces in theAtEDS1-AtSAG101 partner C-terminal domains that are necessary for TNL cell death signaling. Our data suggest that TNL-triggered cell death and pathogen growth restriction are determined by distinctive features of EDS1-SAG101 and EDS1-PAD4 complexes and that these signaling machineries coevolved with further components within plant species or clades to regulate downstream pathways in TNL immunity.

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