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 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 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 Pathogen effector recognition-dependent association of NRG1 with EDS1 and SAG101 in TNL receptor immunity

2020 ◽  
Author(s):  
Xinhua Sun ◽  
Dmitry Lapin ◽  
Joanna M. Feehan ◽  
Sara C. Stolze ◽  
Katharina Kramer ◽  
...  
Keyword(s):  
Disease Susceptibility ◽  
Nucleotide Binding ◽  
Molecular Evidence ◽  
Leucine Rich Repeat ◽  
Pathogen Effectors ◽  
Pathogen Effector ◽  
Family Protein ◽  
Activated State ◽  
Defence Signalling ◽  
Effector Recognition

Plants utilise intracellular nucleotide-binding, leucine-rich repeat (NLR) immune receptors to detect pathogen effectors and activate local and systemic defence. NRG1 and ADR1 "helper" NLRs (RNLs), cooperate with enhanced disease susceptibility 1 (EDS1), senescence-associated gene 101 (SAG101) and phytoalexin-deficient 4 (PAD4) lipase-like proteins to mediate signalling from TIR domain NLR receptors (TNLs). However, the mechanism of RNL/ EDS1 family protein cooperation is poorly understood. Here, we provide genetic and molecular evidence for exclusive EDS1/SAG101/NRG1 and EDS1/PAD4/ADR1 co-functions in TNL immunity. Using immunoprecipitation and mass spectrometry, we show effector recognition dependent association of NRG1 with EDS1 and SAG101, but not PAD4. An EDS1-SAG101 complex associates with NRG1, and EDS1-PAD4 associates with ADR1, only in an immune-activated state. NRG1 requires an intact nucleotide-binding P-loop motif, and EDS1 a functional EP domain and its partner SAG101, for induced association and immunity. Thus, two distinct modules (NRG1/EDS1/SAG101 and ADR1/EDS1/PAD4) are required to execute TNL receptor defence signalling.

scholarly journals NADase and now Ca2+ channel, what else to learn about plant NLRs?

2021 ◽  
Vol 1 (1) ◽  
Author(s):  
Li Wan ◽  
Zuhua He
Keyword(s):  
Cell Death ◽  
Interleukin 1 ◽  
Coiled Coil ◽  
Defense Responses ◽  
Effector Proteins ◽  
Leucine Rich Repeat ◽  
Downstream Signaling ◽  
Pathogen Effectors ◽  
Activate Cell ◽  
Insight Into

AbstractPlant intracellular immune receptors known as NLR (Nucleotide-binding Leucine-rich repeat, NB-LRR) proteins confer resistance and cause cell death upon recognition of cognate effector proteins from pathogens. Plant NLRs contain a variable N-terminal domain: a Toll/interleukin-1 receptor (TIR) domain or a coiled-coil (CC) domain or an RPW8 (Resistance to Powdery Mildew 8)-like CC (CCR) domain. TIR-NLR, CC-NLR and CCR-NLR are known as TNL, CNL and RNL, respectively. TNLs and CNLs recognize pathogen effectors to activate cell death and defense responses, thus are regarded as sensor NLRs. RNLs are required downstream of TNLs to activate cell death and defense responses, thus are regarded as helper NLRs. Previous studies show that some TNLs form tetrameric resistosome as NAD+ cleaving enzymes to transduce signal, while some CNLs form pentameric resistosome with undefined biochemical function. Two recent breakthrough studies show that activated CNL and RNL function as Ca2+ channel to cause cell death and defense responses and provide a completely new insight into the downstream signaling events of CNL and TNL pathways.

scholarly journals Plant Nucleotide Binding Site–Leucine-Rich Repeat (NBS-LRR) Genes: Active Guardians in Host Defense Responses

2013 ◽  
Vol 14 (4) ◽  
pp. 7302-7326 ◽  
Author(s):  
Daniela Marone ◽  
Maria Russo ◽  
Giovanni Laidò ◽  
Anna De Leonardis ◽  
Anna Mastrangelo
Keyword(s):  
Binding Site ◽  
Host Defense ◽  
Nucleotide Binding ◽  
Defense Responses ◽  
Nucleotide Binding Site ◽  
Leucine Rich Repeat

Genome-wide identification and characterization of nucleotide binding site leucine-rich repeat genes in linseed reveal distinct patterns of gene structure

Genome ◽  
2013 ◽  
Vol 56 (2) ◽  
pp. 91-99 ◽  
Author(s):  
Sandip M. Kale ◽  
Varsha C. Pardeshi ◽  
Vitthal T. Barvkar ◽  
Vidya S. Gupta ◽  
Narendra Y. Kadoo
Keyword(s):  
Disease Resistance ◽  
Binding Site ◽  
Regulatory Element ◽  
Nucleotide Binding ◽  
Defense Responses ◽  
Nucleotide Binding Site ◽  
Leucine Rich Repeat ◽  
Quantitative Expression ◽  
Domain Arrangement ◽  
Gene Structures

Plants employ different disease-resistance genes to detect pathogens and to induce defense responses. The largest class of these genes encodes proteins with nucleotide binding site (NBS) and leucine-rich repeat (LRR) domains. To identify the putative NBS–LRR encoding genes from linseed, we analyzed the recently published linseed genome sequence and identified 147 NBS–LRR genes. The NBS domain was used for phylogeny construction and these genes were classified into two well-known families, non-TIR (CNL) and TIR related (TNL), and formed eight clades in the neighbor-joining bootstrap tree. Eight different gene structures were observed among these genes. An unusual domain arrangement was observed in the TNL family members, predominantly in the TNL-5 clade members belonging to class D. About 12% of the genes observed were linseed specific. The study indicated that the linseed genes probably have an ancient origin with few progenitor genes. Quantitative expression analysis of five genes showed inducible expression. The in silico expression evidence was obtained for a few of these genes, and the expression was not correlated with the presence of any particular regulatory element or with unusual domain arrangement in those genes. This study will help in understanding the evolution of these genes, the development of disease resistant varieties, and the mechanism of disease resistance in linseed.

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