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

Martin, Raoul; Qi, Tiancong; Zhang, Haibo; Liu, Furong; King, Miles; Toth, Claire; Nogales, Eva; Staskawicz, Brian J.

doi:10.1101/2020.08.13.246413

Cited by 97 publications

(192 citation statements)

References 68 publications

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“…2017 ; Dong et al. 2018 ; Martin et al. 2020 ); the similar TIR domains between DM10 and RLM1 members make it particularly likely that they oligomerize, which is often an important step in NLR activation.…”

Section: Discussionmentioning

confidence: 99%

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A Truncated Singleton NLR Causes Hybrid Necrosis inArabidopsis thaliana

Barragan

Collenberg

Wang

et al. 2020

Molecular Biology and Evolution

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Hybrid necrosis in plants arises from conflict between divergent alleles of immunity genes contributed by different parents, resulting in autoimmunity. We investigate a severe hybrid necrosis case in Arabidopsis thaliana, where the hybrid does not develop past the cotyledon stage and dies three weeks after sowing. Massive transcriptional changes take place in the hybrid, including the upregulation of most NLR disease resistance genes. This is due to an incompatible interaction between the singleton TIR-NLR gene DANGEROUS MIX 10 (DM10), which was recently relocated from a larger NLR cluster, and an unlinked locus, DANGEROUS MIX 11 (DM11). There are multiple DM10 allelic variants in the global A. thaliana population, several of which have premature stop codons. One of these, which has a truncated LRR-PL region, corresponds to the DM10 risk allele. The DM10 locus and the adjacent genomic region in the risk allele carriers are highly differentiated from those in the non-risk carriers in the global A. thaliana population, suggesting that this allele became geographically widespread only relatively recently. The DM11 risk allele is much rarer and found only in two accessions from southwestern Spain – a region from which the DM10 risk haplotype is absent – indicating that the ranges of DM10 and DM11 risk alleles may be non-overlapping.

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Section: Discussionmentioning

confidence: 99%

“…2015 ). In addition, many TIR-NLRs carry a post-LRR (PL) domain, which is involved in pathogen effector recognition ( Van Ghelder and Esmenjaud 2016 ; Martin et al. 2020 ).…”

Section: Introductionmentioning

confidence: 99%

A Truncated Singleton NLR Causes Hybrid Necrosis inArabidopsis thaliana

Barragan

Collenberg

Wang

et al. 2020

Molecular Biology and Evolution

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“…In Arabidopsis thaliana (Arabidopsis) the RNL subclass consists of two gene families, ACTIVATED DISEASE RESISTANCE 1 (ADR1) and N REQUIREMENT GENE 1 (NRG1), both being required for immune signalling and cell death induction of many other NLRs, particularly TNLs [4][5][6][7][8][9] . CNLs, TNLs and most likely RNLs induce immune signalling and cell death by oligomerization [10][11][12][13] . CNL activation is speculated to result in the formation of a pore-like or membrane disrupting structure of the CC domain (a so-called resistosome) at the plasma membrane (PM) 10,[14][15][16] .…”

Section: Introductionmentioning

confidence: 99%

Coiled-coil and RPW8-type immune receptors function at the plasma membrane in a phospholipid dependent manner

Saile

Sunil

et al. 2020

Preprint

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Activation of intracellular nucleotide-binding leucine-rich repeat receptors (NLRs) results in immunity and a localized cell death response of infected cells. Cell death activity of many NLRs requires oligomerization and in some cases plasma membrane (PM) localization. However, the exact mechanisms underlying PM localization of NLRs lacking recognizable N- or C-terminal lipidation motifs or predicted transmembrane domains remains elusive. Here we show that the PM localization and stability of members of the RPW8-like coiled-coil (CCR) domain NLRs (RNLs) and a CC-type NLR (CNL) depend on the interaction with PM phospholipids. Depletion of phosphatidylinositol-4-phosphate (PI4P) from the PM led to a mislocalization of the analyzed NLRs and consequently inhibited their cell death activity. We further demonstrate activation-dependent self-association of cell death inducing RNLs. Our results provide new insights into the molecular mechanism of NLR PM localization and defines an important role of phospholipids for CNL and RNL activity during immunity.

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“…Activation and signaling by animal NLRs involves oligomerization and interactor recruitment by oligomeric N-terminal assemblies (Bentham et al, 2017). Recent structural elucidation of a full length plant CNL (HOPZ-ACTIVATED RESISTANCE1 (ZAR1); Wang et al, 2019a; Wang et al, 2019b) and TNL (Recognition of XopQ1 (Roq1); Martin et al, 2020b) revealed assembly of pentameric and tetrameric resistosomes by the activated immune receptors, respectively. Resistosome formation is driven by indirect (ZAR1) or direct (Roq1) pathogen effector recognition, nucleotide exchange (ADP/ATP) within the nucleotide-binding domain and profound conformational changes.…”

Section: Introductionmentioning

confidence: 99%

“…In the resistosome formed by activated Roq1, two dimers of TIR domain dimers exhibit a two-fold symmetry. This conformation leads to opening of the NADase active site of the TIR domain and breakdown of NAD + (Horsefield et al, 2019; Wan et al, 2019; Duxbury et al, 2020; Martin et al, 2020b). In the latter case, it is assumed that one of the breakdown products of the TIR domain enzymatic activity, whose molecular identity remains to be determined, functions as a signaling molecule.…”

Section: Introductionmentioning

confidence: 99%

Disentangling cause and consequence: Genetic dissection of theDANGEROUS MIX2risk locus, and activation of the DM2h NLR in autoimmunity

Ordon

Martin

Erickson

et al. 2020

Preprint

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Nucleotide-binding domain–leucine-rich repeat-type immune receptors (NLRs) protect plants against pathogenic microbes through intracellular detection of effector proteins. However, this comes at a cost, as NLRs can also induce detrimental autoimmunity in genetic interactions with foreign alleles. This may occur when independently evolved genomes are combined in inter- or intraspecific crosses, or when foreign alleles are introduced by mutagenesis or transgenesis. Most autoimmunity-inducing NLRs are encoded within highly variable NLR gene clusters with no known immune functions, which were termed autoimmune risk loci. Whether risk NLRs differ from sensor NLRs operating in natural pathogen resistance and how risk NLRs are activated in autoimmunity is unknown. Here, we analyzed the DANGEROUS MIX2 risk locus, a major autoimmunity hotspot in Arabidopsis thaliana. By gene editing and heterologous expression, we show that a single gene, DM2h, is necessary and sufficient for autoimmune induction in three independent cases of autoimmunity in accession Landsberg erecta. We focus on autoimmunity provoked by an EDS1-YFPNLS fusion protein to functionally characterize DM2h and determine features of EDS1-YFPNLS activating the immune receptor. Our data suggest that risk NLRs function reminiscent of sensor NLRs, while autoimmunity-inducing properties of EDS1-YFPNLS are in this context unrelated to the protein’s functions as immune regulator. We propose that autoimmunity may, at least in some cases, be caused by spurious, stochastic interactions of foreign alleles with co-incidentally matching risk NLRs.

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

Cited by 97 publications

References 68 publications

A Truncated Singleton NLR Causes Hybrid Necrosis inArabidopsis thaliana

A Truncated Singleton NLR Causes Hybrid Necrosis inArabidopsis thaliana

Coiled-coil and RPW8-type immune receptors function at the plasma membrane in a phospholipid dependent manner

Disentangling cause and consequence: Genetic dissection of theDANGEROUS MIX2risk locus, and activation of the DM2h NLR in autoimmunity

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