Activation of a Plant NLR Complex through Heteromeric Association with an Autoimmune Risk Variant of Another NLR

Tran, Diep Thi Ngoc; Chung, Eui Hwan; Habring-Müller, Anette; Demar, Monika; Schwab, Rebecca; Dangl, Jeffery L.; Weigel, Detlef; Chae, Eunyoung

doi:10.1016/j.cub.2017.03.018

Cited by 76 publications

(85 citation statements)

References 56 publications

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“…Certain conventional NLRs work as heteromeric pairs, through interacting N-terminal domains (Césari et al, 2014;Tran et al, 2017;Williams et al, 2014). RPP7 proteins are canonical CNLs, while RPW8/HR proteins are non-NLR, CCR-only proteins.…”

Section: Rpp7b Oligomerization Induced By Association With Hr4 Fei-0mentioning

confidence: 99%

Oligomerization of NLR immune receptor RPP7 triggered by atypical resistance protein RPW8/HR as ligand

Li¹,

Habring²,

Wang³

et al. 2019

Preprint

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In certain plant hybrids, autoimmunity is triggered by immune components that interactin the absence of a pathogen trigger. Often, NLR immune receptors are involved, with a particularly interesting case in Arabidopsis thaliana involving variants of the NLR RPP7 as well as variants of RPW8/HR proteins, which are homologs of animal MLKL and fungal HELL domain proteins. We demonstrate that HR4 Fei-0 but not the closely related HR4 Col-0 protein directly disrupts intramolecular association of RPP7b Lerik1-3 , which in turn initiates P-loop dependent NLR signaling. In agreement, RPP7b Lerik1-3 forms a higher-order complex only in the presence of HR4 Fei-0 but not HR4 Col-0 . In addition, we find that HR4 Fei-0 on its own can form detergent-resistant oligomers suggestive of amyloid-like aggregates, which in turn can directly kill cells in an RPP7b Lerik1-3 -independent manner. Our work provides in vivo biochemical evidence for a plant resistosome complex and the mechanisms by which RPW8/HR proteins trigger cell death.

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Section: Rpp7b Oligomerization Induced By Association With Hr4 Fei-0mentioning

confidence: 99%

Oligomerization of NLR immune receptor RPP7 triggered by atypical resistance protein RPW8/HR as ligand

Li¹,

Habring²,

Wang³

et al. 2019

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…Such a mode of action would have enabled massive duplication and functional diversification without accumulation of deleterious effects. Interestingly, recent studies have shown that mismatched NLRs, which probably operate through positive regulation, trigger autoimmunity leading to hybrid necrosis, adding another layer of complexity in NLR evolution (43,45). Future studies on how NRC and NRC-dependent NLR proteins function should shed light on the mechanistic detail of how this NRC network mediates immune responses and disease resistance.…”

Section: Nrc2 Nrc3 and Nrc4 Redundantly Contribute To Rx-mediatedmentioning

confidence: 99%

NLR network mediates immunity to diverse plant pathogens

Abd-El-Haliem

Bozkurt

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

353

548

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Both plants and animals rely on nucleotide-binding domain and leucine-rich repeat-containing (NLR) proteins to respond to invading pathogens and activate immune responses. An emerging concept of NLR function is that "sensor" NLR proteins are paired with "helper" NLRs to mediate immune signaling. However, our fundamental knowledge of sensor/helper NLRs in plants remains limited. In this study, we discovered a complex NLR immune network in which helper NLRs in the NRC (NLR required for cell death) family are functionally redundant but display distinct specificities toward different sensor NLRs that confer immunity to oomycetes, bacteria, viruses, nematodes, and insects. The helper NLR NRC4 is required for the function of several sensor NLRs, including Rpi-blb2, Mi-1.2, and R1, whereas NRC2 and NRC3 are required for the function of the sensor NLR Prf. Interestingly, NRC2, NRC3, and NRC4 redundantly contribute to the immunity mediated by other sensor NLRs, including Rx, Bs2, R8, and Sw5. NRC family and NRC-dependent NLRs are phylogenetically related and cluster into a well-supported superclade. Using extensive phylogenetic analysis, we discovered that the NRC superclade probably emerged over 100 Mya from an NLR pair that diversified to constitute up to one-half of the NLRs of asterids. These findings reveal a complex genetic network of NLRs and point to a link between evolutionary history and the mechanism of immune signaling. We propose that this NLR network increases the robustness of immune signaling to counteract rapidly evolving plant pathogens.immunity | host-microbe interactions | evolution

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“…Such incompatibilities between independently evolved NLRs have been described in Arabidopsis; DM1 and DM2d are two TNLs from two different Arabidopsis ecotypes, Uk‐3 and Uk‐1, and underlie hybrid necrosis observed in F1 progeny. The necrosis results from incompatibility between these two TNLs that triggers the auto‐activation of immune responses (Chae et al ., ; Tran et al ., ). Similarly, earlier work in Arabidopsis has also established NLR incompatibility as the basis for hybrid necrosis (Bomblies et al ., ).…”

Section: Regulation At the Protein Levelmentioning

confidence: 97%

Molecular mechanisms that limit the costs of NLR‐mediated resistance in plants

Richard

Gratias

Meyers

et al. 2018

Molecular Plant Pathology

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Crop diseases cause significant yield losses, and the use of resistant cultivars can effectively mitigate these losses and control many plant diseases. Most plant resistance (R) genes encode immune receptors composed of nucleotide-binding and leucine-rich repeat (NLR) domains. These proteins mediate the specific recognition of pathogen avirulence effectors to induce defence responses. However, NLR-triggered immunity can be associated with a reduction in growth and yield, so-called 'fitness costs'. Recent data have shown that plants use an elaborate interplay of different mechanisms to control NLR gene transcript levels, as well as NLR protein abundance and activity, to avoid the associated cost of resistance in the absence of a pathogen. In this review, we discuss the different levels of NLR regulation (transcriptional, post-transcriptional and at the protein level). We address the apparent need for plants to maintain diverse modes of regulation. A recent model suggesting an equilibrium 'ON/OFF state' of NLR proteins, in the absence of a pathogen, provides the context for our discussion.

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Activation of a Plant NLR Complex through Heteromeric Association with an Autoimmune Risk Variant of Another NLR

Cited by 76 publications

References 56 publications

Oligomerization of NLR immune receptor RPP7 triggered by atypical resistance protein RPW8/HR as ligand

Oligomerization of NLR immune receptor RPP7 triggered by atypical resistance protein RPW8/HR as ligand

NLR network mediates immunity to diverse plant pathogens

Molecular mechanisms that limit the costs of NLR‐mediated resistance in plants

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