Sensor NLR immune proteins activate oligomerization of their NRC helper

Contreras, Mauricio P; Pai, Hsuan; Tümtaş, Yasin; Duggan, Cian; Yuen, Enoch Lok Him; Cruces, Angel Vergara; Kourelis, Jiorgos; Ahn, Hee-Kyung; Wu, Chih‐Hang; Bozkurt, Tolga O.; Derevnina, Lida; Kamoun, Sophien

doi:10.1101/2022.04.25.489342

Cited by 16 publications

(36 citation statements)

References 60 publications

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“…The NRC2 EEE -Myc oligomerization patterns resulting from Rpi-amr1 and Rpi-amr3 activation were indistinguishable (Fig 2C, D). In a companion paper (Contreras et al , 2022), the NRC-dependent CC-NLRs Bs2 and Rx were also shown to activate NRC2 oligomerization into slower migrating forms indistinguishable from what we report here. This indicates that NRC2 oligomerization to ~900 kDa is a universal mode of action for NRC-dependent Solanaceae sensor NLRs, and further supports the conclusion that sensor NLRs are not included in the NRC2 resistosome.…”

Section: Discussionsupporting

confidence: 77%

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Effector-dependent activation and oligomerization of NRC helper NLRs by Rpi-amr3 and Rpi-amr1

Ahn

Lin

Olave-Achury

et al. 2022

Preprint

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Plant pathogens compromise crop yields. Plants have evolved robust innate immunity that depends in part on intracellular Nucleotide-binding, Leucine Rich-Repeat (NLR) immune receptors that activate defense responses upon detection of pathogen-derived effectors. Most “sensor” NLRs that detect effectors require the activity of “helper” NLRs, but how helper NLRs support sensor NLR function is poorly understood. Many Solanaceae NLRs require the NRC (NLR-Required for Cell death) class of helper NLRs. We show here that Rpi-amr3, a sensor NLR from Solanum americanum, detects AVRamr3 from the potato late blight pathogen, Phytophthora infestans, and activates oligomerization of the helper NLR NRC2 into a high-molecular weight resistosome. The NRC2 resistosome also forms upon recognition of P. infestans effector AVRamr1 by another sensor NLR, Rpi-amr1. The ATP-binding motif of Rpi-amr3 is required for NRC2 resistosome formation, but not for interaction with the cognate effector. The NRC2 resistosome can be activated by AVRamr3 homologs from other Phytophthora species. Mechanistic understanding of NRC resistosome formation will underpin engineering crops with durable disease resistance.

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Section: Discussionsupporting

confidence: 77%

“…This implies that the N-terminal MADA motif mutation of L9E/L13E/L17E of NRC2 is likely to only affect any possible channel activity and prevent cell death but should not compromise oligomerization. Contreras et al . (2022) show that activation of NRC2 EEE -Myc by Rx results in enhanced association with the membrane fraction.…”

Section: Discussionmentioning

confidence: 99%

Effector-dependent activation and oligomerization of NRC helper NLRs by Rpi-amr3 and Rpi-amr1

Ahn

Lin

Olave-Achury

et al. 2022

Preprint

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“…3). This also contrasts with the quantitative conversion of inactive to oligomerized helper NLR NRC in Solanaceae (36, 37). It may be that very few activated forms of NRG1-EDS1-SAG101 Resistosomes are sufficient for defense, which potentially increase Ca 2+ influx to the cytoplasm (15).…”

Section: Discussionmentioning

confidence: 87%

“…3). This also contrasts with the quantitative conversion of inactive to oligomerized helper NLR NRC in Solanaceae (36,37). It may be that very few activated forms of NRG1-EDS1-SAG101…”

Section: Discussionmentioning

confidence: 91%

Oligomerisation of a plant helper NLR requires cell-surface and intracellular immune receptor activation

Feehan

Wang

Choi

et al. 2022

Preprint

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Plant disease resistance involves both detection of microbial molecular patterns by cell-surface pattern recognition receptors and detection of pathogen effectors by intracellular NLR immune receptors. NLRs are classified as sensor NLRs, involved in effector detection, or helper NLRs required for sensor NLR signalling. TIR-domain-containing sensor NLRs (TNLs) require helper NLRs NRG1 and ADR1 for resistance, and their activation of defense also requires the lipase-domain proteins EDS1, SAG101 and PAD4. We investigated how the helper NLR NRG1 supports TNL-initiated immunity with EDS1 and SAG101. We find that NRG1 associates with EDS1 and SAG101 at the plasma membrane and in the nucleus, but only self-associates at the plasma membrane. Activation of TNLs is sufficient to trigger NRG1-EDS1-SAG101 interaction, but cell-surface receptor-initiated defense is also required to form an oligomeric Resistosome. The data point to formation of NRG1-EDS1-SAG101 heterotrimers in the nucleus upon intracellular receptor activation alone and indicate formation of NRG1-EDS1-SAG101 Resistosomes at the plasma membrane upon co-activation of intracellular and cell surface-receptor pathways.

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“…Ca 2+ plays important signalling roles in plant defence, and misregulation of Ca 2+ influx in plant cells can induce HR cell death and auto‐immunity (Wang et al ., 2019b; Thor et al ., 2020; Tian et al ., 2020; Ren et al ., 2021; Kim et al ., 2022; Xu et al ., 2022). The activated Nicotiana benthamiana ( Nb ) helpers NRC2 and NRC4 also form homo‐oligomers and dynamically reorganise into plasma‐membrane localised punctate structures upon sensor activation (Adachi et al ., 2019a; Duggan et al ., 2021; Ahn et al ., 2022; Contreras et al ., 2022). This suggests that activated CC‐type singleton/helper NLR resistosomes act as membrane channels that initiate downstream responses, likely to involve Ca 2+ signalling‐mediated transcriptional changes and cell death (Fig.…”

Section: Plant Immunity Relies On Nonself and Modified‐self Recogniti...mentioning

confidence: 99%

NLR we there yet? Nucleocytoplasmic coordination of NLR‐mediated immunity

Lüdke¹,

Yan²,

Rohmann³

et al. 2022

New Phytologist

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Plant intracellular nucleotide-binding leucine-rich repeat immune receptors (NLRs) perceive the activity of pathogen-secreted effector molecules that, when undetected, promote colonisation of hosts. Signalling from activated NLRs converges with and potentiates downstream responses from activated pattern recognition receptors (PRRs) that sense microbial signatures at the cell surface. Efficient signalling of both receptor branches relies on the host cell nucleus as an integration point for transcriptional reprogramming, and on the macromolecular transport processes that mediate the communication between cytoplasm and nucleoplasm. Studies on nuclear pore complexes (NPCs), the nucleoporin proteins (NUPs) that compose NPCs, and nuclear transport machinery constituents that control nucleocytoplasmic transport, have revealed that they play important roles in regulating plant immune responses. Here, we discuss the contributions of nucleoporins and nuclear transport receptor (NTR)-mediated signal transduction in plant immunity with an emphasis on NLR immune signalling across the nuclear compartment boundary and within the nucleus. We also highlight and discuss cytoplasmic and nuclear functions of NLRs and their signalling partners and further consider the potential implications of NLR activation and resistosome formation in both cellular compartments for mediating plant pathogen resistance and programmed host cell death.

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Sensor NLR immune proteins activate oligomerization of their NRC helper

Cited by 16 publications

References 60 publications

Effector-dependent activation and oligomerization of NRC helper NLRs by Rpi-amr3 and Rpi-amr1

Effector-dependent activation and oligomerization of NRC helper NLRs by Rpi-amr3 and Rpi-amr1

Oligomerisation of a plant helper NLR requires cell-surface and intracellular immune receptor activation

NLR we there yet? Nucleocytoplasmic coordination of NLR‐mediated immunity

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