Identification and receptor mechanism of TIR-catalyzed small molecules in plant immunity

Science, Journal Year: 2022, Volume and Issue: 377(6605)

Published: July 7, 2022

Plant nucleotide-binding leucine-rich repeat-containing (NLR) receptors with an N-terminal Toll/interleukin-1 receptor (TIR) domain sense pathogen effectors to enable TIR-encoded nicotinamide adenine dinucleotide hydrolase (NADase) activity for immune signaling. TIR-NLR signaling requires the helper NLRs N requirement gene 1 (NRG1), Activated Disease Resistance (ADR1), and Enhanced Susceptibility (EDS1), which forms a heterodimer each of its paralogs Phytoalexin Deficient 4 (PAD4) Senescence-Associated Gene 101 (SAG101). Here, we show that TIR-containing proteins catalyze production 2'-(5''-phosphoribosyl)-5'-adenosine monophosphate (pRib-AMP) diphosphate (pRib-ADP) in vitro planta. Biochemical structural data demonstrate EDS1-PAD4 is complex pRib-AMP pRib-ADP, allosterically promote interaction ADR1-L1 but not NRG1A. Our study identifies TIR-catalyzed pRib-ADP as missing link TIR through likely second messengers plant immunity.

Language: Английский

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TIR-catalyzed ADP-ribosylation reactions produce signaling molecules for plant immunity

Science, Journal Year: 2022, Volume and Issue: 377(6605)

Published: July 7, 2022

Plant pathogen-activated immune signaling by nucleotide-binding leucine-rich repeat (NLR) receptors with an N-terminal Toll/interleukin-1 receptor (TIR) domain converges on Enhanced Disease Susceptibility 1 (EDS1) and its direct partners, Phytoalexin Deficient 4 (PAD4) or Senescence-Associated Gene 101 (SAG101). TIR-encoded nicotinamide adenine dinucleotide hydrolase (NADase) produces molecules to promote exclusive EDS1-PAD4 EDS1-SAG101 interactions helper NLR subclasses. In this work, we show that TIR-containing proteins catalyze adenosine diphosphate (ADP)-ribosylation of triphosphate (ATP) ADP ribose (ADPR) through ADPR polymerase-like NADase activity, forming ADP-ribosylated ATP (ADPr-ATP) ADPr-ADPR (di-ADPR), respectively. Specific binding ADPr-ATP di-ADPR allosterically promotes interaction N requirement gene 1A (NRG1A) in vitro planta. Our data reveal enzymatic activity TIRs enables specific activation the EDS1-SAG101-NRG1 immunity branch.

Language: Английский

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TIR domains of plant immune receptors are 2′,3′-cAMP/cGMP synthetases mediating cell death

Cell, Journal Year: 2022, Volume and Issue: 185(13), P. 2370 - 2386.e18

Published: May 20, 2022

Language: Английский

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

Proceedings of the National Academy of Sciences, Journal Year: 2023, Volume and Issue: 120(11)

Published: March 6, 2023

Plant disease resistance involves both detection of microbial molecular patterns by cell-surface pattern recognition receptors and pathogen effectors intracellular NLR immune receptors. NLRs are classified as sensor NLRs, involved in effector detection, or helper required for signaling. TIR-domain-containing (TNLs) require NRG1 ADR1 resistance, activation defense requires the lipase-domain proteins EDS1, SAG101, PAD4. Previously, we found that associates with EDS1 SAG101 a TNL activation-dependent manner [X. Sun et al. , Nat. Commun. 12 3335 (2021)]. We report here how itself during TNL-initiated immunity. Full immunity coactivation mutual potentiation receptor-initiated signaling [B. P. M. Ngou, H.-K. Ahn, Ding, J. D. G. Jones, Nature 592 110–115 (2021), Yuan 105–109 find while TNLs is sufficient to promote NRG1–EDS1–SAG101 interaction, formation an oligomeric resistosome additional defense. These data suggest vivo part mechanism links receptor pathways.

Language: Английский

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Plant and prokaryotic TIR domains generate distinct cyclic ADPR NADase products

Science Advances, Journal Year: 2023, Volume and Issue: 9(11)

Published: March 17, 2023

Toll/interleukin-1 receptor (TIR) domain proteins function in cell death and immunity. In plants bacteria, TIR domains are often enzymes that produce isomers of cyclic adenosine 5′-diphosphate–ribose (cADPR) as putative immune signaling molecules. The identity functional conservation cADPR isomer signals is unclear. A previous report found a plant could cross-activate the prokaryotic Thoeris TIR–immune system, suggesting TIR-immune signals. Here, we generate autoactive TIRs test converse hypothesis: Do also immunity? Using planta vitro assays, find overlapping sets further clarify how activate system via producing 3′cADPR. This study demonstrates requirements for systems distinct across kingdoms diversity small-molecule products.

Language: Английский

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Time-resolved single-cell and spatial gene regulatory atlas of plants under pathogen attack

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2023, Volume and Issue: unknown

Published: April 10, 2023

Abstract Plant leaf intercellular space provides a nutrient-rich and heterogeneous niche for microbes that critically impacts plant health. However, how individual cells respond to microbial colonization remains largely elusive. Here, by time-resolved simultaneous single-cell transcriptome epigenome profiling of plants ( Arabidopsis thaliana ) infected virulent avirulent bacterial pathogens Pseudomonas syringae ), we present cell atlases with gene regulatory logic involving transcription factors, putative cis -regulatory elements, target genes associated disease immunity. We also identify previously uncharacterized populations distinct immune expression within major developmental types. Furthermore, employ spatial transcriptomics reveal heterogeneity responses linked pathogen distribution. Integrating our multiomics omics data enables spatiotemporal mapping defense cells. Our study molecularly-defined map plant-microbe interaction at the resolution.

Language: Английский

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Substrate-induced condensation activates plant TIR domain proteins

Nature, Journal Year: 2024, Volume and Issue: 627(8005), P. 847 - 853

Published: March 13, 2024

Abstract Plant nucleotide-binding leucine-rich repeat (NLR) immune receptors with an N-terminal Toll/interleukin-1 receptor (TIR) domain mediate recognition of strain-specific pathogen effectors, typically via their C-terminal ligand-sensing domains 1 . Effector binding enables TIR-encoded enzymatic activities that are required for TIR–NLR (TNL)-mediated immunity 2,3 Many truncated TNL proteins lack effector-sensing but retain similar and 4,5 The mechanism underlying the activation these TIR remain unclear. Here we show substrates NAD + ATP induces phase separation in vitro. A condensation occurs a protein expressed its native promoter response to inoculation planta. formation condensates is mediated by conserved self-association interfaces predicted intrinsically disordered loop region TIRs. Mutations disrupt impair cell death activity proteins. Our data reveal as provide insight into substrate-induced autonomous signalling confer plant immunity.

Language: Английский

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Plant NLR immunity activation and execution: a biochemical perspective

Open Biology, Journal Year: 2024, Volume and Issue: 14(1)

Published: Jan. 1, 2024

Plants deploy cell-surface and intracellular receptors to detect pathogen attack trigger innate immune responses. Inside host cells, families of nucleotide-binding/leucine-rich repeat (NLR) proteins serve as sensors or downstream mediators defence outputs cell death, which prevent disease. Established genetic underpinnings NLR-mediated immunity revealed various strategies plants adopt combat rapidly evolving microbial pathogens. The molecular mechanisms NLR activation signal transmission components controlling execution were less clear. Here, we review recent protein structural biochemical insights plant sensor signalling functions. When put together, the data show how different families, whether transducers, converge on nucleotide-based second messengers cellular calcium confer immunity. Although pathogen-activated NLRs in engage plant-specific machineries promote defence, comparisons with mammalian receptor counterparts highlight some shared working principles for across kingdoms.

Language: Английский

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Convergent reduction of immune receptor repertoires during plant adaptation to diverse special lifestyles and habitats

Nature Plants, Journal Year: 2025, Volume and Issue: unknown

Published: Jan. 16, 2025

Language: Английский

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Structure, biochemical function, and signaling mechanism of plant NLRs

Molecular Plant, Journal Year: 2022, Volume and Issue: 16(1), P. 75 - 95

Published: Nov. 22, 2022

To counter pathogen invasion, plants have evolved a large number of immune receptors, including membrane-resident pattern recognition receptors (PRRs) and intracellular nucleotide-binding leucine-rich repeat (NLRs). Our knowledge about PRR NLR signaling mechanisms has expanded significantly over the past few years. Plant NLRs form multi-protein complexes called resistosomes in response to effectors, mediated by converges on Ca2+-permeable channels. channels important for also been identified. These findings highlight crucial role Ca2+ triggering plant signaling. In this review, we first discuss structural biochemical non-canonical then summarize our immune-related their roles We potential intricate interaction between

Language: Английский

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