NLR signaling in plants: from resistosomes to second messengers

Trends in Biochemical Sciences, Journal Year: 2023, Volume and Issue: 48(9), P. 776 - 787

Published: June 30, 2023

Pathogen effector-induced assembly of resistosomes has been established as an important event for nucleotide binding and leucine-rich repeat-containing receptor (NLR) signaling in plants.The pentameric coiled-coil domain-containing NLR (CNL) act Ca2+-permeable channels, whereas the tetrameric Toll-interleukin 1-like (TIR) (TNL) are NADase holoenzymes.TNL catalyze production nucleotide-derived second messengers to activate downstream helper NLRs activated disease resistance 1 (ADR1) N requirement gene (NRG1) CNL class. Thus, CNLs TNLs converge on Ca2+ signals trigger plant immunity.NLR cross-talks with pattern-triggered immunity (PTI) pathways.NLR pathways plants negatively regulated by both hosts pathogens. Nucleotide receptors (NLRs) have a critical role through direct or indirect recognition pathogen effectors. Recent studies demonstrated that such induces formation large protein complexes called mediate immune signaling. Some influx acting others function active NADases messengers. 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Adv. 8eabq5108Crossref (13) 25.Forderer al.A defines common principles channels.Nature. 610: 532-539Crossref 26.Salcedo al.Variation determines stem race Ug99.Science. 358: 1604-1606Crossref (117) spp, Hyaloperonospora parasitica, Puccinia graminis tritici, respectively. monitoring effector-mediated perturbations targets. example ZAR1 (HOPZ-ACTIVATED RESISTANCE [27.Lewis al.Allele-specific attenuation syringae HopZ1a type III protein.PLoS Genet. 6e1000894Crossref (111) exists preformed kinase RKS1 (resistance-related normal conditions recognizes AvrAC indirectly uridylylation another PBL2 (PBS1-like 2) [28.Wang al.Ligand-triggered allosteric ADP release primes complex.Science. 364aav5868Crossref (231) Scholar,29.Wang G. al.The decoy substrate pseudokinase specify modified-self plants.Cell Host Microbe. 2015; 18: 285-295Abstract (156) Scholar]; AvrAC-uridylylated associates consequently activates ZAR1-mediated immunity. Alternatively, cases, may not necessarily CHS3 (CHILLING SENSITIVE 3)/CSA1 (CONSTITUTIVE SHADE-AVOIDANCE pair detects PRR coreceptor BAK1 (BRASSINOSTEROID INSENSITIVE 1-associated [30.Yang al.Allelic variation CHS3/CSA1 reveals functional cell-death regulatory modes.Cell 30: 1701-1716Abstract (7) malectin-like receptor-like LET1 autoimmunity SUMM2 (SUPPRESSOR OF MKK1 MKK2) MEKK2 (MAP/ERK kinase-2) scaffolding [31.Liu LETUM1 modulates scaffolding.Nat. Plants. 6: 1106-1115Crossref (26) Effector leads termed 1). Cryoelectron microscopy (cryoEM) analyses show containing ZAR1, RKS1, uridylylated (PBL2UMP) forms wheel-like [32.Wang al.Reconstitution structure conferring immunity.Science. 364aav5870Crossref (368) 1, left). Pentamerization mainly NOD module PBL2UMP being presented rim wheel 2). contrast AvrSr35, remarkably similar Scholar,25.Forderer more study showed oligomeric NRG1 likely formed plasma membrane (PM) [33.Feehan al.Oligomerization requires activation.Proc. 120e2210406120Crossref (3) Interestingly, resistosomes, underlying await further elucidation By comparison, end results right). induced [21.Martin As seen primarily Structural modeling sequestered inactive Scholar,24.Zhao Scholar,32.Wang suggesting oligomerization. it remains unknown whether all resistosomes. Many pairs, executor initiating [34.Xi al.Insight mode action paired receptors.Essays 513-526Crossref (2) Whether how represent challenge understanding mechanisms. cryoEM resistosome, five α1-helices solvent-exposed shaped like channel pore Functional data support ETI. Importantly, electrophysiological evidence supports [35.Bi calcium-permeable triggering 184: 3528-3541Abstract (181) bottom Single molecule imaging hours before loss PM integrity These suggest acts α1 distantly related [36.Adachi al.An motif functionally across species.eLife. 8e49956Crossref (92) Ca2+-channel among Indeed, bears [25.Forderer essential helix well-defined resistosome. It environment funnel-shaped localization shown RPM1 (resistance pv. maculicola [37.El Kasmi F. al.Signaling plasma-membrane self-association full-length protein.Proc. E7385-E7394Crossref (70) RPS2 P. [38.Axtell M.J. Staskawicz B.J. Initiation RPS2-specified coupled AvrRpt2-directed elimination RIN4.Cell. 2003; 112: 369-377Abstract (643) bethamiana Tm-22 [39.Wang NB-ARC domain-mediated CC domain.PLoS Pathog. 16e1008475Crossref (20) ZAR1-like examined. 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Nucleocytoplasmic coordination immunity.New 236: 24-42Crossref mechanism associated enigmatic. Several interact factors [48.Wang al.Diversity, receptors.J. Integr. 63: 283-296Crossref (11) programming nucleus. transcription set genes, other reprogramming. NRG1A PM- nucleus-localized activation, only PM-resident oligomers oligomerization-independent function. Increases nuclear free reported various stresses [49.Pauly nucleus together cytosol generates specific signatures tobacco suspension culture cells.Cell Calcium. 2001; 413-421Crossref 50.van Der Luit A.H. al.Distinct calmodulin expression tobacco.Plant Physiol. 1999; 121: 705-714Crossref 51.Xiong T.C. al.Isolated nuclei mechanical thermal sensors signalling.Plant 2004; 40: 12-21Crossref should kept mind spatial distribution uniform, steep gradients few nanometers away [52.Pangršič al.EF-hand buffers exocytosis sensory hair cells.Proc. E1028-E1037Crossref transported PM-localized and/or reach possible continuum organelle endoplasmic reticulum (ER). Such result An CNGC15 symbiotic oscillation [53.Charpentier al.Nuclear-localized oscillations.Science. 352: 1102-1105Crossref While signals, they TNLs, CNLs, NADases. ATR1-induced significantly enhances activity, holoenzyme enzymatic encoded TIR [54.Wan L. al.TIR NAD+-cleaving enzymes promote death.Science. 365: 799-803Crossref (226) Scholar,55.Horsefield al.NAD+ cleavage animal pathways.Science. 793-799Crossref (244) TIR-only bacterial HopBA1 (RBA1) [56.Nishimura M.T. al.TIR-only RBA1 Arabidopsis.Proc. E2053-E2062Crossref (93) Tetramerization composite sites Scholar,22.Ma [57.Shi SARM1 recognition, small molecules.Mol. 82: 1643-1659Abstract (27) 58.Manik M.K. al.Cyclic ribose isomers: production, chemical structures, signaling.Science. 377eadc8969Crossref 59.Hogrel nucleotide-induced helical effector.Nature. 608: 808-812Crossref analogs PAD4 (phytoalexin deficient 4)

Language: Английский

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Pathogen perception and signaling in plant immunity

The Plant Cell, Journal Year: 2024, Volume and Issue: 36(5), P. 1465 - 1481

Published: Jan. 23, 2024

Abstract Plant diseases are a constant and serious threat to agriculture ecological biodiversity. Plants possess sophisticated innate immunity system capable of detecting responding pathogen infection prevent disease. Our understanding this has grown enormously over the past century. Early genetic descriptions plant disease resistance virulence were embodied in gene-for-gene hypothesis, while physiological studies identified pathogen-derived elicitors that could trigger defense responses cells tissues. Molecular these phenomena have now coalesced into an integrated model involving cell surface intracellular detection specific molecules proteins culminating induction various cellular responses. Extracellular receptors engage distinct signaling processes but converge on many similar outputs with substantial evidence for integration pathways interdependent networks controlling outcomes. Many molecular details recognition known, providing opportunities bioengineering enhance protection from Here we provide overview current main principles immunity, emphasis key scientific milestones leading insights.

Language: Английский

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Plasma membrane association and resistosome formation of plant helper immune receptors

Proceedings of the National Academy of Sciences, Journal Year: 2023, Volume and Issue: 120(32)

Published: July 31, 2023

Intracellular plant immune receptors, termed NLRs (Nucleotide-binding Leucine-rich repeat Receptors), confer effector-triggered immunity. Sensor are responsible for pathogen effector recognition. Helper function downstream of sensor to transduce signaling and induce cell death Activation that contain TIR (Toll/interleukin-1receptor) domains generates small molecules an association between a heterodimer signalosome EDS1 (EnhancedDisease Susceptibility 1)/SAG101 (Senescence-AssociatedGene 101) the helper NLR NRG1 (NRequired Gene 1). Autoactive NRG1s oligomerize form calcium channels largely localized at plasma membrane (PM). The molecular mechanisms PM effector-induced oligomerization not well characterized. We demonstrate require positively charged residues in their N-terminal phospholipid binding before after activation, despite conformational changes accompany activation. activation TIR-containing induces cytoplasmic pool EDS1/SAG101 is critical function. cannot be detected oligomerized resistosome, suggesting additional unknown triggers might required dissociation from previously described NRG1/EDS1/SAG101 heterotrimer subsequent oligomerization. Alternatively, resulting abrogate interface association. Our data provide observations regarding dynamic during underpin updated model resistosome formation.

Language: Английский

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Plant Toll/interleukin-1 receptor/resistance protein domains physically associate with enhanced disease susceptibility1 family proteins in immune signaling

iScience, Journal Year: 2024, Volume and Issue: 27(2), P. 108817 - 108817

Published: Jan. 24, 2024

Plant Toll/interleukin-1 receptor/resistance protein (TIR) type nucleotide-binding and leucine-rich repeat immune receptors (NLRs) require enhanced disease susceptibility 1 (EDS1) family proteins the helper NLRs NRG1 ADR1 for activation. We show that

Language: Английский

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Plasma membrane association and resistosome formation of plant helper immune receptors

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

Published: Jan. 24, 2023

Abstract Intracellular plant immune receptors, termed NLRs, respond to pathogen effectors delivered into cells. Activation of NLRs typically confers immunity. Sensor involved in effector recognition, are either TIR-NLRs (TNLs) or CC-NLRs (CNLs). Helper required for sensor NLR signaling, include CC R -NLRs (RNLs) and a special class CNLs known as NRCs. Activated TNLs produce small molecules that induce an association between the EDS1/SAG101 heterodimer NRG1s helper RNLs. Auto active oligomerize form calcium signaling channels largely localized at plasma membrane (PM). The molecular mechanisms PM induced NRG1 oligomerization not well characterized. We find both RNLs NRCs require positively charged residues second fourth helices their domain phospholipid binding before after activation, despite conformational changes accompany activation. demonstrate activation induces cytoplasmic pool is critical cell death function. cannot be detected oligomerized resistosome, suggesting additional unknown triggers might dissociation from previously described NRG1/EDS1/SAG101 heterotrimer subsequent oligomerization, resulting abrogate interface association. Our data provide new observations regarding dynamic during underpin updated model resistosome formation.

Language: Английский

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Downstream signaling induced by several plant Toll/interleukin-1 receptor-containing immune proteins is stable at elevated temperature

Cell Reports, Journal Year: 2025, Volume and Issue: 44(3), P. 115326 - 115326

Published: Feb. 19, 2025

Language: Английский

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Knockout of the Agrobacterium ILVC gene generates a valine-isoleucine auxotrophic strain for plant transformation

Transgenic Research, Journal Year: 2025, Volume and Issue: 34(1)

Published: May 2, 2025

Language: Английский

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Priming of plant’s immune system: the future sustainable approach for tea improvement

Discover Plants., Journal Year: 2024, Volume and Issue: 1(1)

Published: Nov. 11, 2024

Plant has an inherent or induced immunity to counter any abiotic biotic stress. Such a response is possible due physiological, molecular and cellular adaptations. Combined effect of stress can provoke cross-tolerance in plants, which may be synergistic antagonistic with the involvement protein kinases, transcription factors, phytohormones, reactive oxygen species (ROS). Priming plant's immune system leads accumulation certain biomolecules like phytoalexins PR proteins inside plant system. Exogenous application beta-aminobutyric acid, benzothiadiazole, azelaic acid been reported prime plants. Indian tea industry holds vital position economy. However, there enormous crop loss yearly tea. This happens despite using recommended agrochemicals disease-resistant cultivars. Non judicious chemical practices have created environmental pollution deposition pesticide residues made Therefore, sustainable approach improvement utmost requirement. done by screening followed identifying their pathway genes responsible for enhanced plant. Then candidate gene(s) over-expressed transgenic approach. In present review, we aim address two important issues: (i) system, (ii) encounter stresses priming its

Language: Английский

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A PRA-Rab trafficking machinery modulates NLR immune receptor plasma membrane microdomain anchoring and blast resistance in rice

Science Bulletin, Journal Year: 2024, Volume and Issue: unknown

Published: Dec. 1, 2024

Language: Английский

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The Hypersensitive Response to Plant Viruses

Viruses, Journal Year: 2023, Volume and Issue: 15(10), P. 2000 - 2000

Published: Sept. 26, 2023

Plant proteins with domains rich in leucine repeats play important roles detecting pathogens and triggering defense reactions, both at the cellular surface for pattern-triggered immunity cell to ensure effector-triggered immunity. As intracellular parasites, viruses are mostly detected intracellularly by a nucleotide binding site leucine-rich but receptor-like kinases repeats, known localize surface, have also been involved response viruses. In present review we report on progress that has achieved last decade role of these antiviral immunity, special focus our current understanding hypersensitive response.

Language: Английский

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