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. In this review we summarize these resistosome-mediated derivatives. We also discuss events regulation resistosome Plants rely multiple detect invading microbial pathogens mount responses [1.Ngou B.P.M. et al.Thirty years resistance: zig-zag system.Plant Cell. 2022; 34: 1447-1478Crossref PubMed Scopus (45) Google Scholar,2.Zhou J.M. Zhang Y. Plant immunity: danger perception signaling.Cell. 2020; 181: 978-989Abstract Full Text PDF (328) Scholar]. One subfamily pattern-recognition (PRRs) (see Glossary) at cell surface Scholar, 2.Zhou 3.DeFalco T.A. Zipfel C. Molecular mechanisms early signaling.Mol. 2021; 81: 3449-3467Abstract (0) PRRs recognize pathogen-associated molecular patterns (PAMPs) host-derived damage-associated (DAMPs), leading (PTI). PTI constitutes first line inducible defense against can breach layer secreting effector proteins into cells dampen PTI. 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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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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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New Biochemical Principles for NLR Immunity in Plants

Molecular Plant-Microbe Interactions, Journal Year: 2023, Volume and Issue: 36(8), P. 468 - 475

Published: Aug. 1, 2023

While working for the United States Department of Agriculture on North Dakota Agricultural College campus in Fargo, Dakota, 1940s and 1950s, Harold H. Flor formulated genetic principles coevolving plant host-pathogen interactions that govern disease resistance or susceptibility. His ‘gene-for-gene’ legacy runs deep modern pathology continues to inform molecular models immune recognition signaling. In this review, we discuss recent biochemical insights immunity conferred by nucleotide-binding domain/leucine-rich-repeat (NLR) receptors, which are major gene-for-gene determinants nature cultivated crops. Structural analyses pathogen-activated NLR oligomers (resistosomes) reveal how different subtypes converge various ways calcium (Ca 2+ ) signaling promote pathogen host cell death. Especially striking is identification nucleotide-based signals generated enzymatically toll-interleukin 1 receptor (TIR) domain NLRs. These small molecules part an emerging family TIR-produced cyclic noncyclic nucleotide steer cell-death responses bacteria, mammals, plants. A combined genetic, molecular, understanding activation provides exciting new opportunities combatting diseases [Formula: see text] Copyright © 2023 The Author(s). This open access article distributed under CC BY-NC-ND 4.0 International license .

Language: Английский

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Calcium (Ca2+) signaling in plants: A plant stress perspective

South African Journal of Botany, Journal Year: 2024, Volume and Issue: 169, P. 464 - 485

Published: May 4, 2024

Language: Английский

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Evolutionary and immune‐activating character analyses of NLR genes in algae suggest the ancient origin of plant intracellular immune receptors

The Plant Journal, Journal Year: 2024, Volume and Issue: 119(5), P. 2316 - 2330

Published: July 7, 2024

SUMMARY Nucleotide‐binding leucine‐rich repeat (NLR) proteins are crucial intracellular immune receptors in plants, responsible for detecting invading pathogens and initiating defense responses. While previous studies on the evolution function of NLR genes were mainly limited to land evolutionary trajectory immune‐activating character algae remain less explored. In this study, genome‐wide gene analysis was conducted 44 chlorophyte species across seven classes charophyte five classes. A few but variable number genes, ranging from one 20, identified chlorophytes three charophytes, whereas no remaining algal genomes. Compared with genomes possess fewer or usually implying that expansion plants can be attributed their adaptation more complex terrestrial pathogen environments. Through phylogenetic analysis, domain composition conserved motifs profiling NBS domain, we detected shared lineage‐specific features between supporting common origin continuous green plant genes. Immune‐activation assays revealed both TNL RNL elicit hypersensitive responses Nicotiana benthamiana , indicating molecular basis activation has emerged early stage different types proteins. summary, results study suggest may have taken a role as ancestor plants.

Language: Английский

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Structure-guided insights into TIR-mediated bacterial and eukaryotic immunity

Structure, Journal Year: 2025, Volume and Issue: unknown

Published: Jan. 1, 2025

Language: Английский

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Fine mapping of stripe rust resistance gene YrAn1589 in common wheat using Wheat660K SNP array and BSR-Seq

Theoretical and Applied Genetics, Journal Year: 2025, Volume and Issue: 138(3)

Published: March 1, 2025

Language: Английский

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Proteome-wide discovery of phage anti-defense proteins by Alphafold2

Molecular Cell, Journal Year: 2025, Volume and Issue: 85(6), P. 1052 - 1053

Published: March 1, 2025

Language: Английский

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Systemic analysis of metabolome reconfiguration in Arabidopsis after abiotic stressors uncovers metabolites that modulate defense against pathogens

Plant Communications, Journal Year: 2023, Volume and Issue: 5(1), P. 100645 - 100645

Published: July 4, 2023

Understanding plant immune responses is complex due to the high interdependence among biological processes in homeostatic networks. Hence, integration of environmental cues causes network rewiring that interferes with defence responses. Similarly, plants retain molecular signatures configured under abiotic stress periods rapidly respond recurrent can alter immunity. Metabolome changes imposed by stressors are persistent, although impact on elusive. In this study, we profiled metabolomes Arabidopsis several treatments applied individually or simultaneously capture temporal trajectories metabolite composition during adverse conditions and recovery. Further systemic analysis was conducted address relevance metabolome extract central features be tested planta. Our results demonstrate irreversibility major fractions as a general pattern response periods. Functional co-abundance networks points convergences reconfiguration metabolism organic acids secondary metabolites. mutant lines for components related these metabolic pathways displayed altered capacities against different pathogens. Collectively, our data support sustained environments act modulators provide evidence new layer regulation defence.

Language: Английский

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Unveiling the role of vermicompost in modulating phenylpropanoid metabolism in basil (Ocimum basilicum L.): A single-cell type PGT approach

Current Plant Biology, Journal Year: 2024, Volume and Issue: 38, P. 100335 - 100335

Published: March 5, 2024

This research delves into phenylpropanoid metabolism, focusing on phenylpropene biosynthesis in the methyleugenol chemotype of basil (Ocimum basilicum L.). We isolated peltate glandular trichomes (PGTs) from leaves to eliminate primary metabolic influences, offering a unique perspective these complex processes. Vermicompost, chosen for its eco-friendly composition and superiority invigorating metabolism. In this study, we investigated impacts solid tea-form vermicompost applications at 0%, 10%, 25% doses basil, expression levels PAL, 4CL, EGS, EOMT, CVOMT genes accumulation trichomes. Results showed that 10% (SV) application increased 4CL level 236%, while SV further enhanced EOMT expressions towering values by7494-fold 19643-fold, respectively. did not significantly impact eugenol but suppressed chavicol biosynthesis. Methyleugenol methylchavicol rose dose-dependent manner, with significant increases observed application. A positive correlation was found between rates phenylpropenes following applications. Conversely, tea (VT) led mixed gene patterns reduced ratios compared control. summary, notably high results our preliminary study offer new field underscores value utilizing single-cell type PGTs examining secondary pathways plants demonstrates production. Keywords:

Language: Английский

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