NLR signaling in plants: from resistosomes to second messengers

Trends in Biochemical Sciences, Год журнала: 2023, Номер 48(9), С. 776 - 787

Опубликована: Июнь 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. To counteract virulence activity effectors, evolved receptors: intracellular NLRs. specifically proteins, inducing effector-triggered (ETI) confer race-specific site entry Scholar,4.Jones J.D.G. al.Intracellular innate surveillance devices animals.Science. 2016; 354aaf6395Crossref different structures subcellular localizations but conserved responses, including influx, bursts reactive oxygen species (ROS), phytocytokines phytohormones, transcriptional reprogramming Probably reason, ETI tightly connected [5.Yuan M. al.Pattern-recognition required NLR-mediated immunity.Nature. 592: 105-109Crossref (351) Scholar,6.Ngou al.Mutual potentiation cell-surface receptors.Nature. 110-115Crossref (329) However, differ timing, amplitude, duration defense, which could be determining their physiological outcomes. addition includes hypersensitive response (HR), form rapid localized programmed death infection [7.Jones J.D. Dangl J.L. The system.Nature. 2006; 444: 323-329Crossref (8693) largest hundreds distinct members [4.Jones two domains: central nucleotide-binding oligomerization domain (NOD), C-terminal repeat (LRR) domain. A variable (CC) is attached terminus, resulting TIR-NLR CC-NLR (CNL), respectively [8.Maruta N. al.Structural basis activation signalling plants.Immunogenetics. 74: 5-26Crossref (25) Scholar,9.Hu Z. Chai J. Assembly architecture inflammasomes.Annu. Rev. Biophys. 52: 8.1-8.22Google pathogen-sensing NLRs, there some (h) translate from [10.Feehan al.Plant get little help friends.Curr. Opin. Biol. 56: 99-108Crossref (18) Scholar,11.Jubic L.M. al.Help wanted: responses.Curr. 2019; 50: 82-94Crossref (139) Examples hNLRs include Resistance Powdery Mildew 8 (RPW8) family [12.Wu al.Differential TNL-mediated redundant CNLs.New Phytol. 222: 938-953Crossref (118) 13.Castel B. al.Diverse defence via RPW8-NLR NRG1.New 966-980Crossref (144) 14.Qi T. al.NRG1 functions EDS1 regulate TIR-NLR-mediated Nicotiana benthamiana.Proc. Natl. Acad. Sci. U. S. A. 2018; 115: E10979-E10987Crossref (121) 15.Collier S.M. al.Cell mediated N-terminal domains unique highly class NB-LRR protein.Mol. Microbe Interact. 2011; 24: 918-931Crossref (230) Scholar] (Figure 1) (NRCs) [16.Adachi H. Kamoun networks plants.Essays Biochem. 66: 541-549Crossref (4) Scholar,17.Wu C.H. al.NLR network mediates diverse pathogens.Proc. 2017; 114: 8113-8118Crossref (211) More recent signaling, many sensor Solanaceae, depends NRCs upon [18.Ahn H.K. al.Effector-dependent NRC Rpi-amr3 Rpi-amr1.EMBO 2023; 42e111484Crossref (5) Scholar,19.Contreras M.P. al.Sensor helpers pathogens.EMBO 42e111519PubMed messengers, calcium ion derivations. crosstalk between negative effectors host regulators. directly indirectly. For example, interaction benthamiana TNL Roq1 (recognition XopQ its recognized (Xanthomonas outer Q) [20.Schultink al.Roq1 Xanthomonas Pseudomonas HopQ1.Plant 92: 787-795Crossref (82) Scholar,21.Martin R. al.Structure ROQ1 recognizing XopQ.Science. 370eabd9993Crossref (174) Scholar], arabidopsis RPP1 Peronospora parasitica ATR1 (Arabidopsis thaliana [22.Ma al.Direct pathogen-induced complex holoenzyme.Science. 370abe3069Crossref (169) Scholar,23.Krasileva K.V. al.Activation Arabidopsis specified planta association cognate oomycete effector.Plant 2010; 22: 2444-2458Crossref (220) wheat Sr35 (stem rust 35) AvrSr35 [24.Zhao Y.-B. al.Pathogen triggers mechanism.Sci. 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. TNL-activated hNLRs, NRG1s, ADR1s display autoactive Scholar,40.Jacob "helper" nonselective cation channels.Science. 373: 420-425Crossref (125) indicating Solanaceae (SD) found noncanonical [41.Seong K. al.Evolution genes wild tomato species.New 227: 1530-1543Crossref (36) themselves structures. undetermined activity. Multiple lines extracellular [42.Xu tale families: channels immunity.Plant 1551-1567Crossref (19) Scholar,43.Kim N.H. al.Con-Ca2+-tenating channels.New 234: 813-818Crossref (8) Elevation concentrations one earliest during Gain-of-function mutations CNGC19/20 (CYCLIC NUCLEOTIDE GATED CHANNEL19/20) increased constitutively (enhanced susceptibility 1)- SA (salicylic acid)-dependent [44.Yu X. kinases BAK1/SERK4 channel-mediated cellular homeostasis containment.Curr. 29: 3778-3790Abstract (64) Scholar,45.Zhao mis-regulated cyclic nucleotide-gated cytosolic elevation Arabidopsis.New 230: 1078-1094Crossref (33) Unregulated Sr35, NRG1, ADR1 sufficient recapitulate CNL-mediated eukaryotic Although released internal pools contribute pharmacological blocking compartments ruthenium red (RR) less efficient inhibition HR than blocker LaCl3 [46.Gao heat-activated 6 involved heat shock responses.Plant 2012; 70: 1056-1069Crossref supporting notion major responses. Nuclear [47.Ludke D. yet? 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)

Язык: Английский

---

Plant NLR immunity activation and execution: a biochemical perspective

Open Biology, Год журнала: 2024, Номер 14(1)

Опубликована: Янв. 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.

Язык: Английский

---

New Biochemical Principles for NLR Immunity in Plants

Molecular Plant-Microbe Interactions, Год журнала: 2023, Номер 36(8), С. 468 - 475

Опубликована: Авг. 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 .

Язык: Английский

---

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

South African Journal of Botany, Год журнала: 2024, Номер 169, С. 464 - 485

Опубликована: Май 4, 2024

Язык: Английский

---

Nucleotides and nucleotide derivatives as signal molecules in plants

Journal of Experimental Botany, Год журнала: 2024, Номер 75(22), С. 6918 - 6938

Опубликована: Сен. 9, 2024

Abstract In reaction to a stimulus, signaling molecules are made, generate response, and then degraded. Nucleotides classically associated with central metabolism nucleic acid biosynthesis, but there number of nucleotides nucleotide derivatives in plants which this simple definition molecule applies whole or at least part. These include cytokinins chloroplast guanosine tetraposphate (ppGpp), as well extracellular canonical such ATP (eATP) NAD+ (eNAD+). addition, is series compounds derived from ADP ribose (ADPR), ATP–ADPR dinucleotides their hydrolysis products (e.g. pRib-AMP) together different variants cyclic ADPR (cADPR, 2´-cADPR, 3´-cADPR), also 3´,5´-cAMP 2´,3´-cyclic nucleoside monophosphates. Interestingly, some these have recently been shown play role pathogen defense. review, we highlight exciting new developments. We review that considered candidates for molecules, example purine deoxynucleosides, discuss more controversial cases.

Язык: Английский

---

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

The Plant Journal, Год журнала: 2024, Номер 119(5), С. 2316 - 2330

Опубликована: Июль 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.

Язык: Английский

---

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

Structure, Год журнала: 2025, Номер unknown

Опубликована: Янв. 1, 2025

Язык: Английский

---

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

Theoretical and Applied Genetics, Год журнала: 2025, Номер 138(3)

Опубликована: Март 1, 2025

Язык: Английский

---

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

Molecular Cell, Год журнала: 2025, Номер 85(6), С. 1052 - 1053

Опубликована: Март 1, 2025

Язык: Английский

---

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

Plant Communications, Год журнала: 2023, Номер 5(1), С. 100645 - 100645

Опубликована: Июль 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.

Язык: Английский

---