NLR receptors in plant immunity: making sense of the alphabet soup

EMBO Reports, Год журнала: 2023, Номер 24(10)

Опубликована: Авг. 21, 2023

Plants coordinately use cell-surface and intracellular immune receptors to perceive pathogens mount an response. Intracellular events of pathogen recognition are largely mediated by the nucleotide binding leucine rich-repeat (NLR) classes. Upon perception, NLRs trigger a potent broad-spectrum reaction, usually accompanied form programmed cell death termed hypersensitive Some plant act as multifunctional singleton which combine detection signaling. However, can also function in higher order pairs networks functionally specialized interconnected receptors. In this article, we cover basic aspects NLR biology with emphasis on networks. We highlight some recent advances structure, function, activation discuss emerging topics such modulator NLRs, suppression bioengineering. Multi-disciplinary approaches required disentangle how these receptor evolve. Answering questions holds potential deepen our understanding system unlock new era disease resistance breeding.

Язык: Английский

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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. 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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. 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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)

Язык: Английский

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Tandem kinase proteins across the plant kingdom

Nature Genetics, Год журнала: 2025, Номер 57(1), С. 254 - 262

Опубликована: Янв. 1, 2025

Язык: Английский

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Structure, biochemical function, and signaling mechanism of plant NLRs

Molecular Plant, Год журнала: 2022, Номер 16(1), С. 75 - 95

Опубликована: Ноя. 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

Язык: Английский

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Allelic compatibility in plant immune receptors facilitates engineering of new effector recognition specificities

The Plant Cell, Год журнала: 2023, Номер 35(10), С. 3809 - 3827

Опубликована: Июль 24, 2023

Engineering the plant immune system offers genetic solutions to mitigate crop diseases caused by diverse agriculturally significant pathogens and pests. Modification of intracellular receptors nucleotide-binding leucine-rich repeat (NLR) receptor superfamily for expanded recognition pathogen virulence proteins (effectors) is a promising approach engineering disease resistance. However, can cause NLR autoactivation, resulting in constitutive defense responses that are deleterious plant. This may be due NLRs associating highly complex signaling networks coevolve together, changes through breeding or modification generate incompatible combinations, autoimmune phenotypes. The sensor helper rice (Oryza sativa) pair Pik have coevolved, mismatching between noncoevolved alleles triggers activation cell death. limits extent which protein modifications used engineer enhance resistance mediated these NLRs. Here, we dissected incompatibility determinants Nicotiana benthamiana found heavy metal-associated (HMA) domains integrated Pik-1 not only evolved bind effectors but also likely coevolved with other maintain homeostasis. explains why lead autoactivation. We then this knowledge facilitate new effector specificities, overcoming initial penalties. show Pik-2, enable integration synthetic novel enhanced specificities. Taken our results reveal strategy NLRs, has potential allow an set integrations therefore specificities plants.

Язык: Английский

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Alternative splicing of a potato disease resistance gene maintains homeostasis between growth and immunity

The Plant Cell, Год журнала: 2024, Номер 36(9), С. 3729 - 3750

Опубликована: Июнь 28, 2024

Abstract Plants possess a robust and sophisticated innate immune system against pathogens must balance growth with rapid pathogen detection defense. The intracellular receptors nucleotide-binding leucine-rich repeat (NLR) motifs recognize pathogen-derived effector proteins thereby trigger the response. expression of genes encoding NLR is precisely controlled in multifaceted ways. alternative splicing (AS) introns response to infection recurrently observed but poorly understood. Here we report that potato (Solanum tuberosum) gene RB undergoes AS its intron, resulting 2 transcriptional isoforms, which coordinately regulate plant immunity homeostasis. During normal growth, predominantly exists as an intron-retained isoform RB_IR, truncated protein containing only N-terminus NLR. Upon late blight infection, induces intron RB, increasing abundance RB_CDS, encodes full-length active R protein. By deploying isoforms fused luciferase reporter system, identified IPI-O1 (also known Avrblb1), cognate effector, facilitator AS. directly interacts factor StCWC15, altered localization StCWC15 from nucleoplasm nucleolus nuclear speckles. Mutations eliminate binding also disrupt re-localization splicing. Thus, our study reveals serves surveillance senses pathogen-secreted regulates trade-off between RB-mediated expanding understanding molecular plant–microbe interactions.

Язык: Английский

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Assembly and functional mechanisms of plant NLR resistosomes

Current Opinion in Structural Biology, Год журнала: 2025, Номер 90, С. 102977 - 102977

Опубликована: Янв. 13, 2025

Язык: Английский

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Deciphering Plant NLR Genomic Evolution: Synteny-Informed Classification Unveils Insights into TNL Gene Loss

Molecular Biology and Evolution, Год журнала: 2025, Номер unknown

Опубликована: Янв. 21, 2025

Abstract Nucleotide-binding leucine-rich repeat receptor (NLR) genes encode a pivotal class of plant immune receptors. However, their rampant duplication and loss have made inferring genomic evolutionary trajectory difficult, exemplified by the TNL family in monocots. In this study, we introduce novel classification system for angiosperm NLR genes, grounded network analysis micro-synteny information. This refined categorizes these into five classes: CNL_A, CNL_B, CNL_C, TNL, RNL. Compared to previous classification, further subdivided CNLs three subclasses. The credibility is supported phylogenetic examination protein domain structures. Importantly, enabled model explain extinction Compelling evidence underscores revelation, indicating clear synteny correspondence between non-TNLs monocots extinct subclass. Our study provides crucial insights origin divergence subfamilies, unveiling malleability-driven journey that has shaped functionality diversity genes.

Язык: Английский

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Subcellular localization requirements and specificities for plant immune receptor Toll‐interleukin‐1 receptor signaling

The Plant Journal, Год журнала: 2023, Номер 114(6), С. 1319 - 1337

Опубликована: Март 18, 2023

SUMMARY Recent work shed light on how plant intracellular immune receptors of the nucleotide‐binding leucine‐rich repeat (NLR) family are activated upon pathogen effector recognition to trigger responses. Activation Toll‐interleukin‐1 receptor (TIR) domain‐containing NLRs (TNLs) induces oligomerization and close proximity TIR domain, which is required for enzymatic activity. TIR‐catalyzed small signaling molecules bind EDS1 heterodimers subsequently activate downstream helper NLRs, function as Ca 2+ permeable channel responses eventually leading cell death. Subcellular localization requirements TNLs partners not well understood, although they understand fully mechanisms underlying NLR early signaling. show diverse subcellular while shows nucleocytosolic localization. Here, we studied impact mislocalization activation different TNLs. In Nicotiana benthamiana , our results suggest that domains isolated from flax L6 Arabidopsis RPS4 SNC1 drives compartments. Nevertheless, both Golgi‐membrane anchored have same in thaliana . By using mislocalized variants EDS1, found autoimmune domain can induce seedling death when present cytosol. However, restricted nucleus, a stunting phenotype but no Our data point out importance thoroughly investigating dynamics TNL fully.

Язык: Английский

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The roles of Magnaporthe oryzae avirulence effectors involved in blast resistance/susceptibility

Frontiers in Plant Science, Год журнала: 2024, Номер 15

Опубликована: Окт. 9, 2024

Phytopathogens represent an ongoing threat to crop production and a significant impediment global food security. During the infection process, these pathogens spatiotemporally deploy large array of effectors sabotage host defense machinery and/or manipulate cellular pathways, thereby facilitating colonization infection. However, besides their pivotal roles in pathogenesis, certain effectors, known as avirulence (AVR) can be directly or indirectly perceived by plant resistance (R) proteins, leading race-specific resistance. An in-depth understanding intricate AVR-R interactions is instrumental for genetic improvement crops safeguarding them from diseases. Magnaporthe oryzae ( M . ), causative agent rice blast disease, exceptionally virulent devastating fungal pathogen that induces disease on over 50 monocot species, including economically important crops. Rice- M. pathosystem serves prime model functional dissection AVR with R proteins other target due its scientific advantages economic importance. Significant progress has been made elucidating potential interaction between past two decades. This review comprehensively discusses recent advancements field specific focus multifaceted through corresponding R/target during Furthermore, we deliberated emerging strategies engineering leveraging structural insights gained effectors.

Язык: Английский

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