植物NLR蛋白的多维调控机制

刘颖; 周涛; 江其朋; 李石力; 丁伟

doi:10.13718/j.cnki.zwyx.2026.01.004

FLOR H H. Host-Parasite Interaction in Flax Rust-Its Genetics and Other Implications[J]. Phytopathology, 2025, 115(8V): 680-685. doi: 10.1094/Phyto-45-680

JONES J D G, DANGL J L. The Plant Immune System[J]. Nature, 2006, 444(7117): 323-329. doi: 10.1038/nature05286

YUAN M H, NGOU B P M, DING P T, et al. PTI-ETI Crosstalk: An Integrative View of Plant Immunity[J]. Current Opinion in Plant Biology, 2021, 62: 102030. doi: 10.1016/j.pbi.2021.102030

ZIPFEL C, OLDROYD G E D. Plant Signalling in Symbiosis and Immunity[J]. Nature, 2017, 543(7645): 328-336. doi: 10.1038/nature22009

NGOU B P M, DING P T, JONES J D G. Thirty Years of Resistance: Zig-Zag through the Plant Immune System[J]. The Plant Cell, 2022, 34(5): 1447-1478. doi: 10.1093/plcell/koac041

LEIPE D D, KOONIN E V, ARAVIND L. STAND, a Class of P-Loop NTPases Including Animal and Plant Regulators of Programmed Cell Death: Multiple, Complex Domain Architectures, Unusual Phyletic Patterns, and Evolution by Horizontal Gene Transfer[J]. Journal of Molecular Biology, 2004, 343(1): 1-28.

CONTRERAS M P, LVDKE D, PAI H, et al. NLR Receptors in Plant Immunity: Making Sense of the Alphabet Soup[J]. EMBO Reports, 2023, 24(10): e57495. doi: 10.15252/embr.202357495

JONES J D G, VANCE R E, DANGL J L. Intracellular Innate Immune Surveillance Devices in Plants and Animals[J]. Science, 2016, 354(6316): aaf6395. doi: 10.1126/science.aaf6395

MARUTA N, BURDETT H, LIM B Y J, et al. Structural Basis of NLR Activation and Innate Immune Signalling in Plants[J]. Immunogenetics, 2022, 74(1): 5-26. doi: 10.1007/s00251-021-01242-5

DUXBURY Z, WU C H, DING P T. A Comparative Overview of the Intracellular Guardians of Plants and Animals: NLRS in Innate Immunity and beyond[J]. Annual Review of Plant Biology, 2021, 72: 155-184. doi: 10.1146/annurev-arplant-080620-104948

TAKKEN F L, ALBRECHT M, TAMELING W I. Resistance Proteins: Molecular Switches of Plant Defence[J]. Current Opinion in Plant Biology, 2006, 9(4): 383-390. doi: 10.1016/j.pbi.2006.05.009

WANG J Z, HU M J, WANG J, et al. Reconstitution and Structure of a Plant NLR Resistosome Conferring Immunity[J]. Science, 2019, 364(6435): eaav5870. doi: 10.1126/science.aav5870

TAKKEN F L, GOVERSE A. How to Build a Pathogen Detector: Structural Basis of NB-LRR Function[J]. Current Opinion in Plant Biology, 2012, 15(4): 375-384. doi: 10.1016/j.pbi.2012.05.001

KOURELIS J, SAKAI T, ADACHI H, et al. RefPlantNLR Is a Comprehensive Collection of Experimentally Validated Plant Disease Resistance Proteins from the NLR Family[J]. PLoS Biology, 2021, 19(10): e3001124. doi: 10.1371/journal.pbio.3001124

BI G Z, SU M, LI N, et al. The ZAR1 Resistosome Is a Calcium-Permeable Channel Triggering Plant Immune Signaling[J]. Cell, 2021, 184(13): 3528-3541. e12. doi: 10.1016/j.cell.2021.05.003

JACOB P, KIM N H, WU F H, et al. Plant "Helper" Immune Receptors Are Ca²⁺-Permeable Nonselective Cation Channels[J]. Science, 2021, 373(6553): 420-425. doi: 10.1126/science.abg7917

HORSEFIELD S, BURDETT H, ZHANG X X, et al. NAD(+) Cleavage Activity by Animal and Plant TIR Domains in Cell Death Pathways[J]. Science, 2019, 365(6455): 793-799. doi: 10.1126/science.aax1911

WAN L, ESSUMAN K, ANDERSON R G, et al. TIR Domains of Plant Immune Receptors Are NAD⁺-Cleaving Enzymes that Promote Cell Death[J]. Science, 2019, 365(6455): 799-803. doi: 10.1126/science.aax1771

YU D L, SONG W, TAN E Y J, et al. TIR Domains of Plant Immune Receptors Are 2', 3'-cAMP/CGMP Synthetases Mediating Cell Death[J]. Cell, 2022, 185(13): 2370-2386. doi: 10.1016/j.cell.2022.04.032

JACOB F, VERNALDI S, MAEKAWA T. Evolution and Conservation of Plant NLR Functions[J]. Frontiers in Immunology, 2013, 4: 297.

SHAO Z Q, XUE J Y, WU P, et al. Large-Scale Analyses of Angiosperm Nucleotide-Binding Site-Leucine-Rich Repeat Genes Reveal Three Anciently Diverged Classes with Distinct Evolutionary Patterns[J]. Plant Physiology, 2016, 170(4): 2095-2109. doi: 10.1104/pp.15.01487

GAO Y X, WANG W Q, ZHANG T, et al. Out of Water: The Origin and Early Diversification of Plant R-Genes[J]. Plant Physiology, 2018, 177(1): 82-89. doi: 10.1104/pp.18.00185

BARRAGAN A C, WEIGEL D. Plant NLR Diversity: The Known Unknowns of Pan-NLRomes[J]. The Plant Cell, 2021, 33(4): 814-831. doi: 10.1093/plcell/koaa002

NGOU B P M, HEAL R, WYLER M, et al. Concerted Expansion and Contraction of Immune Receptor Gene Repertoires in Plant Genomes[J]. Nature Plants, 2022, 8(10): 1146-1152. doi: 10.1038/s41477-022-01260-5

SAUR I M L, PANSTRUGA R, SCHULZE-LEFERT P. NOD-Like Receptor-Mediated Plant Immunity: From Structure to Cell Death[J]. Nature Reviews Immunology, 2021, 21(5): 305-318. doi: 10.1038/s41577-020-00473-z

TARR D E K, ALEXANDER H M. TIR-NBS-LRR Genes Are Rare in Monocots: Evidence from Diverse Monocot Orders[J]. BMC Research Notes, 2009, 2: 197. doi: 10.1186/1756-0500-2-197

BAGGS E L, MONROE J G, THANKI A S, et al. Convergent Loss of an EDS1/PAD4 Signaling Pathway in Several Plant Lineages Reveals Coevolved Components of Plant Immunity and Drought Response[J]. The Plant Cell, 2020, 32(7): 2158-2177. doi: 10.1105/tpc.19.00903

LIU Y, ZENG Z, ZHANG Y M, et al. An Angiosperm NLR Atlas Reveals that NLR Gene Reduction Is Associated with Ecological Specialization and Signal Transduction Component Deletion[J]. Molecular Plant, 2021, 14(12): 2015-2031. doi: 10.1016/j.molp.2021.08.001

NGOU B P M, AHN H K, DING P T, et al. Mutual Potentiation of Plant Immunity by Cell-Surface and Intracellular Receptors[J]. Nature, 2021, 592(7852): 110-115. doi: 10.1038/s41586-021-03315-7

YUAN M H, JIANG Z Y, BI G Z, et al. Pattern-Recognition Receptors Are Required for NLR-Mediated Plant Immunity[J]. Nature, 2021, 592(7852): 105-109. doi: 10.1038/s41586-021-03316-6

袁婷露, 万里, 唐威华, 等. 植物-病原微生物相互作用领域研究进展[J]. 植物生理学报, 2023, 59(9): 1657-1664.

TIAN H N, WU Z S, CHEN S Y, et al. Activation of TIR Signalling Boosts Pattern-Triggered Immunity[J]. Nature, 2021, 598(7881): 500-503. doi: 10.1038/s41586-021-03987-1

NGOU B P M, JONES J D G, DING P T. Plant Immune Networks[J]. Trends in Plant Science, 2022, 27(3): 255-273. doi: 10.1016/j.tplants.2021.08.012

覃磊, 彭志红, 夏石头, 等. 植物NLR免疫受体的识别、免疫激活与信号调控[J]. 植物学报, 2022, 57(1): 12-23.

MA S C, LAPIN D, LIU L, et al. Direct Pathogen-Induced Assembly of an NLR Immune Receptor Complex to Form a Holoenzyme[J]. Science, 2020, 370(6521): eabe3069. doi: 10.1126/science.abe3069

SCHULTINK A, QI T C, LEE A, et al. Roq1 Mediates Recognition of the Xanthomonas and Pseudomonas Effector Proteins XopQ and HopQ1[J]. The Plant Journal, 2017, 92(5): 787-795. doi: 10.1111/tpj.13715

MARTIN R, QI T C, ZHANG H B, et al. Structure of the Activated ROQ1 Resistosome Directly Recognizing the Pathogen Effector XopQ[J]. Science, 2020, 370(6521): eabd9993. doi: 10.1126/science.abd9993

ZHAO Y B, LIU M X, CHEN T T, et al. Pathogen Effector AvrSr35 Triggers Sr35 Resistosome Assembly via a Direct Recognition Mechanism[J]. Science Advances, 2022, 8(36): eabq5108. doi: 10.1126/sciadv.abq5108

FÖRDERER A, LI ERTONG, LAWSON A W, et al. A Wheat Resistosome Defines Common Principles of Immune Receptor Channels[J]. Nature, 2022, 610(7932): 532-539. doi: 10.1038/s41586-022-05231-w

REMICK B C, GAIDT M M, VANCE R E. Effector-Triggered Immunity[J]. Annual Review of Immunology, 2023, 41: 453-481. doi: 10.1146/annurev-immunol-101721-031732

VAN DER HOORN R A L, KAMOUN S. From Guard to Decoy: A New Model for Perception of Plant Pathogen Effectors[J]. The Plant Cell, 2008, 20(8): 2009-2017. doi: 10.1105/tpc.108.060194

CHUNG E H, EL-KASMI F, HE Y J, et al. A Plant Phosphoswitch Platform Repeatedly Targeted by Type Ⅲ Effector Proteins Regulates the Output of both Tiers of Plant Immune Receptors[J]. Cell Host & Microbe, 2014, 16(4): 484-494.

TORUÑO T Y, SHEN M Z, COAKER G, et al. Regulated Disorder: Posttranslational Modifications Control the RIN4 Plant Immune Signaling Hub[J]. Molecular Plant-Microbe Interactions, 2019, 32(1): 56-64. doi: 10.1094/MPMI-07-18-0212-FI

MACKEY D, BELKHADIR Y, ALONSO J M, et al. Arabidopsis RIN4 Is a Target of the Type Ⅲ Virulence Effector AvrRpt2 and Modulates RPS2-Mediated Resistance[J]. Cell, 2003, 112(3): 379-389. doi: 10.1016/S0092-8674(03)00040-0

SHAO F, GOLSTEIN C, ADE J, et al. Cleavage of Arabidopsis PBS1 by a Bacterial Type Ⅲ Effector[J]. Science, 2003, 301(5637): 1230-1233. doi: 10.1126/science.1085671

GONG Z, QI J F, HU M J, et al. The Origin and Evolution of a Plant Resistosome[J]. The Plant Cell, 2022, 34(5): 1600-1620. doi: 10.1093/plcell/koac053

ADACHI H, SAKAI T, KOURELIS J, et al. Jurassic NLR: Conserved and Dynamic Evolutionary Features of the Atypically Ancient Immune Receptor ZAR1[J]. The Plant Cell, 2023, 35(10): 3662-3685. doi: 10.1093/plcell/koad175

LE ROUX C, HUET G, JAUNEAU A, et al. A Receptor Pair with an Integrated Decoy Converts Pathogen Disabling of Transcription Factors to Immunity[J]. Cell, 2015, 161(5): 1074-1088. doi: 10.1016/j.cell.2015.04.025

SARRIS P F, DUXBURY Z, HUH S U, et al. A Plant Immune Receptor Detects Pathogen Effectors that Target WRKY Transcription Factors[J]. Cell, 2015, 161(5): 1089-1100. doi: 10.1016/j.cell.2015.04.024

JONES J D G, STASKAWICZ B J, DANGL J L. The Plant Immune System: From Discovery to Deployment[J]. Cell, 2024, 187(9): 2095-2116. doi: 10.1016/j.cell.2024.03.045

韩志富, 曹禺, 黄诗嘉, 等. 抗病小体: 植物免疫机器[J]. 中国科学: 化学, 2024, 54(5): 726-733.

GONG Y H, TIAN L, KONTOS I, et al. Plant Immune Signaling Network Mediated by Helper NLRS[J]. Current Opinion in Plant Biology, 2023, 73: 102354. doi: 10.1016/j.pbi.2023.102354

PEART J R, MESTRE P, LU R, et al. NRG1, a CC-NB-LRR Protein, Together with N, a TIR-NB-LRR Protein, Mediates Resistance Against Tobacco Mosaic Virus[J]. Current Biology, 2005, 15(10): 968-973. doi: 10.1016/j.cub.2005.04.053

JUBIC L M, SAILE S, FURZER O J, et al. Help Wanted: Helper NLRS and Plant Immune Responses[J]. Current Opinion in Plant Biology, 2019, 50: 82-94. doi: 10.1016/j.pbi.2019.03.013

FEEHAN J M, CASTEL B, BENTHAM A R, et al. Plant NLRS Get by with a Little Help from Their Friends[J]. Current Opinion in Plant Biology, 2020, 56: 99-108. doi: 10.1016/j.pbi.2020.04.006

WU Z S, LI M, DONG O X, et al. Differential Regulation of TNL-Mediated Immune Signaling by Redundant Helper CNLS[J]. The New Phytologist, 2019, 222(2): 938-953. doi: 10.1111/nph.15665

CASTEL B, NGOU P M, CEVIK V, et al. Diverse NLR Immune Receptors Activate Defence via the RPW8-NLR NRG1[J]. The New Phytologist, 2019, 222(2): 966-980. doi: 10.1111/nph.15659

LAPIN D, BHANDARI D D, PARKER J E. Origins and Immunity Networking Functions of EDS1 Family Proteins[J]. Annual Review of Phytopathology, 2020, 58(1): 253-276. doi: 10.1146/annurev-phyto-010820-012840

WU C H, ABD-EL-HALIEM A, BOZKURT T O, et al. NLR Network Mediates Immunity to Diverse Plant Pathogens[J]. Proceedings of the National Academy of Sciences of the United States of America, 2017, 114(30): 8113-8118.

ADACHI H, CONTRERAS M P, HARANT A, et al. An N-Terminal Motif in NLR Immune Receptors Is Functionally Conserved across Distantly Related Plant Species[J]. eLife, 2019, 8: e49956. doi: 10.7554/eLife.49956

SELVARAJ M, TOGHANI A, PAI H, et al. Activation of Plant Immunity through Conversion of a Helper NLR Homodimer into a Resistosome[J]. PLoS Biology, 2024, 22(10): e3002868. doi: 10.1371/journal.pbio.3002868

LIU F R, YANG Z L, WANG C, et al. Activation of the Helper NRC4 Immune Receptor Forms a Hexameric Resistosome[J]. Cell, 2024, 187(18): 4877-4889. doi: 10.1016/j.cell.2024.07.013

刘丹丹, 杜美达, 陈俊斌, 等. 钙通道介导的植物免疫反应的分子机制及其应用[J/OL]. 生命科学, 2024: 1-17. (2024-11-01). https://link.cnki.net/doi/10.13376/j.cbls/202500001.

ZDRZAŁEK R, XI Y X, LANGNER T, et al. Bioengineering a Plant NLR Immune Receptor with a Robust Binding Interface Toward a Conserved Fungal Pathogen Effector[J]. Proceedings of the National Academy of Sciences of the United States of America, 2024, 121(28): e2402872121.