1932

Abstract

Nucleotide-binding domain leucine-rich repeat receptors (NLRs) play important roles in the innate immune systems of both plants and animals. Recent breakthroughs in NLR biochemistry and biophysics have revolutionized our understanding of how NLR proteins function in plant immunity. In this review, we summarize the latest findings in plant NLR biology and draw direct comparisons to NLRs of animals. We discuss different mechanisms by which NLRs recognize their ligands in plants and animals. The discovery of plant NLR resistosomes that assemble in a comparable way to animal inflammasomes reinforces the striking similarities between the formation of plant and animal NLR complexes. Furthermore, we discuss the mechanisms by which plant NLRs mediate immune responses and draw comparisons to similar mechanisms identified in animals. Finally, we summarize the current knowledge of the complex genetic architecture formed by NLRs in plants and animals and the roles of NLRs beyond pathogen detection.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-080620-104948
2021-06-17
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/arplant/72/1/annurev-arplant-080620-104948.html?itemId=/content/journals/10.1146/annurev-arplant-080620-104948&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Abe T, Lee A, Sitharam R, Kesner J, Rabadan R, Shapira SD. 2017. Germ-cell-specific inflammasome component NLRP14 negatively regulates cytosolic nucleic acid sensing to promote fertilization. Immunity 46:4621–34
    [Google Scholar]
  2. 2. 
    Acehan D, Jiang X, Morgan DG, Heuser JE, Wang X, Akey CW 2002. Three-dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding, and activation. Mol. Cell 9:2423–32
    [Google Scholar]
  3. 3. 
    Adachi H, Contreras MP, Harant A, Wu C-H, Derevnina L et al. 2019. An N-terminal motif in NLR immune receptors is functionally conserved across distantly related plant species. eLife 8:e49956
    [Google Scholar]
  4. 4. 
    Adachi H, Derevnina L, Kamoun S. 2019. NLR singletons, pairs, and networks: evolution, assembly, and regulation of the intracellular immunoreceptor circuitry of plants. Curr. Opin. Plant Biol. 50:121–31
    [Google Scholar]
  5. 5. 
    Ade J, DeYoung BJ, Golstein C, Innes RW 2007. Indirect activation of a plant nucleotide binding site–leucine-rich repeat protein by a bacterial protease. PNAS 104:72531–36
    [Google Scholar]
  6. 6. 
    Aravind L. 2000. The BED finger, a novel DNA-binding domain in chromatin-boundary-element-binding proteins and transposases. Trends Biochem. Sci. 25:9421–23
    [Google Scholar]
  7. 7. 
    Ashikawa I, Hayashi N, Yamane H, Kanamori H, Wu J et al. 2008. Two adjacent nucleotide-binding site–leucine-rich repeat class genes are required to confer Pikm-specific rice blast resistance. Genetics 180:42267–76
    [Google Scholar]
  8. 8. 
    Axtell MJ, Staskawicz BJ. 2003. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112:3369–77
    [Google Scholar]
  9. 9. 
    Bai S, Liu J, Chang C, Zhang L, Maekawa T et al. 2012. Structure-function analysis of barley NLR immune receptor MLA10 reveals its cell compartment specific activity in cell death and disease resistance. PLOS Pathog 8:6e1002752
    [Google Scholar]
  10. 10. 
    Bailey PC, Schudoma C, Jackson W, Baggs E, Dagdas G et al. 2018. Dominant integration locus drives continuous diversification of plant immune receptors with exogenous domain fusions. Genome Biol 19:123
    [Google Scholar]
  11. 11. 
    Bao Q, Riedl SJ, Shi Y. 2005. Structure of Apaf-1 in the auto-inhibited form: a critical role for ADP. Cell Cycle 4:81001–3
    [Google Scholar]
  12. 12. 
    Barragan AC, Collenberg M, Wang J, Lee RRQ, Cher WY et al. 2020. A truncated singleton NLR causes hybrid necrosis in Arabidopsis thaliana. Mol. Biol. Evol 38:255774
    [Google Scholar]
  13. 13. 
    Barragan CA, Wu R, Kim S-T, Xi W, Habring A et al. 2019. RPW8/HR repeats control NLR activation in Arabidopsis thaliana. PLOS Genet 15:7e1008313
    [Google Scholar]
  14. 14. 
    Bastedo DP, Khan M, Martel A, Seto D, Kireeva I et al. 2019. Perturbations of the ZED1 pseudokinase activate plant immunity. PLOS Pathog 15:7e1007900
    [Google Scholar]
  15. 15. 
    Bendahmane A, Farnham G, Moffett P, Baulcombe DC. 2002. Constitutive gain-of-function mutants in a nucleotide binding site–leucine rich repeat protein encoded at the Rx locus of potato. Plant J 32:2195–204
    [Google Scholar]
  16. 16. 
    Bentham AR, Zdrzalek R, De la Concepcion JC, Banfield MJ. 2018. Uncoiling CNLs: structure/function approaches to understanding CC domain function in plant NLRs. Plant Cell Physiol 59:122398–408
    [Google Scholar]
  17. 17. 
    Bernoux M, Burdett H, Williams SJ, Zhang X, Chen C et al. 2016. Comparative analysis of the flax immune receptors L6 and L7 suggests an equilibrium-based switch activation model. Plant Cell 28:1146–59
    [Google Scholar]
  18. 18. 
    Bernoux M, Ve T, Williams S, Warren C, Hatters D et al. 2011. Structural and functional analysis of a plant resistance protein TIR domain reveals interfaces for self-association, signaling, and autoregulation. Cell Host Microbe 9:3200–11
    [Google Scholar]
  19. 19. 
    Bomblies K. 2009. Too much of a good thing? Hybrid necrosis as a by-product of plant immune system diversification. Botany 87:111013–22
    [Google Scholar]
  20. 20. 
    Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C et al. 2007. Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. PLOS Biol 5:9e236
    [Google Scholar]
  21. 21. 
    Bomblies K, Weigel D. 2007. Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nat. Rev. Genet. 8:5382–93
    [Google Scholar]
  22. 22. 
    Bonardi V, Cherkis K, Nishimura MT, Dangl JL. 2012. A new eye on NLR proteins: focused on clarity or diffused by complexity?. Curr. Opin. Immunol. 24:141–50
    [Google Scholar]
  23. 23. 
    Bonardi V, Tang S, Stallmann A, Roberts M, Cherkis K, Dangl JL 2011. Expanded functions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors. PNAS 108:3916463–68
    [Google Scholar]
  24. 24. 
    Bratkowsi M, Xie T, Thayer DA, Lad S, Mathur P et al. 2020. Structural and mechanistic regulation of the pro-degenerative NAD hydrolase SARM1. Cell Rep 32:107999
    [Google Scholar]
  25. 25. 
    Burdett H, Bentham AR, Williams SJ, Dodds PN, Anderson PA et al. 2019. The plant “resistosome”: structural insights into immune signaling. Cell Host Microbe 26:2193–201
    [Google Scholar]
  26. 26. 
    Cai X, Chen J, Xu H, Liu S, Jiang Q-X et al. 2014. Prion-like polymerization underlies signal transduction in antiviral immune defense and inflammasome activation. Cell 156:61207–22
    [Google Scholar]
  27. 27. 
    Caruso R, Warner N, Inohara N, Núñez G. 2014. NOD1 and NOD2: signaling, host defense, and inflammatory disease. Immunity 41:6898–908
    [Google Scholar]
  28. 28. 
    Casey LW, Lavrencic P, Bentham AR, Cesari S, Ericsson DJ et al. 2016. The CC domain structure from the wheat stem rust resistance protein Sr33 challenges paradigms for dimerization in plant NLR proteins. PNAS 113:4512856–61
    [Google Scholar]
  29. 29. 
    Castel B, Ngou P-M, Cevik V, Redkar A, Kim D-S et al. 2019. Diverse NLR immune receptors activate defence via the RPW8-NLR NRG1. New Phytol 222:2966–80
    [Google Scholar]
  30. 30. 
    Césari S, Bernoux M, Moncuquet P, Kroj T, Dodds PN. 2014. A novel conserved mechanism for plant NLR protein pairs: the “integrated decoy” hypothesis. Front. Plant Sci. 5:606
    [Google Scholar]
  31. 31. 
    Césari S, Kanzaki H, Fujiwara T, Bernoux M, Chalvon V et al. 2014. The NB-LRR proteins RGA4 and RGA5 interact functionally and physically to confer disease resistance. EMBO J 33:171941–59
    [Google Scholar]
  32. 32. 
    Césari S, Thilliez G, Ribot C, Chalvon V, Michel C et al. 2013. The rice resistance protein pair RGA4/RGA5 recognizes the Magnaporthe oryzae effectors AVR-Pia and AVR1-CO39 by direct binding. Plant Cell 25:41463–81
    [Google Scholar]
  33. 33. 
    Chae E, Bomblies K, Kim S-T, Karelina D, Zaidem M et al. 2014. Species-wide genetic incompatibility analysis identifies immune genes as hot spots of deleterious epistasis. Cell 159:61341–51
    [Google Scholar]
  34. 34. 
    Chavarría-Smith J, Mitchell PS, Ho AM, Daugherty MD, Vance RE. 2016. Functional and evolutionary analyses identify proteolysis as a general mechanism for NLRP1 inflammasome activation. PLOS Pathog 12:12e1006052
    [Google Scholar]
  35. 35. 
    Chavarría-Smith J, Vance RE 2013. Direct proteolytic cleavage of NLRP1B is necessary and sufficient for inflammasome activation by anthrax lethal factor. PLOS Pathog 9:6e1003452
    [Google Scholar]
  36. 36. 
    Chavarría-Smith J, Vance RE 2015. The NLRP1 inflammasomes. Immunol. Rev. 265:122–34
    [Google Scholar]
  37. 37. 
    Chen J, Upadhyaya NM, Ortiz D, Sperschneider J, Li F et al. 2017. Loss of AvrSr50 by somatic exchange in stem rust leads to virulence for Sr50 resistance in wheat. Science 358:63701607–10
    [Google Scholar]
  38. 38. 
    Chopra AP, Boone SA, Liang X, Duesbery NS. 2003. Anthrax lethal factor proteolysis and inactivation of MAPK kinase. J. Biol. Chem. 278:119402–6
    [Google Scholar]
  39. 39. 
    Chui AJ, Okondo MC, Rao SD, Gai K, Griswold AR et al. 2019. N-terminal degradation activates the NLRP1B inflammasome. Science 364:643582–85
    [Google Scholar]
  40. 40. 
    Chung E-H, da Cunha L, Wu A-J, Gao Z, Cherkis K et al. 2011. Specific threonine phosphorylation of a host target by two unrelated type III effectors activates a host innate immune receptor in plants. Cell Host Microbe 9:2125–36
    [Google Scholar]
  41. 41. 
    Collier SM, Hamel L-P, Moffett P. 2011. Cell death mediated by the N-terminal domains of a unique and highly conserved class of NB-LRR protein. Mol. Plant Microbe Interact. 24:8918–31
    [Google Scholar]
  42. 42. 
    Couto D, Zipfel C. 2016. Regulation of pattern recognition receptor signalling in plants. Nat. Rev. Immunol. 16:9537–52
    [Google Scholar]
  43. 43. 
    Dangl JL, Jones JDG 2001. Plant pathogens and integrated defence responses to infection. Nature 411:6839826–33
    [Google Scholar]
  44. 44. 
    Das B, Sengupta S, Prasad M, Ghose TK 2014. Genetic diversity of the conserved motifs of six bacterial leaf blight resistance genes in a set of rice landraces. BMC Genet 15:82
    [Google Scholar]
  45. 45. 
    Daskalov A, Habenstein B, Martinez D, Debets AJM, Sabaté R et al. 2015. Signal transduction by a fungal NOD-like receptor based on propagation of a prion amyloid fold. PLOS Biol 13:2e1002059
    [Google Scholar]
  46. 46. 
    De la Concepcion JC, Franceschetti M, MacLean D, Terauchi R, Kamoun S, Banfield MJ. 2019. Protein engineering expands the effector recognition profile of a rice NLR immune receptor. eLife 8:e47713
    [Google Scholar]
  47. 47. 
    Deguine J, Barton GM. 2014. MyD88: a central player in innate immune signaling. F1000Prime Rep 6:97
    [Google Scholar]
  48. 48. 
    Diebolder CA, Halff EF, Koster AJ, Huizinga EG, Koning RI. 2015. Cryoelectron tomography of the NAIP5/NLRC4 inflammasome: implications for NLR activation. Structure 23:122349–57
    [Google Scholar]
  49. 49. 
    Ding P, Ngou BPM, Furzer OJ, Sakai T, Shrestha RK et al. 2020. High-resolution expression profiling of selected gene sets during plant immune activation. Plant Biotechnol. J. 18:1610–19
    [Google Scholar]
  50. 50. 
    Ding P, Sakai T, Shrestha RK, Perez NM, Guo W et al. 2020. Chromatin accessibility landscapes activated by cell surface and intracellular immune receptors. bioRxiv 2020.06.17.157040. https://doi.org/10.1101/2020.06.17.157040
    [Crossref]
  51. 51. 
    Dodds PN, Lawrence GJ, Catanzariti A-M, Teh T, Wang C-IA et al. 2006. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. PNAS 103:238888–93
    [Google Scholar]
  52. 52. 
    Dodds PN, Rathjen JP. 2010. Plant immunity: towards an integrated view of plant–pathogen interactions. Nat. Rev. Genet. 11:8539–48
    [Google Scholar]
  53. 53. 
    Dong OX, Ao K, Xu F, Johnson KCM, Wu Y et al. 2018. Individual components of paired typical NLR immune receptors are regulated by distinct E3 ligases. Nat. Plants 4:9699–710
    [Google Scholar]
  54. 54. 
    Dorstyn L, Akey CW, Kumar S. 2018. New insights into apoptosome structure and function. Cell Death Differ 25:71194–208
    [Google Scholar]
  55. 55. 
    Duesbery NS, Webb CP, Leppla SH, Gordon VM, Klimpel KR et al. 1998. Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor. Science 280:5364734–37
    [Google Scholar]
  56. 56. 
    Duncan JA, Bergstralht DT, Wang Y, Willingham SB, Ye Z et al. 2007. Cryopyrin/NALP3 binds ATP/dATP, is an ATPase, and requires ATP binding to mediate inflammatory signaling. PNAS 104:198041–46
    [Google Scholar]
  57. 57. 
    Duxbury Z, Ma Y, Furzer OJ, Huh SU, Cevik V et al. 2016. Pathogen perception by NLRs in plants and animals: parallel worlds. Bioessays 38:8769–81
    [Google Scholar]
  58. 58. 
    Duxbury Z, Wang S, MacKenzie CI, Tenthorey JL, Zhang X et al. 2020. Induced proximity of a TIR signaling domain on a plant-mammalian NLR chimera activates defense in plants. PNAS 117:3118832–39Demonstrates that the NLRC4/NAIP inflammasome can assemble when heterologously expressed in plants; the activation of TIR domains was shown to be by induced proximity.
    [Google Scholar]
  59. 59. 
    Essuman K, Summers DW, Sasaki Y, Mao X, DiAntonio A, Milbrandt J. 2017. The SARM1 Toll/interleukin-1 receptor domain possesses intrinsic NAD+ cleavage activity that promotes pathological axonal degeneration. Neuron 93:61334–43.E5
    [Google Scholar]
  60. 60. 
    Faris JD, Zhang Z, Lu H, Lu S, Reddy L et al. 2010. A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. PNAS 107:3013544–49
    [Google Scholar]
  61. 61. 
    Faustin B, Lartigue L, Bruey J-M, Luciano F, Sergienko E et al. 2007. Reconstituted NALP1 inflammasome reveals two-step mechanism of caspase-1 activation. Mol. Cell 25:5713–24
    [Google Scholar]
  62. 62. 
    Feng F, Yang F, Rong W, Wu X, Zhang J et al. 2012. A Xanthomonas uridine 5′-monophosphate transferase inhibits plant immune kinases. Nature 485:7396114–18
    [Google Scholar]
  63. 63. 
    Flor HH. 1956. The complementary genic systems in flax and flax rust. Adv. Genet. 8:29–54
    [Google Scholar]
  64. 64. 
    Frost D, Way H, Howles P, Luck J, Manners J et al. 2004. Tobacco transgenic for the flax rust resistance gene L expresses allele-specific activation of defense responses. Mol. Plant Microbe Interact. 17:2224–32
    [Google Scholar]
  65. 65. 
    Gabriëls SHEJ, Vossen JH, Ekengren SK, van Ooijen G, Abd-El-Haliem AM et al. 2007. An NB-LRR protein required for HR signalling mediated by both extra- and intracellular resistance proteins. Plant J 50:114–28
    [Google Scholar]
  66. 66. 
    Gao W, Yang J, Liu W, Wang Y, Shao F 2016. Site-specific phosphorylation and microtubule dynamics control pyrin inflammasome activation. PNAS 113:33E4857–66
    [Google Scholar]
  67. 67. 
    Gao Y, Wang W, Zhang T, Gong Z, Zhao H, Han G-Z. 2018. Out of water: the origin and early diversification of plant R-genes. Plant Physiol 177:182–89
    [Google Scholar]
  68. 68. 
    Germain H, Séguin A. 2011. Innate immunity: Has poplar made its BED?. New Phytol 189:3678–87
    [Google Scholar]
  69. 69. 
    Grant M, Brown I, Adams S, Knight M, Ainslie A, Mansfield J 2000. The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J 23:4441–50
    [Google Scholar]
  70. 70. 
    Grimes CL, Ariyananda LDZ, Melnyk JE, O'Shea EK 2012. The innate immune protein Nod2 binds directly to MDP, a bacterial cell wall fragment. J. Am. Chem. Soc. 134:3313535–37
    [Google Scholar]
  71. 71. 
    Grund E, Tremousaygue D, Deslandes L. 2019. Plant NLRs with integrated domains: Unity makes strength. Plant Physiol 179:41227–35
    [Google Scholar]
  72. 72. 
    Halff EF, Diebolder CA, Versteeg M, Schouten A, Brondijk THC, Huizinga EG. 2012. Formation and structure of a NAIP5-NLRC4 inflammasome induced by direct interactions with conserved N- and C-terminal regions of flagellin. J. Biol. Chem. 287:4638460–72
    [Google Scholar]
  73. 73. 
    Hart CM, Zhao K, Laemmli UK. 1997. The scs′ boundary element: characterization of boundary element-associated factors. Mol. Cell. Biol. 17:2999–1009
    [Google Scholar]
  74. 74. 
    Harton JA, Linhoff MW, Zhang J, Ting JP-Y. 2002. Cutting edge: CATERPILLER: a large family of mammalian genes containing CARD, pyrin, nucleotide-binding, and leucine-rich repeat domains. J. Immunol. 169:84088–93
    [Google Scholar]
  75. 75. 
    Heller J, Clavé C, Gladieux P, Saupe SJ, Glass NL 2018. NLR surveillance of essential SEC-9 SNARE proteins induces programmed cell death upon allorecognition in filamentous fungi. PNAS 115:10E2292–301
    [Google Scholar]
  76. 76. 
    Horsefield S, Burdett H, Zhang X, Manik MK, Shi Y et al. 2019. NAD+ cleavage activity by animal and plant TIR domains in cell death pathways. Science 365:6455793–99Shows that NAD+ cleavage by TIR domains is a conserved feature of animal and plant cell death signaling pathways (see also 182).
    [Google Scholar]
  77. 77. 
    Howe K, Schiffer PH, Zielinski J, Wiehe T, Laird GK et al. 2016. Structure and evolutionary history of a large family of NLR proteins in the zebrafish. Open Biol 6:4160009
    [Google Scholar]
  78. 78. 
    Howles P, Lawrence G, Finnegan J, McFadden H, Ayliffe M et al. 2005. Autoactive alleles of the flax L6 rust resistance gene induce non-race-specific rust resistance associated with the hypersensitive response. Mol. Plant Microbe Interact. 18:6570–82
    [Google Scholar]
  79. 79. 
    Hu M, Qi J, Bi G, Zhou J-M. 2020. Bacterial effectors induce oligomerization of immune receptor ZAR1 in vivo. Mol. Plant 13:5793–801
    [Google Scholar]
  80. 80. 
    Hu Y, Ding L, Spencer DM, Núñez G. 1998. WD-40 repeat region regulates Apaf-1 self-association and procaspase-9 activation. J. Biol. Chem. 273:5033489–94
    [Google Scholar]
  81. 81. 
    Hu Z, Yan C, Liu P, Huang Z, Ma R et al. 2013. Crystal structure of NLRC4 reveals its autoinhibition mechanism. Science 341:6142172–75
    [Google Scholar]
  82. 82. 
    Hu Z, Zhou Q, Zhang C, Fan S, Cheng W et al. 2015. Structural and biochemical basis for induced self-propagation of NLRC4. Science 350:6259399–404
    [Google Scholar]
  83. 83. 
    Huh SU, Cevik V, Ding P, Duxbury Z, Ma Y et al. 2017. Protein-protein interactions in the RPS4/RRS1 immune receptor complex. PLOS Pathog 13:5e1006376
    [Google Scholar]
  84. 84. 
    Hyun K-G, Lee Y, Yoon J, Yi H, Song J-J. 2016. Crystal structure of Arabidopsis thaliana SNC1 TIR domain. Biochem. Biophys. Res. Commun. 481:1–2146–52
    [Google Scholar]
  85. 85. 
    Inohara N, Nuñez G. 2001. The NOD: a signaling module that regulates apoptosis and host defense against pathogens. Oncogene 20:446473–81
    [Google Scholar]
  86. 86. 
    Jacob F, Kracher B, Mine A, Seyfferth C, Blanvillain-Baufumé S et al. 2018. A dominant-interfering camta3 mutation compromises primary transcriptional outputs mediated by both cell surface and intracellular immune receptors in Arabidopsis thaliana. New Phytol 217:41667–80
    [Google Scholar]
  87. 86a. 
    Jacob PM, Kim NH, Wu F, El-Kasmi F, Walton WGet al 2021. The plant immune receptors NRG1.1 and ADR1 are calcium influx channels. bioRxiv 2021.02.25.431980 https://doi.org/10.1101/2021.02.25.431980
    [Crossref] [Google Scholar]
  88. 87. 
    Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B. 2000. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J 19:154004–14
    [Google Scholar]
  89. 88. 
    Jin T, Curry J, Smith P, Jiang J, Xiao TS. 2013. Structure of the NLRP1 caspase recruitment domain suggests potential mechanisms for its association with procaspase-1. Proteins 81:71266–70
    [Google Scholar]
  90. 89. 
    Jones JDG, Vance RE, Dangl JL. 2016. Intracellular innate immune surveillance devices in plants and animals. Science 354:6316aaf6395
    [Google Scholar]
  91. 90. 
    Jubic LM, Saile S, Furzer OJ, El Kasmi F, Dangl JL. 2019. Help wanted: helper NLRs and plant immune responses. Curr. Opin. Plant Biol. 50:82–94
    [Google Scholar]
  92. 91. 
    Kayagaki N, Stowe IB, Lee BL, O'Rourke K, Anderson K et al. 2015. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 526:7575666–71
    [Google Scholar]
  93. 92. 
    Keen NT. 1990. Gene-for-gene complementarity in plant-pathogen interactions. Annu. Rev. Genet. 24:447–63
    [Google Scholar]
  94. 93. 
    Kim H-E, Du F, Fang M, Wang X 2005. Formation of apoptosome is initiated by cytochrome c-induced dATP hydrolysis and subsequent nucleotide exchange on Apaf-1. PNAS 102:4917545–50
    [Google Scholar]
  95. 94. 
    Kim YK, Shin JS, Nahm MH. 2016. NOD-like receptors in infection, immunity, and diseases. Yonsei Med. J. 57:15–14
    [Google Scholar]
  96. 95. 
    Kofoed EM, Vance RE. 2011. Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature 477:7366592–95
    [Google Scholar]
  97. 96. 
    Kortmann J, Brubaker SW, Monack DM. 2015. Cutting edge: Inflammasome activation in primary human macrophages is dependent on flagellin. J. Immunol. 195:3815–19
    [Google Scholar]
  98. 97. 
    Kourelis J, Kamoun S. 2020. RefPlantNLR: a comprehensive collection of experimentally validated plant NLRs. bioRxiv 2020.07.08.193961. https://doi.org/10.1101/2020.07.08.193961
    [Crossref]
  99. 98. 
    Krasileva KV, Dahlbeck D, Staskawicz BJ. 2010. Activation of an Arabidopsis resistance protein is specified by the in planta association of its leucine-rich repeat domain with the cognate oomycete effector. Plant Cell 22:72444–58
    [Google Scholar]
  100. 99. 
    Kuchmiy AA, D'Hont J, Hochepied T, Lamkanfi M 2016. NLRP2 controls age-associated maternal fertility. J. Exp. Med. 213:132851–60
    [Google Scholar]
  101. 100. 
    Lacey CA, Miao EA. 2019. NLRP1–one NLR to guard them all. EMBO J 38:13e102494
    [Google Scholar]
  102. 101. 
    Laflamme B, Dillon MM, Martel A, Almeida RND, Desveaux D, Guttman DS. 2020. The pan-genome effector-triggered immunity landscape of a host-pathogen interaction. Science 367:6479763–68
    [Google Scholar]
  103. 102. 
    Lange C, Hemmrich G, Klostermeier UC, López-Quintero JA, Miller DJ et al. 2011. Defining the origins of the NOD-like receptor system at the base of animal evolution. Mol. Biol. Evol. 28:51687–702
    [Google Scholar]
  104. 103. 
    Lapin D, Kovacova V, Sun X, Dongus JA, Bhandari D et al. 2019. A coevolved EDS1-SAG101-NRG1 module mediates cell death signaling by TIR-domain immune receptors. Plant Cell 31:102430–55
    [Google Scholar]
  105. 104. 
    Laroui H, Yan Y, Narui Y, Ingersoll SA, Ayyadurai S et al. 2011. l-Ala-γ-d-Glu-meso-diaminopimelic acid (DAP) interacts directly with leucine-rich region domain of nucleotide-binding oligomerization domain 1, increasing phosphorylation activity of receptor-interacting serine/threonine-protein kinase 2 and its interaction with nucleotide-binding oligomerization domain 1. J. Biol. Chem. 286:3531003–13
    [Google Scholar]
  106. 105. 
    Lauro ML, D'Ambrosio EA, Bahnson BJ, Grimes CL 2017. Molecular recognition of muramyl dipeptide occurs in the leucine-rich repeat domain of Nod2. ACS Infect. Dis. 3:4264–70
    [Google Scholar]
  107. 106. 
    Le Roux C, Huet G, Jauneau A, Camborde L, Trémousaygue D et al. 2015. A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity. Cell 161:51074–88
    [Google Scholar]
  108. 107. 
    Lechtenberg BC, Mace PD, Riedl SJ. 2014. Structural mechanisms in NLR inflammasome signaling. Curr. Opin. Struct. Biol. 29:17–25
    [Google Scholar]
  109. 108. 
    Leibman-Markus M, Pizarro L, Schuster S, Lin ZJD, Gershony O et al. 2018. The intracellular nucleotide-binding leucine-rich repeat receptor (SlNRC4a) enhances immune signalling elicited by extracellular perception. Plant Cell Environ 41:102313–27
    [Google Scholar]
  110. 109. 
    Leipe DD, Koonin EV, Aravind L. 2004. 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. Mol. Biol. 343:11–28
    [Google Scholar]
  111. 110. 
    Leonelli L, Pelton J, Schoeffler A, Dahlbeck D, Berger J et al. 2011. Structural elucidation and functional characterization of the Hyaloperonospora arabidopsidis effector protein ATR13. PLOS Pathog 7:12e1002428
    [Google Scholar]
  112. 111. 
    Lewis JD, Lee AH-Y, Hassan JA, Wan J, Hurley B et al. 2013. The Arabidopsis ZED1 pseudokinase is required for ZAR1-mediated immunity induced by the Pseudomonas syringae type III effector HopZ1a. PNAS 110:4618722–27
    [Google Scholar]
  113. 112. 
    Li L, Habring A, Wang K, Weigel D. 2020. Atypical resistance protein RPW8/HR triggers oligomerization of the NLR immune receptor RPP7 and autoimmunity. Cell Host Microbe 27:3405–17.e6
    [Google Scholar]
  114. 113. 
    Li X, Zhang Y, Clarke JD, Li Y, Dong X. 1999. Identification and cloning of a negative regulator of systemic acquired resistance, SNI1, through a screen for suppressors of npr1-1. Cell 98:3329–39
    [Google Scholar]
  115. 114. 
    Liao K-C, Mogridge J. 2013. Activation of the Nlrp1b inflammasome by reduction of cytosolic ATP. Infect. Immun. 81:2570–79
    [Google Scholar]
  116. 115. 
    Liu J, Elmore JM, Lin Z-JD, Coaker G. 2011. A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe 9:2137–46
    [Google Scholar]
  117. 116. 
    Liu X, Zhang Z, Ruan J, Pan Y, Magupalli VG et al. 2016. Inflammasome-activated gasdermin D causes pyroptosis by forming membrane pores. Nature 535:7610153–58
    [Google Scholar]
  118. 117. 
    Lu C, Wang A, Wang L, Dorsch M, Ocain TD, Xu Y. 2005. Nucleotide binding to CARD12 and its role in CARD12-mediated caspase-1 activation. Biochem. Biophys. Res. Commun. 331:41114–19
    [Google Scholar]
  119. 118. 
    Lukasik E, Takken FLW. 2009. STANDing strong, resistance proteins instigators of plant defence. Curr. Opin. Plant Biol. 12:4427–36
    [Google Scholar]
  120. 119. 
    Ma S, Lapin D, Liu L, Sun Y, Song W et al. 2020. Direct pathogen-induced assembly of an NLR immune receptor complex to form a holoenzyme. Science 370:6521eabe3069Along with 128, provides the first structural insight into the plant TNL resistosome with direct recognition of the effector through the LRR domain.
    [Google Scholar]
  121. 120. 
    Ma Y, Guo H, Hu L, Martinez PP, Moschou PN et al. 2018. Distinct modes of derepression of an Arabidopsis immune receptor complex by two different bacterial effectors. PNAS 115:4110218–27
    [Google Scholar]
  122. 121. 
    Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL. 2003. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112:3379–89
    [Google Scholar]
  123. 122. 
    Maekawa T, Cheng W, Spiridon LN, Töller A, Lukasik E et al. 2011. Coiled-coil domain-dependent homodimerization of intracellular barley immune receptors defines a minimal functional module for triggering cell death. Cell Host Microbe 9:3187–99
    [Google Scholar]
  124. 123. 
    Maekawa T, Kufer TA, Schulze-Lefert P. 2011. NLR functions in plant and animal immune systems: so far and yet so close. Nat. Immunol. 12:9817–26
    [Google Scholar]
  125. 124. 
    Man SM, Kanneganti T-D. 2016. Converging roles of caspases in inflammasome activation, cell death and innate immunity. Nat. Rev. Immunol. 16:17–21
    [Google Scholar]
  126. 125. 
    Maqbool A, Saitoh H, Franceschetti M, Stevenson CEM, Uemura A et al. 2015. Structural basis of pathogen recognition by an integrated HMA domain in a plant NLR immune receptor. eLife 4:e08709
    [Google Scholar]
  127. 126. 
    Marchal C, Zhang J, Zhang P, Fenwick P, Steuernagel B et al. 2018. BED-domain-containing immune receptors confer diverse resistance spectra to yellow rust. Nat. Plants 4:9662–68
    [Google Scholar]
  128. 127. 
    Marquenet E, Richet E. 2007. How integration of positive and negative regulatory signals by a STAND signaling protein depends on ATP hydrolysis. Mol. Cell 28:2187–99
    [Google Scholar]
  129. 128. 
    Martin R, Qi T, Zhang H, Liu F, King M et al. 2020. Structure of the activated ROQ1 resistosome directly recognizing the pathogen effector XopQ. Science 370:6521eabd9993
    [Google Scholar]
  130. 129. 
    Messaed C, Chebaro W, Di Roberto RB, Rittore C, Cheung A et al. 2011. NLRP7 in the spectrum of reproductive wastage: Rare non-synonymous variants confer genetic susceptibility to recurrent reproductive wastage. J. Med. Genet. 48:8540–48
    [Google Scholar]
  131. 130. 
    Mestre P, Baulcombe DC. 2006. Elicitor-mediated oligomerization of the tobacco N disease resistance protein. Plant Cell 18:2491–501
    [Google Scholar]
  132. 131. 
    Mo J, Boyle JP, Howard CB, Monie TP, Davis BK, Duncan JA. 2012. Pathogen sensing by nucleotide-binding oligomerization domain-containing protein 2 (NOD2) is mediated by direct binding to muramyl dipeptide and ATP. J. Biol. Chem. 287:2723057–67
    [Google Scholar]
  133. 132. 
    Moreira LO, Zamboni DS. 2012. NOD1 and NOD2 signaling in infection and inflammation. Front. Immunol. 3:328
    [Google Scholar]
  134. 133. 
    Neiman-Zenevich J, Liao K-C, Mogridge J. 2014. Distinct regions of NLRP1B are required to respond to anthrax lethal toxin and metabolic inhibition. Infect. Immun. 82:93697–703
    [Google Scholar]
  135. 134. 
    Ngou BPM, Ahn H-K, Ding P, Jones JDG. 2020. Mutual potentiation of plant immunity by cell-surface and intracellular receptors. bioRxiv 2020.04.10.034173. https://doi.org/10.1101/2020.04.10.034173
    [Crossref]
  136. 134a. 
    Ofir G, Herbst E, Baroz M, Cohen D, Millman Aet al 2021. Antiviral activity of bacterial TIR domains via signaling molecules that trigger cell death. bioRxiv 2021.01.06.425286 https://doi.org/10.1101/2021.01.06.425286
    [Crossref]
  137. 135. 
    Pandey SP, Somssich IE. 2009. The role of WRKY transcription factors in plant immunity. Plant Physiol 150:41648–55
    [Google Scholar]
  138. 136. 
    Park YH, Wood G, Kastner DL, Chae JJ 2016. Pyrin inflammasome activation and RhoA signaling in the autoinflammatory diseases FMF and HIDS. Nat. Immunol. 17:8914–21
    [Google Scholar]
  139. 137. 
    Qi D, DeYoung BJ, Innes RW. 2012. Structure-function analysis of the coiled-coil and leucine-rich repeat domains of the RPS5 disease resistance protein. Plant Physiol 158:41819–32
    [Google Scholar]
  140. 138. 
    Qi S, Pang Y, Hu Q, Liu Q, Li H et al. 2010. Crystal structure of the Caenorhabditis elegans apoptosome reveals an octameric assembly of CED-4. Cell 141:3446–57
    [Google Scholar]
  141. 139. 
    Qi T, Seong K, Thomazella DPT, Kim JR, Pham J et al. 2018. NRG1 functions downstream of EDS1 to regulate TIR-NLR-mediated plant immunity in Nicotiana benthamiana. PNAS 115:46E10979–87
    [Google Scholar]
  142. 140. 
    Ravensdale M, Bernoux M, Ve T, Kobe B, Thrall PH et al. 2012. Intramolecular interaction influences binding of the flax L5 and L6 resistance proteins to their AvrL567 ligands. PLOS Pathog 8:11e1003004
    [Google Scholar]
  143. 141. 
    Rayamajhi M, Zak DE, Chavarria-Smith J, Vance RE, Miao EA. 2013. Cutting edge: Mouse NAIP1 detects the type III secretion system needle protein. J. Immunol. 191:83986–89
    [Google Scholar]
  144. 142. 
    Redditt TJ, Chung E-H, Karimi HZ, Rodibaugh N, Zhang Y et al. 2019. AvrRpm1 functions as an ADP-ribosyl transferase to modify NOI domain-containing proteins, including Arabidopsis and soybean RPM1-interacting protein4. Plant Cell 31:112664–81
    [Google Scholar]
  145. 143. 
    Reyes Ruiz VM, Ramirez J, Naseer N, Palacio NM, Siddarthan IJ et al. 2017. Broad detection of bacterial type III secretion system and flagellin proteins by the human NAIP/NLRC4 inflammasome. PNAS 114:5013242–47
    [Google Scholar]
  146. 144. 
    Riedl SJ, Li W, Chao Y, Schwarzenbacher R, Shi Y. 2005. Structure of the apoptotic protease-activating factor 1 bound to ADP. Nature 434:7035926–33
    [Google Scholar]
  147. 145. 
    Saile SC, Jacob P, Castel B, Jubic LM, Salas-Gonzalez I et al. 2020. Two unequally redundant “helper” immune receptor families mediate Arabidopsis thaliana intracellular “sensor” immune receptor functions. PLOS Biol 18:9e3000783
    [Google Scholar]
  148. 146. 
    Sandstrom A, Mitchell PS, Goers L, Mu EW, Lesser CF, Vance RE. 2019. Functional degradation: a mechanism of NLRP1 inflammasome activation by diverse pathogen enzymes. Science 364:6435eaau1330
    [Google Scholar]
  149. 147. 
    Sarris PF, Duxbury Z, Huh SU, Ma Y, Segonzac C et al. 2015. A plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell 161:51089–100
    [Google Scholar]
  150. 148. 
    Saur IM, Bauer S, Kracher B, Lu X, Franzeskakis L et al. 2019. Multiple pairs of allelic MLA immune receptor-powdery mildew AVRA effectors argue for a direct recognition mechanism. eLife 8:e44471
    [Google Scholar]
  151. 149. 
    Sborgi L, Rühl S, Mulvihill E, Pipercevic J, Heilig R et al. 2016. GSDMD membrane pore formation constitutes the mechanism of pyroptotic cell death. EMBO J 35:161766–78
    [Google Scholar]
  152. 150. 
    Schultink A, Qi T, Bally J, Staskawicz B. 2019. Using forward genetics in Nicotiana benthamiana to uncover the immune signaling pathway mediating recognition of the Xanthomonas perforans effector XopJ4. New Phytol 221:21001–9
    [Google Scholar]
  153. 151. 
    Seto D, Koulena N, Lo T, Menna A, Guttman DS, Desveaux D. 2017. Expanded type III effector recognition by the ZAR1 NLR protein using ZED1-related kinases. Nat. Plants 3:17027
    [Google Scholar]
  154. 152. 
    Seuring C, Greenwald J, Wasmer C, Wepf R, Saupe SJ et al. 2012. The mechanism of toxicity in HET-S/HET-s prion incompatibility. PLOS Biol 10:12e1001451
    [Google Scholar]
  155. 153. 
    Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW. 2003. Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301:56371230–33
    [Google Scholar]
  156. 154. 
    Shao Z-Q, Xue J-Y, Wu P, Zhang Y-M, Wu Y et al. 2016. Large-scale analyses of angiosperm nucleotide-binding site-leucine-rich repeat genes reveal three anciently diverged classes with distinct evolutionary patterns. Plant Physiol 170:42095–109Systemic phylogenomics analysis of NLRs in angiosperms revealed the three major NLR groups and their evolutionary history.
    [Google Scholar]
  157. 155. 
    Sharif H, Wang L, Wang WL, Magupalli VG, Andreeva L et al. 2019. Structural mechanism for NEK7-licensed activation of NLRP3 inflammasome. Nature 570:7761338–43
    [Google Scholar]
  158. 156. 
    Shi J, Zhao Y, Wang K, Shi X, Wang Y et al. 2015. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 526:7575660–65
    [Google Scholar]
  159. 157. 
    Smakowska-Luzan E, Mott GA, Parys K, Stegmann M, Howton TC et al. 2018. An extracellular network of Arabidopsis leucine-rich repeat receptor kinases. Nature 553:7688342–46
    [Google Scholar]
  160. 158. 
    Srinivasula SM, Ahmad M, Fernandes-Alnemri T, Alnemri ES. 1998. Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. Mol. Cell 1:7949–57
    [Google Scholar]
  161. 159. 
    Stirnweis D, Milani SD, Jordan T, Keller B, Brunner S. 2014. Substitutions of two amino acids in the nucleotide-binding site domain of a resistance protein enhance the hypersensitive response and enlarge the PM3F resistance spectrum in wheat. Mol. Plant Microbe Interact. 27:3265–76
    [Google Scholar]
  162. 160. 
    Sun Y, Zhu Y-X, Balint-Kurti PJ, Wang G-F. 2020. Fine-tuning immunity: players and regulators for plant NLRs. Trends Plant Sci 25:7695–713
    [Google Scholar]
  163. 161. 
    Sutterwala FS, Haasken S, Cassel SL. 2014. Mechanism of NLRP3 inflammasome activation. Ann. N. Y. Acad. Sci. 1319:82–95
    [Google Scholar]
  164. 162. 
    Swanson KV, Deng M, Ting JP-Y. 2019. The NLRP3 inflammasome: molecular activation and regulation to therapeutics. Nat. Rev. Immunol. 19:8477–89
    [Google Scholar]
  165. 163. 
    Swiderski MR, Birker D, Jones JDG. 2009. The TIR domain of TIR-NB-LRR resistance proteins is a signaling domain involved in cell death induction. Mol. Plant Microbe Interact. 22:2157–65
    [Google Scholar]
  166. 164. 
    Takken FL, Albrecht M, Tameling WI. 2006. Resistance proteins: molecular switches of plant defence. Curr. Opin. Plant Biol. 9:4383–90
    [Google Scholar]
  167. 165. 
    Tamborski J, Krasileva KV. 2020. Evolution of plant NLRs: from natural history to precise modifications. Annu. Rev. Plant Biol. 71:355–78
    [Google Scholar]
  168. 166. 
    Tameling WIL, Elzinga SDJ, Darmin PS, Vossen JH, Takken FLW et al. 2002. The tomato R gene products I-2 and Mi-1 are functional ATP binding proteins with ATPase activity. Plant Cell 14:112929–39
    [Google Scholar]
  169. 167. 
    Tameling WIL, Vossen JH, Albrecht M, Lengauer T, Berden JA et al. 2006. Mutations in the NB-ARC domain of I-2 that impair ATP hydrolysis cause autoactivation. Plant Physiol 140:41233–45
    [Google Scholar]
  170. 168. 
    Tanabe T, Chamaillard M, Ogura Y, Zhu L, Qiu S et al. 2004. Regulatory regions and critical residues of NOD2 involved in muramyl dipeptide recognition. EMBO J 23:71587–97
    [Google Scholar]
  171. 169. 
    Tenthorey JL, Haloupek N, López-Blanco JR, Grob P, Adamson E et al. 2017. The structural basis of flagellin detection by NAIP5: a strategy to limit pathogen immune evasion. Science 358:6365888–93Provides structural insights into ligand-induced NLR activation and inflammasome formation.
    [Google Scholar]
  172. 170. 
    Tenthorey JL, Kofoed EM, Daugherty MD, Malik HS, Vance RE. 2014. Molecular basis for specific recognition of bacterial ligands by NAIP/NLRC4 inflammasomes. Mol. Cell 54:117–29
    [Google Scholar]
  173. 170a. 
    Tian X, Pascal G, Monget P 2009. Evolution and functional divergence of NLRP genes in mammalian reproductive systems. BMC Evol. Biol 9:202
    [Google Scholar]
  174. 171. 
    Ting JP-Y, Davis BK. 2005. CATERPILLER: a novel gene family important in immunity, cell death, and diseases. Annu. Rev. Immunol. 23:387–414
    [Google Scholar]
  175. 172. 
    Tong ZB, Gold L, Pfeifer KE, Dorward H, Lee E et al. 2000. Mater, a maternal effect gene required for early embryonic development in mice. Nat. Genet. 26:3267–68
    [Google Scholar]
  176. 173. 
    Tran DTN, Chung E-H, Habring-Müller A, Demar M, Schwab R et al. 2017. Activation of a plant NLR complex through heteromeric association with an autoimmune risk variant of another NLR. Curr. Biol. 27:81148–60
    [Google Scholar]
  177. 174. 
    Ueda H, Yamaguchi Y, Sano H. 2006. Direct interaction between the tobacco mosaic virus helicase domain and the ATP-bound resistance protein, N factor during the hypersensitive response in tobacco plants. Plant Mol. Biol. 61:1–231–45
    [Google Scholar]
  178. 175. 
    Urbach JM, Ausubel FM 2017. The NBS-LRR architectures of plant R-proteins and metazoan NLRs evolved in independent events. PNAS 114:51063–68
    [Google Scholar]
  179. 176. 
    Van Der Biezen EA, Jones JDG 1998. Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 23:12454–56
    [Google Scholar]
  180. 177. 
    van der Burgh AM, Joosten MHAJ. 2019. Plant immunity: thinking outside and inside the box. Trends Plant Sci 24:7587–601
    [Google Scholar]
  181. 178. 
    van der Hoorn RAL, Kamoun S. 2008. From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20:82009–17
    [Google Scholar]
  182. 179. 
    van Ooijen G, Mayr G, Albrecht M, Cornelissen BJC, Takken FLW. 2008. Transcomplementation, but not physical association of the CC-NB-ARC and LRR domains of tomato R protein Mi-1.2 is altered by mutations in the ARC2 subdomain. Mol. Plant 1:3401–10
    [Google Scholar]
  183. 180. 
    Vance RE. 2015. The NAIP/NLRC4 inflammasomes. Curr. Opin. Immunol. 32:84–89
    [Google Scholar]
  184. 181. 
    Walker JE, Saraste M, Runswick MJ, Gay NJ. 1982. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1:8945–51
    [Google Scholar]
  185. 182. 
    Wan L, Essuman K, Anderson RG, Sasaki Y, Monteiro F et al. 2019. TIR domains of plant immune receptors are NAD+-cleaving enzymes that promote cell death. Science 365:6455799–803Shows that plant TNLs require NADase function to transduce pathogen recognition into immune signaling leading to cell death responses (see also 76).
    [Google Scholar]
  186. 183. 
    Wan W-L, Kim S-T, Castel B, Charoennit N, Chae E 2020. Genetics of autoimmunity in plants: an evolutionary genetics perspective. New Phytol 229:3121533
    [Google Scholar]
  187. 184. 
    Wang G, Roux B, Feng F, Guy E, Li L et al. 2015. The decoy substrate of a pathogen effector and a pseudokinase specify pathogen-induced modified-self recognition and immunity in plants. Cell Host Microbe 18:3285–95
    [Google Scholar]
  188. 185. 
    Wang G-F, Ji J, El-Kasmi F, Dangl JL, Johal G, Balint-Kurti PJ 2015. Molecular and functional analyses of a maize autoactive NB-LRR protein identify precise structural requirements for activity. PLOS Pathog 11:2e1004674
    [Google Scholar]
  189. 186. 
    Wang J, Hu M, Wang J, Qi J, Han Z et al. 2019. Reconstitution and structure of a plant NLR resistosome conferring immunity. Science 364:6435eaav5870Provides the first structural insight into plant NLR oligomerization, resistosome formation, and potential mechanisms leading to cell death.
    [Google Scholar]
  190. 187. 
    Wang J, Wang J, Hu M, Wu S, Qi J et al. 2019. Ligand-triggered allosteric ADP release primes a plant NLR complex. Science 364:6435eaav5868Provides structural and biochemical insights into plant NLR activation through an indirect recognition mechanism
    [Google Scholar]
  191. 188. 
    Wang L, Zhao L, Zhang X, Zhang Q, Jia Y et al. 2019. Large-scale identification and functional analysis of NLR genes in blast resistance in the Tetep rice genome sequence. PNAS 116:3718479–87
    [Google Scholar]
  192. 189. 
    Weaver L, Swiderski MR, Li Y, Jones JDG. 2006. The Arabidopsis thaliana TIR-NB-LRR R-protein, RPP1A; protein localization and constitutive activation of defence by truncated alleles in tobacco and Arabidopsis. Plant J 47:6829–40
    [Google Scholar]
  193. 190. 
    Williams SJ, Sohn KH, Wan L, Bernoux M, Sarris PF et al. 2014. Structural basis for assembly and function of a heterodimeric plant immune receptor. Science 344:6181299–303
    [Google Scholar]
  194. 191. 
    Williams SJ, Sornaraj P, deCourcy-Ireland E, Menz RI, Kobe B et al. 2011. An autoactive mutant of the M flax rust resistance protein has a preference for binding ATP, whereas wild-type M protein binds ADP. Mol. Plant Microbe Interact. 24:8897–906
    [Google Scholar]
  195. 192. 
    Wu C-H, Abd-El-Haliem A, Bozkurt TO, Belhaj K, Terauchi R et al. 2017. NLR network mediates immunity to diverse plant pathogens. PNAS 114:308113–18Identifies a network composed of NRCs and matching sensor NLRs that confers robust immunity to diverse pathogens of solanaceous plants.
    [Google Scholar]
  196. 193. 
    Wu C-H, Belhaj K, Bozkurt TO, Birk MS, Kamoun S. 2016. Helper NLR proteins NRC2a/b and NRC3 but not NRC1 are required for Pto-mediated cell death and resistance in Nicotiana benthamiana. New Phytol 209:41344–52
    [Google Scholar]
  197. 194. 
    Wu C-H, Derevnina L, Kamoun S. 2018. Receptor networks underpin plant immunity. Science 360:63951300–1
    [Google Scholar]
  198. 195. 
    Wu Z, Li M, Dong OX, Xia S, Liang W et al. 2019. Differential regulation of TNL-mediated immune signaling by redundant helper CNLs. New Phytol 222:2938–53Demonstrates that TNLs use ADR1 and NRG1 to transduce differential downstream signals, forming a genetic network composed of TNL and RNL.
    [Google Scholar]
  199. 196. 
    Xu H, Shi J, Gao H, Liu Y, Yang Z et al. 2019. The N-end rule ubiquitin ligase UBR2 mediates NLRP1B inflammasome activation by anthrax lethal toxin. EMBO J 38:13e101996
    [Google Scholar]
  200. 197. 
    Xu H, Yang J, Gao W, Li L, Li P et al. 2014. Innate immune sensing of bacterial modifications of Rho GTPases by the Pyrin inflammasome. Nature 513:7517237–41
    [Google Scholar]
  201. 198. 
    Xu Y, Tao X, Shen B, Horng T, Medzhitov R et al. 2000. Structural basis for signal transduction by the Toll/interleukin-1 receptor domains. Nature 408:6808111–15
    [Google Scholar]
  202. 199. 
    Xue Y, Enosi Tuipulotu D, Tan WH, Kay C, Man SM 2019. Emerging activators and regulators of inflammasomes and pyroptosis. Trends Immunol 40:111035–52
    [Google Scholar]
  203. 200. 
    Yang J, Zhao Y, Li P, Yang Y, Zhang E et al. 2018. Sequence determinants of specific pattern-recognition of bacterial ligands by the NAIP-NLRC4 inflammasome. Cell Discov 4:22
    [Google Scholar]
  204. 201. 
    Yang J, Zhao Y, Shi J, Shao F 2013. Human NAIP and mouse NAIP1 recognize bacterial type III secretion needle protein for inflammasome activation. PNAS 110:3514408–13
    [Google Scholar]
  205. 202. 
    Yang X, Lin G, Han Z, Chai J. 2019. Structural biology of NOD-like receptors. Adv. Exp. Med. Biol. 1172:119–41
    [Google Scholar]
  206. 203. 
    Yang X, Yang F, Wang W, Lin G, Hu Z et al. 2018. Structural basis for specific flagellin recognition by the NLR protein NAIP5. Cell Res 28:135–47
    [Google Scholar]
  207. 204. 
    Yoshimura S, Yamanouchi U, Katayose Y, Toki S, Wang ZX et al. 1998. Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. PNAS 95:41663–68
    [Google Scholar]
  208. 205. 
    Yu X, Acehan D, Ménétret J-F, Booth CR, Ludtke SJ et al. 2005. A structure of the human apoptosome at 12.8 Å resolution provides insights into this cell death platform. Structure 13:111725–35
    [Google Scholar]
  209. 206. 
    Yuan M, Jiang Z, Bi G, Nomura K, Liu M et al. 2020. Pattern-recognition receptors are required for NLR-mediated plant immunity. bioRxiv 2020.04.10.031294. https://doi.org/10.1101/2020.04.10.031294
    [Crossref]
  210. 207. 
    Yuan S, Akey CW. 2013. Apoptosome structure, assembly, and procaspase activation. Structure 21:4501–15
    [Google Scholar]
  211. 208. 
    Yuan S, Yu X, Topf M, Ludtke SJ, Wang X, Akey CW 2010. Structure of an apoptosome-procaspase-9 CARD complex. Structure 18:5571–83
    [Google Scholar]
  212. 209. 
    Yuen B, Bayes JM, Degnan SM. 2014. The characterization of sponge NLRs provides insight into the origin and evolution of this innate immune gene family in animals. Mol. Biol. Evol. 31:1106–20
    [Google Scholar]
  213. 210. 
    Zhang L, Chen S, Ruan J, Wu J, Tong AB et al. 2015. Cryo-EM structure of the activated NAIP2-NLRC4 inflammasome reveals nucleated polymerization. Science 350:6259404–9
    [Google Scholar]
  214. 211. 
    Zhang X, Bernoux M, Bentham AR, Newman TE, Ve T et al. 2017. Multiple functional self-association interfaces in plant TIR domains. PNAS 114:10E2046–52
    [Google Scholar]
  215. 212. 
    Zhao K, Hart CM, Laemmli UK. 1995. Visualization of chromosomal domains with boundary element-associated factor BEAF-32. Cell 81:6879–89
    [Google Scholar]
  216. 213. 
    Zhao Y, Shao F. 2015. The NAIP-NLRC4 inflammasome in innate immune detection of bacterial flagellin and type III secretion apparatus. Immunol. Rev. 265:185–102
    [Google Scholar]
  217. 214. 
    Zhao Y, Yang J, Shi J, Gong Y-N, Lu Q et al. 2011. The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature 477:7366596–600
    [Google Scholar]
  218. 215. 
    Zurek B, Bielig H, Kufer TA. 2011. Cell-based reporter assay to analyze activation of Nod1 and Nod2. Methods Mol. Biol. 748:107–19
    [Google Scholar]
  219. 216. 
    Zurek B, Proell M, Wagner RN, Schwarzenbacher R, Kufer TA. 2012. Mutational analysis of human NOD1 and NOD2 NACHT domains reveals different modes of activation. Innate Immun 18:1100–11
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-080620-104948
Loading
/content/journals/10.1146/annurev-arplant-080620-104948
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error