1932

Abstract

The first plant disease resistance () genes were identified and cloned more than two decades ago. Since then, many more genes have been identified and characterized in numerous plant pathosystems. Most of these encode members of the large family of intracellular NLRs (NOD-like receptors), which also includes animal immune receptors. New discoveries in this expanding field of research provide new elements for our understanding of plant NLR function. But what do we know about plant NLR function today? Genetic, structural, and functional analyses have uncovered a number of commonalities and differences in pathogen recognition strategies as well as how NLRs are regulated and activate defense signaling, but many unknowns remain. This review gives an update on the latest discoveries and breakthroughs in this field, with an emphasis on structural findings and some comparison to animal NLRs, which can provide additional insights and paradigms in plant NLR function.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-phyto-080516-035250
2017-08-04
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/phyto/55/1/annurev-phyto-080516-035250.html?itemId=/content/journals/10.1146/annurev-phyto-080516-035250&mimeType=html&fmt=ahah

Literature Cited

  1. Aarts N, Metz M, Holub E, Staskawicz BJ, Daniels MJ, Parker JE. 1.  1998. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene–mediated signaling pathways in Arabidopsis. . PNAS 95:10306–11 [Google Scholar]
  2. Ade J, DeYoung BJ, Golstein C, Innes RW. 2.  2007. Indirect activation of a plant nucleotide binding site–leucine-rich repeat protein by a bacterial protease. PNAS 104:2531–36 [Google Scholar]
  3. Alcazar R, Garcia AV, Kronholm I, de Meaux J, Koornneef M. 3.  et al. 2010. Natural variation at Strubbelig receptor kinase 3 drives immune-triggered incompatibilities between Arabidopsis thaliana accessions. Nat. Genet. 42:1135–39 [Google Scholar]
  4. Alcazar R, von Reth M, Bautor J, Chae E, Weigel D. 4.  et al. 2014. Analysis of a plant complex resistance gene locus underlying immune-related hybrid incompatibility and its occurrence in nature. PLOS Genet 10:e1004848 [Google Scholar]
  5. Axtell MJ, Staskawicz BJ. 5.  2003. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112:369–77 [Google Scholar]
  6. Bai S, Liu J, Chang C, Zhang L, Maekawa T. 6.  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:e1002752 [Google Scholar]
  7. Bao Q, Riedl SJ, Shi Y. 7.  2005. Structure of Apaf-1 in the auto-inhibited form: a critical role for ADP. Cell Cycle 4:1001–3 [Google Scholar]
  8. Bao Q, Shi Y. 8.  2007. Apoptosome: a platform for the activation of initiator caspases. Cell Death Differ 14:56–65 [Google Scholar]
  9. Bendahmane A, Farnham G, Moffett P, Baulcombe DC. 9.  2002. Constitutive gain-of-function mutants in a nucleotide binding site–leucine rich repeat protein encoded at the Rx locus of potato. Plant J 32:195–204 [Google Scholar]
  10. Bentham A, Burdett H, Anderson PA, Williams SJ, Kobe B. 10.  2017. Animal NLRs provide structural insights into plant NLR function. Ann. Bot. 119:827 [Google Scholar]
  11. Bernoux M, Burdett H, Williams SJ, Zhang X, Chen C. 11.  et al. 2016. Comparative analysis of the flax immune receptors L6 and L7 suggests an equilibrium-based switch activation model. Plant Cell 28:146–59 [Google Scholar]
  12. Bernoux M, Ellis JG, Dodds PN. 12.  2011. New insights in plant immunity signaling activation. Curr. Opin. Plant Biol. 14:512–18 [Google Scholar]
  13. Bernoux M, Ve T, Williams S, Warren C, Hatters D. 13.  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 9:200–11 [Google Scholar]
  14. Bhattacharjee S, Halane MK, Kim SH, Gassmann W. 14.  2011. Pathogen effectors target Arabidopsis EDS1 and alter its interactions with immune regulators. Science 334:1405–8 [Google Scholar]
  15. Birker D, Heidrich K, Takahara H, Narusaka M, Deslandes L. 15.  et al. 2009. A locus conferring resistance to Colletotrichum higginsianum is shared by four geographically distinct Arabidopsis accessions. Plant J. 60:602–13 [Google Scholar]
  16. Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C. 16.  et al. 2007. Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. PLOS Biol 5:e236 [Google Scholar]
  17. Bonardi V, Tang S, Stallmann A, Roberts M, Cherkis K, Dangl JL. 17.  2011. Expanded functions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors. PNAS 108:16463–68 [Google Scholar]
  18. Burch-Smith TM, Schiff M, Caplan JL, Tsao J, Czymmek K, Dinesh-Kumar SP. 18.  2007. A novel role for the TIR domain in association with pathogen-derived elicitors. PLOS Biol 5:e68 [Google Scholar]
  19. Caplan JL, Mamillapalli P, Burch-Smith TM, Czymmek K, Dinesh-Kumar SP. 19.  2008. Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector. Cell 132:449–62 [Google Scholar]
  20. Casey LW, Lavrencic P, Bentham AR, Cesari S, Ericsson DJ. 20.  et al. 2016. The CC domain structure from the wheat stem rust resistance protein Sr33 challenges paradigms for dimerization in plant NLR proteins. PNAS 113:12856–61 [Google Scholar]
  21. Catanzariti AM, Dodds PN, Ve T, Kobe B, Ellis JG, Staskawicz BJ. 21.  2010. The AvrM effector from flax rust has a structured C-terminal domain and interacts directly with the M resistance protein. Mol. Plant-Microbe Interact. 23:49–57 [Google Scholar]
  22. Cesari S, Bernoux M, Moncuquet P, Kroj T, Dodds PN. 22.  2014. A novel conserved mechanism for plant NLR protein pairs: the “integrated decoy” hypothesis. Front. Plant Sci. 5:606 [Google Scholar]
  23. Cesari S, Kanzaki H, Fujiwara T, Bernoux M, Chalvon V. 23.  et al. 2014. The NB-LRR proteins RGA4 and RGA5 interact functionally and physically to confer disease resistance. EMBO J 33:1941–59 [Google Scholar]
  24. Cesari S, Moore J, Chen C, Webb D, Periyannan S. 24.  et al. 2016. Cytosolic activation of cell death and stem rust resistance by cereal MLA-family CC-NLR proteins. PNAS 113:10204–9 [Google Scholar]
  25. Cesari S, Thilliez G, Ribot C, Chalvon V, Michel C. 25.  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 25:1463–81 [Google Scholar]
  26. Chae E, Bomblies K, Kim ST, Karelina D, Zaidem M. 26.  et al. 2014. Species-wide genetic incompatibility analysis identifies immune genes as hot spots of deleterious epistasis. Cell 159:1341–51 [Google Scholar]
  27. Chae E, Tran DT, Weigel D. 27.  2016. Cooperation and conflict in the plant immune system. PLOS Pathog 12:e1005452 [Google Scholar]
  28. Chang C, Yu D, Jiao J, Jing S, Schulze-Lefert P, Shen QH. 28.  2013. Barley MLA immune receptors directly interfere with antagonistically acting transcription factors to initiate disease resistance signaling. Plant Cell 25:1158–73 [Google Scholar]
  29. Cheng TC, Hong C, Akey IV, Yuan S, Akey CW. 29.  2016. A near atomic structure of the active human apoptosome. eLife 5:e17755 [Google Scholar]
  30. Cheng YT, Germain H, Wiermer M, Bi D, Xu F. 30.  et al. 2009. Nuclear pore complex component MOS7/Nup88 is required for innate immunity and nuclear accumulation of defense regulators in Arabidopsis. . Plant Cell 21:2503–16 [Google Scholar]
  31. Chung EH, da Cunha L, Wu AJ, Gao Z, Cherkis K. 31.  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 9:125–36 [Google Scholar]
  32. Collier SM, Hamel LP, Moffett P. 32.  2011. Cell death mediated by the N-terminal domains of a unique and highly conserved class of NB-LRR protein. Mol. Plant-Microbe Interact. 24:918–31 [Google Scholar]
  33. Collier SM, Moffett P. 33.  2009. NB-LRRs work a “bait and switch” on pathogens. Trends Plant Sci 14:521–29 [Google Scholar]
  34. Couto D, Zipfel C. 34.  2016. Regulation of pattern recognition receptor signalling in plants. Nat. Rev. Immunol. 16:537–52 [Google Scholar]
  35. Dangl JL, Jones JD. 35.  2001. Plant pathogens and integrated defence responses to infection. Nature 411:826–33 [Google Scholar]
  36. Danot O. 36.  2015. How “arm-twisting” by the inducer triggers activation of the MalT transcription factor, a typical signal transduction ATPase with numerous domains (STAND). Nucleic Acids Res 43:3089–99 [Google Scholar]
  37. Danot O, Marquenet E, Vidal-Ingigliardi D, Richet E. 37.  2009. Wheel of life, wheel of death: a mechanistic insight into signaling by STAND proteins. Structure 17:172–82 [Google Scholar]
  38. Day B, Dahlbeck D, Staskawicz BJ. 38.  2006. NDR1 interaction with RIN4 mediates the differential activation of multiple disease resistance pathways in Arabidopsis. . Plant Cell 18:2782–91 [Google Scholar]
  39. Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M. 39.  et al. 2003. Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. PNAS 100:8024–29 [Google Scholar]
  40. Dinesh-Kumar SP, Baker BJ. 40.  2000. Alternatively spliced N resistance gene transcripts: their possible role in tobacco mosaic virus resistance. PNAS 97:1908–13 [Google Scholar]
  41. Dodds PN, Lawrence GJ, Catanzariti AM, Teh T, Wang CI. 41.  et al. 2006. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. PNAS 103:8888–93 [Google Scholar]
  42. Dodds PN, Rathjen JP. 42.  2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11:539–48 [Google Scholar]
  43. Dong OX, Tong M, Bonardi V, El Kasmi F, Woloshen V. 43.  et al. 2016. TNL-mediated immunity in Arabidopsis requires complex regulation of the redundant ADR1 gene family. New Phytol. 210:960–73 [Google Scholar]
  44. Duncan JA, Bergstralh DT, Wang Y, Willingham SB, Ye Z. 44.  et al. 2007. Cryopyrin/NALP3 binds ATP/dATP, is an ATPase, and requires ATP binding to mediate inflammatory signaling. PNAS 104:8041–46 [Google Scholar]
  45. Duxbury Z, Ma Y, Furzer OJ, Huh SU, Cevik V. 45.  et al. 2016. Pathogen perception by NLRs in plants and animals: parallel worlds. BioEssays 38:769–81 [Google Scholar]
  46. Eitas TK, Dangl JL. 46.  2010. NB-LRR proteins: pairs, pieces, perception, partners, and pathways. Curr. Opin. Plant Biol. 13:472–77 [Google Scholar]
  47. Faustin B, Lartigue L, Bruey JM, Luciano F, Sergienko E. 47.  et al. 2007. Reconstituted NALP1 inflammasome reveals two-step mechanism of caspase-1 activation. Mol. Cell 25:713–24 [Google Scholar]
  48. Feng F, Yang F, Rong W, Wu X, Zhang J. 48.  et al. 2012. A Xanthomonas uridine 5′-monophosphate transferase inhibits plant immune kinases. Nature 485:114–18 [Google Scholar]
  49. Fenyk S, Dixon CH, Gittens WH, Townsend PD, Sharples GJ. 49.  et al. 2016. The tomato nucleotide-binding leucine-rich repeat immune receptor I-2 couples DNA-binding to nucleotide-binding domain nucleotide exchange. J. Biol. Chem. 291:1137–47 [Google Scholar]
  50. Fenyk S, Townsend PD, Dixon CH, Spies GB, de San Eustaquio Campillo A. 50.  et al. 2015. The potato nucleotide-binding leucine-rich repeat (NLR) immune receptor Rx1 is a pathogen-dependent DNA-deforming protein. J. Biol. Chem. 290:24945–60 [Google Scholar]
  51. Feys BJ, Wiermer M, Bhat RA, Moisan LJ, Medina-Escobar N. 51.  et al. 2005. Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. Plant Cell 17:2601–13 [Google Scholar]
  52. Flor HH. 52.  1954. Seed-flax improvement. III. Flax rust. Adv. Agron. 6:152–61 [Google Scholar]
  53. Fradin EF, Zhang Z, Juarez Ayala JC, Castroverde CD, Nazar RN. 53.  et al. 2009. Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiol 150:320–32 [Google Scholar]
  54. Fujisaki K, Abe Y, Ito A, Saitoh H, Yoshida K. 54.  et al. 2015. Rice Exo70 interacts with a fungal effector, AVR-Pii, and is required for AVR-Pii-triggered immunity. Plant J 83:875–87 [Google Scholar]
  55. Fukuoka S, Saka N, Koga H, Ono K, Shimizu T. 55.  et al. 2009. Loss of function of a proline-containing protein confers durable disease resistance in rice. Science 325:998–1001 [Google Scholar]
  56. Gabriels SH, Vossen JH, Ekengren SK, van Ooijen G, Abd-El-Haliem AM. 56.  et al. 2007. An NB-LRR protein required for HR signalling mediated by both extra- and intracellular resistance proteins. Plant J 50:14–28 [Google Scholar]
  57. Gao Z, Chung EH, Eitas TK, Dangl JL. 57.  2011. Plant intracellular innate immune receptor Resistance to Pseudomonas syringae pv. maculicola 1 (RPM1) is activated at, and functions on, the plasma membrane. PNAS 108:7619–24 [Google Scholar]
  58. Gay NJ, Gangloff M, O'Neill LA. 58.  2011. What the Myddosome structure tells us about the initiation of innate immunity. Trends Immunol 32:104–9 [Google Scholar]
  59. Germain H, Seguin A. 59.  2011. Innate immunity: Has poplar made its BED?. New Phytol 189:678–87 [Google Scholar]
  60. Goritschnig S, Steinbrenner AD, Grunwald DJ, Staskawicz BJ. 60.  2016. Structurally distinct Arabidopsis thaliana NLR immune receptors recognize tandem WY domains of an oomycete effector. New Phytol 210:984–96 [Google Scholar]
  61. Guy E, Lautier M, Chabannes M, Roux B, Lauber E. 61.  et al. 2013. xopAC-triggered immunity against Xanthomonas depends on Arabidopsis receptor-like cytoplasmic kinase genes PBL2 and RIPK. . PLOS ONE 8:e73469 [Google Scholar]
  62. Halff EF, Diebolder CA, Versteeg M, Schouten A, Brondijk TH, Huizinga EG. 62.  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. 287:38460–72 [Google Scholar]
  63. Hao W, Collier SM, Moffett P, Chai J. 63.  2013. Structural basis for the interaction between the potato virus X resistance protein (Rx) and its cofactor Ran GTPase-activating protein 2 (RanGAP2). J. Biol. Chem. 288:35868–76 [Google Scholar]
  64. Harris CJ, Slootweg EJ, Goverse A, Baulcombe DC. 64.  2013. Stepwise artificial evolution of a plant disease resistance gene. PNAS 110:21189–94 [Google Scholar]
  65. Heidrich K, Wirthmueller L, Tasset C, Pouzet C, Deslandes L, Parker JE. 65.  2011. Arabidopsis EDS1 connects pathogen effector recognition to cell compartment–specific immune responses. Science 334:1401–4 [Google Scholar]
  66. Howles P, Lawrence G, Finnegan J, McFadden H, Ayliffe M. 66.  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. 18:570–82 [Google Scholar]
  67. Hu Z, Yan C, Liu P, Huang Z, Ma R. 67.  et al. 2013. Crystal structure of NLRC4 reveals its autoinhibition mechanism. Science 341:172–75 [Google Scholar]
  68. Hu Z, Zhou Q, Zhang C, Fan S, Cheng W. 68.  et al. 2015. Structural and biochemical basis for induced self-propagation of NLRC4. Science 350:399–404 [Google Scholar]
  69. Huard-Chauveau C, Perchepied L, Debieu M, Rivas S, Kroj T. 69.  et al. 2013. An atypical kinase under balancing selection confers broad-spectrum disease resistance in Arabidopsis. . PLOS Genet. 9:e1003766 [Google Scholar]
  70. Inohara N, Nunez G. 70.  2001. The NOD: a signaling module that regulates apoptosis and host defense against pathogens. Oncogene 20:6473–81 [Google Scholar]
  71. Inoue H, Hayashi N, Matsushita A, Xinqiong L, Nakayama A. 71.  et al. 2013. Blast resistance of CC-NB-LRR protein Pb1 is mediated by WRKY45 through protein-protein interaction. PNAS 110:9577–82 [Google Scholar]
  72. Johnson KC, Dong OX, Huang Y, Li X. 72.  2012. A rolling stone gathers no moss, but resistant plants must gather their MOSes. Cold Spring Harb. Symp. Quant. Biol. 77:259–68 [Google Scholar]
  73. Jones JDG, Vance RE, Dangl JL. 73.  2016. Intracellular innate immune surveillance devices in plants and animals. Science 354:1017–24 [Google Scholar]
  74. Kanzaki H, Yoshida K, Saitoh H, Fujisaki K, Hirabuchi A. 74.  et al. 2012. Arms race co-evolution of Magnaporthe oryzae AVR-Pik and rice Pik genes driven by their physical interactions. Plant J. 72:894–907 [Google Scholar]
  75. Karasov TL, Kniskern JM, Gao L, DeYoung BJ, Ding J. 75.  et al. 2014. The long-term maintenance of a resistance polymorphism through diffuse interactions. Nature 512:436–40 [Google Scholar]
  76. Kim HS, Desveaux D, Singer AU, Patel P, Sondek J, Dangl JL. 76.  2005. The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation. PNAS 102:6496–501 [Google Scholar]
  77. Kim MG, da Cunha L, McFall AJ, Belkhadir Y, DebRoy S. 77.  et al. 2005. Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis. . Cell 121:749–59 [Google Scholar]
  78. Kim SH, Gao F, Bhattacharjee S, Adiasor JA, Nam JC, Gassmann W. 78.  2010. The Arabidopsis resistance-like gene SNC1 is activated by mutations in SRFR1 and contributes to resistance to the bacterial effector AvrRps4. PLOS Pathog. 6:e1001172 [Google Scholar]
  79. Kim SH, Son GH, Bhattacharjee S, Kim HJ, Nam JC. 79.  et al. 2014. The Arabidopsis immune adaptor SRFR1 interacts with TCP transcription factors that redundantly contribute to effector-triggered immunity. Plant J 78:978–89 [Google Scholar]
  80. Knepper C, Savory EA, Day B. 80.  2011. The role of NDR1 in pathogen perception and plant defense signaling. Plant Signal. Behav. 6:1114–16 [Google Scholar]
  81. Krasileva KV, Dahlbeck D, Staskawicz BJ. 81.  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 22:2444–58 [Google Scholar]
  82. Kroj T, Chanclud E, Michel-Romiti C, Grand X, Morel JB. 82.  2016. Integration of decoy domains derived from protein targets of pathogen effectors into plant immune receptors is widespread. New Phytol 210:618–26 [Google Scholar]
  83. Le Roux C, Huet G, Jauneau A, Camborde L, Tremousaygue D. 83.  et al. 2015. A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity. Cell 161:1074–88 [Google Scholar]
  84. Leipe DD, Koonin EV, Aravind L. 84.  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. 343:1–28 [Google Scholar]
  85. Lewis JD, Lee AH, Hassan JA, Wan J, Hurley B. 85.  et al. 2013. The Arabidopsis ZED1 pseudokinase is required for ZAR1-mediated immunity induced by the Pseudomonas syringae type III effector HopZ1a. PNAS 110:18722–27 [Google Scholar]
  86. Lin SC, Lo YC, Wu H. 86.  2010. Helical assembly in the MyD88-IRAK4-IRAK2 complex in TLR/IL-1R signalling. Nature 465:885–90 [Google Scholar]
  87. Luck JE, Lawrence GJ, Dodds PN, Shepherd KW, Ellis JG. 87.  2000. Regions outside of the leucine-rich repeats of flax rust resistance proteins play a role in specificity determination. Plant Cell 12:1367–77 [Google Scholar]
  88. Lukasik-Shreepaathy E, Slootweg E, Richter H, Goverse A, Cornelissen BJ, Takken FL. 88.  2012. Dual regulatory roles of the extended N terminus for activation of the tomato MI-1.2 resistance protein. Mol. Plant-Microbe Interact. 25:1045–57 [Google Scholar]
  89. Luo Y, Caldwell KS, Wroblewski T, Wright ME, Michelmore RW. 89.  2009. Proteolysis of a negative regulator of innate immunity is dependent on resistance genes in tomato and Nicotiana benthamiana and induced by multiple bacterial effectors. Plant Cell 21:2458–72 [Google Scholar]
  90. Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL. 90.  2003. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112:379–89 [Google Scholar]
  91. Mackey D, 3rd Holt BF, Wiig A, Dangl JL. 91.  2002. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:743–54 [Google Scholar]
  92. Maekawa T, Cheng W, Spiridon LN, Toller A, Lukasik E. 92.  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 9:187–99 [Google Scholar]
  93. Maqbool A, Saitoh H, Franceschetti M, Stevenson CE, Uemura A. 93.  et al. 2015. Structural basis of pathogen recognition by an integrated HMA domain in a plant NLR immune receptor. eLife 4:e08709 [Google Scholar]
  94. Marquenet E, Richet E. 94.  2007. How integration of positive and negative regulatory signals by a STAND signaling protein depends on ATP hydrolysis. Mol. Cell 28:187–99 [Google Scholar]
  95. Mestre P, Baulcombe DC. 95.  2006. Elicitor-mediated oligomerization of the tobacco N disease resistance protein. Plant Cell 18:491–501 [Google Scholar]
  96. Meyers BC, Morgante M, Michelmore RW. 96.  2002. TIR-X and TIR-NBS proteins: two new families related to disease resistance TIR-NBS-LRR proteins encoded in Arabidopsis and other plant genomes. Plant J 32:77–92 [Google Scholar]
  97. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW. 97.  2003. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. . Plant Cell 15:809–34 [Google Scholar]
  98. Mucyn TS, Clemente A, Andriotis VM, Balmuth AL, Oldroyd GE. 98.  et al. 2006. The tomato NBARC-LRR protein Prf interacts with Pto kinase in vivo to regulate specific plant immunity. Plant Cell 18:2792–806 [Google Scholar]
  99. Nandety RS, Caplan JL, Cavanaugh K, Perroud B, Wroblewski T. 99.  et al. 2013. The role of TIR-NBS and TIR-X proteins in plant basal defense responses. Plant Physiol 162:1459–72 [Google Scholar]
  100. Narusaka M, Kubo Y, Shiraishi T, Iwabuchi M, Narusaka Y. 100.  2009. A dual resistance gene system prevents infection by three distinct pathogens. Plant Signal. Behav. 4:954–55 [Google Scholar]
  101. Nishimura MT, Anderson RG, Cherkis KA, Law TF, Liu Q. 101.  et al. 2017. TIR-only protein RBA1 recognizes a pathogen effector to regulate cell death in Arabidopsis. . PNAS 114:E2053–62 [Google Scholar]
  102. Noutoshi Y, Ito T, Seki M, Nakashita H, Yoshida S. 102.  et al. 2005. A single amino acid insertion in the WRKY domain of the Arabidopsis TIR-NBS-LRR-WRKY-type disease resistance protein SLH1 (sensitive to low humidity 1) causes activation of defense responses and hypersensitive cell death. Plant J 43:873–88 [Google Scholar]
  103. Ntoukakis V, Saur IM, Conlan B, Rathjen JP. 103.  2014. The changing of the guard: the Pto/Prf receptor complex of tomato and pathogen recognition. Curr. Opin. Plant Biol. 20:69–74 [Google Scholar]
  104. O'Neill LA. 104.  2006. How Toll-like receptors signal: what we know and what we don't know. Curr. Opin Immunol. 18:3–9 [Google Scholar]
  105. Padmanabhan MS, Ma S, Burch-Smith TM, Czymmek K, Huijser P, Dinesh-Kumar SP. 105.  2013. Novel positive regulatory role for the SPL6 transcription factor in the N TIR-NB-LRR receptor-mediated plant innate immunity. PLOS Pathog 9:e1003235 [Google Scholar]
  106. Peart JR, Mestre P, Lu R, Malcuit I, Baulcombe DC. 106.  2005. NRG1, a CC-NB-LRR protein, together with N, a TIR-NB-LRR protein, mediates resistance against tobacco mosaic virus. Curr. Biol. 15:968–73 [Google Scholar]
  107. Qi D, DeYoung BJ, Innes RW. 107.  2012. Structure-function analysis of the coiled-coil and leucine-rich repeat domains of the RPS5 disease resistance protein. Plant Physiol 158:1819–32 [Google Scholar]
  108. Qi S, Pang Y, Hu Q, Liu Q, Li H. 108.  et al. 2010. Crystal structure of the Caenorhabditis elegans apoptosome reveals an octameric assembly of CED-4. Cell 141:446–57 [Google Scholar]
  109. Rairdan GJ, Collier SM, Sacco MA, Baldwin TT, Boettrich T, Moffett P. 109.  2008. The coiled-coil and nucleotide binding domains of the Potato Rx disease resistance protein function in pathogen recognition and signaling. Plant Cell 20:739–51 [Google Scholar]
  110. Rairdan GJ, Moffett P. 110.  2006. Distinct domains in the ARC region of the potato resistance protein Rx mediate LRR binding and inhibition of activation. Plant Cell 18:2082–93 [Google Scholar]
  111. Ravensdale M, Bernoux M, Ve T, Kobe B, Thrall PH. 111.  et al. 2012. Intramolecular interaction influences binding of the flax L5 and L6 resistance proteins to their AvrL567 ligands. PLOS Pathog 8:e1003004 [Google Scholar]
  112. Ravensdale M, Nemri A, Thrall PH, Ellis JG, Dodds PN. 112.  2011. Co-evolutionary interactions between host resistance and pathogen effector genes in flax rust disease. Mol. Plant Pathol. 12:93–102 [Google Scholar]
  113. Reubold TF, Wohlgemuth S, Eschenburg S. 113.  2009. A new model for the transition of APAF-1 from inactive monomer to caspase-activating apoptosome. J. Biol. Chem. 284:32717–24 [Google Scholar]
  114. Reubold TF, Wohlgemuth S, Eschenburg S. 114.  2011. Crystal structure of full-length Apaf-1: how the death signal is relayed in the mitochondrial pathway of apoptosis. Structure 19:1074–83 [Google Scholar]
  115. Riedl SJ, Li W, Chao Y, Schwarzenbacher R, Shi Y. 115.  2005. Structure of the apoptotic protease-activating factor 1 bound to ADP. Nature 434:926–33 [Google Scholar]
  116. Rietz S, Stamm A, Malonek S, Wagner S, Becker D. 116.  et al. 2011. Different roles of Enhanced Disease Susceptibility1 (EDS1) bound to and dissociated from Phytoalexin Deficient4 (PAD4) in Arabidopsis immunity. New Phytol 191:107–19 [Google Scholar]
  117. Roberts M, Tang S, Stallmann A, Dangl JL, Bonardi V. 117.  2013. Genetic requirements for signaling from an autoactive plant NB-LRR intracellular innate immune receptor. PLOS Genet 9:e1003465 [Google Scholar]
  118. Ruland J. 118.  2014. Inflammasome: putting the pieces together. Cell 156:1127–29 [Google Scholar]
  119. Sacco MA, Mansoor S, Moffett P. 119.  2007. A RanGAP protein physically interacts with the NB-LRR protein Rx, and is required for Rx-mediated viral resistance. Plant J 52:82–93 [Google Scholar]
  120. Sarris PF, Cevik V, Dagdas G, Jones JD, Krasileva KV. 120.  2016. Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens. BMC Biol 14:8 [Google Scholar]
  121. Sarris PF, Duxbury Z, Huh SU, Ma Y, Segonzac C. 121.  et al. 2015. A plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell 161:1089–100 [Google Scholar]
  122. Schreiber KJ, Bentham A, Williams SJ, Kobe B, Staskawicz BJ. 122.  2016. Multiple domain associations within the Arabidopsis immune receptor RPP1 regulate the activation of programmed cell death. PLOS Pathog 12:e1005769 [Google Scholar]
  123. Slootweg E, Roosien J, Spiridon LN, Petrescu AJ, Tameling W. 123.  et al. 2010. Nucleocytoplasmic distribution is required for activation of resistance by the potato NB-LRR receptor Rx1 and is balanced by its functional domains. Plant Cell 22:4195–215 [Google Scholar]
  124. Slootweg EJ, Spiridon LN, Roosien J, Butterbach P, Pomp R. 124.  et al. 2013. Structural determinants at the interface of the ARC2 and leucine-rich repeat domains control the activation of the plant immune receptors Rx1 and Gpa2. Plant Physiol 162:1510–28 [Google Scholar]
  125. Sohn KH, Segonzac C, Rallapalli G, Sarris PF, Woo JY. 125.  et al. 2014. The nuclear immune receptor RPS4 is required for RRS1SLH1-dependent constitutive defense activation in Arabidopsis thaliana. . PLOS Genet. 10:e1004655 [Google Scholar]
  126. Stahl EA, Dwyer G, Mauricio R, Kreitman M, Bergelson J. 126.  1999. Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. . Nature 400:667–71 [Google Scholar]
  127. Steinbrenner AD, Goritschnig S, Staskawicz BJ. 127.  2015. Recognition and activation domains contribute to allele-specific responses of an Arabidopsis NLR receptor to an oomycete effector protein. PLOS Pathog 11:e1004665 [Google Scholar]
  128. Stirnweis D, Milani SD, Jordan T, Keller B, Brunner S. 128.  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. 27:265–76 [Google Scholar]
  129. Stuttmann J, Peine N, Garcia AV, Wagner C, Choudhury SR. 129.  et al. 2016. Arabidopsis thaliana DM2h (R8) within the Landsberg RPP1-like resistance locus underlies three different cases of EDS1-conditioned autoimmunity. PLOS Genet 12:e1005990 [Google Scholar]
  130. Sueldo DJ, Shimels M, Spiridon LN, Caldararu O, Petrescu AJ. 130.  et al. 2015. Random mutagenesis of the nucleotide-binding domain of NRC1 (NB-LRR Required for Hypersensitive Response-Associated Cell Death-1), a downstream signalling nucleotide-binding, leucine-rich repeat (NB-LRR) protein, identifies gain-of-function mutations in the nucleotide-binding pocket. New Phytol 208:210–23 [Google Scholar]
  131. Sukarta OC, Slootweg EJ, Goverse A. 131.  2016. Structure-informed insights for NLR functioning in plant immunity. Semin. Cell Dev. Biol. 56:134–49 [Google Scholar]
  132. Swiderski MR, Birker D, Jones JD. 132.  2009. The TIR domain of TIR-NB-LRR resistance proteins is a signaling domain involved in cell death induction. Mol. Plant-Microbe Interact. 22:157–65 [Google Scholar]
  133. Takemoto D, Rafiqi M, Hurley U, Lawrence GJ, Bernoux M. 133.  et al. 2012. N-terminal motifs in some plant disease resistance proteins function in membrane attachment and contribute to disease resistance. Mol. Plant-Microbe Interact. 25:379–92 [Google Scholar]
  134. Takken FL, Albrecht M, Tameling WI. 134.  2006. Resistance proteins: molecular switches of plant defence. Curr. Opin. Plant Biol. 9:383–90 [Google Scholar]
  135. Takken FL, Goverse A. 135.  2012. How to build a pathogen detector: structural basis of NB-LRR function. Curr. Opin. Plant Biol. 15:375–84 [Google Scholar]
  136. Tameling WI, Elzinga SD, Darmin PS, Vossen JH, Takken FL. 136.  et al. 2002. The tomato R gene products I-2 and MI-1 are functional ATP binding proteins with ATPase activity. Plant Cell 14:2929–39 [Google Scholar]
  137. Tameling WI, Nooijen C, Ludwig N, Boter M, Slootweg E. 137.  et al. 2010. RanGAP2 mediates nucleocytoplasmic partitioning of the NB-LRR immune receptor Rx in the Solanaceae, thereby dictating Rx function. Plant Cell 22:4176–94 [Google Scholar]
  138. Tameling WI, Vossen JH, Albrecht M, Lengauer T, Berden JA. 138.  et al. 2006. Mutations in the NB-ARC domain of I-2 that impair ATP hydrolysis cause autoactivation. Plant Physiol 140:1233–45 [Google Scholar]
  139. Tasset C, Bernoux M, Jauneau A, Pouzet C, Briere C. 139.  et al. 2010. Autoacetylation of the Ralstonia solanacearum effector PopP2 targets a lysine residue essential for RRS1-R-mediated immunity in Arabidopsis. PLOS Pathog. 6:e1001202 [Google Scholar]
  140. Thomma BP, Nurnberger T, Joosten MH. 140.  2011. Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4–15 [Google Scholar]
  141. Tran DTN, Chung EH, Habring-Müller A, Demar M, Schwab R. 141.  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]
  142. Van der Biezen EA, Jones JD. 142.  1998. Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 23:454–56 [Google Scholar]
  143. van der Hoorn RA, Kamoun S. 143.  2008. From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20:2009–17 [Google Scholar]
  144. van Ooijen G, Mayr G, Albrecht M, Cornelissen BJ, Takken FL. 144.  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 1:401–10 [Google Scholar]
  145. van Ooijen G, Mayr G, Kasiem MM, Albrecht M, Cornelissen BJ, Takken FL. 145.  2008. Structure-function analysis of the NB-ARC domain of plant disease resistance proteins. J. Exp. Bot. 59:1383–97 [Google Scholar]
  146. Ve T, Williams SJ, Kobe B. 146.  2015. Structure and function of Toll/interleukin-1 receptor/resistance protein (TIR) domains. Apoptosis 20:250–61 [Google Scholar]
  147. Vyncke L, Bovijn C, Pauwels E, Van Acker T, Ruyssinck E. 147.  et al. 2016. Reconstructing the TIR side of the Myddosome: a paradigm for TIR-TIR interactions. Structure 24:437–47 [Google Scholar]
  148. Wagner S, Stuttmann J, Rietz S, Guerois R, Brunstein E. 148.  et al. 2013. Structural basis for signaling by exclusive EDS1 heteromeric complexes with SAG101 or PAD4 in plant innate immunity. Cell Host Microbe 14:619–30 [Google Scholar]
  149. Wang G, Roux B, Feng F, Guy E, Li L. 149.  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 18:285–95 [Google Scholar]
  150. Wang GF, Balint-Kurti PJ. 150.  2015. Cytoplasmic and nuclear localizations are important for the hypersensitive response conferred by maize autoactive Rp1-D21 protein. Mol. Plant-Microbe Interact. 28:1023–31 [Google Scholar]
  151. Wang GF, Ji J, Ei-Kasmi F, Dangl JL, Johal G, Balint-Kurti PJ. 151.  2015. Molecular and functional analyses of a maize autoactive NB-LRR protein identify precise structural requirements for activity. PLOS Pathog 11:e1004674 [Google Scholar]
  152. Wang W, Devoto A, Turner JG, Xiao S. 152.  2007. Expression of the membrane-associated resistance protein RPW8 enhances basal defense against biotrophic pathogens. Mol. Plant-Microbe Interact. 20:966–76 [Google Scholar]
  153. Warren RF, Merritt PM, Holub E, Innes RW. 153.  1999. Identification of three putative signal transduction genes involved in R gene–specified disease resistance in Arabidopsis. . Genetics 152:401–12 [Google Scholar]
  154. Weaver LM, Swiderski MR, Li Y, Jones JD. 154.  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. 47:829–40 [Google Scholar]
  155. Wiermer M, Feys BJ, Parker JE. 155.  2005. Plant immunity: the EDS1 regulatory node. Curr. Opin. Plant Biol. 8:383–89 [Google Scholar]
  156. Williams S, Yin L, Foley G, Casey L, Outram M. 156.  et al. 2016. Structure and function of the TIR domain from the grape NLR protein RPV1. Front. Plant Sci. 7:1850 [Google Scholar]
  157. Williams SJ, Sohn KH, Wan L, Bernoux M, Sarris PF. 157.  et al. 2014. Structural basis for assembly and function of a heterodimeric plant immune receptor. Science 344:299–303 [Google Scholar]
  158. Williams SJ, Sornaraj P, deCourcy-Ireland E, Menz RI, Kobe B. 158.  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. 24:897–906 [Google Scholar]
  159. Wilton M, Subramaniam R, Elmore J, Felsensteiner C, Coaker G, Desveaux D. 159.  2010. The type III effector HopF2Pto targets Arabidopsis RIN4 protein to promote Pseudomonas syringae virulence. PNAS 107:2349–54 [Google Scholar]
  160. Wirthmueller L, Zhang Y, Jones JD, Parker JE. 160.  2007. Nuclear accumulation of the Arabidopsis immune receptor RPS4 is necessary for triggering EDS1-dependent defense. Curr. Biol. 17:2023–29 [Google Scholar]
  161. Wu C-H, Abd-El-Haliem A, Bozkurt TO, Belhaj K, Terauchi R. 161.  et al. 2016. NLR signaling network mediates immunity to diverse plant pathogens. bioRxiv https://doi.org/10.1101/090449 [Crossref]
  162. Wu CH, Belhaj K, Bozkurt TO, Birk MS, Kamoun S. 162.  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. 209:1344–52 [Google Scholar]
  163. Wu W, Wang L, Zhang S, Li Z, Zhang Y. 163.  et al. 2014. Stepwise arms race between AvrPik and Pik alleles in the rice blast pathosystem. Mol. Plant-Microbe Interact. 27:759–69 [Google Scholar]
  164. Xiao S, Ellwood S, Calis O, Patrick E, Li T. 164.  et al. 2001. Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science 291:118–20 [Google Scholar]
  165. Xu F, Cheng YT, Kapos P, Huang Y, Li X. 165.  2014. P-loop-dependent NLR SNC1 can oligomerize and activate immunity in the nucleus. Mol. Plant 7:1801–4 [Google Scholar]
  166. Xu F, Kapos P, Cheng YT, Li M, Zhang Y, Li X. 166.  2014. NLR-associating transcription factor bHLH84 and its paralogs function redundantly in plant immunity. PLOS Pathog 10:e1004312 [Google Scholar]
  167. Xue JY, Wang Y, Wu P, Wang Q, Yang LT. 167.  et al. 2012. A primary survey on bryophyte species reveals two novel classes of nucleotide-binding site (NBS) genes. PLOS ONE 7:e36700 [Google Scholar]
  168. Zhai C, Zhang Y, Yao N, Lin F, Liu Z. 168.  et al. 2014. Function and interaction of the coupled genes responsible for Pik-h encoded rice blast resistance. PLOS ONE 9:e98067 [Google Scholar]
  169. Zhang J, Li W, Xiang T, Liu Z, Laluk K. 169.  et al. 2010. Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 7:290–301 [Google Scholar]
  170. Zhang L, Chen S, Ruan J, Wu J, Tong AB. 170.  et al. 2015. Cryo-EM structure of the activated NAIP2-NLRC4 inflammasome reveals nucleated polymerization. Science 350:404–9 [Google Scholar]
  171. Zhang X, Bernoux M, Bentham AR, Newman TE, Ve T, Casey LW. 171.  et al. 2017. Multiple functional self-interaction interfaces in plant TIR domains. PNAS 114:E2046–52 [Google Scholar]
  172. Zhao T, Rui L, Li J, Nishimura MT, Vogel JP. 172.  et al. 2015. A truncated NLR protein, TIR-NBS2, is required for activated defense responses in the exo70B1 mutant. PLOS Genet 11:e1004945 [Google Scholar]
  173. Zhu Z, Xu F, Zhang Y, Cheng YT, Wiermer M. 173.  et al. 2010. Arabidopsis resistance protein SNC1 activates immune responses through association with a transcriptional corepressor. PNAS 107:13960–65 [Google Scholar]
/content/journals/10.1146/annurev-phyto-080516-035250
Loading
/content/journals/10.1146/annurev-phyto-080516-035250
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