In plant innate immunity, individual cells have the capacity to sense and respond to pathogen attack. Intracellular recognition mechanisms have evolved to intercept perturbations by pathogen virulence factors (effectors) early in host infection and convert it to rapid defense. One key to resistance success is a polymorphic family of intracellular nucleotide-binding/leucine-rich-repeat (NLR) receptors that detect effector interference in different parts of the cell. Effector-activated NLRs connect, in various ways, to a conserved basal resistance network in order to transcriptionally boost defense programs. Effector-triggered immunity displays remarkable robustness against pathogen disturbance, in part by employing compensatory mechanisms within the defense network. Also, the mobility of some NLRs and coordination of resistance pathways across cell compartments provides flexibility to fine-tune immune outputs. Furthermore, a number of NLRs function close to the nuclear chromatin by balancing actions of defense-repressing and defense-activating transcription factors to program cells dynamically for effective disease resistance.


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Literature Cited

  1. Ade J, DeYoung BJ, Golstein C, Innes RW. 1.  2007. Indirect activation of a plant nucleotide binding site-leucine-rich repeat protein by a bacterial protease. PNAS 104:2531–36 [Google Scholar]
  2. Armstrong MR, Whisson SC, Pritchard L, Bos JI, Venter E. 2.  et al. 2005. An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. PNAS 102:7766–71 [Google Scholar]
  3. Axtell MJ, Staskawicz BJ. 3.  2003. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112:369–77 [Google Scholar]
  4. Bai S, Liu J, Chang C, Zhang L, Maekawa T. 4.  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]
  5. Bartels S, Anderson JC, González Besteiro MA, Carreri A, Hirt H. 5.  et al. 2009. MAP KINASE PHOSPHATASE1 and PROTEIN TYROSINE PHOSPHATASE1 are repressors of salicylic acid synthesis and SNC1-mediated responses in Arabidopsis. Plant Cell 21:2884–97 [Google Scholar]
  6. Bartsch M, Gobbato E, Bednarek P, Debey S, Schultze JL. 6.  et al. 2006. Salicylic acid-independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the Nudix hydrolase NUDT7. Plant Cell 18:1038–51 [Google Scholar]
  7. Bendahmane A, Kanyuka K, Baulcombe DC. 7.  1999. The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell 11:781–92 [Google Scholar]
  8. Berkey R, Bendigeri D, Xiao S. 8.  2012. Sphingolipids and plant defense/disease: the “death” connection and beyond. Front. Plant Sci. 3:68 [Google Scholar]
  9. Bernoux M, Ve T, Williams S, Warren C, Hatters D. 9.  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]
  10. Bhattacharjee S, Halane MK, Kim SH, Gassmann W. 10.  2011. Pathogen effectors target Arabidopsis EDS1 and alter its interactions with immune regulators. Science 334:1405–8 [Google Scholar]
  11. Birker D, Heidrich K, Takahara H, Narusaka M, Deslandes L. 11.  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]
  12. Boccara M, Sarazin A, Thiebeauld O, Jay F, Voinnet O. 12.  et al. 2014. The Arabidopsis miR472-RDR6 silencing pathway modulates PAMP- and effector-triggered immunity through the post-transcriptional control of disease resistance genes. PLOS Pathog 10:e1003883 [Google Scholar]
  13. Boch J, Bonas U. 13.  2010. Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu. Rev. Phytopathol. 48:419–36 [Google Scholar]
  14. Bohm H, Albert I, Fan L, Reinhard A, Nuernberger T. 14.  2014. Immune receptor complexes at the plant cell surface. Curr. Opin. Plant Biol. 20:47–54 [Google Scholar]
  15. Bonardi V, Tang S, Stallmann A, Roberts M, Cherkis K, Dangl JL. 15.  2011. Expanded functions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors. PNAS 108:16463–68 [Google Scholar]
  16. Boyes DC, Nam J, Dangl JL. 16.  1998. The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response. PNAS 95:15849–54 [Google Scholar]
  17. Burch-Smith TM, Schiff M, Caplan JL, Tsao J, Czymmek K, Dinesh-Kumar SP. 17.  2007. A novel role for the TIR domain in association with pathogen-derived elicitors. PLOS Biol. 5:e68 [Google Scholar]
  18. Buscaill P, Rivas S. 18.  2014. Transcriptional control of plant defence responses. Curr. Opin. Plant Biol. 20:35–46 [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. Catanzariti AM, Dodds PN, Ve T, Kobe B, Ellis JG, Staskawicz BJ. 20.  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]
  21. Césari S, Kanzaki H, Fujiwara T, Bernoux M, Chalvon V. 21.  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]
  22. Césari S, Thilliez G, Ribot C, Chalvon V, Michel C. 22.  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]
  23. Chang C, Yu D, Jiao J, Jing S, Schulze-Lefert P, Shen QH. 23.  2013. Barley MLA immune receptors directly interfere with antagonistically acting transcription factors to initiate disease resistance signaling. Plant Cell 25:1158–73 [Google Scholar]
  24. Cheng YT, Germain H, Wiermer M, Bi D, Xu F. 24.  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]
  25. Cheng YT, Li X. 25.  2012. Ubiquitination in NB-LRR-mediated immunity. Curr. Opin. Plant Biol. 15:392–99 [Google Scholar]
  26. Chung EH, El-Kasmi F, He Y, Loehr A, Dangl JL. 26.  2014. A plant phosphoswitch platform repeatedly targeted by type III effector proteins regulates the output of both tiers of plant immune receptors. Cell Host Microbe 16:484–94 [Google Scholar]
  27. Coll NS, Epple P, Dangl JL. 27.  2011. Programmed cell death in the plant immune system. Cell Death Differ. 18:1247–56 [Google Scholar]
  28. Coll NS, Vercammen D, Smidler A, Clover C, Van Breusegem F. 28.  et al. 2010. Arabidopsis type I metacaspases control cell death. Science 330:1393–97 [Google Scholar]
  29. Collier SM, Hamel LP, Moffett P. 29.  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]
  30. Collier SM, Moffett P. 30.  2009. NB-LRRs work a “bait and switch” on pathogens. Trends Plant Sci. 14:521–29 [Google Scholar]
  31. Dangl JL, Horvath DM, Staskawicz BJ. 31.  2013. Pivoting the plant immune system from dissection to deployment. Science 341:746–51 [Google Scholar]
  32. Day B, Dahlbeck D, Staskawicz BJ. 32.  2006. NDR1 interaction with RIN4 mediates the differential activation of multiple disease resistance pathways in Arabidopsis. Plant Cell 18:2782–91 [Google Scholar]
  33. Deng D, Yan C, Pan X, Mahfouz M, Wang J. 33.  et al. 2012. Structural basis for sequence-specific recognition of DNA by TAL effectors. Science 335:720–23 [Google Scholar]
  34. Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M. 34.  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]
  35. Deslandes L, Rivas S. 35.  2012. Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci. 17:644–55 [Google Scholar]
  36. Dinesh-Kumar SP, Baker BJ. 36.  2000. Alternatively spliced N resistance gene transcripts: their possible role in tobacco mosaic virus resistance. PNAS 97:1908–13 [Google Scholar]
  37. Dodds PN, Lawrence GJ, Catanzariti AM, Teh T, Wang CI. 37.  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]
  38. Dodds PN, Rathjen JP. 38.  2010. Plant immunity: towards an integrated view of plant–pathogen interactions. Nat. Rev. Genet. 11:539–48 [Google Scholar]
  39. Dou D, Zhou JM. 39.  2012. Phytopathogen effectors subverting host immunity: different foes, similar battleground. Cell Host Microbe 12:484–95 [Google Scholar]
  40. Elmore JM, Liu J, Smith B, Phinney B, Coaker G. 40.  2012. Quantitative proteomics reveals dynamic changes in the plasma membrane during Arabidopsis immune signaling. Mol. Cell. Proteomics 11:M111.014555 [Google Scholar]
  41. Engelhardt S, Boevink PC, Armstrong MR, Ramos MB, Hein I, Birch PR. 41.  2012. Relocalization of late blight resistance protein R3a to endosomal compartments is associated with effector recognition and required for the immune response. Plant Cell 24:5142–58 [Google Scholar]
  42. Feys BJ, Wiermer M, Bhat RA, Moisan LJ, Medina-Escobar N. 42.  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]
  43. Flor HH. 43.  1971. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9:275–96 [Google Scholar]
  44. Fradin EF, Zhang Z, Juarez Ayala JC, Castroverde CD, Nazar RN. 44.  et al. 2009. Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiol. 150:320–32 [Google Scholar]
  45. Fu ZQ, Dong X. 45.  2013. Systemic acquired resistance: turning local infection into global defense. Annu. Rev. Plant Biol. 64:839–63 [Google Scholar]
  46. Gabriels SH, Vossen JH, Ekengren SK, van Ooijen G, Abd-El-Haliem AM. 46.  et al. 2007. An NB-LRR protein required for HR signaling mediated by both extra- and intracellular resistance proteins. Plant J. 50:14–28 [Google Scholar]
  47. Gao X, Chen X, Lin W, Chen S, Lu D. 47.  et al. 2013. Bifurcation of Arabidopsis NLR immune signaling via Ca2+-dependent protein kinases. PLOS Pathog. 9:e1003127 [Google Scholar]
  48. Gao Z, Chung EH, Eitas TK, Dangl JL. 48.  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]
  49. Garcia AV, Blanvillain-Baufumé S, Huibers RP, Wiermer M, Li G. 49.  et al. 2010. Balanced nuclear and cytoplasmic activities of EDS1 are required for a complete plant innate immune response. PLOS Pathog. 6:e1000970 [Google Scholar]
  50. Garcia AV, Parker JE. 50.  2009. Heaven's Gate: nuclear accessibility and activities of plant immune regulators. Trends Plant Sci. 14:479–87 [Google Scholar]
  51. Gassmann W. 51.  2005. Natural variation in the Arabidopsis response to the avirulence gene hopPsyA uncouples the hypersensitive response from disease resistance. Mol. Plant-Microbe Interact. 18:1054–60 [Google Scholar]
  52. Gloggnitzer J, Akimcheva S, Srinivasan A, Kusenda B, Riehs N. 52.  et al. 2014. Nonsense-mediated mRNA decay modulates immune receptor levels to regulate plant antibacterial defense. Cell Host Microbe 16:376–90 [Google Scholar]
  53. Griebel T, Maekawa T, Parker JE. 53.  2014. NOD-like receptor cooperativity in effector-triggered immunity. Trends Immunol. 35:562–70 [Google Scholar]
  54. Gu K, Yang B, Tian D, Wu L, Wang D. 54.  et al. 2005. R gene expression induced by a type-III effector triggers disease resistance in rice. Nature 435:1122–25 [Google Scholar]
  55. Guo YL, Fitz J, Schneeberger K, Ossowski S, Cao J, Weigel D. 55.  2011. Genome-wide comparison of nucleotide-binding site-leucine-rich repeat-encoding genes in Arabidopsis. Plant Physiol. 157:757–69 [Google Scholar]
  56. Hayashi N, Inoue H, Kato T, Funao T, Shirota M. 56.  et al. 2010. Durable panicle blast-resistance gene Pb1 encodes an atypical CC-NBS-LRR protein and was generated by acquiring a promoter through local genome duplication. Plant J. 64:498–510 [Google Scholar]
  57. Heidrich K, Blanvillain-Baufumé S, Parker JE. 57.  2012. Molecular and spatial constraints on NB-LRR receptor signaling. Curr. Opin. Plant Biol. 15:385–91 [Google Scholar]
  58. Heidrich K, Tsuda K, Blanvillain-Baufumé S, Wirthmueller L, Bautor J, Parker JE. 58.  2013. Arabidopsis TNL-WRKY domain receptor RRS1 contributes to temperature-conditioned RPS4 auto-immunity. Front. Plant Sci. 4:403 [Google Scholar]
  59. Heidrich K, Wirthmueller L, Tasset C, Pouzet C, Deslandes L, Parker JE. 59.  2011. Arabidopsis EDS1 connects pathogen effector recognition to cell compartment-specific immune responses. Science 334:1401–4 [Google Scholar]
  60. Holt BF III, Boyes DC, Ellerstrom M, Siefers N, Wiig A. 60.  et al. 2002. An evolutionarily conserved mediator of plant disease resistance gene function is required for normal Arabidopsis development. Dev. Cell 2:807–17 [Google Scholar]
  61. Hoser R, Zurczak M, Lichocka M, Zuzga S, Dadlez M. 61.  et al. 2013. Nucleocytoplasmic partitioning of tobacco N receptor is modulated by SGT1. New Phytol. 200:158–71 [Google Scholar]
  62. Hu Z, Yan C, Liu P, Huang Z, Ma R. 62.  et al. 2013. Crystal structure of NLRC4 reveals its autoinhibition mechanism. Science 341:172–75 [Google Scholar]
  63. Inoue H, Hayashi N, Matsushita A, Xinqiong L, Nakayama A. 63.  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]
  64. Jacob F, Vernaldi S, Maekawa T. 64.  2013. Evolution and conservation of plant NLR functions. Front. Immunol. 4:297 [Google Scholar]
  65. Janssen BJ, Snowden KC. 65.  2012. Strigolactone and karrikin signal perception: receptors, enzymes, or both?. Front. Plant Sci. 3:296 [Google Scholar]
  66. Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B. 66.  2000. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J. 19:4004–14 [Google Scholar]
  67. Jones JD, Dangl JL. 67.  2006. The plant immune system. Nature 444:323–29 [Google Scholar]
  68. Kadota Y, Sklenar J, Derbyshire P, Stransfeld L, Asai S. 68.  et al. 2014. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol. Cell 54:43–55 [Google Scholar]
  69. Kaminaka H, Nake C, Epple P, Dittgen J, Schutze K. 69.  et al. 2006. bZIP10-LSD1 antagonism modulates basal defense and cell death in Arabidopsis following infection. EMBO J. 25:4400–11 [Google Scholar]
  70. Kanzaki H, Yoshida K, Saitoh H, Fujisaki K, Hirabuchi A. 70.  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]
  71. Karasov TL, Horton MW, Bergelson J. 71.  2014. Genomic variability as a driver of plant-pathogen coevolution?. Curr. Opin. Plant Biol. 18:24–30 [Google Scholar]
  72. Katagiri F, Tsuda K. 72.  2010. Understanding the plant immune system. Mol. Plant-Microbe Interact. 23:1531–36 [Google Scholar]
  73. Kim MG, da Cunha L, McFall AJ, Belkhadir Y, DebRoy S. 73.  et al. 2005. Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis. Cell 121:749–59 [Google Scholar]
  74. Kim SH, Kwon SI, Saha D, Anyanwu NC, Gassmann W. 74.  2009. Resistance to the Pseudomonas syringae effector HopA1 is governed by the TIR-NBS-LRR protein RPS6 and is enhanced by mutations in SRFR1. Plant Physiol. 150:1723–32 [Google Scholar]
  75. Kim TH, Kunz HH, Bhattacharjee S, Hauser F, Park J. 75.  et al. 2012. Natural variation in small molecule-induced TIR-NB-LRR signaling induces root growth arrest via EDS1- and PAD4-complexed R protein VICTR in Arabidopsis. Plant Cell 24:5177–92 [Google Scholar]
  76. Knepper C, Savory EA, Day B. 76.  2011. The role of NDR1 in pathogen perception and plant defense signaling. Plant Signal. Behav. 6:1114–16 [Google Scholar]
  77. Kofoed EM, Vance RE. 77.  2011. Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature 477:592–95 [Google Scholar]
  78. Krasileva KV, Dahlbeck D, Staskawicz BJ. 78.  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]
  79. Leister RT, Ausubel FM, Katagiri F. 79.  1996. Molecular recognition of pathogen attack occurs inside of plant cells in plant disease resistance specified by the Arabidopsis genes RPS2 and RPM1. PNAS 93:15497–502 [Google Scholar]
  80. Leonelli L, Pelton J, Schoeffler A, Dahlbeck D, Berger J. 80.  et al. 2011. Structural elucidation and functional characterization of the Hyaloperonospora arabidopsidis effector protein ATR13. PLOS Pathog. 7:e1002428 [Google Scholar]
  81. Li G, Meng X, Wang R, Mao G, Han L. 81.  et al. 2012. Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLOS Genet. 8:e1002767 [Google Scholar]
  82. Li L, Li M, Yu L, Zhou Z, Liang X. 82.  et al. 2014. The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15:329–38 [Google Scholar]
  83. Li M, Ma X, Chiang Y-HH, Yadeta KA, Ding P. 83.  et al. 2014. Proline isomerization of the immune receptor-interacting protein RIN4 by a cyclophilin inhibits effector-triggered immunity in Arabidopsis. Cell Host Microbe 16:473–83 [Google Scholar]
  84. Lilue JT, Müller UB, Steinfeldt T, Howard JC. 84.  2013. Reciprocal virulence and resistance polymorphism in the relationship between Toxoplasma gondii and the house mouse. eLife 2:e01298 [Google Scholar]
  85. Liu J, Elmore JM, Fuglsang AT, Palmgren MG, Staskawicz BJ, Coaker G. 85.  2009. RIN4 functions with plasma membrane H+-ATPases to regulate stomatal apertures during pathogen attack. PLOS Biol. 7:e1000139 [Google Scholar]
  86. Lorang J, Kidarsa T, Bradford CS, Gilbert B, Curtis M. 86.  et al. 2012. Tricking the guard: exploiting plant defense for disease susceptibility. Science 338:659–62 [Google Scholar]
  87. Luo Y, Caldwell KS, Wroblewski T, Wright ME, Michelmore RW. 87.  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]
  88. Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL. 88.  2003. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112:379–89 [Google Scholar]
  89. Maekawa T, Cheng W, Spiridon LN, Toller A, Lukasik E. 89.  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]
  90. Maekawa T, Kufer TA, Schulze-Lefert P. 90.  2011. NLR functions in plant and animal immune systems: so far and yet so close. Nat. Immunol. 12:817–26 [Google Scholar]
  91. Mak AN, Bradley P, Cernadas RA, Bogdanove AJ, Stoddard BL. 91.  2012. The crystal structure of TAL effector PthXo1 bound to its DNA target. Science 335:716–19 [Google Scholar]
  92. Mao G, Meng X, Liu Y, Zheng Z, Chen Z, Zhang S. 92.  2011. Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23:1639–53 [Google Scholar]
  93. Matsushita A, Inoue H, Goto S, Nakayama A, Sugano S. 93.  et al. 2012. The nuclear ubiquitin proteasome degradation affects WRKY45 function in the rice defense program. Plant J. 73:302–13 [Google Scholar]
  94. McNellis TW, Mudgett MB, Li K, Aoyama T, Horvath D. 94.  et al. 1998. Glucocorticoid-inducible expression of a bacterial avirulence gene in transgenic Arabidopsis induces hypersensitive cell death. Plant J. 14:247–57 [Google Scholar]
  95. Meier I, Somers DE. 95.  2011. Regulation of nucleocytoplasmic trafficking in plants. Curr. Opin. Plant Biol. 14:538–46 [Google Scholar]
  96. Meng X, Zhang S. 96.  2013. MAPK cascades in plant disease resistance signaling. Annu. Rev. Phytopathol. 51:245–66 [Google Scholar]
  97. Mestre P, Baulcombe DC. 97.  2006. Elicitor-mediated oligomerization of the tobacco N disease resistance protein. Plant Cell 18:491–501 [Google Scholar]
  98. Mukhtar MS, Carvunis AR, Dreze M, Epple P, Steinbrenner J. 98.  et al. 2011. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333:596–601 [Google Scholar]
  99. Narusaka M, Shirasu K, Noutoshi Y, Kubo Y, Shiraishi T. 99.  et al. 2009. RRS1 and RPS4 provide a dual Resistance-gene system against fungal and bacterial pathogens. Plant J. 60:218–26 [Google Scholar]
  100. Navarro L, Zipfel C, Rowland O, Keller I, Robatzek S. 100.  et al. 2004. The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol. 135:1113–28 [Google Scholar]
  101. Nomura K, Mecey C, Lee YN, Imboden LA, Chang JH, He SY. 101.  2011. Effector-triggered immunity blocks pathogen degradation of an immunity-associated vesicle traffic regulator in Arabidopsis. PNAS 108:10774–79 [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. Padmanabhan MS, Ma S, Burch-Smith TM, Czymmek K, Huijser P, Dinesh-Kumar SP. 104.  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]
  105. Palma K, Thorgrimsen S, Malinovsky FG, Fiil BK, Nielsen HB. 105.  et al. 2010. Autoimmunity in Arabidopsis acd11 is mediated by epigenetic regulation of an immune receptor. PLOS Pathog 6:e1001137 [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. Raffaele S, Farrer RA, Cano LM, Studholme DJ, MacLean D. 108.  et al. 2010. Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science 330:1540–43 [Google Scholar]
  109. Ravensdale M, Bernoux M, Ve T, Kobe B, Thrall PH. 109.  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]
  110. Rietz S, Stamm A, Malonek S, Wagner S, Becker D. 110.  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]
  111. Roberts M, Tang S, Stallmann A, Dangl JL, Bonardi V. 111.  2013. Genetic requirements for signaling from an autoactive plant NB-LRR intracellular innate immune receptor. PLOS Genet 9:e1003465 [Google Scholar]
  112. Romer P, Hahn S, Jordan T, Strauss T, Bonas U, Lahaye T. 112.  2007. Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science 318:645–48 [Google Scholar]
  113. Sato M, Tsuda K, Wang L, Coller J, Watanabe Y. 113.  et al. 2010. Network modeling reveals prevalent negative regulatory relationships between signaling sectors in Arabidopsis immune signaling. PLOS Pathog 6:e1001011 [Google Scholar]
  114. Schornack S, Ballvora A, Gurlebeck D, Peart J, Baulcombe D. 114.  et al. 2004. The tomato resistance protein Bs4 is a predicted non-nuclear TIR-NB-LRR protein that mediates defense responses to severely truncated derivatives of AvrBs4 and overexpressed AvrBs3. Plant J 37:46–60 [Google Scholar]
  115. Schornack S, Moscou MJ, Ward ER, Horvath DM. 115.  2013. Engineering plant disease resistance based on TAL effectors. Annu. Rev. Phytopathol 51:383–406 [Google Scholar]
  116. Selote D, Kachroo A. 116.  2010. RPG1-B-derived resistance to AvrB-expressing Pseudomonas syringae requires RIN4-like proteins in soybean. Plant Physiol 153:1199–211 [Google Scholar]
  117. Selote D, Shine MB, Robin GP, Kachroo A. 117.  2014. Soybean NDR1-like proteins bind pathogen effectors and regulate resistance signaling. New Phytol. 202:485–98 [Google Scholar]
  118. Shan L, He P, Li J, Heese A, Peck SC. 118.  et al. 2008. Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4:17–27 [Google Scholar]
  119. Shen QH, Saijo Y, Mauch S, Biskup C, Bieri S. 119.  et al. 2007. Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315:1098–103 [Google Scholar]
  120. Slootweg E, Roosien J, Spiridon LN, Petrescu AJ, Tameling W. 120.  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]
  121. Sohn KH, Segonzac C, Rallapalli G, Sarris PF, Woo JY. 121.  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]
  122. Spoel SH, Dong X. 122.  2012. How do plants achieve immunity? Defence without specialized immune cells. Nat. Rev. Immunol. 12:89–100 [Google Scholar]
  123. Staiger D, Korneli C, Lummer M, Navarro L. 123.  2013. Emerging role for RNA-based regulation in plant immunity. New Phytol. 197:394–404 [Google Scholar]
  124. Strauss T, van Poecke RM, Strauss A, Romer P, Minsavage GV. 124.  et al. 2012. RNA-seq pinpoints a Xanthomonas TAL-effector activated resistance gene in a large-crop genome. PNAS 109:19480–85 [Google Scholar]
  125. Stuart LM, Paquette N, Boyer L. 125.  2013. Effector-triggered versus pattern-triggered immunity: how animals sense pathogens. Nat. Rev. Immunol. 13:199–206 [Google Scholar]
  126. Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J. 126.  et al. 2008. Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–56 [Google Scholar]
  127. Takemoto D, Rafiqi M, Hurley U, Lawrence GJ, Bernoux M. 127.  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]
  128. Takken FL, Goverse A. 128.  2012. How to build a pathogen detector: structural basis of NB-LRR function. Curr. Opin. Plant Biol. 15:375–84 [Google Scholar]
  129. Tameling WI, Nooijen C, Ludwig N, Boter M, Slootweg E. 129.  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]
  130. Tao Y, Xie Z, Chen W, Glazebrook J, Chang HS. 130.  et al. 2003. Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317–30 [Google Scholar]
  131. Tasset C, Bernoux M, Jauneau A, Pouzet C, Briere C. 131.  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]
  132. Tenthorey JL, Kofoed EM, Daugherty MD, Malik HS, Vance RE. 132.  2014. Molecular basis for specific recognition of bacterial ligands by NAIP/NLRC4 inflammasomes. Mol. Cell 54:17–29 [Google Scholar]
  133. Tian D, Wang J, Zeng X, Gu K, Qiu C. 133.  et al. 2014. The rice TAL effector-dependent resistance protein XA10 triggers cell death and calcium depletion in the endoplasmic reticulum.. Plant Cell 26:497–515 [Google Scholar]
  134. Ting JP, Duncan JA, Lei Y. 134.  2010. How the noninflammasome NLRs function in the innate immune system. Science 327:286–90 [Google Scholar]
  135. Tsuda K, Katagiri F. 135.  2010. Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr. Opin. Plant Biol. 13:459–65 [Google Scholar]
  136. Tsuda K, Mine A, Bethke G, Igarashi D, Botanga CJ. 136.  et al. 2013. Dual regulation of gene expression mediated by extended MAPK activation and salicylic acid contributes to robust innate immunity in Arabidopsis thaliana. PLOS Genet. 9:e1004015 [Google Scholar]
  137. Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F. 137.  2009. Network properties of robust immunity in plants. PLOS Genet. 5:e1000772 [Google Scholar]
  138. van der Hoorn RA, Kamoun S. 138.  2008. From Guard to Decoy: a new model for perception of plant pathogen effectors. Plant Cell 20:2009–17 [Google Scholar]
  139. Venugopal SC, Jeong RD, Mandal MK, Zhu S, Chandra-Shekara AC. 139.  et al. 2009. Enhanced disease susceptibility 1 and salicylic acid act redundantly to regulate resistance gene-mediated signaling. PLOS Genet. 5:e1000545 [Google Scholar]
  140. von Moltke J, Ayres JS, Kofoed EM, Chavarria-Smith J, Vance RE. 140.  2013. Recognition of bacteria by inflammasomes. Annu. Rev. Immunol. 31:73–106 [Google Scholar]
  141. Wagner S, Stuttmann J, Rietz S, Guerois R, Brunstein E. 141.  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]
  142. Wang D, Weaver ND, Kesarwani M, Dong XN. 142.  2005. Induction of protein secretory pathway is required for systemic acquired resistance. Science 308:1036–40 [Google Scholar]
  143. Wang H, Lu Y, Liu P, Wen W, Zhang J. 143.  et al. 2013. The ammonium/nitrate ratio is an input signal in the temperature-modulated, SNC1-mediated and EDS1-dependent autoimmunity of nudt6-2 nudt7. Plant J. 73:262–75 [Google Scholar]
  144. Wang Y, Zhang Y, Wang Z, Zhang X, Yang S. 144.  2013. A missense mutation in CHS1, a TIR-NB protein, induces chilling sensitivity in Arabidopsis. Plant J. 75:553–65 [Google Scholar]
  145. Wessling R, Epple P, Altmann S, He Y, Yang L. 145.  et al. 2014. Convergent targeting of a common host protein-network by pathogen effectors from three kingdoms of life. Cell Host Microbe 16:364–75 [Google Scholar]
  146. Wiermer M, Feys BJ, Parker JE. 146.  2005. Plant immunity: the EDS1 regulatory node. Curr. Opin. Plant Biol. 8:383–89 [Google Scholar]
  147. Williams SJ, Sohn KH, Wan L, Bernoux M, Sarris PF. 147.  et al. 2014. Structural basis for assembly and function of a heterodimeric plant immune receptor. Science 344:299–303 [Google Scholar]
  148. Wilton M, Subramaniam R, Elmore J, Felsensteiner C, Coaker G, Desveaux D. 148.  2010. The type III effector HopF2 Pto targets Arabidopsis RIN4 protein to promote Pseudomonas syringae virulence. PNAS 107:2349–54 [Google Scholar]
  149. Wirthmueller L, Zhang Y, Jones JD, Parker JE. 149.  2007. Nuclear accumulation of the Arabidopsis immune receptor RPS4 is necessary for triggering EDS1-dependent defense. Curr. Biol. 17:2023–29 [Google Scholar]
  150. Wu L, Goh ML, Sreekala C, Yin Z. 150.  2008. XA27 depends on an amino-terminal signal-anchor-like sequence to localize to the apoplast for resistance to Xanthomonas oryzae pv oryzae. Plant Physiol. 148:1497–509 [Google Scholar]
  151. Wu Y, Wood MD, Tao Y, Katagiri F. 151.  2003. Direct delivery of bacterial avirulence proteins into resistant Arabidopsis protoplasts leads to hypersensitive cell death. Plant J. 33:131–37 [Google Scholar]
  152. Xiang T, Zong N, Zou Y, Wu Y, Zhang J. 152.  et al. 2008. Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr. Biol. 18:74–80 [Google Scholar]
  153. Xing W, Zou Y, Liu Q, Liu J, Luo X. 153.  et al. 2007. The structural basis for activation of plant immunity by bacterial effector protein AvrPto. Nature 449:243–47 [Google Scholar]
  154. Xu F, Kapos P, Cheng YT, Li M, Zhang Y, Li X. 154.  2014. NLR-associating transcription factor bHLH84 and its paralogs function redundantly in plant immunity. PLOS Pathog 10:e1004312 [Google Scholar]
  155. Yue JX, Meyers BC, Chen JQ, Tian D, Yang S. 155.  2012. Tracing the origin and evolutionary history of plant nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes. New Phytol. 193:1049–63 [Google Scholar]
  156. Zbierzak AM, Porfirova S, Griebel T, Melzer M, Parker JE, Dormann P. 156.  2013. A TIR-NBS protein encoded by Arabidopsis Chilling Sensitive 1 (CHS1) limits chloroplast damage and cell death at low temperature. Plant J. 75:539–52 [Google Scholar]
  157. Zhang J, Li W, Xiang T, Liu Z, Laluk K. 157.  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]
  158. Zhang XC, Gassmann W. 158.  2003. RPS4-mediated disease resistance requires the combined presence of RPS4 transcripts with full-length and truncated open reading frames. Plant Cell 15:2333–42 [Google Scholar]
  159. Zhang Z, Wu Y, Gao M, Zhang J, Kong Q. 159.  et al. 2012. Disruption of PAMP-induced MAP kinase cascade by a Pseudomonas syringae effector activates plant immunity mediated by the NB-LRR protein SUMM2. Cell Host Microbe 11:253–63 [Google Scholar]
  160. Zhao Y, Yang J, Shi J, Gong YN, Lu Q. 160.  et al. 2011. The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature 477:596–600 [Google Scholar]
  161. Zhu Z, Xu F, Zhang Y, Cheng YT, Wiermer M. 161.  et al. 2010. Arabidopsis resistance protein SNC1 activates immune responses through association with a transcriptional corepressor. PNAS 107:13960–65 [Google Scholar]
  162. Zipfel C. 162.  2014. Plant pattern-recognition receptors. Trends Immunol. 35:345–51 [Google Scholar]

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