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Plant Innate Immunity

  • Jacqueline Monaghan
  • Tabea Weihmann
  • Xin Li
Chapter
Part of the Signaling and Communication in Plants book series (SIGCOMM)

Abstract

Plants possess an elaborate multilayered defense system that relies on the intrinsic ability of plant cells to perceive the presence of pathogens and trigger local and systemic responses. Transmembrane receptors detect highly conserved microbial features and activate signaling cascades that induce defense gene expression. Pathogens deliver effector proteins into plant cells that suppress these responses by interfering with signaling components. Plants, in turn, evolved intracellular resistance (R) protein receptors to recognize these effector proteins or their activities in the plant cell. Activated R proteins trigger a series of physiological changes in the infected cell that restrict pathogen growth locally and resonate systemically to enhance immunity throughout the plant. In this chapter we summarize our current understanding of defense responses employed by plants during pathogen infection.

Notes

Acknowledgments

We thank Dr. Marcel Wiermer for helpful discussions and critical reading of the manuscript, and we are grateful to Yuti Cheng for research assistance.

References

  1. Aarts N, Metz M, Holub E, Staskawicz BJ, Daniels MJ, Parker JE (1998) Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc Nat Acad Sci USA 95:10306–10311PubMedCrossRefGoogle Scholar
  2. Abramovitch RB, Janjusevic R, Stebbins CE, Martin G (2006) Type III effector AvrPtoB requires intrinsic E3 ubiquitin ligase activity to suppress plant cell death and immunity. Proc Nat Acad Sci USA 103:2851–2856PubMedCrossRefGoogle Scholar
  3. Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124:783–801PubMedCrossRefGoogle Scholar
  4. Alfano JR, Collmer A (1996) Bacterial pathogenesis in plants: life up against the wall. Plant Cell 9:1683–1698Google Scholar
  5. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu W-L, Gómez-Gómez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signaling cascade in Arabidopsis innate immunity. Nature 415:977–983PubMedCrossRefGoogle Scholar
  6. Ausubel FM (2005) Are innate immune signaling pathways in plants and animals conserved? Nature Immunol 6:973–979CrossRefGoogle Scholar
  7. Axtell MJ, Chisholm ST, Dahlbeck D, Staskawicz BJ (2003) Genetic and molecular evidence that the Pseudomonas syringae type III effector protein AvrRpt2 is a cysteine protease. Mol Microbiol 49:1537–1546PubMedCrossRefGoogle Scholar
  8. Belkhadir Y, Nimchuk Z, Hubert DA, Mackey D, Dangl JL (2004) Arabidopsis RIN4 negatively regulates disease resistance mediated by RPS2 and PRM1 downstream or independent of the NDR1 signal modulator and is not required for the virulence functions of bacterial type III effectors AvrRpt2 or AvrRpm1. Plant Cell 16:2822–2835PubMedCrossRefGoogle Scholar
  9. Birch PRJ, Boevink PC, Gilroy EM, Hein I, Pritchard L, Whisson SC (2008) Oomycete RXLR effectors: delivery, functional redundancy and durable disease resistance. Curr Opin Plant Biol 11:1–7CrossRefGoogle Scholar
  10. Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, Gwinn ML, Dodson RJ, Deboy RT, Durkin AS, Kolonay JF, Madupu R, Daugherty S, Brinkac L, Beanan MJ, Haft DH, Nelson WC, Davidsen T, Zafar N, Zhou L, Liu J, Yuan Q, Khouri H, Fedorova N, Tran B, Russell D, Berry K, Utterback T, Van Aken SE, Feldblyum TV, D'Ascenzo M, Deng WL, Ramos AR, Alfano JR, Cartinhour S, Chatterjee AK, Delaney TP, Lazarowitz SG, Martin GB, Schneider DJ, Tang X, Bender CL, White O, Fraser CM, Collmer A (2003) The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc Nat Acad Sci USA 100:10181–10186PubMedCrossRefGoogle Scholar
  11. Burch-Smith TM, Schiff M, Caplan JL, Tsao J, Czymmek K, Dinesh-Kumar SP (2007) A novel role for the TIR domain in association with pathogen-derived elicitors. PLoS Biol 5:501–514CrossRefGoogle Scholar
  12. Chen Z, Agnew JL, Cohen JD, He P, Shan L, Sheen J, Kunkel BN (2007) Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. Proc Nat Acad Sci U S A 204:20131–20136CrossRefGoogle Scholar
  13. Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G (2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 2:465–476Google Scholar
  14. Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JDG, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500PubMedCrossRefGoogle Scholar
  15. Coaker G, Falick A, Staskawicz B (2005) Activation of a phytopathogenic bacterial effector protein by a eukaryotic cyclophilin. Science 308:548–550PubMedCrossRefGoogle Scholar
  16. Dangl JL, Jones JDG (2001) Plant pathogens and integrated defense responses to infection. Nature 411:826–833PubMedCrossRefGoogle Scholar
  17. Day B, Dahlbeck D, Staskawicz BJ (2006) NDR1 interaction with RIN4 mediates the differential activation of multiple disease resistance pathways in Arabidopsis. Plant Cell 18:2782–2791PubMedCrossRefGoogle Scholar
  18. Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, Orbach MJ, Thon M, Kulkarni R, Xu J-R, Pan H, Read ND, Lee Y-W, Carbone I, Brown D, Oh YY, Donofrio N, Jeong JS, Soanes DM, Djonovic S, Kolomiets E, Rehmeyer C, Li W, Harding M, Kim S, Lebrun M-H, Bohnert H, Coughlan S, Butler J, Calvo S, Ma L-J, Nicol R, Purcell S, Nusbaum C, Galagan JE, Birren BW (2005) The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434:980–986PubMedCrossRefGoogle Scholar
  19. Deslandes L, Olivier J, Theulieres F, Hirsch J, Feng DX, Bittner-Eddy P, Beyon J, Marco Y (2002) Resistance to Ralstonia solanacerum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. Proc Nat Acad USA 99:2404–2409CrossRefGoogle Scholar
  20. Dong X (2004) NPR1, all things considered. Curr Opin Plant Biol 7:547–552PubMedCrossRefGoogle Scholar
  21. Dong X, Mindrinos M, Davis KR, Ausubel FM (1991) Induction of Arabidopsis defense genes by virulent and avirulent Pseudomonas syringae strains and by a cloned avirulence gene. Plant Cell 3:61–72PubMedGoogle Scholar
  22. Dow M, Newman MA, von Roepenack E (2000) The induction and modulation of plant defense responses by bacterial lipopolysaccharides. Annu Rev Phytopathol 38:241–261PubMedCrossRefGoogle Scholar
  23. Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209PubMedCrossRefGoogle Scholar
  24. Euglem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371CrossRefGoogle Scholar
  25. Farmer EE, Almeeras E, Krishnamurthy V (2003) Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr Opin Plant Biol 6:372–378PubMedCrossRefGoogle Scholar
  26. Felix G, Duran JD, Volko S, Boller T (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18:265–276PubMedCrossRefGoogle Scholar
  27. Feys BJ, Wiermer M, Bhat RA, Moisan LJ, Medina-Escobar N, Neu C, Cabral A, Parker JE (2005) Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. Plant Cell 17:2601–2613PubMedCrossRefGoogle Scholar
  28. Finlay BB, McFadden G (2006) Anti-immunology: evasion of the host immune system by bacterial and viral pathogens. Cell 124:767–782PubMedCrossRefGoogle Scholar
  29. Flor HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275–296CrossRefGoogle Scholar
  30. Frye CA, Tang D, Innes RW (2000) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc Nat Acad Sci USA 98:373–378CrossRefGoogle Scholar
  31. Glazebrook J (2001) Genes controlling expression of defense responses in Arabidopsis: 2001 status. Curr Opin Plant Biol 4:301–308PubMedCrossRefGoogle Scholar
  32. Göhre V, Robatzek S (2008) Breaking the barriers: microbial effector molecules subvert plant immunity. Annu Rev Phytopathol 46:189–215PubMedCrossRefGoogle Scholar
  33. Gómez-Gómez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011PubMedCrossRefGoogle Scholar
  34. Gómez-Gómez L, Boller T (2002) Flagellin perception: a paradigm for innate immunity. Trends Plant Sci 7:251–256PubMedCrossRefGoogle Scholar
  35. Gómez-Gómez L, Bauer Z, Boller T (2001) Both the extracellular leucine-rich repeat domain and the kinase activity of FSL2 are required for flagellin binding and signaling in Arabidopsis. Plant Cell 13:1155–1163PubMedGoogle Scholar
  36. He P, Shan L, Lin N-C, Martin GB, Kemmerling B, Nürnberger T, Sheen J (2006) Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125:563–575PubMedCrossRefGoogle Scholar
  37. Hesse A, Hann DR, Simenes-Ibanez S, Jones AM, He K, Li J, Schroeder JI, Peck SC, Rathjen JP (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Nat Acad Sci USA 104:12217–12222CrossRefGoogle Scholar
  38. Holub EB (2001) The arms race is ancient history in Arabidopsis, the wildflower. Nat Rev Gen 2:516–527CrossRefGoogle Scholar
  39. Janjusevic R, Abramovitch RB, Martin G, Stebbins CE (2006) A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase. Science 311:222–226PubMedCrossRefGoogle Scholar
  40. Jin Q, He S-Y (2001) Role of the Hrp pilus in type III protein secretion in Pseudomonas syringae. Science 294: 2556–2558PubMedCrossRefGoogle Scholar
  41. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329PubMedCrossRefGoogle Scholar
  42. Judelson HS, Blanco FA (2005) The spores of Phytophthora: weapons of the plant destroyer. Nat Rev Microbiol 3:47–58PubMedCrossRefGoogle Scholar
  43. Katagiri F, Thilmony R, He S-Y (2002) The Arabidopsis thalianaPseudomonas syringae interaction. In: The Arabidopsis book. American Society of Plant Biologists, Rockville (available via DIALOG; www.aspb.org/publications/arabidopsis, cited 30 Sept 2002)
  44. Kay S, Hahn S, Marois E, Hause G, Bonas U (2007) A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318:648–651PubMedCrossRefGoogle Scholar
  45. Kim HS, Desveaux D, Singer AU, Patel P, Sondek J, Dangl JL (2005) The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation. Proc Nat Acad Sci USA 102:6496–6501PubMedCrossRefGoogle Scholar
  46. Kobe B, Deisenhofer J (1995) Proteins with leucine-rich repeats. Curr Opin Struct Biol 5:409–416PubMedCrossRefGoogle Scholar
  47. Li X, Zhang Y, Clarke JD, Li Y, Dong X (1999) Identification and cloning of a negative regulator of systemic acquire resistance, SNI1, through a screen for suppressors of NPR1-1. Cell 98:329–339PubMedCrossRefGoogle Scholar
  48. Li X, Clark JD, Zhang Y, Dong X (2001) Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance. Mol Plant Microbe Interact 14:1131–1139PubMedCrossRefGoogle Scholar
  49. Mackey D, Holt BF III, Wiig A, Dangl JL (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:743–754PubMedCrossRefGoogle Scholar
  50. Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Staskawicz BJ (2003) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 7:379–389CrossRefGoogle Scholar
  51. Marathe R, Dinesh-Kumar SP (2003) Plant defense: one post, multiple guards?! Mol Cell 11:284–286PubMedCrossRefGoogle Scholar
  52. Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu T, Earle ED, Tanksley SD (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432–1436PubMedCrossRefGoogle Scholar
  53. Martin GB, Bogdanove AJ, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 54:23–61PubMedCrossRefGoogle Scholar
  54. McDowell JM, Cuzick A, Can C, Beyon J, Dangl JL, Holub EB (2000) Downy mildew (Peronospora parasitica) resistance genes in Arabidopsis vary in functional requirements for NDR1, EDS1, NPR1, and salicylic acid accumulation. Plant J 22:523–529PubMedCrossRefGoogle Scholar
  55. Menke FL, Van Pelt JA, Pieterse CM, Klessig DF (2004) Silencing of the mitogen-activated protein kinase MPK6 compromises disease resistance in Arabidopsis. Plant Cell 16:897–907PubMedCrossRefGoogle Scholar
  56. Moffett P, Farnham G, Peart J, Baulcombe DC (2002) Interaction between domains of a plant NBS-LRR protein in disease resistance-related cell death. EMBO J 21:4511–4519PubMedCrossRefGoogle Scholar
  57. Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944PubMedCrossRefGoogle Scholar
  58. Mucyn TS, Clemente A, Andriotis VM, Balmuth AL, Oldroyd GE, Staskawicz BJ, Rathjen JP (2006) The tomato NBARC-LRR protein Prf interacts with Pto kinase in vivo to regulate specific plant immunity. Plant Cell 18:2792–2806PubMedCrossRefGoogle Scholar
  59. Nakagami H, Pitzschke A, Hirt H (2005) Emerging MAP kinase pathways in plant stress signaling. Trends Plant Sci 10:339–346PubMedCrossRefGoogle Scholar
  60. Nawrath C, Métraux J-P (1999) Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11:1393–1404PubMedGoogle Scholar
  61. Nawrath C, Heck S, Parinthawong N, Métraux J-P (2002) EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell 14:275–286PubMedCrossRefGoogle Scholar
  62. Noël LD, Cagna G, Stuttmann J, Wirthmüler L, Betsuyaku S, Witte CP, Bhat R, Pochon N, Colby T, Parker JE (2007) Interaction between SGT1 and cytosolic/nuclear HSC70 chaperones regulates Arabidopsis immune responses. Plant Cell 19:4061–4076PubMedCrossRefGoogle Scholar
  63. Nürnberger T, Brunner F, Kemmerling B, Piater L (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198:249–266PubMedCrossRefGoogle Scholar
  64. Palma K, Zhao Q, Cheng Y, Bi D, Monaghan J, Cheng W, Zhang Y, Li X (2007) Regulation of plant innate immunity by three proteins in a complex conserved across the plant and animal kingdoms. Genes Dev 21:1484–1493PubMedCrossRefGoogle Scholar
  65. Petersen M, Brodersen A, Naested H, Andreasson E, Lindhart U, Johansen B, Nielsen HB, Lacy M, Austin MJ, Parker JE, Sharma SB, Klessig DF, Martienssen R, Mattsson O, Jensen AB, Mundy J (2000) Arabidopsis MAP Kinase 4 negatively regulates systemic acquired resistance. Cell 103:111–1120CrossRefGoogle Scholar
  66. Rivas S, Thomas CM (2005) Molecular interactions between tomato and the leaf mold pathogen Cladosporium fulvum. Annu Rev Phytopathol 43:395–436PubMedCrossRefGoogle Scholar
  67. Robatzek S, Chinchilla D, Boller T (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev 20:537–542PubMedCrossRefGoogle Scholar
  68. Schilmiller AL, Howe GA (2005) Systemic signaling in the wound response. Curr Opin Plant Biol 8:369–377PubMedCrossRefGoogle Scholar
  69. Seo Y-S, Lee S-K, Song M-Y, Suh J-P, Han T-R, Ronald P, Jeon J-S (2008) The HSP90-SCT1-RAR1 molecular chaperone complex: a core modulator in plant immunity. J Plant Biol 51:1–10CrossRefGoogle Scholar
  70. Shan L, He P, Sheen J (2007) Intercepting host MAPK signaling cascades by bacterial type III effectors. Cell Host Microbe 1:167–174PubMedCrossRefGoogle Scholar
  71. Shen Q-H, Saijo Y, Mauch S, Christoph B, Bieri S, Beat K, Hikary S, Üker B, Somssich IE, Schulze-Lefert P (2007) Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315:1098–1103PubMedCrossRefGoogle Scholar
  72. Shirano Y, Kachroo P, Shah J, Klessig DF (2002) A gain-of-function mutation in an Arabidopsis Toll-Interleukin1 receptor-nucleotide binding site-leucine-rich repeat type R gene triggers defense responses and results in enhanced disease resistance. Plant Cell 14:3149–3162PubMedCrossRefGoogle Scholar
  73. Shirasu K, Schulze-Lefert P (2003) Complex formation, promiscuity and multi-functionality: protein interactions in disease-resistance pathways. Trends Plant Sci 8:252–258PubMedCrossRefGoogle Scholar
  74. Slusarenko AJ, Schlaich NL (2003) Pathogen profile: downy mildew of Arabidopsis thaliana caused by Hyaloperonospora parasitica (formerly Peronospora parasitica). Mol Plant Pathol 4:159–170PubMedCrossRefGoogle Scholar
  75. Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, Gardner J, Wang B, Zhai WX, Zhu LH, Fauquet C, Ronald P (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–1806PubMedCrossRefGoogle Scholar
  76. Suarez-Rodriguez MC, Adams-Phillips L, Liu Y, Wang H, Su S-H, Jester PJ, Zhang S, Bent AF, Krysan PJ (2006) MEKK1 is required for flg22-induced MPK4 activation in Arabidopsis plants. Plant Physiol 143:661–669PubMedCrossRefGoogle Scholar
  77. Takeda K, Kaisho T, Akira S (2003) Toll-like receptors. Annu Rev Immunol 21:335–376PubMedCrossRefGoogle Scholar
  78. Takken FLW, Albrecht M, Tameling WIL (2006) Resistance proteins: molecular switches of plant defence. Curr Opin Plant Biol 9:1–8CrossRefGoogle Scholar
  79. Tameling WIL, Vossen JH, Albrecht M, Lengauer T, Berden JA, Haring MA, Cornelissen BJC, Takken FLW (2006) Mutations in the NB-ARC domain of I-2 that impair ATP hydrolysis cause autoactivation. Plant Physiol 140:1233–1245PubMedCrossRefGoogle Scholar
  80. Tang X, Frederick RD, Zhou J, Halterman DA, Jia Y, Martin GB (1996) Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274:2060–2063PubMedCrossRefGoogle Scholar
  81. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815CrossRefGoogle Scholar
  82. Thordal-Christensen H (2003) Fresh insights into processes of nonhost resistance. Curr Opin Plant Biol 6:351–357PubMedCrossRefGoogle Scholar
  83. Ülker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 7:491–498PubMedCrossRefGoogle Scholar
  84. Van Der Biezen EA, Jones JDG (1998) Plant disease resistance proteins and the gene-for-gene concept. Trends Biochem Sci 23:454–456PubMedCrossRefGoogle Scholar
  85. Whalen MC, Innes RW, Bent AF, Staskawicz BJ (1991) Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell 2:49–59Google Scholar
  86. Wiermer M, Feys BJ, Parker JE (2005) Plant immunity: the EDS1 regulatory node. Curr Opin Plant Biol 8:383–389PubMedCrossRefGoogle Scholar
  87. Wiermer M, Palma K, Zhang Y, Li X (2007) Should I stay or should I go? Nucleocytoplasmic trafficking in plant innate immunity. Cell Microbiol 9:1880–1890PubMedCrossRefGoogle Scholar
  88. Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565PubMedCrossRefGoogle Scholar
  89. Wirthmueller L, Zhang Y, Jones JDG, Parker JE (2007) Nuclear accumulation of the Arabidopsis immune receptor RPS4 is necessary for triggering EDS1-dependent defense. Curr Biol 17:2023–2029PubMedCrossRefGoogle Scholar
  90. Xiang T, Zong N, Zou Y, Wu Y, Zhang J, Xing W, Li Y, Tang X, Zhu L, Chai J, Zhou JM (2008) Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol 18:74–80PubMedCrossRefGoogle Scholar
  91. Xiao S, Ellwood S, Calis O, Patrick E, Li T, Coleman M, Turner JG (2001) Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science 291:118–120PubMedCrossRefGoogle Scholar
  92. Xing W, Zou Y, Liu Q, Liu J, Luo X, Huang Q, Chen S, Zhu L, Bi R, Hao Q, Wu J-W, Zhou J-M, Chai J (2007) The structural basis for activation of plant immunity by bacterial effector protein AvrPto. Nature 449:243–247PubMedCrossRefGoogle Scholar
  93. Zhang Y, Goritschnig S, Dong X, Li X (2003a) A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1–1, constitutive 1. Plant Cell 15:2636–2646CrossRefGoogle Scholar
  94. Zhang Y, Tessaro MJ, Lassner M, Li X (2003b) Knockout analysis of Arabidopsis transcription factors TGA2, TGA5, and TGA6 reveals their redundant and essential roles in systemic acquired resistance. Plant Cell 15:2647–2653CrossRefGoogle Scholar
  95. Zhou J-M, Chai J (2008) Plant pathogenic bacterial type III effectors subdue host responses. Curr Opin Microbiol 11:179–185PubMedCrossRefGoogle Scholar
  96. Zipfel C (2008) Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol 20:10–16PubMedCrossRefGoogle Scholar
  97. Zipfel C, Rathjen JP (2008) Plant immunity: AvrPto targets the frontline. Curr Opin Plant Biol 18:R218–R220Google Scholar
  98. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JDG, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–767PubMedCrossRefGoogle Scholar
  99. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JDG, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–760PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2009

Authors and Affiliations

  1. 1.Michael Smith LaboratoriesUniversity of British ColumbiaVancouverCanada
  2. 2.Department of BotanyUniversity of British ColumbiaVancouverCanada

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