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Plant pathogens and integrated defence responses to infection

Abstract

Plants cannot move to escape environmental challenges. Biotic stresses result from a battery of potential pathogens: fungi, bacteria, nematodes and insects intercept the photosynthate produced by plants, and viruses use replication machinery at the host's expense. Plants, in turn, have evolved sophisticated mechanisms to perceive such attacks, and to translate that perception into an adaptive response. Here, we review the current knowledge of recognition-dependent disease resistance in plants. We include a few crucial concepts to compare and contrast plant innate immunity with that more commonly associated with animals. There are appreciable differences, but also surprising parallels.

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Figure 1: Representation of the location and structure of the five main classes of plant disease resistance proteins.
Figure 2: Comparison of R proteins with proteins involved in cell death in animal cells.
Figure 3: Comparison of R proteins with proteins involved in animal innate immunity.
Figure 4: R-gene monoculture and R-gene polycultures.
Figure 5: The guard hypothesis for R-protein function.

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References

  1. Flor, H. H. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9, 275–296 (1971).

    Article  Google Scholar 

  2. Glazebrook, J., Rogers, E. E. & Ausubel, F. M. Use of Arabidopsis for genetic dissection of plant defense responses. Annu. Rev. Genet. 31, 547–569 (1997).

    Article  CAS  PubMed  Google Scholar 

  3. Yang, Y., Shah, J. & Klessig, D. F. Signal perception and transduction in plant defense responses. Genes Dev. 11, 1621–1639 (1997).

    Article  CAS  PubMed  Google Scholar 

  4. McDowell, J. M. & Dangl, J. L. Signal transduction in the plant innate immune response. Trends Biochem. Sci. 25, 79–82 (2000).

    Article  CAS  PubMed  Google Scholar 

  5. Bent, A. Function meets structure in the study of plant disease resistance genes. Plant Cell 8, 1757–1771 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Ellis, J., Dodds, P. & Pryor, T. Structure, function, and evolution of plant disease resistance genes. Curr. Opin. Plant Biol. 3, 278–284 (2000).

    Article  CAS  PubMed  Google Scholar 

  7. Jones, J. D. G. Putting knowledge of plant disease resistance genes to work. Curr. Opin. Plant Biol. (in the press).

  8. Boyes, D. C., Nam, J. & Dangl, J. L. The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response. Proc. Natl Acad. Sci. USA 95, 15849–15854 (1998).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  9. Jones, D. A. & Jones, J. D. G. The roles of leucine rich repeats in plant defences. Adv. Bot. Res. Adv. Plant Pathol. 24, 90–167 (1996).

    Google Scholar 

  10. Kajava, A. V. Structural diversity of leucine-rich repeat proteins. J. Mol. Biol. 277, 519–527 (1998).

    Article  CAS  PubMed  Google Scholar 

  11. Saraste, M., Sibbald, P. R. & Wittinghofer, A. The P-loop - a common motif in ATP- and GTP-binding proteins. Trends Biotechnol. 15, 430–435 (1990).

    Google Scholar 

  12. Aravind, L., Dixit, V. M. & Koonin, E. V. The domains of death: evolution of the apoptosis machinery. Trends Biochem. 24, 47–53 (1999).

    Article  CAS  Google Scholar 

  13. van der Biezen, E. A. & Jones, J. D. G. Homologies between plant resistance gene products and regulators of cell death in animals. Current Biol. 8, R226–R227 (1998).

    Article  CAS  Google Scholar 

  14. Parniske, M. et al. Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell 91, 821–832 (1997).

    Article  CAS  PubMed  Google Scholar 

  15. McDowell, J. M. et al. Intragenic recombination and diversifying selection contribute to the evolution of Downy Mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell 10, 1861–1874 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Botella, M. A. et al. Three genes of the Arabidopsis RPP1 complex resistance locus recognize distinct Peronospora parasitica avirulence determinants. Plant Cell 10, 1847–1860 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Meyers, B. C. et al. The major resistance gene cluster in lettuce is highly duplicated and spans several megabases. Plant Cell 10, 1817–1832 (1998).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  18. Michelmore, R. W. & Meyers, B. C. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 8, 1113–1130 (1998).

    Article  CAS  PubMed  Google Scholar 

  19. Wang, G.-L. et al. Xa21D encodes a receptor-like molecule with a leucine-rich repeat domain that determines race-specific recognition and is subject to adaptive evolution. Plant Cell 10, 765–779 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Ellis, J. G., Lawrence, G. J., Luck, J. E. & Dodds, P. N. Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 11, 495–506 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Wulff, B. B. H., Thomas, C. M., Smoker, M., Grant, M. & Jones, J. D. G. Domain swapping and gene shuffling identify specificity determinants required for induction of an Avr-dependent hypersensitive response by the tomato Cf-4 and Cf-9 proteins. Plant Cell 13, 255–272 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Van der Hoorn, R. A. L., Roth, R. & De Wit, P. J. G. M. Identification of distinct specificity determinants in resistance protein Cf-4 allows construction of a Cf-9 mutant that confers recognition of avirulence protein AVR4. Plant Cell 13, 273–285 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Luck, J. E., Lawrence, G. J., Dodds, P. N., Shepherd, K. W. & Ellis, J. G. Regions outside of the leucine-rich repeats of Flax Rust resistance proteins play a role in specificity determination. Plant Cell 12, 1367–1377 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Initiative, T. A. G. Analysis of the genome of the flowering plant Arabidopsis thaliana . Nature 408, 796–815 (2000).

    Article  ADS  Google Scholar 

  25. Bisgrove, S. R., Simonich, M. T., Smith, N. M., Sattler, N. M. & Innes, R. W. A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell 6, 927–933 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Grant, M. R. et al. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269, 843–846 (1995).

    Article  ADS  CAS  PubMed  Google Scholar 

  27. Rossi, M. et al. The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc. Natl Acad. Sci. USA 95, 9570–9754 (1998).

    Article  Google Scholar 

  28. Cooley, M. B., Pathirana, S., Wu, H.-J., Kachroo, P. & Klessig, D. F. Members of the Arabidopsis HRT/RPP8 family of resistance genes confer resistance to both viral and oomycete pathogens. Plant Cell 12, 663–676 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. van der Vossen, E. A. et al. Homologues of a single resistance-gene cluster in potato confer resistance to distinct pathogens: a virus and a nematode. Plant J. 23, 567–576 (2000).

    Article  CAS  PubMed  Google Scholar 

  30. Stahl, E. A., Dwyer, G., Mauricio, R., Kreitman, M. & Bergelson, J. Dynamics of disease resistance polymorphism at the RPM1 locus of Arabidopsis . Nature 400, 667–671 (1999).

    Article  ADS  CAS  PubMed  Google Scholar 

  31. Riely, B. K. & Martin, G. B. Ancient origin of pathogen recognition specificity conferred by the tomato disease resistance gene Pto. Proc. Natl Acad. Sci. USA 98, 2059–2064 (2001).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  32. Dangl, J. L. in Bacterial Pathogenesis of Plants and Animals: Molecular and Cellular Mechanisms (ed. Dangl, J. L.) 99–118 (Springer, Heidelberg, 1994).

    Book  Google Scholar 

  33. Medzhitov, R. et al. MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol. Cell 2, 253–258 (1998).

    Article  CAS  PubMed  Google Scholar 

  34. Dinesh-Kumar, S. P. & Baker, B. J. Alternatively spliced N resistance gene transcripts: their possible role in tobacco mosaic virus resistance. Proc. Natl Acad. Sci. USA 97, 1908–1913 (2000).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  35. Eulgem, T., Rushton, P. J., Robatzek, S. & Somssich, I. E. The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5, 199–206 (2000).

    Article  CAS  PubMed  Google Scholar 

  36. Grant, M. R. et al. Independent deletions of a pathogen-resistance gene in Brassica and Arabidopsis . Proc. Natl Acad. Sci. USA 95, 15843–15848 (1998).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  37. Xiao, S. et al. Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8 . Science 291, 118–120 (2001).

    Article  ADS  CAS  PubMed  Google Scholar 

  38. Noël, L. et al. Pronounced intraspecific haplotype divergence at the RPP8 complex disease resistance locus of Arabidopsis. Plant Cell 11, 2099–2111 (1999).

    Article  PubMed  PubMed Central  Google Scholar 

  39. Scofield, S. R. et al. Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science 274, 2063–2065 (1996).

    Article  ADS  CAS  PubMed  Google Scholar 

  40. Tang, X. et al. Physical interaction of avrPto and the Pto kinase defines a recognition event involved in plant disease resistance. Science 274, 2060–2063 (1996).

    Article  ADS  CAS  PubMed  Google Scholar 

  41. Salmeron, J. M. et al. Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell 86, 123–133 (1996).

    Article  CAS  PubMed  Google Scholar 

  42. Song, W.-Y. et al. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21 . Science 270, 1804–1806 (1995).

    Article  ADS  CAS  PubMed  Google Scholar 

  43. He, Z. et al. Perception of Brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science 288, 2360–2363 (2000).

    Article  ADS  CAS  PubMed  Google Scholar 

  44. Wang, Z.-Y., Seto, H., Fujioka, S., Yoshida, S. & Chory, J. BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410, 380–383 (2001).

    Article  ADS  CAS  PubMed  Google Scholar 

  45. Jones, D. A., Thomas, C. M., Hammond-Kosack, K. E., Balint-Kurti, P. J. & Jones, J. D. G. Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266, 789–793 (1994).

    Article  ADS  CAS  PubMed  Google Scholar 

  46. Trotochaud, A. E., Hao, T., Wu, G., Yang, Z. & Clark, S. E. The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rho-related protein. Plant Cell 11, 393–405 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Gómez-Gómez, L. & Boller, T. FLS2: an LRR receptor like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5, 1003–1011 (2000).

    Article  PubMed  Google Scholar 

  48. Swiderski, M. R. & Innes, R. W. The Arabidopsis PBS1 resistance gene encodes a member of a novel protein kinase subfamily. Plant J. 26, 101–112 (2001).

    Article  CAS  PubMed  Google Scholar 

  49. Aderem, A. & Ulevitch, R. J. Toll-like receptors in the induction of the innate immune response. Nature 406, 782–787 (2000).

    Article  CAS  PubMed  Google Scholar 

  50. Medzhitov, R. & Janeway, C. Jr The Toll receptor family and microbial recognition. Trends Microbiol. 8, 452–456 (2000).

    Article  CAS  PubMed  Google Scholar 

  51. Ozinsky, A. et al. The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between Toll-like receptors. Proc. Natl Acad. Sci. USA 97, 13766–13771 (2000).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  52. Inohara, N., Ogura, Y., Chen, F. & Nunez, G. Human Nod1 confers responsiveness to bacterial lipopolysaccharides. J. Biol. Chem. 276, 2551–2554 (2001).

    Article  CAS  PubMed  Google Scholar 

  53. Ogura, Y. et al. Nod2, a Nod1/Apaf-1 family member that is restricted to monocytes and activates NF-κB. J. Biol. Chem. 276, 4812–4818 (2001).

    Article  CAS  PubMed  Google Scholar 

  54. Hugot, J.-P. et al. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 411, 599–603 (2001).

    Article  ADS  CAS  PubMed  Google Scholar 

  55. Ogura, Y. et al. A frameshift in Nod2 associated with susceptibility to Crohn's disease. Nature 411, 603–606 (2001).

    Article  ADS  CAS  PubMed  Google Scholar 

  56. Hartman, J. L. IV Garvik, B. & Hartwell, L. Principles for the buffering of genetic variation. Science 291, 1001–1004 (2001).

    Article  ADS  CAS  PubMed  Google Scholar 

  57. Hamilton, W. D., Axelrod, R. & Tanese, R. Sexual reproduction as an adaptation to resist parasites. Proc. Natl Acad. Sci. USA 87, 3566–3573 (1990).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  58. Gálan, J. E. & Collmer, A. Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284, 1322–1328 (1999).

    Article  ADS  PubMed  Google Scholar 

  59. Hueck, C. J. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62, 379–433 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Kjemtrup, S., Nimchuk, Z. & Dangl, J. L. Effector proteins of phytopathogenic bacteria: bifunctional signals in virulence and host recognition. Curr. Opin. Microbiol. 3, 73–78 (2000).

    Article  CAS  PubMed  Google Scholar 

  61. Gopalan, S. et al. Expression of the Pseudomonas syringae avirulence protein AvrB in plant cells alleviates its dependence on the hypersensitive response and pathogenicity (Hrp) secretion system in eliciting genotype-specific hypersensitive cell death. Plant Cell 8, 1095–1105 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. McNellis, T. W. et al. Glucocorticoid-inducible expression of a bacterial avirulence gene in transgenic Arabidopsis thaliana induces hypersensitive cell death. Plant J. 14, 247–258 (1998).

    Article  CAS  PubMed  Google Scholar 

  63. Nimchuk, Z. et al. Eukaryotic fatty acylation drives plasma membrane targeting and enhances function of several Type III effector proteins from Pseudomonas syringae . Cell 101, 353–363 (2000).

    Article  CAS  PubMed  Google Scholar 

  64. Mudgett, M. & Staskawicz, B. Characterization of the Pseudomonas syringae pv. tomato AvrRpt2 protein: demonstration of secretion and processing during bacterial pathogenesis. Mol. Microbiol. 32, 927–941 (1999).

    Article  CAS  PubMed  Google Scholar 

  65. Nimchuk, Z., Rohmer, L., Chang, J. H. & Dangl, J. L. Knowing the dancer from the dance: R gene products and their interactions with other proteins from host and pathogen. Curr. Opin. Plant Biol. (in the press).

  66. Laugé, R., Joosten, M. H. A., Van den Ackerveken, G. F. J. M., Van den Broek, H. W. J. & De Wit, P. J. G. M. The in-planta produced extracellular proteins ECP1 and ECP2 of Cladosporium fulvum are virulence factors. Mol. Plant-Microbe Interact. 10, 725–734 (1997).

    Article  Google Scholar 

  67. Laugé, R. et al. Successful search for a resistance gene in tomato targeted against a virulence factor of a fungal pathogen. Proc. Natl Acad. Sci. USA 95, 9014–9018 (1998).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  68. Laugé, R., Dmitriev, A. P., Joosten, M. H. A. J. & De Wit, P. G. J. M. Additional resistance gene(s) against Cladosporium fulvum present on the Cf-9 introgression segment are associated with strong PR protein accumulation. Mol. Plant-Microbe Interact. 11, 301–308 (1998).

    Article  Google Scholar 

  69. Lauge, R., Goodwin, P. H., de Wit, P. J. & Joosten, M. H. Specific HR-associated recognition of secreted proteins from Cladosporium fulvum occurs in both host and non-host plants. Plant J. 23, 735–745 (2000).

    Article  CAS  PubMed  Google Scholar 

  70. Kooman-Gersman, M., Honée, G., Bonnema, G. & De Wit, P. J. G. M. A high-affinity binding site for the AVR9 peptide elicitor of Cladosporium fulvum is present on plasma membranes of tomato and other Solanaceous plants. Plant Cell 8, 929–938 (1996).

    Article  Google Scholar 

  71. Bryan, G. T. et al. A single amino acid difference distinguishes resistant and susceptible alleles of the rice resistance gene Pi-ta . Plant Cell 12, 2033–2045 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. van der Biezen, E. A. & Jones, J. D. G. Plant disease resistance proteins and the “gene-for-gene” concept. Trends Biochem. Sci. 23, 454–456 (1998).

    Article  CAS  PubMed  Google Scholar 

  73. Oldroyd, G. E. D. & Staskawicz, B. J. Genetically engineered broad-spectrum disease resistance in tomato. Proc. Natl Acad. Sci. USA 95, 10300–10305 (1998).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  74. Chen, Z., Kloek, A. P., Boch, J., Katagiri, F. & Kunkel, B. N. The pseudomonas syringae avrRpt2 gene product promotes pathogenicity from inside the plant cell. Mol. Plant Pathol. 13, 1312–1321 (2000).

    CAS  Google Scholar 

  75. Ren, T., Qu, F. & Morris, T. J. HRT gene function requires interaction between a NAC protein and viral capsid protein to confer resistance to Turnip Crinkle Virus. Plant Cell 12, 1917–1925 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Ritter, C. & Dangl, J. L. Interference between two specific pathogen recognition events mediated by distinct plant disease resistance genes. Plant Cell 8, 251–257 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Reuber, T. L. et al. Correlation of defense gene induction defects with powdery mildew susceptibility in Arabidopsis enhanced disease susceptibility mutants. Plant J. 16, 473–485 (1998).

    Article  CAS  PubMed  Google Scholar 

  78. Leister, R. T. & Katagiri, F. A resistance gene product of the nucleotide binding site-leucine rich repeats class can form a complex with bacterial avirulence proteins in vitro . Plant J. 22, 345–354 (2000).

    Article  CAS  PubMed  Google Scholar 

  79. Dixon, M. S., Golstein, C., Thomas, C. M., van Der Biezen, E. A. & Jones, J. D. Genetic complexity of pathogen perception by plants: the example of Rcr3, a tomato gene required specifically by Cf-2. Proc. Natl Acad. Sci. USA 97, 8807–8814 (2000).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  80. Glazebrook, J. Genes controlling expression of defense responses in Arabidopsis - 2001 status. Curr. Opin. Plant Biol. (in the press).

  81. Jorgensen, J. H. Genetic analysis of barley mutants with modifications of the powdery mildew resistance gene Mla 12 . Genome 30, 129–132 (1988).

    Article  Google Scholar 

  82. Century, K. S., Holub, E. B. & Staskawicz, B. J. NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. Proc. Natl Acad. Sci. USA 92, 6597–6601 (1995).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  83. Parker, J. E. et al. Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell 8, 2033–2046 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Aarts, N. et al. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene mediated signalling pathways in Arabidopsis. Proc. Natl Acad. Sci. USA 95, 10306–10311 (1998).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  85. McDowell, J. M. et al. Downy mildew (Peronospora parasitica) resistance genes in Arabidopsis vary in functional requirements for NDR1, EDS1, NPR1, and Salicylic Acid accumulation. Plant J. 22, 523–530 (2000).

    Article  CAS  PubMed  Google Scholar 

  86. Freialdenhoven, A. et al. Nar-1 and Nar-2, two loci required for Mla-12-specified race resistance to powdery mildew in barley. Plant Cell 6, 983–994 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Zhou, F. et al. Cell-autonomous expression of barley Mla1confers race specific resistance to the powdery mildew fungus via a Rar1 independent signaling pathway. Plant Cell 13, 337–350 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Halterman, D., Zhou, F., Wei, F., Wise, R. P. & Schulze-Lefert, P. The Mla6 coiled-coil, NBS-LRR protein functions in barley and wheat to confer resistance specificity to Blumeria graminis f. sp. hordei. Plant J. (in the press).

  89. Kitigawa, K., Skowyra, D., Elledge, S. J., Harper, J. W. & Hieter, P. SGT1 encodes an essential component of the yeast kinetochore assembly pathway and a novel subunit of the SCF ubiquitin complex. Mol. Cell 4, 21–33 (1999).

    Article  Google Scholar 

  90. Jabs, T., Colling, C., Tschöpe, M., Hahlbrock, K. & Scheel, D. Elicitor-stimulated ion fluxes and reactive oxygen species from the oxidative burst signal defense gene activation and phytoalexin synthesis in parsley. Proc. Natl Acad. Sci. USA 94, 4800–4805 (1997).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  91. Felix, G., Duran, J. D., Volko, S. & Boller, T. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18, 265–276 (1999).

    Article  CAS  PubMed  Google Scholar 

  92. Piedras, P., Hammond-Kosack, K. E., Harrison, K. & Jones, J. D. G. Rapid, Cf-9 and Avr9 dependent, production of active oxygen species in tobacco suspension cultures. Mol. Plant-Microbe Interact. 11, 1155–1166 (1998).

    Article  CAS  Google Scholar 

  93. Ligternik, W., Kroj, T., zur Nieden, U., Hirt, H. & Scheel, D. Receptor-mediated activation of a MAP kinase in pathogen defense of plants. Science 276, 2054–2057 (1997).

    Article  Google Scholar 

  94. Romeis, T. et al. Rapid, Avr9- and Cf-9-dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound and salicylate responses. Plant Cell 11, 273–287 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Grant, M. et al. The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J. 23, 441–450 (2000).

    Article  ADS  CAS  PubMed  Google Scholar 

  96. Durner, J., Wendehenne, D. & Klessig, D. F. Defense gene induction in tobacco by nitric oxide, cyclic GMP and cyclic ADP ribose. Proc. Natl Acad. Sci. USA 95, 10328–10333 (1998).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  97. Delledonne, M., Xia, Y., Dixon, R. A. & Lamb, C. J. Nitric oxide functions as a signal in plant disease resistance. Nature 394, 585–588 (1998).

    Article  ADS  CAS  PubMed  Google Scholar 

  98. Delledonne, M., Zeier, J., Marocco, A. & Lamb, C. J. Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc. Natl Acad. Sci. USA (in the press).

  99. Durrant, W. E., Rowland, O., Piedras, P., Hammond-Kossak, K. E. & Jones, J. D. G. cDNA-AFLP reveals a striking overlap in the race-specific resistance and wound response expression profiles. Plant Cell 12, 963–977 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Dröge-Laser, W. et al. Rapid stimulation of a soybean protein serine-threonine kinase which phosphorylates a novel bZIP DNA-binding protein, G/HBF-1, during the induction of early transcription-dependent defenses. EMBO J. 16, 726–738 (1997).

    Article  PubMed  PubMed Central  Google Scholar 

  101. Scheel, D. Resistance response physiology and signal transduction. Curr. Opin. Plant Biol. 1, 305–310 (1998).

    Article  CAS  PubMed  Google Scholar 

  102. Delaney, T. P. Genetic dissection of acquired resistance to disease. Plant Physiol. 113, 5–12 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Gaffney, T. et al. Requirement for salicylic acid for the induction of systemic acquired resistance. Science 261, 754–756 (1993).

    Article  ADS  CAS  PubMed  Google Scholar 

  104. Nawrath, C. & Métraux, J.-P. Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen attack. Plant Cell 11, 1393–1404 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  105. Cao, H., Glazebrook, J., Clark, J. D., Volko, S. & Dong, X. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88, 57–64 (1997).

    Article  CAS  PubMed  Google Scholar 

  106. Ryals, J. et al. The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor IκB. Plant Cell 9, 425–439 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  107. Clarke, J. D., Volko, S. M., Ledford, H., Ausubel, F. M. & Dong, X. Roles of salicylic acid, jasmonic acid, and ethylene in cpr-induced resistance in Arabidopsis. Plant Cell 12, 2175–2190 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Reymond, P. & Farmer, E. E. Jasmonate and salicylate as global signals for defense gene expression. Curr. Opin. Plant Biol. 1, 404–411 (1998).

    Article  CAS  PubMed  Google Scholar 

  109. Reymond, P., Weber, H., Damond, M. & Farmer, E. E. Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12, 707–719 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Maleck, K. et al. The transcriptome of Arabidopsis during systemic acquired resistance. Nature Genet. 26, 403–410 (2000).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Work in the Dangl laboratory is supported by grants from the NSF, NIH, DOE, USDA-NRI and Syngenta. The Jones laboratory is supported by the Gatsby Charitable Trust and the BBSRC. We thank P. Epple, T. Eulgem, J. McDowell, S. Peck, J. Rathjen and B. Staskawicz for critical reading of this manuscript, and G. Nuñez and D. Golenbock for useful suggestions.

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Dangl, J., Jones, J. Plant pathogens and integrated defence responses to infection. Nature 411, 826–833 (2001). https://doi.org/10.1038/35081161

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