Host-microbe interactions: Shaping the evolution of the plant immune response

Cell

Volumn 124, Issue 4, 2006, Pages 803-814

  Chisholm, Stephen T ^a,b   Coaker, Gitta ^a   Day, Brad ^a,c   Staskawicz, Brian J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Department of Environmental and Radiological Health Sciences   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; BACTERIAL PROTEIN; FLAGELLIN; LEUCINE; MITOGEN ACTIVATED PROTEIN KINASE; NUCLEOTIDE BINDING PROTEIN; PHOSPHOTRANSFERASE; PROTEIN; PROTEIN SUBUNIT; TOLL LIKE RECEPTOR 1; VEGETABLE PROTEIN;

ARABIDOPSIS; BACTERIAL GENOME; BACTERIAL VIRULENCE; DNA SEQUENCE; ENZYME ACTIVITY; FLAGELLUM; FUNGAL STRAIN; GENE; GENETIC RESISTANCE; HOST CELL; HOST RESISTANCE; IMMUNE RESPONSE; INNATE IMMUNITY; MICROBIAL GROWTH; MICROBIAL IMMUNITY; MICROORGANISM DETECTION; NONHUMAN; OOMYCETES; PHENOTYPE; PLANT CELL; PLANT EVOLUTION; PLANT RESPONSE; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW; VIRUS VIRULENCE; YEAST;

ARABIDOPSIS; BACTERIA (MICROORGANISMS); OOMYCETES;

EID: 32944479048     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2006.02.008     Document Type: Review

References (78)

1. R.B. Abramovitch, Y.J. Kim, S. Chen, M.B. Dickman, and G.B. Martin Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death EMBO J. 22 2003 60 69
2. Y. Akeda, and J.E. Galan Chaperone release and unfolding of substrates in type III secretion Nature 437 2005 911 915
3. R.L. Allen, P.D. Bittner-Eddy, L.J. Grenville-Briggs, J.C. Meitz, A.P. Rehmany, L.E. Rose, and J.L. Beynon Host-parasite coevolutionary conflict between Arabidopsis and downy mildew Science 306 2004 1957 1960
4. M.R. Armstrong, S.C. Whisson, L. Pritchard, J.I. Bos, E. Venter, A.O. Avrova, A.P. Rehmany, U. Bohme, K. Brooks, and I. Cherevach An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm Proc. Natl. Acad. Sci. USA 102 2005 7766 7771
5. T. Asai, G. Tena, J. Plotnikova, M.R. Willmann, W.L. Chiu, L. Gomez-Gomez, T. Boller, F.M. Ausubel, and J. Sheen MAP kinase signalling cascade in Arabidopsis innate immunity Nature 415 2002 977 983
6. T. Ashfield, L.E. Ong, K. Nobuta, C.M. Schneider, and R.W. Innes Convergent evolution of disease resistance gene specificity in two flowering plant families Plant Cell 16 2004 309 318
7. M.J. Axtell, and B.J. Staskawicz Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4 Cell 112 2003 369 377
8. M.J. Axtell, S.T. Chisholm, D. Dahlbeck, and B.J. Staskawicz Genetic and molecular evidence that the Pseudomonas syringae type III effector protein AvrRpt2 is a cysteine protease Mol. Microbiol. 49 2003 1537 1546
9. S.R. Bisgrove, M.T. Simonich, N.M. Smith, A. Sattler, and R.W. Innes A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes Plant Cell 6 1994 927 933
10. F. Brunner, S. Rosahl, J. Lee, J.J. Rudd, C. Geiler, S. Kauppinen, G. Rasmussen, D. Scheel, and T. Nurnberger Pep-13, a plant defense-inducing pathogen-associated pattern from Phytophthora transglutaminases EMBO J. 21 2002 6681 6688
11. A.M. Catanzariti, P.N. Dodds, G.J. Lawrence, M.A. Ayliffe, and J.G. Ellis Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors Plant Cell 18 2005 243 256 10.1105/tpc.105.035980 Published online February 2, 2005
12. J.H. Chang, J.M. Urbach, T.F. Law, L.W. Arnold, A. Hu, S. Gombar, S.R. Grant, F.M. Ausubel, and J.L. Dangl A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringae Proc. Natl. Acad. Sci. USA 102 2005 2549 2554
13. S.T. Chisholm, D. Dahlbeck, N. Krishnamurthy, B. Day, K. Sjolander, and B.J. Staskawicz Molecular characterization of proteolytic cleavage sites of the Pseudomonas syringae effector AvrRpt2 Proc. Natl. Acad. Sci. USA 102 2005 2087 2092
14. G. Coaker, A. Falick, and B. Staskawicz Activation of a phytopathogenic bacterial effector protein by a eukaryotic cyclophilin Science 308 2005 548 550
15. J.L. Dangl, and J.D. Jones Plant pathogens and integrated defence responses to infection Nature 411 2001 826 833
16. B. Day, D. Dahlbeck, J. Huang, S.T. Chisholm, D. Li, and B.J. Staskawicz Molecular basis for the RIN4 negative regulation of RPS2 disease resistance Plant Cell 17 2005 1292 1305
17. S. DebRoy, R. Thilmony, Y.B. Kwack, K. Nomura, and S.Y. He A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants Proc. Natl. Acad. Sci. USA 101 2004 9927 9932
18. L. Deslandes, J. Olivier, N. Peeters, D.X. Feng, M. Khounlotham, C. Boucher, I. Somssich, S. Genin, and Y. Marco Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus Proc. Natl. Acad. Sci. USA 100 2003 8024 8029
19. P.J. de Wit Cf9 and Avr9, two major players in the gene-for-gene game Trends Microbiol. 3 1995 251 252
20. P.N. Dodds, G.J. Lawrence, A.M. Catanzariti, M.A. Ayliffe, and J.G. Ellis The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells Plant Cell 16 2004 755 768
21. G. Felix, J.D. Duran, S. Volko, and T. Boller Plants have a sensitive perception system for the most conserved domain of bacterial flagellin Plant J. 18 1999 265 276
22. B.J. Feys, and J.E. Parker Interplay of signaling pathways in plant disease resistance Trends Genet. 16 2000 449 455
23. H.H. Flor Current status of the gene-for-gene concept Annu. Rev. Phytopathol. 9 1971 275 296
24. L.K. Fritz-Laylin, N. Krishnamurthy, M. Tor, K.V. Sjolander, and J.D. Jones Phylogenomic analysis of the receptor-like proteins of rice and Arabidopsis Plant Physiol. 138 2005 611 623
25. H. Gehrig, A. Schussler, and M. Kluge Geosiphon pyriforme, a fungus forming endocytobiosis with Nostoc (cyanobacteria), is an ancestral member of the Glomales: evidence by SSU rRNA analysis J. Mol. Evol. 43 1996 71 81
26. L. Gomez-Gomez, and T. Boller FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis Mol. Cell 5 2000 1003 1011
27. L. Gomez-Gomez, and T. Boller Flagellin perception: a paradigm for innate immunity Trends Plant Sci. 7 2002 251 256
28. K. Gu, B. Yang, D. Tian, L. Wu, D. Wang, C. Sreekala, F. Yang, Z. Chu, G.L. Wang, F.F. White, and Z. Yin R gene expression induced by a type-III effector triggers disease resistance in rice Nature 435 2005 1122 1125
29. P. Hauck, R. Thilmony, and S.Y. He A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants Proc. Natl. Acad. Sci. USA 100 2003 8577 8582
30. P. He, S. Chintamanani, Z. Chen, L. Zhu, B.N. Kunkel, J.R. Alfano, X. Tang, and J.M. Zhou Activation of a COI1-dependent pathway in Arabidopsis by Pseudomonas syringae type III effectors and coronatine Plant J. 37 2004 589 602
31. D.S. Heckman, D.M. Geiser, B.R. Eidell, R.L. Stauffer, N.L. Kardos, and S.B. Hedges Molecular evidence for the early colonization of land by fungi and plants Science 293 2001 1129 1133
32. R.S. Hilgarth, L.A. Murphy, H.S. Skaggs, D.C. Wilkerson, H. Xing, and K.D. Sarge Regulation and function of SUMO modification J. Biol. Chem. 279 2004 53899 53902
33. N.L. Hiller, S. Bhattacharjee, C. van Ooij, K. Liolios, T. Harrison, C. Lopez-Estrano, and K. Haldar A host-targeting signal in virulence proteins reveals a secretome in malarial infection Science 306 2004 1934 1937
34. Y. Jamir, M. Guo, H.S. Oh, T. Petnicki-Ocwieja, S. Chen, X. Tang, M.B. Dickman, A. Collmer, and J.R. Alfano Identification of Pseudomonas syringae type III effectors that can suppress programmed cell death in plants and yeast Plant J. 37 2004 554 565
35. R. Janjusevic, R.B. Abramovitch, G.B. Martin, and C.E. Strebbins A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase Science 311 2005 222 226 10.1126/science.1120131 Published online December 22, 2005
36. Y. Jia, S.A. McAdams, G.T. Bryan, H.P. Hershey, and B. Valent Direct interaction of resistance gene and avirulence gene products confers rice blast resistance EMBO J. 19 2000 4004 4014
37. D.A. Jones, and D. Takemoto Plant innate immunity - direct and indirect recognition of general and specific pathogen-associated molecules Curr. Opin. Immunol. 16 2004 48 62
38. D.A. Jones, C.M. Thomas, K.E. Hammond-Kosack, P.J. Balint-Kurti, and J.D. Jones Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging Science 266 1994 789 793
39. M.H. Joosten, T.J. Cozijnsen, and P.J. De Wit Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene Nature 367 1994 384 386
40. M. Keshavarzi, S. Soylu, I. Brown, U. Bonas, M. Nicole, J. Rossiter, and J. Mansfield Basal defenses induced in pepper by lipopolysaccharides are suppressed by Xanthomonas campestris pv. vesicatoria Mol. Plant Microbe Interact. 17 2004 805 815
41. H.S. Kim, D. Desveaux, A.U. Singer, P. Patel, J. Sondek, and J.L. Dangl The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation Proc. Natl. Acad. Sci. USA 102 2005 6496 6501
42. M.G. Kim, L. da Cunha, A.J. McFall, Y. Belkhadir, S. DebRoy, J.L. Dangl, and D. Mackey Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis Cell 121 2005 749 759
43. B.N. Kunkel, and D.M. Brooks Cross talk between signaling pathways in pathogen defense Curr. Opin. Plant Biol. 5 2002 325 331
44. G. Kunze, C. Zipfel, S. Robatzek, K. Niehaus, T. Boller, and G. Felix The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants Plant Cell 16 2004 3496 3507
45. R. Lauge, and P.J. De Wit Fungal avirulence genes: structure and possible functions Fungal Genet. Biol. 24 1998 285 297
46. D. Mackey, B.F. Holt 3rd, A. Wiig, and J.L. Dangl RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis Cell 108 2002 743 754
47. D. Mackey, Y. Belkhadir, J.M. Alonso, J.R. Ecker, and J.L. Dangl Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance Cell 112 2003 379 389
48. M.B. Mudgett New insights to the function of phytopathogenic bacterial type III effectors in plants Annu. Rev. Plant Biol. 56 2005 509 531
49. K. Nomura, M. Melotto, and S.Y. He Suppression of host defense in compatible plant-Pseudomonas syringae interactions Curr. Opin. Plant Biol. 8 2005 361 368
50. T. Nurnberger, F. Brunner, B. Kemmerling, and L. Piater Innate immunity in plants and animals: striking similarities and obvious differences Immunol. Rev. 198 2004 249 266
51. M.J. Orbach, L. Farrall, J.A. Sweigard, F.G. Chumley, and B. Valent A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta Plant Cell 12 2000 2019 2032
52. A.P. Rehmany, A. Gordon, L.E. Rose, R.L. Allen, M.R. Armstrong, S.C. Whisson, S. Kamoun, B.M. Tyler, P.R. Birch, and J.L. Beynon Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines Plant Cell 17 2005 1839 1850
53. P. Reymond, and E.E. Farmer Jasmonate and salicylate as global signals for defense gene expression Curr. Opin. Plant Biol. 1 1998 404 411
54. C. Ritter, and J.L. Dangl Interference between two specific pathogen recognition events mediated by distinct plant disease resistance genes Plant Cell 8 1996 251 257
55. S. Rivas, and C.M. Thomas Molecular interactions between tomato and the leaf mold pathogen Cladosporium fulvum Annu. Rev. Phytopathol. 43 2005 395 436
56. J. Roden, L. Eardley, A. Hotson, Y. Cao, and M.B. Mudgett Characterization of the Xanthomonas AvrXv4 effector, a SUMO protease translocated into plant cells Mol. Plant Microbe Interact. 17 2004 633 643
57. P.C. Ronald, B. Albano, R. Tabien, L. Abenes, K.S. Wu, S. McCouch, and S.D. Tanksley Genetic and physical analysis of the rice bacterial blight disease resistance locus, Xa21 Mol. Gen. Genet. 236 1992 113 120
58. H.C. Rooney, J.W. Van't Klooster, R.A. van der Hoorn, M.H. Joosten, J.D. Jones, and P.J. de Wit Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance Science 308 2005 1783 1786
59. L.E. Rose, P.D. Bittner-Eddy, C.H. Langley, E.B. Holub, R.W. Michelmore, and J.L. Beynon The maintenance of extreme amino acid diversity at the disease resistance gene, RPP13, in Arabidopsis thaliana Genetics 166 2004 1517 1527
60. W. Shan, M. Cao, D. Leung, and B.M. Tyler The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance gene Rps1b Mol. Plant Microbe Interact. 17 2004 394 403
61. F. Shao, C. Golstein, J. Ade, M. Stoutemyer, J.E. Dixon, and R.W. Innes Cleavage of Arabidopsis PBS1 by a bacterial type III effector Science 301 2003 1230 1233
62. Y. Shen, and P. Ronald Molecular determinants of disease and resistance in interactions of Xanthomonas oryzae pv. oryzae and rice Microbes Infect. 4 2002 1361 1367
63. W.Y. Song, G.L. Wang, L.L. Chen, H.S. Kim, L.Y. Pi, T. Holsten, J. Gardner, B. Wang, W.X. Zhai, and L.H. Zhu A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21 Science 270 1995 1804 1806
64. J.L. Soosaar, T.M. Burch-Smith, and S.P. Dinesh-Kumar Mechanisms of plant resistance to viruses Nat. Rev. Microbiol. 3 2005 789 798
65. B.J. Staskawicz, M.B. Mudgett, J.L. Dangl, and J.E. Galan Common and contrasting themes of plant and animal diseases Science 292 2001 2285 2289
66. W.I. Tameling, S.D. Elzinga, P.S. Darmin, J.H. Vossen, F.L. Takken, M.A. Haring, and B.J. Cornelissen The tomato R gene products I-2 and MI-1 are functional ATP binding proteins with ATPase activity Plant Cell 14 2002 2929 2939
67. B.P. Thomma, I.A. Penninckx, W.F. Broekaert, and B.P. Cammue The complexity of disease signaling in Arabidopsis Curr. Opin. Immunol. 13 2001 63 68
68. M. Tian, E. Huitema, L. Da Cunha, T. Torto-Alalibo, and S. Kamoun A Kazal-like extracellular serine protease inhibitor from Phytophthora infestans targets the tomato pathogenesis-related protease P69B J. Biol. Chem. 279 2004 26370 26377
69. M. Tian, B. Benedetti, and S. Kamoun A Second Kazal-like protease inhibitor from Phytophthora infestans inhibits and interacts with the apoplastic pathogenesis-related protease P69B of tomato Plant Physiol. 138 2005 1785 1793
70. C.M. Tobias, G.E. Oldroyd, J.H. Chang, and B.J. Staskawicz Plants expressing the Pto disease resistance gene confer resistance to recombinant PVX containing the avirulence gene AvrPto Plant J. 17 1999 41 50
71. D.M. Underhill, and A. Ozinsky Toll-like receptors: key mediators of microbe detection Curr. Opin. Immunol. 14 2002 103 110
72. H.A. van den Burg, N. Westerink, K.J. Francoijs, R. Roth, E. Woestenenk, S. Boeren, P.J. de Wit, M.H. Joosten, and J. Vervoort Natural disulfide bond-disrupted mutants of AVR4 of the tomato pathogen Cladosporium fulvum are sensitive to proteolysis, circumvent Cf-4-mediated resistance, but retain their chitin binding ability J. Biol. Chem. 278 2003 27340 27346
73. E.A. Van der Biezen, and J.D. Jones Plant disease-resistance proteins and the gene-for-gene concept Trends Biochem. Sci. 23 1998 454 456
74. G.L. Wang, W.Y. Song, D.L. Ruan, S. Sideris, and P.C. Ronald The cloned gene, Xa21, confers resistance to multiple Xanthomonas oryzae pv. oryzae isolates in transgenic plants Mol. Plant Microbe Interact. 9 1996 850 855
75. B. Yang, W. Zhu, L.B. Johnson, and F.F. White The virulence factor AvrXa7 of Xanthomonas oryzae pv. oryzae is a type III secretion pathway-dependent nuclear-localized double-stranded DNA-binding protein Proc. Natl. Acad. Sci. USA 97 2000 9807 9812
76. W. Zhu, B. Yang, J.M. Chittoor, L.B. Johnson, and F.F. White AvrXa10 contains an acidic transcriptional activation domain in the functionally conserved C terminus Mol. Plant Microbe Interact. 11 1998 824 832
77. C. Zipfel, and G. Felix Plants and animals: a different taste for microbes? Curr. Opin. Plant Biol. 8 2005 353 360
78. C. Zipfel, S. Robatzek, L. Navarro, E.J. Oakeley, J.D. Jones, G. Felix, and T. Boller Bacterial disease resistance in Arabidopsis through flagellin perception Nature 428 2004 764 767