Type III secretion system effector proteins: Double agents in bacterial disease and plant defense

Annual Review of Phytopathology

Volumn 42, Issue , 2004, Pages 385-414

  Alfano, James R ^a   Collmer, Alan ^b  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

Avirulence genes; Hop proteins; hrp genes; Hypersensitive response; Plant disease

Indexed keywords

BACTERIAL PROTEIN;

ANIMAL; BACTERIUM; BIOLOGICAL MODEL; GENE EXPRESSION REGULATION; GENETICS; HOST PARASITE INTERACTION; IMMUNOLOGY; METABOLISM; PARASITOLOGY; PATHOGENICITY; PLANT; PLANT DISEASE; REVIEW;

ANIMALS; BACTERIA; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HOST-PARASITE RELATIONS; MODELS, IMMUNOLOGICAL; PLANT DISEASES; PLANTS;

ANIMALIA; BACTERIA (MICROORGANISMS); HUMULUS; PSEUDOMONAS; RALSTONIA; XANTHOMONAS;

EID: 4744364745     PISSN: 00664286     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.phyto.42.040103.110731     Document Type: Review

References (180)

1. Abramovitch RB, Kim YJ, Chen S, Dickman MB, Martin GB. 2003. Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J. 22:60-69
2. Ahmad M, Majerczak DR, Pike S, Hoyos ME, Novacky A, Coplin DL. 2001. Biological activity of harpin produced by Pantoea stewartii subsp stewartii. Mol. Plant-Microbe Interact. 14:1223-34
3. Alfano JR, Charkowski AO, Deng WL, Badel JL, Petnicki-Ocwieja T, et al. 2000. The Pseudomonas syringae Hrp pathogenicity island has a tripartite mosaic structure composed of a cluster of type III secretion genes bounded by exchangeable effector and conserved effector loci that contribute to parasitic fitness and pathogenicity in plants. Proc. Natl. Acad. Sci. USA 97:4856-61
4. Alfano JR, Collmer A. 1997. The type III (Hrp) secretion pathway of plant pathogenic bacteria: trafficking harpins, Avr proteins, and death. J. Bacteriol. 179:5655-62
5. Alfano JR, Guo M. 2003. The Pseudomonas syringae Hrp (type III) protein secretion system: advances in the new millenium. See Ref. 143a, pp. 227-58
6. Alonso A, Bottini N, Bruckner S, Rahmouni S, Williams S, et al. 2004. Lck dephosphorylation at Tyr-394 and inhibition of T cell antigen receptor signaling by Yersinia phosphatase YopH. J. Biol. Chem. 279:4922-28
7. Anderson DM, Fouts DE, Collmer A, Schneewind O. 1999. Reciprocal secretion of proteins by the bacterial type III machines of plant and animal pathogens suggests universal recognition of mRNA targeting signals. Proc. Natl. Acad. Sci. USA 96:12839-43
8. Anderson DM, Schneewind O. 1997. A mRNA signal for the type III secretion of Yop proteins by Yersinia enterocolitica. Science 278:1140-43
9. Arlat M, Van Gijsegem F, Huet JC, Pernollet JC, Boucher CA. 1994. PopA1, a protein which induces a hypersensitive-like response on specific Petunia genotypes, is secreted via the Hrp pathway of Pseudomonas solanacearum. EMBO J. 13:543-53
10. Arnold DL, Jackson RW, Fillingham AJ, Goss SC, Taylor JD, et al. 2001. Highly conserved sequences flank avirulence genes: isolation of novel avirulence genes from Pseudomonas syringae pv. pisi. Microbiology 147:1171-82
11. Arnold DL, Pitman A, Jackson RW. 2003. Pathogenicity and other genomic islands in plant pathogenic bacteria. Mol. Plant Pathol. 4:407-20
12. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, et al. 2002. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977-83
13. Astua-Monge G, Minsavage GV, Stall RE, Davis MJ, Bonas U, Jones JB. 2000. Resistance of tomato and pepper to T3 strains of Xanthomonas campestris pv. vesicatoria is specified by a plant-inducible avirulence gene. Mol. Plant-Microbe Interact. 13:911-21
14. 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. 49:1531-46
15. Axtell MJ, Staskawicz BJ. 2003. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112:369-77
16. Badel JL, Charkowski AO, Deng WL, Collmer A. 2002. A gene in the Pseudomonas syringae pv. tomato Hrp pathogenicity island conserved effector locus, hopPtoA1, contributes to efficient formation of bacterial colonies in planta and is duplicated elsewhere in the genome. Mol. Plant-Microbe Interact. 15:1014-24
17. Badel JL, Nomura K, Bandyopadhyay S, Shimizu R, Collmer A, He SY. 2003. Pseudomonas syringae. pv. tomato DC3000 HopPtoM (CEL ORF3) is important for lesion formation but not growth in tomato and is secreted and translocated by the Hrp type III secretion system in a chaperone-dependent manner. Mol. Microbiol. 49:1239-51
18. Baron-Epel O, Gharyal PK, Schindler M. 1988. Pectins as mediators of wall porosity in soybean cells. Planta 175:389-95
19. Bartsev AV, Deakin WJ, Boukli NM, McAlvin CB, Stacey G, et al. 2004. NopL, an effector protein of Rhizobium sp. NGR234, thwarts activation of plant defense reactions. Plant Physiol. 134:871-79
20. Bestwick CS, Bennett MH, Mansfield JW. 1995. hrp mutant of Pseudomonas syringae pv. phaseolicola induces cell wall alterations but not membrane damage leading to the hypersensitive reaction in lettuce. Plant Physiol. 108:503-16
21. Blocker A, Komoriya K, Aizawa S. 2003. Type III secretion systems and bacterial flagella: Insights into their function from structural similarities. Proc. Natl. Acad. Sci. USA 100:3027-30
22. Boch J, Joardar V, Gao L, Robertson TL, Lim M, Kunkel BN. 2002. Identification of Pseudomonas syringae genes induced during infection of Arabidopsis thaliana. Mol. Microbiol. 44:73-88
23. Bogdanove AJ, Beer SV, Bonas U, Boucher CA, Collmer A, et al. 1996. Unified nomenclature for broadly conserved hrp genes of phytopathogenic bacteria. Mol. Microbiol. 20:681-83
24. Bonas U, Lahaye T. 2002. Plant disease resistance triggered by pathogen-derived molecules: refined models of specific recognition. Curr. Opin. Microbiol. 5:44-50
25. Boyd AP, Lambermont I, Cornelis GR. 2000. Competition between the Yops of Yersinia enterocolitica for delivery into eukaryotic cells: role of the SycE chaperone binding domain of YopE. J. Bacteriol. 182:4811-21
26. Bretz JR, Mock NM, Charity JC, Zeyad S, Baker CJ, Hutcheson SW. 2003. A translocated protein tyrosine phosphatase of Pseudomonas syringae pv. tomato DC3000 modulates plant defence response to infection. Mol. Microbiol. 49:389-400
27. Brown I, Mansfield J, Bonas U. 1995. hrp genes in Xanthomonas campestris pv. vesicatoria determine ability to suppress papilla deposition in pepper mesophyll cells. Mol. Plant-Microbe Interact. 8:825-36
28. Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, et al. 2003. The complete sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. USA 100:10181-86
29. Buttner D, Bonas U. 2002. Getting across - bacterial type III effector proteins on their way to the plant cell. EMBO J. 21:5313-22
30. Buttner D, Bonas U. 2002. Port of entry - the type III secretion translocon. Trends Microbiol. 10:186-92
31. Buttner D, Bonas U. 2003. Common infection strategies of plant and animal pathogenic bacteria. Curr. Opin. Plant Biol. 6:312-19
32. Buttner D, Nennstiel D, Klusener B, Bonas U. 2002. Functional analysis of HrpF, a putative type III translocon protein from Xanthomonas campestris pv. vesicatoria. J. Bacteriol. 184:2389-98
33. Buttner D, Noel L, Thieme F, Bonas U. 2003. Genomic approaches in Xanthomonas campestris pv. vesicatoria allow fishing for virulence genes. J. Biotechnol. 106:203-14
34. Casper-Lindley C, Dahlbeck D, Clark ET, Staskawicz BJ. 2002. Direct biochemical evidence for type III secretion-dependent translocation of the AvrBs2 effector protein into plant cells. Proc. Natl. Acad. Sci USA 99:8336-41
35. Chang JH, Goel AK, Grant SR, Dangl JL. 2004. Wake of the flood: ascribing functions to the wave of type III effector proteins of phytopathogenic bacteria. Curr. Opin. Microbiol. 7:11-18
36. Charity JC, Pak K, Delwiche CF, Hutcheson SW. 2003. Novel exchangeable effector loci associated with the Pseudomonas syringae hrp pathogenicity island: evidence for integron-like assembly from transposed gene cassettes. Mol. Plant-Microbe Interact. 16:496-507
37. Charkowski AO, Alfano JR, Preston G, Yuan J, He SY, Collmer A. 1998. The Pseudomonas syringae pv. tomato Hrp W protein has domains similar to harpins and pectate lyases and can elicit the plant hypersensitive response and bind to pectate. J. Bacteriol. 180:5211-17
38. Ecc), which encodes an extracytoplasmic function subfamily of sigma factor required for expression of the HRP regulon. Mol. Plant-Microbe Interact. 15:971-80
39. Chen Z, Kloek AP, Cuzick A, Moeder W, Tang D, et al. 2004. The Pseudomonas syringae type III effector AvrRpt2 functions downstream or independently of SA to promote virulence on Arabidopsis thaliana. Plant J. 37:494-504
40. Cheng LW, Anderson DM, Schneewind O. 1997. Two independent type III secretion mechanisms for YopE in Yersinia enterocolitica. Mol. Microbiol. 24:757-65
41. Collmer A, Lindeberg M, Petnicki-Ocwieja T, Schneider DJ, Alfano JR. 2002. Genomic mining type III secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectors. Trends Microbiol. 10:462-69
42. Cornelis GR. 2000. Molecular and cell biology aspects of plague. Proc. Natl. Acad. Sci. USA 97:8778-83
43. Cornelis GR. 2002. Yersinia type III secretion: send in the effectors. J. Cell Biol. 158:401-8
44. Cornelis GR. 2002. The Yersinia Ysc-Yop 'type III' weaponry. Nat. Rev. Mol. Cell Biol. 3:742-52
45. Cornelis GR, Van Gijsegem F. 2000. Assembly and function of type III secretory systems. Annu. Rev. Microbiol. 54:735-74
46. Da Silva AC, Ferro JA, Reinach FC, Farah CS, Furlan LR, et al. 2002. Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417:459-63
47. Dangl JL, Jones JD. 2001. Plant pathogens and integrated defence responses to infection. Nature 411:826-33
48. Deng W-L, Rehm A, Charkowski A, Rojas CM, Collmer A. 2003. Pseudomonas syringae exchangeable effector loci: sequence diversity in representative pathovars and virulence function in P. syringae pv. syringae B728a. J. Bacteriol. 185:2592-602
49. Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M, 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. Proc. Natl. Acad. Sci. USA 100:8024-29
50. Dong H, Delaney TP, Bauer DW, Beer SV. 1999. Harpin induces disease resistance in Arabidopsis through the systemic acquired resistance pathway mediated by salicylic acid and the NIM1 gene. Plant J. 20:207-15
51. Dow M, Newman MA, von Roepenack E. 2000. The induction and modulation of plant defense responses by bacterial lipopolysaccharides. Annu. Rev. Phytopathol. 38:241-61
52. Duan YP, Castaneda A, Zhao G, Erdos G, Gabriel DW. 1999. Expression of a single, host-specific, bacterial pathogenicity gene in plant cells elicits division, enlargement, and cell death. Mol. Plant-Microbe Interact. 12:556-60
53. Espinosa A, Guo M, Tam VC, Fu ZQ, Alfano JR. 2003. The Pseudomonas syringae type III-secreted protein HopP-toD2 possesses protein tyrosine phosphatase activity and suppresses programmed cell death in plants. Mol. Microbiol. 49:377-87
54. Eulgem T, Rushton PJ, Robatzek S, Somssich IE. 2000. The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5:199-206
55. Ezra D, Barash I, Weinthal DM, Gaba V, Manulis S. 2004. pthG from Pantoea agglomerans pv. gypsophilae encodes an avirulence effector that determines incompatibility in multiple beet species. Mol. Plant Pathol. 5:105-13
56. Feldman MF, Cornelis GR. 2003. The multitalented type III chaperones: all you can do with 15 kDa. FEMS Microbiol. Lett. 219:151-58
57. Felix G, Boller T. 2003. Molecular sensing of bacteria in plants. The highly conserved RNA-binding motif RNP-1 of bacterial cold shock proteins is recognized as an elicitor signal in tobacco. J. Biol. Chem. 278:6201-8
58. 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. 18:265-76
59. Fouts DE, Abramovitch RB, Alfano JR, Baldo AM, Buell CR, et al. 2002. Genomewide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor. Proc. Natl. Acad. Sci. USA 99:2275-80
60. Fouts DE, Badel JL, Ramos AR, Rapp RA, Collmer A. 2003. A Pseudomonas syringae pv. tomato DC3000 Hrp (type III secretion) deletion mutant expressing the Hrp system of bean pathogen P. syringae pv. syringae 61 retains normal host specificity for tomato. Mol. Plant-Microbe Interact. 16:43-52
61. Francis MS, Wolf-Watz H, Forsberg A. 2002. Regulation of type III secretion systems. Curr. Opin. Microbiol. 5:166-72
62. Gabriel DW, Rolfe BG. 1990. Working models of specific recognition in plant-microbe interactions. Annu. Rev. Phytopathol. 28:365-91
63. Ganesan AK, Mende-Mueller L, Selzer J, Barbieri JT. 1999. Pseudomonas aeruginosa exoenzyme S, a double ADP-ribosyltransferase, resembles vertebrate mono-ADP-ribosyltransferases. J. Biol. Chem. 274:9503-8
64. Gaudriault S, Paulin JP, Barny MA. 2002. The DspB/F protein of Erwinia amylovora is a type III secretion chaperone ensuring efficient intrabacterial production of the Hrp-secreted DspA/E pathogenicity factor. Mol. Plant Pathol. 3:313-20
65. Gomez-Gomez L, Boller T. 2000. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5:1003-11
66. Gomez-Gomez L, Boller T. 2002. Flagellin perception: a paradigm for innate immunity. Trends Plant Sci. 7:251-56
67. Greenberg JT, Vinatzer BA. 2003. Identifying type III effectors of plant pathogens and analyzing their interaction with plant cells. Curr. Opin. Microbiol. 6:20-28
68. Gueneron M, Timmers AC, Boucher C, Arlat M. 2000. Two novel proteins, PopB, which has functional nuclear localization signals, and PopC, which has a large leucine-rich repeat domain, are secreted through the hrp-secretion apparatus of Ralstonia solanacearum. Mol. Microbiol. 36:261-77
69. Guttman DS, Sarkar SF. 2003. Evolutionary and functional genomics of host specificity in Pseudomonas syringae. In Int. Congr. Mol. Plant-Microbe Interact. St. Petersberg, Russia. In press
70. Guttman DS, Vinatzer BA, Sarkar SF, Ranall MV, Kettler G, Greenberg JT. 2002. A functional screen for the Type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295:1722-26
71. Hauck P, Thilmony R, He SY. 2003. A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc. Natl. Acad. Sci. USA 100:8577-82
72. He SY, Jin Q. 2003. The Hrp pilus: learning from flagella. Curr. Opin. Microbiol. 6:15-99
73. Hotson A, Chosed R, Shu H, Orth K, Mudgett MB. 2003. Xanthomonas type III effector XopD targets SUMO-conjugated proteins in planta. Mol. Microbiol. 50:377-89
74. Innes R. 2003. New effects of type III effectors. Mol. Microbiol. 50:363-65
75. Iriarte M, Cornelis GR. 1998. YopT, a new Yersinia Yop effector protein, affects the cytoskeleton of host cells. Mol. Microbiol. 29:915-29
76. Jackson RW, Athanassopoulos E, Tsiamis G, Mansfield JW, Sesma A, et al. 1999. Identification of a pathogenicity island, which contains genes for virulence and avirulence, on a large native plasmid in the bean pathogen Pseudomonas syringae pathovar phaseolicola. Proc. Natl. Acad. Sci. USA 96:10875-80
77. Jakobek JL, Lindgren PB. 1993. Generalized induction of defense responses in bean is not correlated with the induction of the hypersensitive reaction. Plant Cell 5:49-56
78. Jakobek JL, Smith JA, Lindgren PB. 1993. Suppression of bean defense responses by Pseudomonas syringae. Plant Cell 5:57-63
79. Jamir Y, Guo M, Oh H-S, Petnicki-Ocwieja T, Chen S, Tang X, et al. 2004. Identification of Pseudomonas syringae type III secreted effectors that suppress programmed cell death in plants and yeast. Plant J. 37:554-65
80. Jamir Y, Tang X, Alfano JR. 2004. The genome of Pseudomonas syringae pv. tomato DC3000 and functional genomic studies to better understand plant pathogenesis. In Pseudomonas, Vol. 1: Genomics, Life Style and Molecular Architecture, ed. JL Ramos. London: Kluwer/Plenum. In press
81. Jin P, Wood MD, Wu Y, Xie ZY, Katagiri F. 2003. Cleavage of the Pseudomonas syringae type III effector AvrRpt2 requires a host factor(s) common among eukaryotes and is important for AvrRpt2 localization in the host cell. Plant Physiol. 133:1072-82
82. Jin Q, He SY. 2001. Role of the Hrp pilus in type III protein secretion in Pseudomonas syringae. Science 294:2556-58
83. Jin Q, Hu W, Brown I, McGhee G, Hart P, et al. 2001. Visualization of secreted Hrp and Avr proteins along the Hrp pilus during type III secretion in Erwinia amylovora and Pseudomonas syringae. Mol. Microbiol. 40:1129-39
84. Jones DA, Takemoto D. 2004. Plant innate immunity - direct and indirect recognition of general and specific pathogen-associated molecules. Curr. Opin. Immunol. 16:48-62
85. Kanda A, Yasukohchi M, Ohnishi K, Kiba A, Okuno T, Hikichi Y. 2003. Ectopic expression of Ralstonia solanacearum effector protein PopA early in invasion results in loss of virulence. Mol. Plant-Microbe Interact. 16:447-55
86. Keen NT. 1990. Gene-for-gene complementarity in plant-pathogen interactions. Annu. Rev. Genet. 24:447-63
87. Kim JF, Alfano JR. 2002. Pathogenicity islands and virulence plasmids of bacterial plant pathogens. Curr. Top. Microbiol. Immunol. 264:121-41
88. Kim JF, Beer SV. 1998. HrpW of Erwinia amylovora, a new harpin that contains a domain homologous to pectate lyases of a distinct class. J. Bacteriol. 180:5203-510
89. Kim JG, Park BK, Yoo CH, Jeon E, Oh J, Hwang I. 2003. Characterization of the Xanthomonas axonopodis pv. glycines Hrp pathogenicity island. J. Bacteriol. 185:3155-66
90. Kjemtrup S, Nimchuk Z, Dangl JL. 2000. Effector proteins of phytopathogenic bacteria: bifunctional signals in virulence and host recognition. Curr. Opin. Microbiol. 3:73-78
91. Klement Z. 1982. Hypersensitivity. In Phytopathogenic Prokaryotes, ed. MS Mount, GH Lacy, 2:149-77. New York: Academic
92. Klement Z, Bozso Z, Besenyei E, Czelleng A, Kecskes ML, Ott PG. 2003. Early induced resistance, a general, symptomless plant response to bacteria. In Pseudomonas syringae and Related Pathogens: Biology and Genetics, ed. NS Iacobellis, A Collmer, SW Hutcheson, JW Mansfield, CE Morris, et al., pp. 301-9. Dordrecht: Kluwer
93. Klement Z, Bozso Z, Kecskes ML, Besenyei E, Arnold C, Ott PG. 2003. Local early induced resistance of plants as the first line of defence against bacteria. Pest Manag. Sci. 59:465-74
94. Kobayashi DY, Tamaki SJ, Keen NT. 1989. Cloned avirulence genes from the tomato pathogen Pseudomonas syringae pv. tomato confer cultivar specificity on soybean. Proc. Natl. Acad. Sci. USA 86: 157-61
95. Lafont F, Abrami L, van der Goot FG. 2004. Bacterial subversion of lipid rafts. Curr. Opin. Microbiol. 7:4-10
96. Lahaye T, Bonas U. 2001. Molecular secrets of bacterial type III effector proteins. Trends Plant Sci. 6:479-85
97. Lavie M, Shillington E, Eguiluz C, Grimsley N, Boucher C. 2002. PopP1, a new member of the YopJ/AvrRxv family of type III effector proteins, acts as a host-specificity factor and modulates aggressiveness of Ralstonia solanacearum. Mol. Plant-Microbe Interact. 15:1058-68
98. Psph from the plant pathogen Pseudomonas syringae pv. phaseolicola binds to lipid bilayers and forms an ion-conducting pore in vitro. Proc. Natl. Acad. Sci. USA 98:289-94
99. Lee SH, Galan JE. 2004. Salmonella type III secretion-associated chaperones confer secretion-pathway specificity. Mol. Microbiol. 51:483-95
100. Li CM, Brown I, Mansfield J, Stevens C, Boureau T, et al. 2002. The Hrp pilus of Pseudomonas syringae elongates from its tip and acts as a conduit for translocation of the effector protein HrpZ. EMBO J. 21:1909-15
101. Lincoln JE, Richael C, Overduin B, Smith K, Bostock R, Gilchrist DG. 2002. Expression of the antiapoptotic baculovirus p35 gene in tomato blocks programmed cell death and provides broadspectrum resistance to disease. Proc. Natl. Acad. Sci. USA 99:15217-21
102. Lopéz-Solanilla E, Bronstein PA, Schneider AR, Collmer A. 2004. HopPtoN is a Pseudomonas syringae TTSS effector and cysteine protease that suppresses pathogen-induced necrosis associated with both compatible and incompatible plant interactions. Mol. Microbiol. Submitted
103. Lorang JM, Shen H, Kobayashi D, Cooksey D, Keen NT. 1994. avrA and avrE in Pseudomonas syringae pv. tomato PT23 play a role in virulence on tomato plants. Mol. Plant-Microbe Interact. 7:508-15
104. Losada L, Sussan T, Pak K, Zeyad S, Rozenbaum I, Hutcheson SW. 2004. Identification of a novel Pseudomonas syringae Psy61 effector with virulence and avirulence functions by a HrpL-dependent promoter-trap assay. Mol. Plant-Microbe Interact. 17:254-62
105. Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL. 2003. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112:379-89
106. Mackey D, Holt BF, Wiig A, Dangl JL. 2002. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:743-54
107. Manulis A, Barash I. 2003. Molecular basis for transformation of an epiphyte into a gall-forming pathogen as exemplified by Erwinia herbicola pv. gypsophilae. See Reference 143a, pp. 19-52
108. Marois E, Van den Ackerveken G, Bonas U. 2002. The Xanthomonas type III effector protein AvrBs3 modulates plant gene expression and induces cell hypertrophy in the susceptible host. Mol. Plant-Microbe Interact. 15:637-46
109. Martin GB, Bogdanove AJ, Sessa G. 2003. Understanding the functions of plant disease resistance proteins. Annu. Rev. Plant Biol. 54:23-61
110. Maurer-Stroh S, Eisenhaber F. 2004. Myristoylation of viral and bacterial proteins. Trends Microbiol. 12:178-85
111. Medzhitov R, Janeway CA Jr. 2002. Decoding the patterns of self and nonself by the innate immune system. Science 296:298-300
112. Merighi M, Majerczak DR, Stover EH, Coplin DL. 2003. The HrpX/HrpY two-component system activates hrpS expression, the first step in the regulatory cascade controlling the Hrp regulon in Pantoea stewartii subsp. stewartii. Mol. Plant-Microbe Interact. 16:238-48
113. Midland SL, Keen NT, Sims JJ, Midland MM, Stayton MM, et al. 1993. The structures of syringolides 1 and 2: novel C glycosidic elicitors from Pseudomonas syringae pv. tomato. J. Org. Chem. 58:2940-45
114. Mudgett MB, Chesnokova O, Dahlbeck D, Clark ET, Rossier O, et al. 2000. Molecular signals required for type III secretion and translocation of the Xanthomonas campestris AvrBs2 protein to pepper plants. Proc. Natl. Acad. Sci. USA 97:13324-29
115. Nimchuk Z, Eulgem T, Holt BF 3rd, Dangl JL. 2003. Recognition and response in the plant immune system. Annu. Rev. Genet. 37:579-609
116. Nimchuk Z, Marois E, Kjemtrup S, Leister RT, Katagiri F, Dangl JL. 2000. Eukaryotic fatty acylation drives plasma membrane targeting and enhances function of several type III effector proteins from Pseudomonas syringae. Cell 101:353-63
117. Noel L, Thieme F, Gabler J, Buttner D, Bonas U. 2003. XopC and XopJ, two novel type III effector proteins from Xanthomonas campestris pv. vesicatoria. J. Bacteriol. 185:7092-102
118. Noel L, Thieme F, Nennstie D, Bonas U. 2001. cDNA-AFLP analysis unravels a genome-wide hrpG-regulon in the plant pathogen Xanthomonas campestris pv. vesicatoria. Mol. Microbiol. 41:1271-81
119. Nurnberger T, Brunner F. 2002. Innate immunity in plants and animals: emerging parallels between the recognition of general elicitors and pathogen-associated molecular patterns. Curr. Opin. Plant Biol. 5:318-24
120. Orth K. 2002. Function of the Yersinia effector YopJ. Curr. Opin. Microbiol. 5:38-43
121. Orth K, Palmer LE, Bao ZQ, Stewart S, Rudolph AE, et al. 1999. Inhibition of the mitogen-activated protein kinase kinase superfamily by a Yersinia effector. Science 285:1920-23
122. Orth K, Xu Z, Mudgett MB, Bao ZQ, Palmer LE, et al. 2000. Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science 290:1594-97
123. Page AL, Parsot C. 2002. Chaperones of the type III secretion pathway: jacks of all trades. Mol. Microbiol. 46:1-11
124. Parkhill J. 2002. The importance of complete genome sequences. Trends Microbiol. 10:219-20
125. Parsot C, Hamiaux C, Page AL. 2003. The various and varying roles of specific chaperones in type III secretion systems. Curr. Opin. Microbiol. 6:7-14
126. Pedley KF, Martin GB. 2003. Molecular basis of Pto-mediated resistance to bacterial speck disease in tomato. Annu. Rev. Phytopathol. 41:215-43
127. Peng JL, Dong HS, Dong HP, Delaney TP, Bonasera JM, Beer SV. 2003. Harpin-elicited hypersensitive cell death and pathogen resistance require the NDR1 and EDS1 genes. Physiol. Mol. Plant Pathol. 62:317-26
128. Petnicki-Ocwieja T, Schneider DJ, Tam VC, Chancey ST, Shan L, et al. 2002. Genomewide identification of proteins secreted by the Hrp type III protein secretion system of Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. USA 99:7652-57
129. Preston G, Huang H-C, He SY, Collmer A. 1995. The HrpZ proteins of Pseudomonas syringae pvs. syringae, glycinea, and tomato are encoded by an operon containing Yersinia ysc homologs and elicit the hypersensitive response in tomato but not soybean. Mol. Plant-Microbe Interact. 8:717-32
130. Puri N, Jenner C, Bennett M, Stewart R, Mansfield J, et al. 1997. Expression of avrPphB, an avirulence gene from Pseudomonas syringae pv. phaseolicola, and the delivery of signals causing the hypersensitive reaction in bean. Mol. Plant-Microbe Interact. 10:247-56
131. Reuber TL, Ausubel FM. 1996. Isolation of Arabidopsis genes that differentiate between resistance responses mediated by the RPS2 and RPMI disease resistance genes. Plant Cell 8:241-49
132. Ritter C, Dangl JL. 1996. Interference between two specific pathogen recognition events mediated by distinct plant disease resistance genes. Plant Cell 8:251-57
133. Rohmer L, Kjemtru S, Marchesin P, Dangl JL. 2003. Nucleotide sequence, functional characterization and evolution of pFKN, a virulence plasmid in Pseudomonas syringae pathovar maculicola. Mol. Microbiol. 47:1545-62
134. Rossier O, Van den Ackerveken G, Bonas U. 2000. HrpB2 and HrpF from Xanthomonas are type III-secreted proteins and essential for pathogenicity and recognition by the host plant. Mol. Microbiol. 38:828-38
135. Salanoubat M, Genin S, Artiguenave F, Gouzy J, Mangenot S, et al. 2002. Genome sequence of the plant pathogen Ralstonia solanacearum. Nature 415:497-502
136. Schechter LM, Roberts KA, Jamir Y, Alfano JR, Collmer A. 2004. Pseudomonas syringae type III secretion system targeting signals and novel effectors studied with a Cya translocation reporter. J. Bacteriol. 186:543-55
137. Shan L, Oh H-S, Guo M, Zhou J, Alfano JR, et al. 2004. The hopPtoF locus of Pseudomonas syringae pv. tomato DC3000 encodes a type III chaperone and a cognate effector. Mol. Plant-Microbe Interact. In press
138. Shan LB, Thara VK, Martin GB, Zhou JM, Tang XY. 2000. The Pseudomonas AvrPto protein is differentially recognized by tomato and tobacco and is localized to the plant plasma membrane. Plant Cell 12:2323-37
139. Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW. 2003. Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301:1230-33
140. Shao F, Merritt PM, Bao Z, Innes RW, Dixon JE. 2002. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109:575-88
141. Shimizu R, Taguchi F, Marutani M, Mukaihara T, Inagaki Y, et al. 2003. The deltafliD mutant of Pseudomonas syringae pv. tabaci, which secretes flagellin monomers, induces a strong hypersensitive reaction (HR) in non-host tomato cells. Mol. Genet. Genomics 269:21-30
142. Sorg I, Goehring UM, Aktories K, Schmidt G. 2001. Recombinant Yersinia YopT leads to uncoupling of RhoA-effector interaction. Infect. Immun. 69:7535-43
143. Sory M-P, Cornelis GR. 1994. Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol. Microbiol. 14:583-94
144. 143a. Stacey G, Keen NT, eds. 2003. Plant-Microbe Interactions, Vol. 6. St. Paul; APS Press
145. Staskawicz BJ, Dahlbeck D, Keen NT, Napoli C. 1987. Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea. J. Bacteriol. 169:5789-94
146. Staskawicz BJ, Dahlbeck D, Keen NT. 1984. Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race specific incompatibility on Glycine max (L.) Merr. Proc. Natl. Acad. Sci. USA 81:6024-28
147. Stebbins CE, Galan JE. 2001. Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature 414:77-81
148. Stevens C, Bennett MA, Athanassopoulos E, Tsiamis G, Taylor JD, Mansfield JW. 1998. Sequence variations in alleles of the avirulence gene avrPphE.R2 from Pseudomonas syringae pv. phaseolicola lead to loss of recognition of the AvrPphE protein within bean cells and a gain in cultivar-specific virulence. Mol. Microbiol. 29:165-77
149. Stone JM, Heard JE, Asai T, Ausubel FM. 2000. Simulation of fungal-mediated cell death by fumonisin B1 and selection of fumonisin B1-resistant (fbr) Arabidopsis mutants. Plant Cell 12:1811-22
150. Pss protein. Plant J. 9:431-39
151. Sun J, Barbieri JT. 2003. Pseudomonas aeruginosa ExoT ADP-ribosylates CT10 regulator of kinase (Crk) proteins. J. Biol. Chem. 278:32794-800
152. Swiderski MR, Innes RW. 2001. The Arabidopsis PBS1 resistance gene encodes a member of a novel protein kinase subfamily. Plant J. 26:101-12
153. Swords KMM, Dahlbeck D, Kearney B, Roy M, Staskawicz BJ. 1996. Spontaneous and induced mutations in a single open reading frame alters both virulence and avirulence in Xanthomonas campestris pv. vesicatoria avrBs2. J. Bacteriol. 178:4661-69
154. Szurek B, Marois E, Bonas U, Van den Ackerveken G. 2001. Eukaryotic features of the Xanthomonas type III effector AvrBsS: protein domains involved in transcriptional activation and the interaction with nuclear import receptors from pepper. Plant J. 26:523-34
155. Taguchi F, Shimizu R, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y. 2003. Post-translational modification of flagellin determines the specificity of HR induction. Plant Cell Physiol. 44:342-49
156. Taguchi F, Shimizu R, Nakajima R, Toyoda K, Shiraishi T, Ichinose Y 2003. Differential effects of flagellins from Pseudomonas syringae pv. tabaci, tomato and glycinea on plant defense response. Plant Physiol. Biochem. 41:165-74
157. Takeuchi K, Taguchi F, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y. 2003. Flagellin glycosylation island in Pseudomonas syringaepv. glycinea and its role in host specificity. J. Bacteriol. 185:6658-65
158. Tampakaki AP, Panopoulos NJ. 2000. Elicitation of hypersensitive cell death by extracellularly targeted HrpZPsph produced in planta. Mol. Plant-Microbe Interact. 13:1366-74
159. Tao Y, Xie Z, Chen W, Glazebrook J, Chang HS, et al. 2003. Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317-30
160. Thomas NA, Brett Finlay B. 2003. Establishing order for type III secretion substrates - a hierarchical process. Trends Microbiol. 11:398-403
161. Tsiamis G, Mansfield JW, Hockenhull R, Jackson RW, Sesma A, et al. 2000. Cultivar-specific avirulence and virulence functions assigned to avrPphF in Pseudomonas syringae pv. phaseolicola, the cause of bean halo-blight disease. EMBO J. 19:3204-14
162. Van den Ackerveken G, Marois E, Bonas U. 1996. Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell. Cell 87:1307-16
163. Van der Biezen EA, Jones JD. 1998. Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 23:454-56
164. van Dijk K, Tam VC, Records AR, Petnicki-Ocwieja T, Alfano JR. 2002. The ShcA protein is a molecular chaperone that assists in the secretion of the HopPsyA effector from the type III (Hrp) protein secretion system of Pseudomonas syringae. Mol. Microbiol. 44:1469-81
165. Viboud GI, So SS, Ryndak MB, Bliska JB. 2003. Proinflammatory signalling stimulated by the type III translocation factor YopB is counteracted by multiple effectors in epithelial cells infected with Yersinia pseudotuberculosis. Mol. Microbiol. 47:1305-15
166. Wattiau P, Bernier B, Deslee P, Michiels T, Cornelis GR. 1994. Individual chaperones required for Yop secretion by Yersinia. Proc. Natl. Acad. Sci. USA 91:10493-97
167. Wattiau P, Woestyn S, Cornelis GR. 1996. Customized secretion chaperones in pathogenic bacteria. Mol. Microbiol. 20:255-62
168. Wehling MD, Guo M, Fu ZQ, Alfano JR. 2004. The Pseudomonas syringae HopP-toV protein is secreted in culture and translocated into plant cells via the type III protein secretion system in a manner dependent on the ShcV type III chaperone. J. Bacteriol. In press
169. Wei Z-M, Beer SV. 1996. Harpin from Erwinia amylovora induces plant resistance. Acta Hortic. 411:223-25
170. Whalen MC, Wang JF, Carland FM, Heiskell ME, Dahlbeck D, et al. 1993. Avirulence gene avrRxv from Xanthomonas campestris pv. vesicatoria specifies resistance on tomato line Hawaii 7998. Mol. Plant-Microbe Interact. 6:616-27
171. White FF, Yang B, Johnson LB. 2000. Prospects for understanding avirulence gene function. Curr. Opin. Plant Biol. 3:291-98
172. Yang Y, DeFeyter R, Gabriel DW. 1994. Host-specific symptoms and increased release of Xanthomonas citri and X. campestris pv. malvacearum from leaves are determined by the 102 bp tandem repeats of pthA and avrb6, respectively. Mol. Plant-Microbe Interact. 7:345-55
173. Yang Y, Gabriel DW. 1995. Xanthomonas avirulence/pathogenicity gene family encodes functional plant nuclear targeting signals. Mol. Plant-Microbe Interact. 8:627-31
174. Yao T, Mecsas J, Healy JI, Falkow S, Chien YH. 1999. Suppression of T and B lymphocyte activation by a Yersinia pseudotuberculosis virulence factor, yopH. J. Exp. Med. 190:1343-45
175. Zhang S, Klessig DF. 2001. MAPK cascades in plant defense signaling. Trends Plant Sci. 6:520-27
176. Zhu MF, Shao F, Innes RW, Dixon JE, Xu ZH, et al. 2004. The crystal structure of Pseudomonas avirulence protein AvrPphB: a papain-like fold with a distinct substrate-binding site. Proc. Natl. Acad. Sci. USA 101:302-7
177. Zhu WG, Mabanua MM, White FF. 2000. Identification of two novel hrp-associated genes in the hrp gene cluster of Xanthomonas oryzae pv. oryzae. J. Bacteriol. 182:1844-53
178. Zhu WG, Yang B, Chittoor JM, Johnson LB, White FF. 1998. AvrXa10 contains an acidic transcriptional activation domain in the functionally conserved C terminus. Mol. Plant-Microbe Interact. 11:824-32
179. Zhu W, Yang B, Wills N, Johnson LB, White FF. 1999. The C terminus of AvrXa10 can be replaced by the transcriptional activation domain of VP16 from the herpes simplex virus. Plant Cell 11:1665-74
180. Zwiesler-Vollick J, Plovanich-Jones AE, Nomura K, Brandyopadhyay S, Joardar V, et al. 2002. Identification of novel hrp-regulated genes through functional genomic analysis of the Pseudomonas syringae pv. tomato DC3000 genome. Mol. Microbiol. 45:1207-18