Plants as models for the study of human pathogenesis

Biotechnology Advances

Volumn 22, Issue 5, 2004, Pages 363-382

  Guttman, David S ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Animal pathogens; Extracellular polysaccharides; Innate immunity; Plant pathogens; Type III secretion; Virulence

Indexed keywords

BACTERIA; DISEASES; GENES; PATHOLOGY; PLANTS (BOTANY); POLYSACCHARIDES;

PATHOGENESIS; VIRULENCE FACTORS;

BIOTECHNOLOGY;

BACTERIAL DISEASE; IMMUNE RESPONSE; PATHOGEN;

ANIMALIA; BACTERIA (MICROORGANISMS);

EID: 3042737389     PISSN: 07349750     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biotechadv.2003.11.001     Document Type: Article

References (126)

1. Adams M.H., Park B.H. An enzyme produced by a phage-host cell system: II. The properties of the polysaccharides. Microbiol. Eur. 1956;16-19. [Nov/Dec]
2. Aderem A., Ulevitch R.J. Toll-like receptors in the induction of the innate immune response. Nature. 406:2000;782-787
3. Aepfelbacher M., Heesemann J. Modulation of Rho GTPases and the actin cytoskeleton by Yersinia outer proteins (Yops). Int. J. Med. Microbiol. 291:2001;269-276
4. Aepfelbacher M., Trasak C., Wilharm G., Wiedemann A., Trulzsch K., Krauss K., et al. Characterization of YopT effects on Rho GTPases in Yersinia enterocolitica-infected cells. J. Biol. Chem. 278:2003;33217-33223
5. Aizawa S. Bacterial flagella and type III secretion systems. FEMS Microbiol. 202:2001;157-164
6. Allewelt M., Coleman F.T., Grout M., Priebe G.P., Pier G.B. Acquisition of expression of the Pseudomonas aeruginosa ExoU cytotoxin leads to increased bacterial virulence in a murine model of acute pneumonia and systemic spread. Infect. Immun. 68:2000;3998-4004
7. Anonymous Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 408:2000;796-815
8. Arakawa Y., Wacharotayankun R., Nagatsuka T., Ito H., Kato N., Ohta M. Genomic organization of the Klebsiella pneumoniae cps region responsible for serotype K2 capsular polysaccharide synthesis in the virulent-strain chedid. J. Bacteriol. 177:1995;1788-1796
9. Bender C.L., Alarcon-Chaidez F., Gross D.C. Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. Microbiol. Mol. Biol. Rev. 63:1999;266-292
10. Binet R., Letoffe S., Ghigo J.M., Delepelaire P., Wandersman C. Protein secretion by Gram-negative bacterial ABC exporters - a review. Gene. 192:1997;7-11
11. Blocker A., Gounon P., Larquet E., Niebuhr K., Cabiaux V., Parsot C., et al. The tripartite type III secretion of Shigella flexneri inserts IpaB and IpaC into host membranes. J. Cell Biol. 147:1999;683-693
12. Bohin J.P. Osmoregulated periplasmic glucans in Proteobacteria. FEMS Microbiol. Lett. 186:2000;11-19
13. Buttner D., Bonas U. Common infection strategies of plant and animal pathogenic bacteria. Curr. Opin. Plant Biol. 6:2003;312-319
14. Cao H., Baldini R.L., Rahme L.G. Common mechanisms for pathogens of plants and animals. Annu. Rev. Phytopathol. 39:2001;259-284
15. Choi J.Y., Sifri C.D., Goumnerov B.C., Rahme L.G., Ausubel F.M., Calderwood S.B. Identification of virulence genes in a pathogenic strain of Pseudomonas aeruginosa by representational difference analysis. J. Bacteriol. 184:2002;952-961
16. Ciesiolka L.D., Hwin T., Gearlds J.D., Minsavage G.V., Saenz R., Bravo M., et al. Regulation of expression of avirulence gene avrRxv and identification of a family of host interaction factors by sequence analysis of avrBsT. Mol. Plant-Microbe Interact. 12:1999;35-44
17. Cleaveland S., Laurenson M.K., Taylor L.H. Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence. Philos. Trans. R. Soc. Lond., B. Biol. Sci. 356:2001;991-999
18. Collmer A., Lindeberg M., Petnicki-Ocwieja T., Schneider D., Alfano J. Genomic mining type III secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectors. TIM. 10:2002;462
19. Corbin B.D., McLean R.J., Aron G.M. Bacteriophage T4 multiplication in a glucose-limited Escherichia coli biofilm. Can. J. Microbiol. 47:2001;680-684
20. Cornelis G.R., Van Gijsegem F. Assembly and function of type III secretory systems. Annu. Rev. Microbiol. 54:2000;735-774
21. Costerton J.W. Cystic fibrosis pathogenesis and the role of biofilms in persistent infection. Trends Microbiol. 9:2001;50-52
22. Costerton J.W., Stewart P.S., Greenberg E.P. Bacterial biofilms: a common cause of persistent infections. Science. 284:1999;1318-1322
23. Cui Y., Chatterjee A., Chatterjee A.K. Effects of the two-component system comprising GacA and GacS of Erwinia carotovora subsp. carotovora on the production of global regulatory rsmB RNA, extracellular enzymes, and harpinEcc. Mol. Plant-Microbe Interact. 14:2001;516-526
24. Dangl J.L., Jones J.D. Plant pathogens and integrated defence responses to infection. Nature. 411:2001;826-833
25. Davey M.E., O'Toole G.A. Microbial Biofilms: from Ecology to Molecular Genetics. Microbiol. Mol. Biol. Rev. 64:2000;847-867
26. Davies J.C. New therapeutic approaches for cystic fibrosis lung disease. J. R. Soc. Med. 95:2002;58-67
27. Donabedian H. Quorum sensing and its relevance to infectious diseases. J. Infect. 46:2003;207-214
28. Donlan R.M. Biofilm formation: a clinically relevant microbiological process. Clin. Infect. Dis. 33:2001;1387-1392
29. Doolittle M.M., Cooney J.J., Caldwell D.E. Lytic infection of Escherichia coli biofilms by bacteriophage T4. Can. J. Microbiol. 41:1995;12-18
30. Dow J.M., Crossman L., Findlay K., He Y.Q., Feng J.X., Tang J.L. Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signaling and is required for full virulence to plants. Proc. Natl. Acad. Sci. 100:2003;10995-11000
31. Drenkard E., Ausubel F.M. Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature. 416:2002;740-743
32. Dunne W.M. Jr. Bacterial adhesion: seen any good biofilms lately? Clin. Microbiol. Rev. 15:2002;155-166
33. Ernst J.D. Bacterial inhibition of phagocytosis. Cell. Microbiol. 2:2000;379-386
34. Finlay B.B., Falkow S. Common themes in microbial pathogenicity. Microbiol. Rev. 53:1989;210-230
35. Finlay B.B., Falkow S. Common themes in microbial pathogenicity revisited. Microbiol. Mol. Biol. Rev. 61:1997;136-169
36. Foulongne V., Michaux-Charachon S., O'Callghan D., Ramuz M. Type IV secretion systems and bacterial virulence. MS. Med. Sci. 18:2002;439-447
37. Frithz-Lindsten E., Du Y., Rosqvist R., Forsberg A. Intracellular targeting of exoenzyme S of Pseudomonas aeruginosa via type III-dependent translocation induces phagocytosis resistance, cytotoxicity and disruption of actin microfilaments. Mol. Microbiol. 25:1997;1125-1139
38. Galan J.E., Collmer A. Type III secretion machines: bacterial devices for protein delivery into host cells. Science. 284:1999;1322-1328
39. Gentschev I., Dietrich G., Goebel W. The E. coli alpha-hemolysin secretion system and its use in vaccine development. TIM. 10:2002;39-45
40. Guttman D.S., Vinatzer B.A., Sarkar S.F., Ranall M., Greenberg J.T. A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science. 295:2002;1722-1726
41. Ha U.H., Wang Y., Jin S. DsbA of Pseudomonas aeruginosa is essential for multiple virulence factors. Infect. Immun. 71:2003;1590-1595
42. Hahn H.P. The type IV pilus is the major virulence-associated adhesion of Pseudomonas aeruginosa - a review. Gene. 192:1997;99-108
43. Hauser A.R., Kang P.J., Engel J.N. PepA, a secreted protein of Pseudomonas aeruginosa, is necessary for cytotoxicity and virulence. Mol. Microbiol. 27:1998;807-818
44. He S.Y. Type III protein secretion systems in plant and animal pathogenic bacteria. Annu. Rev. Phytopathol. 36:1998;363-392
45. Hendrickson E.L., Guevera P., Ausubel F.M. The alternative sigma factor rpoN is required for hrp activity in Pseudomonas syringae pv. maculicola and acts at the level of hrpL transcription. J. Bacteriol. 182:2000;3508-3516
46. Hendrickson E.L., Guevera P., Penaloza-Vazquez A., Shao J., Bender C., Ausubel F.M. Virulence of the phytopathogen Pseudomonas syringae pv. maculicola is rpoN dependent. J. Bacteriol. 182:2000;3498-3507
47. Hendrickson E.L., Plotnikova J., Mahajan-Miklos S., Rahme L.G., Ausubel F.M. Differential roles of the Pseudomonas aeruginosa PA14 rpoN gene in pathogenicity in plants, nematodes, insects, and mice. J. Bacteriol. 183:2001;7126-7134
48. Hirano S.S., Charkowski A.O., Collmer A., Willis D.K., Upper C.D. Role of the Hrp type III protein secretion system in growth of Pseudomonas syringae pv. syringae B728a on host plants in the field. Proc. Natl. Acad. Sci. U. S. A. 96:1999;9851-9856
49. Hogan D.A., Kolter R. Pseudomonas-Candida interactions: an ecological role for virulence factors. Science. 296:2002;2229-2232
50. Hueck C. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:1998;379-433
51. Hughes K.A., Sutherland I.W., Jones M.V. Biofilm susceptibility to bacteriophage attack: the role of phage-borne polysaccharide depolymerase. Microbiology (UK). 144:1998;3039-3047
52. Inohara N., Nunez G. NODs: intracellular proteins involved in inflammation and apoptosis. Nat. Rev. Immunol. 3:2003;371-382
53. Inohara N., Ogura Y., Nunez G. Nods: a family of cytosolic proteins that regulate the host response to pathogens. Curr. Opin. Microbiol. 5:2002;76-80
54. Jander G., Rahme L.G., Ausubel F.M. Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J. Bacteriol. 182:2000;3843-3845
55. Jebanathirajah J.A., Peri S., Pandey A. Toll and interleukin-1 receptor (TIR) domain-containing proteins in plants: a genomic perspective. TPS. 7:2002;388-391
56. Johnston C., Pegues D.A., Hueck C.J., Lee C.A., Miller S.I. Transcriptional activation of Salmonella typhimurium invasion genes by a member of the phosphorylated response-regulator superfamily. Mol. Microbiol. 22:1996;715-727
57. Kajava A.V. Structural diversity of leucine-rich repeat proteins. J. Mol. Biol. 277:1998;519-527
58. Kauppi A.M., Nordfelth R., Uvell H., Wolf-Watz H., Elofsson M. Targeting bacterial virulence. Inhibitors of type III secretion in Yersinia. Chem. Biol. 10:2003;241-249
59. Kazmierczak B.I., Engel J.N. Pseudomonas aeruginosa ExoT acts in vivo as a GTPase-activating protein for RhoA Rac1, and Cdc42. Infect. Immun. 70:2002;2198-2205
60. Keith R.C., Keith L.M., Hernandez-Guzman G., Uppalapati S.R., Bender C.L. Alginate gene expression by Pseudomonas syringae pv. tomato DC3000 in host and non-host plants. Microbiology (UK). 149:2003;1127-1138
61. Kinscherf T.G., Willis D.K. Swarming by Pseudomonas syringae B728a requires gacS (lemA) and gacA but not the acyl-homoserine lactone biosynthetic gene ahlI. J. Bacteriol. 181:1999;4133-4136
62. Kobe B., Kajava A.V. The leucine-rich repeat as a protein recognition motif. Curr. Opin. Struct. Biol. 11:2001;725-732
63. Lai E.M., Kado C.I. The T-pilus of Agrobacterium tumefaciens. TIM. 8:2000;361-369
64. Lavie M., Shillington E., Eguiluz C., Grimsley N., Boucher C. 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. 15:2002;1058-1068
65. Lee C.A. Type III secretion systems: machines to deliver bacterial proteins into eukaryotic cells? TIM. 5:1997;148-156
66. Lee V.T., Schneewind O. Type III secretion machines and the pathogenesis of enteric infections caused by Yersinia and Salmonella spp. Immunol. Rev. 168:1999;241-255
67. Lee J., Klusener B., Tsiamis G., Stevens C., Neyt C., Tampakaki A.P., et al. HrpZ(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. U. S. A. 98:2001;289-294
68. Letoffe S., Ghigo J.M., Wandersman C. Secretion of the Serratia marcescens HasA protein by an ABC transporter. J. Bacteriol. 176:1994;5372-5377
69. Lindgren P.B. The role of hrp genes during plant-bacterial interactions. Annu. Rev. Phytopathol. 35:1997;129-152
70. Lugtenberg B.J., Chin A.W.T.F., Bloemberg G.V. Microbe-plant interactions: principles and mechanisms. Antonie van Leeuwenhoek. 81:2002;373-383
71. Lyczak J.B., Cannon C.L., Pier G.B. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect. 2:2000;1051-1060
72. Mahajan-Miklos S., Tan M.W., Rahme L.G., Ausubel F.M. Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa Caenorhabditis elegans pathogenesis model. Cell. 96:1999;47-56
73. Mahajan-Miklos S., Rahme L.G., Ausubel F.M. Elucidating the molecular mechanisms of bacterial virulence using non-mammalian hosts. Mol. Microbiol. 37:2000;981-988
74. Maleck K., Dietrich R.A. Defense on multiple fronts: how do plants cope with diverse enemies? Trends Plant Sci. 4:1999;215-219
75. Mecsas J., Strauss E.J. Molecular mechanisms of bacterial virulence: type III secretion and pathogenicity islands. Emerg. Infect. Dis. 2:1996;271-288
76. Miller M.B., Bassler B.L. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55:2001;165-199
77. Miyata S., Casey M., Frank D.W., Ausubel F.M., Drenkard E. Use of the Galleria mellonella caterpillar as a model host to study the role of the type III secretion system in Pseudomonas aeruginosa pathogenesis. Infect. Immun. 71:2003;2404-2413
78. Mukhopadhyay P., Williams J., Mills D. Molecular analysis of a pathogenicity locus in Pseudomonas syringae pv. syringae. J. Bacteriol. 170:1988;5479-5488
79. Muller S., Feldman M.F., Cornelis G.R. The Type III secretion system of Gram-negative bacteria: a potential therapeutic target? Expert. Opin. Ther. Targets. 5:2001;327-339
80. Mulvey M.A. Adhesion and entry of uropathogenic Escherichia coli. Cell. Microbiol. 4:2002;257-271
81. Nougayrede J.P., Fernandes P.J., Donnenberg M.S. Adhesion of enteropathogenic Escherichia coli to host cells. Cell. Microbiol. 5:2003;359-372
82. Ojanen-Reuhs T., Kalkkinen N., Westerlund-Wikstrom B., van Doorn J., Haahtela K., Nurmiaho-Lassila E.L., et al. Characterization of the fimA gene encoding bundle-forming fimbriae of the plant pathogen Xanthomonas campestris pv. vesicatoria. J. Bacteriol. 179:1997;1280-1290
83. Okazaki I.J., Moss J. Common structure of the catalytic sites of mammalian and bacterial toxin ADP-ribosyltransferases. Mol. Cell. Biochem. 138:1994;177-181
84. Orth K. Function of the Yersinia effector YopJ. Curr. Opin. Microbiol. 5:2002;38-43
85. Orth K., Xu Z.H., Mudgett M.B., Bao Z.Q., Palmer L.E., Bliska J.B., et al. Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science. 290:2000;1594-1597
86. Osman S.F., Fett W.F., Fishman M.L. Exopolysaccharides of the phytopathogen Pseudomonas syringae pv. glycinea. J. Bacteriol. 166:1986;66-71
87. Page F., Altabe S., Hugouvieux-Cotte-Pattat N., Lacroix J.M., Robert-Baudouy J., Bohin J.P. Osmoregulated periplasmic glucan synthesis is required for Erwinia chrysanthemi pathogenicity. J. Bacteriol. 183:2001;3134-3141
88. Pallen M.J., Wren B.W. The HtrA family of serine proteases. Mol. Microbiol. 26:1997;209-221
89. Parniske M., HammondKosack K.E., Golstein C., Thomas C.M., Jones D.A., Harrison K., et al. Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell. 91:1997;821-832
90. Plotnikova J.M., Rahme L.G., Ausubel F.M. Pathogenesis of the human opportunistic pathogen Pseudomonas aeruginosa PA14 in Arabidopsis. Plant Physiol. 124:2000;1766-1774
91. Pukatzki S., Kessin R.H., Mekalanos J.J. The human pathogen Pseudomonas aeruginosa utilizes conserved virulence pathways to infect the social amoeba Dictyostelium discoideum. Proc. Natl. Acad. Sci. 99:2002;3159-3164
92. Pulcini E.D. Bacterial biofilms: a review of current research. Nephrologie. 22:2001;439-441
93. Rabin S.D., Hauser A.R. Pseudomonas aeruginosa ExoU, a toxin transported by the type III secretion system, kills Saccharomyces cerevisiae. Infect. Immun. 71:2003;4144-4150
94. Rahme L.G., Stevens E.J., Wolfort S.F., Shao J., Tompkins R.G., Ausubel F.M. Common virulence factors for bacterial pathogenicity in plants and animals. Science. 268:1995;1899-1902
95. Rahme L.G., Tan M.W., Le L., Wong S.M., Tompkins R.G., Calderwood S.B., et al. Use of model plant hosts to identify Pseudomonas aeruginosa virulence factors. Proc. Natl. Acad. Sci. U. S. A. 94:1997;13245-13250
96. Rahme L.G., Ausubel F.M., Cao H., Drenkard E., Goumnerov B.C., Lau G.W., et al. Plants and animals share functionally common bacterial virulence factors. Proc. Natl. Acad. Sci. U. S. A. 97:2000;8815-8821
97. Reimmann C., Beyeler M., Latifi A., Winteler H., Foglino M., Lazdunski A., et al. The global activator GacA of Pseudomonas aeruginosa PAO positively controls the production of the autoinducer N-butyryl-homoserine lactone and the formation of the virulence factors pyocyanin, cyanide, and lipase. Mol. Microbiol. 24:1997;309-319
98. Roine E., Raineri D.M., Romantschuk M., Wilson M., Nunn D.N. Characterization of type IV pilus genes in Pseudomonas syringae pv. tomato DC3000. Mol. Plant-Microbe Interact. 11:1998;1048-1056
99. Romantschuk M., Bamford D.H. The causal agent of halo blight in bean, Pseudomonas syringae pv. phaseolicola, attaches to stomata via its pili. Microb. Pathog. 1:1986;139-148
100. Romantschuk M., Nurmiaholassila E.L., Roine E., Suoniemi A. Pilus-mediated adsorption of Pseudomonas syringae to the surface of host and nonhost plant-leaves. J. Gen. Microbiol. 139:1993;2251-2260
101. Rubin G.M., Yandell M.D., Wortman J.R., Gabor Miklos G.L., Nelson C.R., Hariharan I.K., et al. Comparative genomics of the eukaryotes. Science. 287:2000;2204-2215
102. Sauer F.G., Mulvey M.A., Schilling J.D., Martinez J.J., Hultgren S.J. Bacterial pili: molecular mechanisms of pathogenesis. Curr. Opin. Microbiol. 3:2000;65-72
103. Sessa G., Martin G.B. Signal recognition and transduction mediated by the tomato Pto kinase: a paradigm of innate immunity in plants. Microbes Infect. 2:2000;1591-1597
104. Sexton J.A., Vogel J.P. Type IVB secretion by intracellular pathogens. Traffic. 3:2002;178-185
105. Shao F., Merritt P.M., Bao Z., Innes R.W., Dixon J.E. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell. 109:2002;575-588
106. Smith R.S., Iglewski B.H. P. aeruginosa quorum-sensing systems and virulence. Curr. Opin. Microbiol. 6:2003;56-60
107. Soto G.E., Hultgren S.J. Bacterial adhesins: common themes and variations in architecture and assembly. J. Bacteriol. 181:1999;1059-1071
108. Staskawicz B.J., Mudgett M.B., Dangl J.L., Galan J.E. Common and contrasting themes of plant and animal diseases. Science. 292:2001;2285-2289
109. Stenson T.H., Weiss A.A. DsbA and DsbC are required for secretion of pertussis toxin by Bordetella pertussis. Infect. Immun. 70:2002;2297-2303
110. Suoniemi A., Bjorklof K., Haahtela K., Romantschuk M. Pili of Pseudomonas syringae pathovar syringae enhance initiation of bacterial epiphytic colonization of bean. Microbiology (UK). 141:1995;497-503
111. Takeda K., Akira S. Toll receptors and pathogen resistance. Cell. Microbiol. 5:2003;143-153
112. Tan M.W., Rahme L.G., Sternberg J.A., Tompkins R.G., Ausubel F.M. Pseudomonas aeruginosa killing of Caenorhabditis elegans used to identify P. aeruginosa virulence factors. Proc. Natl. Acad. Sci. 96:1999;2408-2413
113. Tardy F., Homble F., Neyt C., Wattiez R., Cornelis G.R., Ruysschaert J.M., et al. Yersinia enterocolitica type III secretion-translocation system: channel formation by secreted Yops. EMBO J. 18:1999;6793-6799
114. Taylor L.H., Latham S.M., Woolhouse M.E.J. Risk factors for human disease emergence. Philos. Trans. R. Soc. Lond., B Biol. Sci. 356:2001;983-999
115. Thanassi D.G., Hultgren S.J. Multiple pathways allow protein secretion across the bacterial outer membrane. Curr. Opin. Cell Biol. 12:2000;420-430
116. Vincent-Sealy L.V., Thomas J.D., Commander P., Salmond G.P. Erwinia carotovora DsbA mutants: evidence for a periplasmic-stress signal transduction system affecting transcription of genes encoding secreted proteins. Microbiology (UK). 145:1999;1945-1958
117. Von Bodman S.B., Bauer W.D., Coplin D.L. Quorum sensing in plant-pathogenic bacteria. Annu. Rev. Phytopathol. 29:2003;29
118. Wall D., Kaiser D. Type IV pili and cell motility. Mol. Microbiol. 32:1999;1-10
119. Watnick P.I., Kolter R. Steps in the development of a Vibrio cholerae El Tor biofilm. Mol. Microbiol. 34:1999;586-595
120. Weiss A.A., Johnson F.D., Burns D.L. Molecular characterization of an operon required for pertussis toxin secretion. Proc. Natl. Acad. Sci. 90:1993;2970-2974
121. Wong S.M., Carroll P.A., Rahme L.G., Ausubel F.M., Calderwood S.B. Modulation of expression of the ToxR regulon in Vibrio cholerae by a member of the two-component family of response regulators. Infect. Immun. 66:1998;5854-5861
122. Yorgey P., Rahme L.G., Tan M.W., Ausubel F.M. The roles of mucD and alginate in the virulence of Pseudomonas aeruginosa in plants, nematodes and mice. Mol. Microbiol. 41:2001;1063-1076
123. Young N.D. The genetic architecture of resistance. Curr. Opin. Plant Biol. 3:2000;285-290
124. Yu J., Penaloza-Vazquez A., Chakrabarty A.M., Bender C.L. Involvement of the exopolysaccharide alginate in the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae. Mol. Microbiol. 33:1999;712-720
125. Yu J., Edwards-Jones B., Neyrolles O., Kroll J.S. Key role for DsbA in cell-to-cell spread of Shigella flexneri, permitting secretion of Ipa proteins into interepithelial protrusions. Infect. Immun. 68:2000;6449-6456
126. Zhang Y.X., Bak D.D., Heid H., Geider K. Molecular characterization of a protease secreted by Erwinia amylovora. J. Mol. Biol. 289:1999;1239-1251