The ABCs and 123s of bacterial secretion systems in plant pathogenesis

Annual Review of Phytopathology

Volumn 52, Issue , 2014, Pages 317-345

  Chang, Jeff H ^a   Desveaux, Darrell ^b,c   Creason, Allison L ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Effector; Export; Injection; Phytopathogen; Translocation; Virulence

Indexed keywords

BACTERIA; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PLANT;

BACTERIA; HOST-PATHOGEN INTERACTIONS; PLANTS;

EID: 84905483676     PISSN: 00664286     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev-phyto-011014-015624     Document Type: Article

References (229)

1. Abdallah AM, Bestebroer J, Savage NDL, de Punder K, van Zon M, et al. 2011. Mycobacterial secretion systems ESX-1 and ESX-5 play distinct roles in host cell death and inflammasome activation. J. Immunol. 187(9):4744-53
2. Afzal AJ, da Cunha L, Mackey D. 2011. Separable fragments and membrane tethering of Arabidopsis RIN4 regulate its suppression of PAMP-triggered immunity. Plant Cell 23(10):3798-811
3. Ahrens S, Geissler B, Satchell KJF. 2013. Identification of a His-Asp-Cys catalytic triad essential for function of the Rho inactivation domain (RID) of Vibrio cholerae MARTX toxin. J. Biol. Chem. 288(2):1397-408
4. Akeda Y, Galn JE. 2005. Chaperone release and unfolding of substrates in type III secretion. Nature 437(7060):911-15
5. Alfano JR, Collmer A. 2004. Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu. Rev. Phytopathol. 42:385-414
6. Bahar O, Pruitt R, Luu DD, Schwessinger B, Daudi A, et al. 2014. The Xanthomonas Ax21 protein is processed by the general secretory system and is secreted in association with outer membrane vesicles. PeerJ 2:e242
7. Barrozo RM, Cooke CL, Hansen LM, Lam AM, Gaddy JA, et al. 2013. Functional plasticity in the type IV secretion system of Helicobacter pylori. PLoS Pathog. 9(2):e1003189
8. Basler M, Mekalanos JJ. 2012. Type 6 secretion dynamics within and between bacterial cells. Science 337(6096):815
9. Basler M, Pilhofer M, Henderson GP, Jensen GJ, Mekalanos JJ. 2012. Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483(7388):182-86
10. Beck D, Vasisht N, Baglieri J, Monteferrante CG, vanDijl JM, et al. 2013. Ultrastructural characterisation of Bacillus subtilis TatA complexes suggests they are too small to form homooligomeric translocation pores. Biochim. Biophys. Acta 1833(8):1811-19
11. Bhatty M, Laverde Gomez JA, Christie PJ. 2013. The expanding bacterial type IV secretion lexicon. Res. Microbiol. 164(6):620-39
12. Bitter W, Houben ENG, Luirink J, Appelmelk BJ. 2009. Type VII secretion in mycobacteria: classification in line with cell envelope structure. Trends Microbiol. 17(8):337-38
13. Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, et al. 2009. Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326(5959):1509-12
14. Bocsanczy AM, Nissinen RM, Oh C-S, Beer SV. 2008. HrpN of Erwinia amylovora functions in the translocation of DspA/E into plant cells. Mol. Plant Pathol. 9(4):425-34
15. 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(3):681-83
16. Boquet P, Ricci V. 2012. Intoxication strategy of Helicobacter pylori VacA toxin. Trends Microbiol. 20(4):165-74
17. Bronstein PA, Marrichi M, Cartinhour S, Schneider DJ, DeLisa MP. 2005. Identification of a twinarginine translocation system in Pseudomonas syringae pv. tomato DC3000 and its contribution to pathogenicity and fitness. J. Bacteriol. 187(24):8450-61
18. Browning C, Shneider MM, Bowman VD, Schwarzer D, Leiman PG. 2012. Phage pierces the host cell membrane with the iron-loaded spike. Structure 20(2):326-39
19. Buttner D. 2012. Protein export according to schedule: architecture, assembly, and regulation of type III secretion systems from plant- and animal-pathogenic bacteria. Microbiol. Mol. Biol. Rev. 76(2):262-310
20. Buttner D, Gurlebeck D, Nol LD, Bonas U. 2004. HpaB from Xanthomonas campestris pv. vesicatoria acts as an exit control protein in type III-dependent protein secretion. Mol. Microbiol. 54(3):755-68
21. Buttner D, Lorenz C, Weber E, Bonas U. 2006. Targeting of two effector protein classes to the type III secretion system by a HpaC- and HpaB-dependent protein complex from Xanthomonas campestris pv. vesicatoria. Mol. Microbiol. 59(2):513-27
22. Caldelari I, Mann S, Crooks C, Palmer T. 2006. The Tat pathway of the plant pathogen Pseudomonas syringae is required for optimal virulence. Mol. Plant-Microbe Interact. 19(2):200-12
23. Cascales E, Christie PJ. 2004. Definition of a bacterial type IV secretion pathway for a DNA substrate. Science 304(5674):1170-73
24. Celik N, Webb CT, Leyton DL, Holt KE, Heinz E, et al. 2012.Abioinformatic strategy for the detection, classification and analysis of bacterial autotransporters. PLoS ONE 7(8):e43245
25. Champion PAD, Champion MM, Manzanillo P, Cox JS. 2009. ESX-1 secreted virulence factors are recognized by multiple cytosolic AAA ATPases in pathogenic mycobacteria. Mol. Microbiol. 73(5):950-62
26. Charkowski A, Blanco C, Condemine G, Expert D, Franza T, et al. 2012. The role of secretion systems and small molecules in soft-rot Enterobacteriaceae pathogenicity. Annu. Rev. Phytopathol. 50:425-49
27. Charkowski AO, Alfano JR, Preston G, Yuan J, He SY, Collmer A. 1998. The Pseudomonas syringae pv. tomato HrpW protein has domains similar to harpins and pectate lyases and can elicit the plant hypersensitive response and bind to pectate. J. Bacteriol. 180(19):5211-17
28. Charkowski AO, Huang HC, Collmer A. 1997. Altered localization of HrpZ in Pseudomonas syringae pv. syringae hrp mutants suggests that different components of the type III secretion pathway control protein translocation across the inner and outer membranes of gram-negative bacteria. J. Bacteriol. 179(12):3866-74
29. Chen J, de Felipe KS, Clarke M, Lu H, Anderson OR, et al. 2004. Legionella effectors that promote nonlytic release from protozoa. Science 303(5662):1358-61
30. Chen L, Hu B, Qian G, Wang C, Yang W, et al. 2009. Identification and molecular characterization of twin-arginine translocation system (Tat) in Xanthomonas oryzae pv. oryzae strain PXO99. Arch.Microbiol. 191(2):163-70
31. Chen L-Q, Hou B-H, Lalonde S, Takanaga H, Hartung ML, et al. 2010. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468(7323):527-32
32. Choi M-S, Kim W, Lee C, Oh C-S. 2013. Harpins, multifunctional proteins secreted by gram-negative plant-pathogenic bacteria. Mol. Plant-Microbe Interact. 26(10):1115-22
33. Christie PJ, Vogel JP. 2000. Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol. 8(8):354-60
34. Chung E-H, da Cunha L, Wu A-J, Gao Z, Cherkis K, et al. 2011. Specific threonine phosphorylation of a host target by two unrelated type III effectors activates a host innate immune receptor in plants. Cell Host Microbe 9(2):125-36
35. Cisneros DA, Bond PJ, Pugsley AP, Campos M, Francetic O. 2012. Minor pseudopilin self-assembly primes type II secretion pseudopilus elongation. EMBO J. 31(4):1041-53
36. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, et al. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393(6685):537-44
37. Corbett M, Virtue S, Bell K, Birch P, Burr T, et al. 2005. Identification of a new quorum-sensingcontrolled virulence factor in Erwinia carotovora subsp. atroseptica secreted via the type II targeting pathway. Mol. Plant-Microbe Interact. 18(4):334-42
38. Coros A, Callahan B, Battaglioli E, Derbyshire KM. 2008. The specialized secretory apparatus ESX-1 is essential for DNA transfer in Mycobacterium smegmatis. Mol. Microbiol. 69(4):794-808
39. Cunnac S, Chakravarthy S, Kvitko BH, Russell AB, Martin GB, Collmer A. 2011. Genetic disassembly and combinatorial reassembly identify aminimal functional repertoire of type III effectors in Pseudomonas syringae. Proc. Natl. Acad. Sci. USA 108(7):2975-80
40. da Silva FG, Shen Y, Dardick C, Burdman S, Yadav RC, et al. 2004. Bacterial genes involved in type I secretion and sulfation are required to elicit the rice Xa21-mediated innate immune response. Mol. Plant-Microbe Interact. 17(6):593-601
41. Daleke MH, Ummels R, Bawono P, Heringa J, Vandenbroucke-Grauls CMJE, et al. 2012. General secretion signal for the mycobacterial typeVII secretion pathway. Proc. Natl. Acad. Sci. USA 109(28):11342-47
42. Daleke MH, van derWoude AD, Parret AHA, Ummels R, de Groot AM, et al. 2012. Specific chaperones for the type VII protein secretion pathway. J. Biol. Chem. 287(38):31939-47
43. Das C, Ghosh TS, Mande SS. 2011. Computational analysis of the ESX-1 region of Mycobacterium tuberculosis: insights into the mechanism of type VII secretion system. PLoS ONE 6(11):e27980
44. de Jonge MI, Pehau-Arnaudet G, Fretz MM, Romain F, Bottai D, et al. 2007. ESAT-6 from Mycobacterium tuberculosis dissociates from its putative chaperone CFP-10 under acidic conditions and exhibits membrane-lysing activity. J. Bacteriol. 189(16):6028-34
45. De Maayer P, Venter SN, Kamber T, Duffy B, Coutinho TA, Smits THM. 2011. Comparative genomics of the type VI secretion systems of Pantoea and Erwinia species reveals the presence of putative effector islands that may be translocated by the VgrG and Hcp proteins. BMC Genomics 12:576
46. Delattre A-S, Saint N, Clantin B, Willery E, Lippens G, et al. 2011. Substrate recognition by thePOTRA domains of TpsB transporter FhaC. Mol. Microbiol. 81(1):99-112
47. Delepelaire P, Wandersman C. 1989. Protease secretion by Erwinia chrysanthemi. Proteases B and C are synthesized and secreted as zymogens without a signal peptide. J. Biol. Chem. 264(15):9083-89
48. Delepelaire P, Wandersman C. 1991. Characterization, localization and transmembrane organization of the three proteins PrtD, PrtE and PrtF necessary for protease secretion by the gram-negative bacterium Erwinia chrysanthemi. Mol. Microbiol. 5(10):2427-34
49. Deng WL, Preston G, Collmer A, Chang CJ, Huang HC. 1998. Characterization of the hrpC and hrpRS operons of Pseudomonas syringae pathovars syringae, tomato, and glycinea and analysis of the ability of hrpF, hrpG, hrcC, hrpT, and hrpV mutants to elicit the hypersensitive response and disease in plants. J. Bacteriol. 180(17):4523-31
50. Deslandes L, Rivas S. 2012. Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci. 17(11):644-55
51. Desvaux M, Hbraud M, Talon R, Henderson IR. 2009. Secretion and subcellular localizations of bacterial proteins: a semantic awareness issue. Trends Microbiol. 17(4):139-45
52. Desvaux M, Parham NJ, Scott-Tucker A, Henderson IR. 2004. The general secretory pathway: a general misnomer? Trends Microbiol. 12(7):306-9
53. Desveaux D, Singer AU, Wu A-J, McNulty BC, Musselwhite L, et al. 2007. Type III effector activation via nucleotide binding, phosphorylation, and host target interaction. PLoS Pathog. 3(3):e48
54. Ding Z, Christie PJ. 2003. Agrobacterium tumefaciens twin-arginine- dependent translocation is important for virulence, flagellation, and chemotaxis but not type IV secretion. J. Bacteriol. 185(3):760-71
55. Djamei A, Pitzschke A, Nakagami H, Rajh I, Hirt H. 2007. Trojan horse strategy in Agrobacterium transformation: abusing MAPK defense signaling. Science 318(5849):453-56
56. Doyle EL, Stoddard BL, Voytas DF, Bogdanove AJ. 2013.TALeffectors: highly adaptable phytobacterial virulence factors and readily engineered DNA-targeting proteins. Trends Cell Biol. 23(8):390-98
57. Duquesne S, Destoumieux-Garzn D, Peduzzi J, Rebuffat S. 2007. Microcins, gene-encoded antibacterial peptides from enterobacteria. Nat. Prod. Rep. 24(4):708-34
58. Engelhardt S, Lee J, Gbler Y, Kemmerling B, Haapalainen M-L, et al. 2009. Separable roles of the Pseudomonas syringae pv. phaseolicola accessory protein HrpZ1 in ion-conducting pore formation and activation of plant immunity. Plant J. 57(4):706-17
59. Esko JD, Doering TL, Raetz CR. 2009. Eubacteria and Archaea. In Essentials of Glycobiology, ed. A Varki, RD Cummings, JD Esko, HH Freeze, P Stanley, et al. Cold Spring Harbor: Cold Spring Harbor Lab. Press. 2nd ed.
60. Feng F, Zhou J-M. 2012. Plant-bacterial pathogen interactions mediated by type III effectors. Curr. Opin. Plant Biol. 15(4):469-76
61. Ferrandez Y, Condemine G. 2008. Novel mechanism of outer membrane targeting of proteins in gramnegative bacteria. Mol. Microbiol. 69(6):1349-57
62. Filloux A. 2010. Secretion signal and protein targeting in bacteria: a biological puzzle. J. Bacteriol. 192(15):3847-49
63. Flint JL, Kowalski JC, Karnati PK, Derbyshire KM. 2004. The RD1 virulence locus of Mycobacterium tuberculosis regulatesDNAtransfer in Mycobacterium smegmatis. Proc. Natl. Acad. Sci. USA 101(34):12598-603
64. Fortune SM, Jaeger A, Sarracino DA, Chase MR, Sassetti CM, et al. 2005. Mutually dependent secretion of proteins required for mycobacterial virulence. Proc. Natl. Acad. Sci. USA 102(30):10676-81
65. Fronzes R, Christie PJ, Waksman G. 2009. The structural biology of type IV secretion systems. Nat. Rev. Microbiol. 7(10):703-14
66. Fronzes R, Schfer E, Wang L, Saibil HR, Orlova EV, Waksman G. 2009. Structure of a type IV secretion system core complex. Science 323(5911):266-68
67. Fu ZQ, Guo M, Jeong B-R, Tian F, Elthon TE, et al. 2007. A type III effector ADP-ribosylates RNAbinding proteins and quells plant immunity. Nature 447(7142):284-88
68. Fyans JK, Bignell D, Loria R, Toth I, Palmer T. 2013. The ESX/type VII secretion system modulates development, but not virulence, of the plant pathogen Streptomyces scabies. Mol. Plant Pathol. 14(2):119-30
69. Galn JE, Wolf-Watz H. 2006. Protein delivery into eukaryotic cells by type III secretion machines. Nature 444(7119):567-73
70. Genin S, Denny TP. 2012. Pathogenomics of the Ralstonia solanacearum species complex. Annu. Rev. Phytopathol. 50:67-89
71. Gey Van Pittius NC, Gamieldien J, Hide W, Brown GD, Siezen RJ, Beyers AD. 2001. The ESAT-6 gene cluster of Mycobacterium tuberculosis and other high G + C gram-positive bacteria. Genome Biol. 2(10):RESEARCH0044
72. Gonzlez A, Plener L, Restrepo S, Boucher C, Genin S. 2011. Detection and functional characterization of a large genomic deletion resulting in decreased pathogenicity in Ralstonia solanacearum race 3 biovar 2 strains. Environ. Microbiol. 13(12):3172-85
73. Gonzlez ET, Brown DG, Swanson JK, Allen C. 2007. Using the Ralstonia solanacearum Tat secretome to identify bacterial wilt virulence factors. Appl. Environ. Microbiol. 73(12):3779-86
74. Goodner B, Hinkle G, Gattung S, Miller N, Blanchard M, et al. 2001. Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294(5550):2323-28
75. Gottig N, Garavaglia BS, Garofalo CG, Orellano EG, Ottado J. 2009. A filamentous hemagglutinin-like protein of Xanthomonas axonopodis pv. citri, the phytopathogen responsible for citrus canker, is involved in bacterial virulence. PLoS ONE 4(2):e4358
76. Gray TA, Krywy JA, Harold J, Palumbo MJ, Derbyshire KM. 2013. Distributive conjugal transfer in mycobacteria generates progeny with meiotic-like genome-wide mosaicism, allowing mapping of a mating identity locus. PLoS Biol. 11(7):e1001602
77. Grijpstra J, Arenas J, Rutten L, Tommassen J. 2013. Autotransporter secretion: varying on a theme. Res. Microbiol. 164(6):562-82
78. 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(5560):1722-26
79. Haapalainen M, Mosorin H, Dorati F, Wu R-F, Roine E, et al. 2012. Hcp2, a secreted protein of the phytopathogen Pseudomonas syringae pv. tomato DC3000, is required for fitness for competition against bacteria and yeasts. J. Bacteriol. 194(18):4810-22
80. Hartmann N, Schulz S, Lorenz C, Fraas S, Hause G, Buttner D. 2012. Characterization of HrpB2 from Xanthomonas campestris pv. vesicatoria identifies protein regions that are essential for type III secretion pilus formation. Microbiology 158(Pt. 5):1334-49
81. Hassan S, Shevchik VE, Robert X, Hugouvieux-Cotte-Pattat N. 2013. PelN is a new pectate lyase of Dickeya dadantii with unusual characteristics. J. Bacteriol. 195(10):2197-206
82. Hausner J, Hartmann N, Lorenz C, Buttner D. 2013. The periplasmic HrpB1 protein from Xanthomonas spp. binds to peptidoglycan and to components of the type III secretion system. Appl. Environ.Microbiol. 79(20):6312-24
83. He SY, Jin Q. 2003. The Hrp pilus: learning from flagella. Curr. Opin. Microbiol. 6(1):15-19
84. Henrichfreise B, Schiefer A, Schneider T, Nzukou E, Poellinger C, et al. 2009. Functional conservation of the lipid II biosynthesis pathway in the cell wall-less bacteria Chlamydia and Wolbachia: Why is lipid II needed? Mol. Microbiol. 73(5):913-23
85. Hodak H, Clantin B, Willery E, Villeret V, Locht C, Jacob-Dubuisson F. 2006. Secretion signal of the filamentous haemagglutinin, a model two-partner secretion substrate. Mol. Microbiol. 61(2):368-82
86. Hood RD, Singh P, Hsu F, Guvener T, Carl MA, et al. 2010. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7(1):25-37
87. Houben D, Demangel C, van Ingen J, Perez J, Balden L, et al. 2012. ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria. Cell Microbiol. 14(8):1287-98
88. Houben ENG, Bestebroer J, Ummels R, Wilson L, Piersma SR, et al. 2012. Composition of the type VII secretion system membrane complex. Mol. Microbiol. 86(2):472-84
89. Ieva R, Bernstein HD. 2009. Interaction of an autotransporter passenger domain with BamA during its translocation across the bacterial outer membrane. Proc. Natl. Acad. Sci. USA 106(45):19120-25
90. Jacob-Dubuisson F, Gurin J, Baelen S, Clantin B. 2013. Two-partner secretion: as simple as it sounds? Res. Microbiol. 164(6):583-95
91. Jeong B-R, Lin Y, Joe A, Guo M, Korneli C, et al. 2011. Structure function analysis of an ADPribosyltransferase type III effector and its RNA-binding target in plant immunity. J. Biol. Chem. 286(50):43272-81
92. Jerse AE, Yu J, Tall BD, Kaper JB. 1990. A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells. Proc. Natl. Acad. Sci. USA 87(20):7839-43
93. Jimnez-Soto LF, Kutter S, Sewald X, Ertl C, Weiss E, et al. 2009. Helicobacter pylori type IV secretion apparatus exploits1 integrin in a novel RGD-independent manner. PLoS Pathog. 5(12):e1000684
94. Jin Q, He SY. 2001. Role of the Hrp pilus in type III protein secretion in Pseudomonas syringae. Science 294(5551):2556-58
95. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444(7117):323-29
96. Joshi MV, Mann SG, Antelmann H, Widdick DA, Fyans JK, et al. 2010. The twin arginine protein transport pathway exports multiple virulence proteins in the plant pathogen Streptomyces scabies. Mol. Microbiol. 77(1):252-71
97. Journet L, Agrain C, Broz P, Cornelis GR. 2003. The needle length of bacterial injectisomes is determined by a molecular ruler. Science 302(5651):1757-60
98. Kang Y, Huang J, Mao G, He LY, Schell MA. 1994. Dramatically reduced virulence of mutants of Pseudomonas solanacearum defective in export of extracellular proteins across the outer membrane. Mol. Plant-Microbe Interact. 7(3):370-77
99. Kanonenberg K, Schwarz CKW, Schmitt L. 2013. Type I secretion systems: a story of appendices. Res. Microbiol. 164(6):596-604
100. Kaplan-Turkoz B, Jimnez-Soto LF, Dian C, Ertl C, Remaut H, et al. 2012. Structural insights into Helicobacter pylori oncoproteinCagA interactionwith-1 integrin. Proc.Natl. Acad. Sci.USA109(36):14640-45
101. Kay S, Hahn S, Marois E, Hause G, Bonas U. 2007. A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318(5850):648-51
102. Kazemi-Pour N, Condemine G, Hugouvieux-Cotte-Pattat N. 2004. The secretome of the plant pathogenic bacterium Erwinia chrysanthemi. Proteomics 4(10):3177-86
103. Kenny B, DeVinney R, Stein M, Reinscheid DJ, Frey EA, Finlay BB. 1997. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91(4):511-20
104. Kimbrel JA, Thomas WJ, Jiang Y, Creason AL, Thireault CA, et al. 2013. Mutualistic co-evolution of type III effector genes in Sinorhizobium fredii and Bradyrhizobium japonicum. PLoS Pathog. 9(2):e1003204
105. Knowles TJ, Scott-Tucker A, Overduin M, Henderson IR. 2009. Membrane protein architects: the role of the BAM complex in outer membrane protein assembly. Nat. Rev. Microbiol. 7(3):206-14
106. Korotkov KV, Sandkvist M, Hol WGJ. 2012. The type II secretion system: biogenesis, molecular architecture and mechanism. Nat. Rev. Microbiol. 10(5):336-51
107. Koskiniemi S, Lamoureux JG, Nikolakakis KC, T'Kint de Roodenbeke C, Kaplan MD, et al. 2013. Rhs proteins from diverse bacteria mediate intercellular competition. Proc.Natl. Acad. Sci. USA110(17):7032-37
108. Kudryashov DS, Durer ZAO, Ytterberg AJ, Sawaya MR, Pashkov I, et al. 2008. Connecting actin monomers by iso-peptide bond is a toxicity mechanism of the Vibrio cholerae MARTX toxin. Proc. Natl. Acad. Sci. USA 105(47):18537-42
109. Kuper U, Meyer C, Muller V, Rachel R, Huber H. 2010. Energized outer membrane and spatial separation of metabolic processes in the hyperthermophilic archaeon Ignicoccus hospitalis. Proc. Natl. Acad. Sci. USA 107(7):3152-56
110. Kvitko BH, Park DH, Velsquez AC, Wei C-F, Russell AB, et al. 2009. Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector genes reveal functional overlap among effectors. PLoS Pathog. 5(4):e1000388
111. Kvitko BH, Ramos AR, Morello JE, Oh H-S, Collmer A. 2007. Identification of harpins in Pseudomonas syringae pv. tomato DC3000, which are functionally similar to HrpK1 in promoting translocation of type III secretion system effectors. J. Bacteriol. 189(22):8059-72
112. Lacroix B, Tzfira T, Vainstein A, Citovsky V. 2006. A case of promiscuity: Agrobacterium's endless hunt for new partners. Trends Genet. 22(1):29-37
113. Lara-Tejero M, Kato J, Wagner S, Liu X, Galn JE. 2011. A sorting platform determines the order of protein secretion in bacterial type III systems. Science 331(6021):1188-91
114. Leiman PG, Basler M, Ramagopal UA, Bonanno JB, Sauder JM, et al. 2009. Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc. Natl. Acad. Sci. USA 106(11):4154-59
115. Leo JC, Grin I, Linke D. 2012. Type V secretion: mechanism(s) of autotransport through the bacterial outer membrane. Philos. Trans. R. Soc. Lond. B 367(1592):1088-101
116. Ltoff S, Delepelaire P, Wandersman C. 1989. Characterization of a protein inhibitor of extracellular proteases produced by Erwinia chrysanthemi. Mol. Microbiol. 3(1):79-86
117. Leyton DL, Rossiter AE, Henderson IR. 2012. From self sufficiency to dependence: mechanisms and factors important for autotransporter biogenesis. Nat. Rev. Microbiol. 10(3):213-25
118. Li J-G, Liu H-X, Cao J, Chen L-F, Gu C, et al. 2010. PopW of Ralstonia solanacearum, a new two-domain harpin targeting the plant cell wall. Mol. Plant Pathol. 11(3):371-81
119. Li M, Le Trong I, Carl MA, Larson ET, Chou S, et al. 2012. Structural basis for type VI secretion effector recognition by a cognate immunity protein. PLoS Pathog. 8(4):e1002613
120. Lightbody KL, Ilghari D, Waters LC, Carey G, Bailey MA, et al. 2008. Molecular features governing the stability and specificity of functional complex formation by Mycobacterium tuberculosis CFP-10/ESAT-6 family proteins. J. Biol. Chem. 283(25):17681-90
121. Lindgren PB, Peet RC, Panopoulos NJ. 1986. Gene cluster of Pseudomonas syringae pv. "phaseolicola" controls pathogenicity of bean plants and hypersensitivity of nonhost plants. J. Bacteriol. 168(2):512-22
122. Linhartov I, Bumba L, Mas J, Basler M, Osicka R, et al. 2010. RTX proteins: a highly diverse family secreted by a common mechanism. FEMS Microbiol. Rev. 34(6):1076-112
123. Liu J, Elmore JM, Lin Z-JD, Coaker G. 2011. A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe 9(2):137-46
124. Locht C, Coutte L, Mielcarek N. 2011. The ins and outs of pertussis toxin. FEBS J. 278(23):4668-82
125. Loper JE, Hassan KA, Mavrodi DV, Davis EW, Lim CK, et al. 2012. Comparative genomics of plantassociated Pseudomonas spp.: insights into diversity and inheritance of traits involved in multitrophic interactions. PLoS Genet. 8(7):e1002784
126. Lorenz C, Buttner D. 2009. Functional characterization of the type III secretion ATPase HrcN from the plant pathogen Xanthomonas campestris pv. vesicatoria. J. Bacteriol. 191(5):1414-28
127. Lorenz C, Buttner D. 2011. Secretion of early and late substrates of the type III secretion system from Xanthomonas is controlled by HpaC and the C-terminal domain of HrcU. Mol. Microbiol. 79(2):447-67
128. Lorenz C, Hausner J, Buttner D. 2012. HrcQ provides a docking site for early and late type III secretion substrates from Xanthomonas. PLoS ONE 7(11):e51063
129. Lorenz C, Schulz S, Wolsch T, Rossier O, Bonas U, Buttner D. 2008. HpaC controls substrate specificity of the Xanthomonas type III secretion system. PLoS Pathog. 4(6):e1000094
130. Lu YY, Franz B, Truttmann MC, Riess T, Gay Fraret J, et al. 2013. Bartonella henselae trimeric autotransporter adhesin BadA expression interferes with effector translocation by the VirB/D4 type IV secretion system. Cell Microbiol. 15(5):759-78
131. Luo Z-Q. 2012. Legionella secreted effectors and innate immune responses. Cell Microbiol. 14(1):19-27
132. Lycklama A, Nijeholt JA, Driessen AJM. 2012. The bacterial Sec-translocase: structure and mechanism. Philos. Trans. R. Soc. Lond. B 367(1592):1016-28
133. Ma AT, McAuley S, Pukatzki S, Mekalanos JJ. 2009. Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe 5(3):234-43
134. 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(6):743-54
135. MakAN-S, Bradley P, Bogdanove AJ, Stoddard BL. 2013.TALeffectors: function, structure, engineering and applications. Curr. Opin. Struct. Biol. 23(1):93-99
136. Marits R, Koiv V, Laasik E, Me A. 1999. Isolation of an extracellular protease gene of Erwinia carotovora subsp. carotovora strain SCC3193 by transposon mutagenesis and the role of protease in phytopathogenicity. Microbiology 145(Pt. 8):1959-66
137. Marlovits TC, Kubori T, Sukhan A, Thomas DR, Galn JE, Unger VM. 2004. Structural insights into the assembly of the type III secretion needle complex. Science 306(5698):1040-42
138. Matsumoto A, Huston SL, Killiny N, Igo MM. 2012. XatA, an AT-1 autotransporter important for the virulence of Xylella fastidiosa Temecula1. MicrobiologyOpen 1(1):33-45
139. Mattinen L, Somervuo P, Nykyri J, Nissinen R, Kouvonen P, et al. 2008. Microarray profiling of host-extract-induced genes and characterization of the type VI secretion cluster in the potato pathogen Pectobacterium atrosepticum. Microbiology 154(Pt. 8):2387-96
140. Meibom KL, Blokesch M, Dolganov NA, Wu C-Y, Schoolnik GK. 2005. Chitin induces natural competence in Vibrio cholerae. Science 310(5755):1824-27
141. Miyata S, Casey M, Frank DW, Ausubel FM, Drenkard E. 2003. 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(5):2404-13
142. Moscou MJ, Bogdanove AJ. 2009. A simple cipher governs DNA recognition by TAL effectors. Science 326(5959):1501
143. Mota LJ. 2006. Type III secretion gets an LcrV tip. Trends Microbiol. 14(5):197-200
144. Nicaise V, Joe A, Jeong B-R, Korneli C, Boutrot F, et al. 2013. Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7. EMBO J. 32(5):701-12
145. Niederweis M, Danilchanka O, Huff J, Hoffmann C, Engelhardt H. 2010. Mycobacterial outer membranes: in search of proteins. Trends Microbiol. 18(3):109-16
146. Niepold F, Anderson D, Mills D. 1985. Cloning determinants of pathogenesis from Pseudomonas syringae pathovar syringae. Proc. Natl. Acad. Sci. USA 82(2):406-10
147. Nomura K, Debroy S, Lee Y, Pumplin N, Jones J, He S. 2006. A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313(5784):220-23
148. Nomura K, Mecey C, Lee YN, Imboden LA, Chang JH, He SY. 2011. Effector-triggered immunity blocks pathogen degradation of an immunity-associated vesicle traffic regulator in Arabidopsis. Proc. Natl. Acad. Sci. USA 108(26):10774-79
149. Nykyri J, Niemi O, Koskinen P, Nokso-Koivisto J, Pasanen M, et al. 2012. Revised phylogeny and novel horizontally acquired virulence determinants of the model soft rot phytopathogen Pectobacterium wasabiae SCC3193. PLoS Pathog. 8(11):e1003013
150. Oberhettinger P, Schutz M, Leo JC, Heinz N, Berger J, et al. 2012. Intimin and invasin export their C-terminus to the bacterial cell surface using an inverse mechanism compared to classical autotransport. PLoS ONE 7(10):e47069
151. Ohol YM, Goetz DH, Chan K, Shiloh MU, Craik CS, Cox JS. 2010. Mycobacterium tuberculosis MycP1 protease plays a dual role in regulation of ESX-1 secretion and virulence. Cell Host Microbe 7(3):210-20
152. Okuda S, Tokuda H. 2011. Lipoprotein sorting in bacteria. Annu. Rev. Microbiol. 65:239-59
153. Oldani A, Cormont M, Hofman V, Chiozzi V, Oregioni O, et al. 2009. Helicobacter pylori counteracts the apoptotic action of its VacA toxin by injecting the CagA protein into gastric epithelial cells. PLoS Pathog. 5(10):e1000603
154. Pallen MJ. 2002. The ESAT-6/WXG100 superfamily-and a new Gram-positive secretion system? Trends Microbiol. 10(5):209-12
155. Palmer T, Berks BC. 2012. The twin-arginine translocation (Tat) protein export pathway. Nat. Rev. Microbiol. 10(7):483-96
156. Park E, Rapoport TA. 2012. Mechanisms of Sec61/SecY-mediated protein translocation across membranes. Annu. Rev. Biophys. 41:21-40
157. Pavlova O, Peterson JH, Ieva R, Bernstein HD. 2013. Mechanistic link betweenbarrel assembly and the initiation of autotransporter secretion. Proc. Natl. Acad. Sci. USA 110(10):E938-47
158. Prez-Mendoza D, Coulthurst SJ, Humphris S, Campbell E, Welch M, et al. 2011. A multi-repeat adhesin of the phytopathogen, Pectobacterium atrosepticum, is secreted by a Type I pathway and is subject to complex regulation involving a non-canonical diguanylate cyclase. Mol. Microbiol. 82(3):719-33
159. Pitzschke A, Djamei A, Teige M, Hirt H. 2009. VIP1 response elements mediate mitogen-activated protein kinase 3-induced stress gene expression. Proc. Natl. Acad. Sci. USA 106(43):18414-19
160. Preston GM, Studholme DJ, Caldelari I. 2005. Profiling the secretomes of plant pathogenic Proteobacteria. FEMS Microbiol. Rev. 29(2):331-60
161. Pukatzki S, Ma AT, Revel AT, Sturtevant D, Mekalanos JJ. 2007. Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc. Natl. Acad. Sci. USA 104(39):15508-13
162. Ray SK, Rajeshwari R, Sonti RV. 2000. Mutants of Xanthomonas oryzae pv. oryzae deficient in general secretory pathway are virulence deficient and unable to secrete xylanase. Mol. Plant-Microbe Interact. 13(4):394-401
163. Records AR. 2011. The type VI secretion system: a multipurpose delivery system with a phage-like machinery. Mol. Plant-Microbe Interact. 24(7):751-57
164. Records AR, Gross DC. 2010. Sensor kinases RetS and LadS regulate Pseudomonas syringae type VI secretion and virulence factors. J. Bacteriol. 192(14):3584-96
165. Rees DC, Johnson E, Lewinson O. 2009. ABC transporters: the power to change. Nat. Rev. Mol. Cell Biol. 10(3):218-27
166. Reichow SL, Korotkov KV, Hol WGJ, Gonen T. 2010. Structure of the cholera toxin secretion channel in its closed state. Nat. Struct. Mol. Biol. 17(10):1226-32
167. Renshaw PS, Panagiotidou P, Whelan A, Gordon SV, Hewinson RG, et al. 2002. Conclusive evidence that the major T-cell antigens of the Mycobacterium tuberculosis complex ESAT-6 and CFP-10 form a tight, 1:1 complex and characterization of the structural properties of ESAT-6, CFP-10, and the ESAT- 6CFP-10 complex. Implications for pathogenesis and virulence. J. Biol. Chem. 277(24):21598-603
168. Reva O, Tmmler B. 2008. Think big: giant genes in bacteria. Environ. Microbiol. 10(3):768-77
169. Rodriguez F, Rouse SL, Tait CE, Harmer J, De Riso A, et al. 2013. Structural model for the proteintranslocating element of the twin-arginine
170. Rodruez E, Gaggero C, Lavi na M. 1999. The structural gene for microcin H47 encodes a peptide precursor with antibiotic activity. Antimicrob. Agents Chemother. 43(9):2176-82
171. Rojas CM, Ham JH, Deng W-L, Doyle JJ, Collmer A. 2002. HecA, a member of a class of adhesins produced by diverse pathogenic bacteria, contributes to the attachment, aggregation, epidermal cell killing, and virulence phenotypes of Erwinia chrysanthemi EC16 on Nicotiana clevelandii seedlings. Proc. Natl. Acad. Sci. USA 99(20):13142-47
172. Rmer P, Hahn S, Jordan T, Strauss T, Bonas U, Lahaye T. 2007. Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science 318(5850):645-48
173. Rosch JW, Caparon MG. 2005. The ExPortal: an organelle dedicated to the biogenesis of secreted proteins in Streptococcus pyogenes. Mol. Microbiol. 58(4):959-68
174. Ruhe ZC, Low DA, Hayes CS. 2013. Bacterial contact-dependent growth inhibition. Trends Microbiol. 21(5):230-37
175. Russell AB, Hood RD, Bui NK, LeRoux M, Vollmer W, Mougous JD. 2011. Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475(7356):343-47
176. Salama NR, Hartung ML, Muller A. 2013. Life in the human stomach: persistence strategies of the bacterial pathogen Helicobacter pylori. Nat. Rev. Microbiol. 11(6):385-99
177. Salomon D, Orth K. 2013. What pathogens have taught us about posttranslational modifications. Cell Host Microbe 14(3):269-79
178. Snchez J, Holmgren J. 2008. Cholera toxin structure, gene regulation and pathophysiological and immunological aspects. Cell. Mol. Life Sci. 65(9):1347-60
179. Snchez-Magrane rL, Cortajarena AL, Garc-Pacios M, Arrondo J-LR, Agirre J, et al. 2010. Interdomain Ca2+ effects in Escherichia coli-haemolysin: Ca2+ binding to the C-terminal domain stabilizes both C- and N-terminal domains. Biochim. Biophys. Acta 1798(6):1225-33
180. Satchell KJF. 2011. Structure and function of MARTX toxins and other large repetitive RTX proteins. Annu. Rev. Microbiol. 65:71-90
181. Schraidt O, Marlovits TC. 2011. Three-dimensional model of Salmonella's needle complex at subnanometer resolution. Science 331(6021):1192-95
182. Schreiber KJ, Desveaux D. 2011. AlgW regulates multiple Pseudomonas syringae virulence strategies. Mol. Microbiol. 80(2):364-77
183. Schwarz S, West TE, Boyer F, Chiang W-C, Carl MA, et al. 2010. Burkholderia typeVI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog. 6(8):e1001068
184. Serafini A, Boldrin F, Pal uG, Manganelli R. 2009. Characterization of a Mycobacterium tuberculosis ESX-3 conditional mutant: essentiality and rescue by iron and zinc. J. Bacteriol. 191(20):6340-44
185. Shneider MM, Buth SA, Ho BT, Basler M, Mekalanos JJ, Leiman PG. 2013. PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 500(7462):350-53
186. Sikora AE. 2013. Proteins secreted via the type II secretion system: smart strategies of Vibrio cholerae to maintain fitness in different ecological niches. PLoS Pathog. 9(2):e1003126
187. Silverman JM, Brunet YR, Cascales E, Mougous JD. 2012. Structure and regulation of the type VI secretion system. Annu. Rev. Microbiol. 66:453-72
188. Simeone R, Bobard A, Lippmann J, Bitter W, Majlessi L, et al. 2012. Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death. PLoS Pathog. 8(2):e1002507
189. Simeone R, Bottai D, Brosch R. 2009. ESX/type VII secretion systems and their role in host-pathogen interaction. Curr. Opin. Microbiol. 12(1):4-10
190. Simpson AJ, Reinach FC, Arruda P, Abreu FA, Acencio M, et al. 2000. The genome sequence of the plant pathogen Xylella fastidiosa. The Xylella fastidiosa Consortium of the Organization for Nucleotide Sequencing and Analysis. Nature 406(6792):151-59
191. Smith J, Manoranjan J, Pan M, Bohsali A, Xu J, et al. 2008. Evidence for pore formation in host cell membranes by ESX-1-secreted ESAT-6 and its role in Mycobacterium marinum escape from the vacuole. Infect. Immun. 76(12):5478-87
192. Solomonson M, Huesgen PF, Wasney GA, Watanabe N, Gruninger RJ, et al. 2013. Structure of the mycosin-1 protease from the mycobacterial ESX-1 protein type VII secretion system. J. Biol. Chem. 288(24):17782-90
193. Sory MP, Cornelis GR. 1994. Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol. Microbiol. 14(3):583-94
194. Soscia C, Hachani A, Bernadac A, Filloux A, Bleves S. 2007. Cross talk between type III secretion and flagellar assembly systems in Pseudomonas aeruginosa. J. Bacteriol. 189(8):3124-32
195. Stingl K, Muller S, Scheidgen-Kleyboldt G, Clausen M, Maier B. 2010. Composite system mediates two-step DNA uptake into Helicobacter pylori. Proc. Natl. Acad. Sci. USA 107(3):1184-89
196. Stoop EJM, Bitter W, van der Sar AM. 2012. Tubercle bacilli rely on a type VII army for pathogenicity. Trends Microbiol. 20(10):477-84
197. Suarez G, Sierra JC, Erova TE, Sha J, Horneman AJ, Chopra AK. 2010. A type VI secretion system effector protein, VgrG1, from Aeromonas hydrophila that induces host cell toxicity by ADP ribosylation of actin. J. Bacteriol. 192(1):155-68
198. Sun Y-H, Roln HG, Tsolis RM. 2007. Injection of flagellin into the host cell cytosol by Salmonella enterica serotype Typhimurium. J. Biol. Chem. 282(47):33897-901
199. Szczesny R, Jordan M, Schramm C, Schulz S, Cogez V, et al. 2010. Functional characterization of the Xcs and Xps type II secretion systems from the plant pathogenic bacterium Xanthomonas campestris pv vesicatoria. New Phytol. 187(4):983-1002
200. Tampakaki AP, Skandalis N, Gazi AD, Bastaki MN, Sarris PF, et al. 2010. Playing the "Harp": evolution of our understanding of hrp/hrc genes. Annu. Rev. Phytopathol. 48:347-70
201. Toth IK, Bell KS, Holeva MC, Birch PRJ. 2003. Soft rot erwiniae: from genes to genomes. Mol. Plant Pathol. 4(1):17-30
202. Trachtenberg S. 1998. Mollicutes-wall-less bacteria with internal cytoskeletons. J. Struct. Biol. 124(2- 3):244-56
203. Troisfontaines P, Cornelis GR. 2005. Type III secretion: more systems than you think. Physiology (Bethesda) 20:326-39
204. Tsugawa H, Suzuki H, Saya H, Hatakeyama M, Hirayama T, et al. 2012. Reactive oxygen species- induced autophagic degradation of Helicobacter pylori CagA is specifically suppressed in cancer stem-like cells. Cell Host Microbe 12(6):764-77
205. Tzfira T, Vaidya M, Citovsky V. 2001. VIP1, an Arabidopsis protein that interacts with Agrobacterium VirE2, is involved in VirE2 nuclear import and Agrobacterium infectivity. EMBO J. 20(13):3596-607
206. Tzfira T, Vaidya M, Citovsky V. 2004. Involvement of targeted proteolysis in plant genetic transformation by Agrobacterium. Nature 431(7004):87-92
207. van den Berg B. 2010. Crystal structure of a full-length autotransporter. J. Mol. Biol. 396(3):627-33
208. van der Wel N, Hava D, Houben D, Fluitsma D, van Zon M, et al. 2007. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 129(7):1287-98
209. Veena Jiang H, Doerge RW, Gelvin SB. 2003. Transfer of T-DNA and Vir proteins to plant cells by Agrobacterium tumefaciens induces expression of host genes involved in mediating transformation and suppresses host defense gene expression. Plant J. 35(2):219-36
210. Voegel TM, Warren JG, Matsumoto A, Igo MM, Kirkpatrick BC. 2010. Localization and characterization of Xylella fastidiosa haemagglutinin adhesins. Microbiology 156(Pt. 7):2172-79
211. Vojtova J, Kamanov J, Sebo P. 2006. Bordetella adenylate cyclase toxin: a swift saboteur of host defense. Curr. Opin. Microbiol. 9(1):69-75
212. Voulhoux R, Ball G, Ize B, Vasil ML, Lazdunski A, et al. 2001. Involvement of the twin-arginine translocation system in protein secretion via the type II pathway. EMBO J. 20(23):6735-41
213. Wagner JM, Evans TJ, Chen J, Zhu H, Houben ENG, et al. 2013. Understanding specificity of the mycosin proteases in ESX/typeVII secretion by structural and functional analysis. J. Struct. Biol. 184(2):115-28
214. Wagner JM, Evans TJ, Korotkov KV. 2014. Crystal structure of the N-terminal domain of EccA1 ATPase from the ESX-1 secretion system of Mycobacterium tuberculosis. Proteins 82(1):159-63
215. Walker D, Lancaster L, James R, Kleanthous C. 2004. Identification of the catalyticmotif of themicrobial ribosome inactivating cytotoxin colicin E3. Protein Sci. 13(6):1603-11
216. Wallden K, Williams R, Yan J, Lian PW, Wang L, et al. 2012. Structure of the VirB4 ATPase, alone and bound to the core complex of a type IV secretion system. Proc. Natl. Acad. Sci. USA 109(28):11348-53
217. Weerdenburg EM, Abdallah AM, Mitra S, de Punder K, van der Wel NN, et al. 2012. ESX-5-deficient Mycobacterium marinum is hypervirulent in adult zebrafish. Cell Microbiol. 14(5):728-39
218. Wei H-L, Chakravarthy S, Worley JN, Collmer A. 2012. Consequences of flagellin export through the type III secretion system of Pseudomonas syringae reveal a major difference in the innate immune systems of mammals and the model plant Nicotiana benthamiana. Cell Microbiol. 15:601-18
219. Wood DW, Setubal JC, Kaul R, Monks DE, Kitajima JP, et al. 2001. The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294(5550):2317-23
220. Wu C-F, Lin J-S, Shaw G-C, Lai E-M. 2012. Acid-induced type VI secretion system is regulated by ExoR-ChvG/ChvI signaling cascade in Agrobacterium tumefaciens. PLoS Pathog. 8(9):e1002938
221. WuH-Y, Chung P-C, Shih H-W, Wen S-R, Lai E-M. 2008. Secretome analysis uncovers anHcp-family protein secreted via a type VI secretion system in Agrobacterium tumefaciens. J. Bacteriol. 190(8):2841-50
222. Yang J, Zhao Y, Shi J, Shao F. 2013. Human NAIP and mouse NAIP1 recognize bacterial type III secretion needle protein for inflammasome activation. Proc. Natl. Acad. Sci. USA 110(35):14408-13
223. Yokoyama K, Higashi H, Ishikawa S, Fujii Y, Kondo S, et al. 2005. Functional antagonism between Helicobacter pylori CagA and vacuolating toxin VacA in control of the NFAT signaling pathway in gastric epithelial cells. Proc. Natl. Acad. Sci. USA 102(27):9661-66
224. Young GM, Schmiel DH, Miller VL. 1999. A new pathway for the secretion of virulence factors by bacteria: The flagellar export apparatus functions as a protein-secretion system. Proc. Natl. Acad. Sci. USA 96(11):6456-61
225. Zaltsman A, Krichevsky A, Loyter A, Citovsky V. 2010. Agrobacterium induces expression of a host F-box protein required for tumorigenicity. Cell Host Microbe 7(3):197-209
226. Zechner EL, Lang S, Schildbach JF. 2012. Assembly and mechanisms of bacterial type IV secretion machines. Philos. Trans. R. Soc. Lond. B 367(1592):1073-87
227. Zgurskaya HI, Krishnamoorthy G, Ntreh A, Lu S. 2011. Mechanism and function of the outer membrane channel TolC in multidrug resistance and physiology of enterobacteria. Front. Microbiol. 2:189
228. Zhang Y, Bak DD, Heid H, Geider K. 1999. Molecular characterization of a protease secreted by Erwinia amylovora. J. Mol. Biol. 289(5):1239-51
229. Zhao Y, Qi M. 2011. Comparative genomics of Erwinia amylovora and related Erwinia species: What do we learn? Genes 2(3):627-39