1932

Abstract

Bacteria have many export and secretion systems that translocate cargo into and across biological membranes. Seven secretion systems contribute to pathogenicity by translocating proteinaceous cargos that can be released into the extracellular milieu or directly into recipient cells. In this review, we describe these secretion systems and how their complexities and functions reflect differences in the destinations, states, functions, and sizes of the translocated cargos as well as the architecture of the bacterial cell envelope. We examine the secretion systems from the perspective of pathogenic bacteria that proliferate within plant tissues and highlight examples of translocated proteins that contribute to the infection and disease of plant hosts.

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2014-08-04
2024-04-26
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Literature Cited

  1. Abdallah AM, Bestebroer J, Savage NDL, de Punder K, van Zon M. 1.  et al. 2011. Mycobacterial secretion systems ESX-1 and ESX-5 play distinct roles in host cell death and inflammasome activation. J. Immunol. 187:94744–53 [Google Scholar]
  2. Afzal AJ, da Cunha L, Mackey D. 2.  2011. Separable fragments and membrane tethering of Arabidopsis RIN4 regulate its suppression of PAMP-triggered immunity. Plant Cell 23:103798–811 [Google Scholar]
  3. Ahrens S, Geissler B, Satchell KJF. 3.  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. 288:21397–408 [Google Scholar]
  4. Akeda Y, Galán JE. 4.  2005. Chaperone release and unfolding of substrates in type III secretion. Nature 437:7060911–15 [Google Scholar]
  5. Alfano JR, Collmer A. 5.  2004. Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu. Rev. Phytopathol. 42:385–414 [Google Scholar]
  6. Bahar O, Pruitt R, Luu DD, Schwessinger B, Daudi A. 6.  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 [Google Scholar]
  7. Barrozo RM, Cooke CL, Hansen LM, Lam AM, Gaddy JA. 7.  et al. 2013. Functional plasticity in the type IV secretion system of Helicobacter pylori. PLoS Pathog. 9:2e1003189 [Google Scholar]
  8. Basler M, Mekalanos JJ. 8.  2012. Type 6 secretion dynamics within and between bacterial cells. Science 337:6096815 [Google Scholar]
  9. Basler M, Pilhofer M, Henderson GP, Jensen GJ, Mekalanos JJ. 9.  2012. Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483:7388182–86 [Google Scholar]
  10. Beck D, Vasisht N, Baglieri J, Monteferrante CG, van Dijl JM. 10.  et al. 2013. Ultrastructural characterisation of Bacillus subtilis TatA complexes suggests they are too small to form homooligomeric translocation pores. Biochim. Biophys. Acta 1833:81811–19 [Google Scholar]
  11. Bhatty M, Laverde Gomez JA, Christie PJ. 11.  2013. The expanding bacterial type IV secretion lexicon. Res. Microbiol. 164:6620–39 [Google Scholar]
  12. Bitter W, Houben ENG, Luirink J, Appelmelk BJ. 12.  2009. Type VII secretion in mycobacteria: classification in line with cell envelope structure. Trends Microbiol. 17:8337–38 [Google Scholar]
  13. Boch J, Scholze H, Schornack S, Landgraf A, Hahn S. 13.  et al. 2009. Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326:59591509–12 [Google Scholar]
  14. Bocsanczy AM, Nissinen RM, Oh C-S, Beer SV. 14.  2008. HrpN of Erwinia amylovora functions in the translocation of DspA/E into plant cells. Mol. Plant Pathol. 9:4425–34 [Google Scholar]
  15. Bogdanove AJ, Beer SV, Bonas U, Boucher CA, Collmer A. 15.  et al. 1996. Unified nomenclature for broadly conserved hrp genes of phytopathogenic bacteria. Mol. Microbiol. 20:3681–83 [Google Scholar]
  16. Boquet P, Ricci V. 16.  2012. Intoxication strategy of Helicobacter pylori VacA toxin. Trends Microbiol. 20:4165–74 [Google Scholar]
  17. Bronstein PA, Marrichi M, Cartinhour S, Schneider DJ, DeLisa MP. 17.  2005. Identification of a twin-arginine translocation system in Pseudomonas syringae pv. tomato DC3000 and its contribution to pathogenicity and fitness. J. Bacteriol. 187:248450–61 [Google Scholar]
  18. Browning C, Shneider MM, Bowman VD, Schwarzer D, Leiman PG. 18.  2012. Phage pierces the host cell membrane with the iron-loaded spike. Structure 20:2326–39 [Google Scholar]
  19. Büttner D. 19.  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. 76:2262–310 [Google Scholar]
  20. Büttner D, Gürlebeck D, Noël LD, Bonas U. 20.  2004. HpaB from Xanthomonas campestris pv. vesicatoria acts as an exit control protein in type III–dependent protein secretion. Mol. Microbiol. 54:3755–68 [Google Scholar]
  21. Büttner D, Lorenz C, Weber E, Bonas U. 21.  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. 59:2513–27 [Google Scholar]
  22. Caldelari I, Mann S, Crooks C, Palmer T. 22.  2006. The Tat pathway of the plant pathogen Pseudomonas syringae is required for optimal virulence. Mol. Plant-Microbe Interact. 19:2200–12 [Google Scholar]
  23. Cascales E, Christie PJ. 23.  2004. Definition of a bacterial type IV secretion pathway for a DNA substrate. Science 304:56741170–73 [Google Scholar]
  24. Celik N, Webb CT, Leyton DL, Holt KE, Heinz E. 24.  et al. 2012. A bioinformatic strategy for the detection, classification and analysis of bacterial autotransporters. PLoS ONE 7:8e43245 [Google Scholar]
  25. Champion PAD, Champion MM, Manzanillo P, Cox JS. 25.  2009. ESX-1 secreted virulence factors are recognized by multiple cytosolic AAA ATPases in pathogenic mycobacteria. Mol. Microbiol. 73:5950–62 [Google Scholar]
  26. Charkowski A, Blanco C, Condemine G, Expert D, Franza T. 26.  et al. 2012. The role of secretion systems and small molecules in soft-rot Enterobacteriaceae pathogenicity. Annu. Rev. Phytopathol. 50:425–49 [Google Scholar]
  27. Charkowski AO, Alfano JR, Preston G, Yuan J, He SY, Collmer A. 27.  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. 180:195211–17 [Google Scholar]
  28. Charkowski AO, Huang HC, Collmer A. 28.  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. 179:123866–74 [Google Scholar]
  29. Chen J, de Felipe KS, Clarke M, Lu H, Anderson OR. 29.  et al. 2004. Legionella effectors that promote nonlytic release from protozoa. Science 303:56621358–61 [Google Scholar]
  30. Chen L, Hu B, Qian G, Wang C, Yang W. 30.  et al. 2009. Identification and molecular characterization of twin-arginine translocation system (Tat) in Xanthomonas oryzae pv. oryzae strain PXO99. Arch. Microbiol. 191:2163–70 [Google Scholar]
  31. Chen L-Q, Hou B-H, Lalonde S, Takanaga H, Hartung ML. 31.  et al. 2010. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:7323527–32 [Google Scholar]
  32. Choi M-S, Kim W, Lee C, Oh C-S. 32.  2013. Harpins, multifunctional proteins secreted by gram-negative plant-pathogenic bacteria. Mol. Plant-Microbe Interact. 26:101115–22 [Google Scholar]
  33. Christie PJ, Vogel JP. 33.  2000. Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol. 8:8354–60 [Google Scholar]
  34. Chung E-H, da Cunha L, Wu A-J, Gao Z, Cherkis K. 34.  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 9:2125–36 [Google Scholar]
  35. Cisneros DA, Bond PJ, Pugsley AP, Campos M, Francetic O. 35.  2012. Minor pseudopilin self-assembly primes type II secretion pseudopilus elongation. EMBO J. 31:41041–53 [Google Scholar]
  36. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C. 36.  et al. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:6685537–44 [Google Scholar]
  37. Corbett M, Virtue S, Bell K, Birch P, Burr T. 37.  et al. 2005. Identification of a new quorum-sensing-controlled virulence factor in Erwinia carotovora subsp. atroseptica secreted via the type II targeting pathway. Mol. Plant-Microbe Interact. 18:4334–42 [Google Scholar]
  38. Coros A, Callahan B, Battaglioli E, Derbyshire KM. 38.  2008. The specialized secretory apparatus ESX-1 is essential for DNA transfer in Mycobacterium smegmatis. Mol. Microbiol. 69:4794–808 [Google Scholar]
  39. Cunnac S, Chakravarthy S, Kvitko BH, Russell AB, Martin GB, Collmer A. 39.  2011. Genetic disassembly and combinatorial reassembly identify a minimal functional repertoire of type III effectors in Pseudomonas syringae. Proc. Natl. Acad. Sci. USA 108:72975–80 [Google Scholar]
  40. Silva FG, Shen Y, Dardick C, Burdman S, Yadav RC. 40.  da 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. 17:6593–601 [Google Scholar]
  41. Daleke MH, Ummels R, Bawono P, Heringa J, Vandenbroucke-Grauls CMJE. 41.  et al. 2012. General secretion signal for the mycobacterial type VII secretion pathway. Proc. Natl. Acad. Sci. USA 109:2811342–47 [Google Scholar]
  42. Daleke MH, van der Woude AD, Parret AHA, Ummels R, de Groot AM. 42.  et al. 2012. Specific chaperones for the type VII protein secretion pathway. J. Biol. Chem. 287:3831939–47 [Google Scholar]
  43. Das C, Ghosh TS, Mande SS. 43.  2011. Computational analysis of the ESX-1 region of Mycobacterium tuberculosis: insights into the mechanism of type VII secretion system. PLoS ONE 6:11e27980 [Google Scholar]
  44. de Jonge MI, Pehau-Arnaudet G, Fretz MM, Romain F, Bottai D. 44.  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. 189:166028–34 [Google Scholar]
  45. De Maayer P, Venter SN, Kamber T, Duffy B, Coutinho TA, Smits THM. 45.  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 [Google Scholar]
  46. Delattre A-S, Saint N, Clantin B, Willery E, Lippens G. 46.  et al. 2011. Substrate recognition by the POTRA domains of TpsB transporter FhaC. Mol. Microbiol. 81:199–112 [Google Scholar]
  47. Delepelaire P, Wandersman C. 47.  1989. Protease secretion by Erwinia chrysanthemi. Proteases B and C are synthesized and secreted as zymogens without a signal peptide. J. Biol. Chem. 264:159083–89 [Google Scholar]
  48. Delepelaire P, Wandersman C. 48.  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. 5:102427–34 [Google Scholar]
  49. Deng WL, Preston G, Collmer A, Chang CJ, Huang HC. 49.  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. 180:174523–31 [Google Scholar]
  50. Deslandes L, Rivas S. 50.  2012. Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci. 17:11644–55 [Google Scholar]
  51. Desvaux M, Hébraud M, Talon R, Henderson IR. 51.  2009. Secretion and subcellular localizations of bacterial proteins: a semantic awareness issue. Trends Microbiol. 17:4139–45 [Google Scholar]
  52. Desvaux M, Parham NJ, Scott-Tucker A, Henderson IR. 52.  2004. The general secretory pathway: a general misnomer?. Trends Microbiol. 12:7306–9 [Google Scholar]
  53. Desveaux D, Singer AU, Wu A-J, McNulty BC, Musselwhite L. 53.  et al. 2007. Type III effector activation via nucleotide binding, phosphorylation, and host target interaction. PLoS Pathog. 3:3e48 [Google Scholar]
  54. Ding Z, Christie PJ. 54.  2003. Agrobacterium tumefaciens twin-arginine-dependent translocation is important for virulence, flagellation, and chemotaxis but not type IV secretion. J. Bacteriol. 185:3760–71 [Google Scholar]
  55. Djamei A, Pitzschke A, Nakagami H, Rajh I, Hirt H. 55.  2007. Trojan horse strategy in Agrobacterium transformation: abusing MAPK defense signaling. Science 318:5849453–56 [Google Scholar]
  56. Doyle EL, Stoddard BL, Voytas DF, Bogdanove AJ. 56.  2013. TAL effectors: highly adaptable phytobacterial virulence factors and readily engineered DNA-targeting proteins. Trends Cell Biol. 23:8390–98 [Google Scholar]
  57. Duquesne S, Destoumieux-Garzón D, Peduzzi J, Rebuffat S. 57.  2007. Microcins, gene-encoded antibacterial peptides from enterobacteria. Nat. Prod. Rep. 24:4708–34 [Google Scholar]
  58. Engelhardt S, Lee J, Gäbler Y, Kemmerling B, Haapalainen M-L. 58.  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. 57:4706–17 [Google Scholar]
  59. Esko JD, Doering TL, Raetz CR. 59.  2009. Eubacteria and Archaea. Essentials of Glycobiology 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. 60.  2012. Plant-bacterial pathogen interactions mediated by type III effectors. Curr. Opin. Plant Biol. 15:4469–76 [Google Scholar]
  61. Ferrandez Y, Condemine G. 61.  2008. Novel mechanism of outer membrane targeting of proteins in gram-negative bacteria. Mol. Microbiol. 69:61349–57 [Google Scholar]
  62. Filloux A. 62.  2010. Secretion signal and protein targeting in bacteria: a biological puzzle. J. Bacteriol. 192:153847–49 [Google Scholar]
  63. Flint JL, Kowalski JC, Karnati PK, Derbyshire KM. 63.  2004. The RD1 virulence locus of Mycobacterium tuberculosis regulates DNA transfer in Mycobacterium smegmatis. Proc. Natl. Acad. Sci. USA 101:3412598–603 [Google Scholar]
  64. Fortune SM, Jaeger A, Sarracino DA, Chase MR, Sassetti CM. 64.  et al. 2005. Mutually dependent secretion of proteins required for mycobacterial virulence. Proc. Natl. Acad. Sci. USA 102:3010676–81 [Google Scholar]
  65. Fronzes R, Christie PJ, Waksman G. 65.  2009. The structural biology of type IV secretion systems. Nat. Rev. Microbiol. 7:10703–14 [Google Scholar]
  66. Fronzes R, Schäfer E, Wang L, Saibil HR, Orlova EV, Waksman G. 66.  2009. Structure of a type IV secretion system core complex. Science 323:5911266–68 [Google Scholar]
  67. Fu ZQ, Guo M, Jeong B-R, Tian F, Elthon TE. 67.  et al. 2007. A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature 447:7142284–88 [Google Scholar]
  68. Fyans JK, Bignell D, Loria R, Toth I, Palmer T. 68.  2013. The ESX/type VII secretion system modulates development, but not virulence, of the plant pathogen Streptomyces scabies. Mol. Plant Pathol. 14:2119–30 [Google Scholar]
  69. Galán JE, Wolf-Watz H. 69.  2006. Protein delivery into eukaryotic cells by type III secretion machines. Nature 444:7119567–73 [Google Scholar]
  70. Genin S, Denny TP. 70.  2012. Pathogenomics of the Ralstonia solanacearum species complex. Annu. Rev. Phytopathol. 50:67–89 [Google Scholar]
  71. Gey Van Pittius NC, Gamieldien J, Hide W, Brown GD, Siezen RJ, Beyers AD. 71.  2001. The ESAT-6 gene cluster of Mycobacterium tuberculosis and other high G + C gram-positive bacteria. Genome Biol. 2:10RESEARCH0044 [Google Scholar]
  72. González A, Plener L, Restrepo S, Boucher C, Genin S. 72.  2011. Detection and functional characterization of a large genomic deletion resulting in decreased pathogenicity in Ralstonia solanacearum race 3 biovar 2 strains. Environ. Microbiol. 13:123172–85 [Google Scholar]
  73. González ET, Brown DG, Swanson JK, Allen C. 73.  2007. Using the Ralstonia solanacearum Tat secretome to identify bacterial wilt virulence factors. Appl. Environ. Microbiol. 73:123779–86 [Google Scholar]
  74. Goodner B, Hinkle G, Gattung S, Miller N, Blanchard M. 74.  et al. 2001. Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294:55502323–28 [Google Scholar]
  75. Gottig N, Garavaglia BS, Garofalo CG, Orellano EG, Ottado J. 75.  2009. A filamentous hemagglutinin-like protein of Xanthomonas axonopodis pv. citri, the phytopathogen responsible for citrus canker, is involved in bacterial virulence. PLoS ONE 4:2e4358 [Google Scholar]
  76. Gray TA, Krywy JA, Harold J, Palumbo MJ, Derbyshire KM. 76.  2013. Distributive conjugal transfer in mycobacteria generates progeny with meiotic-like genome-wide mosaicism, allowing mapping of a mating identity locus. PLoS Biol. 11:7e1001602 [Google Scholar]
  77. Grijpstra J, Arenas J, Rutten L, Tommassen J. 77.  2013. Autotransporter secretion: varying on a theme. Res. Microbiol. 164:6562–82 [Google Scholar]
  78. Guttman DS, Vinatzer BA, Sarkar SF, Ranall MV, Kettler G, Greenberg JT. 78.  2002. A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295:55601722–26 [Google Scholar]
  79. Haapalainen M, Mosorin H, Dorati F, Wu R-F, Roine E. 79.  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. 194:184810–22 [Google Scholar]
  80. Hartmann N, Schulz S, Lorenz C, Fraas S, Hause G, Büttner D. 80.  2012. Characterization of HrpB2 from Xanthomonas campestris pv. vesicatoria identifies protein regions that are essential for type III secretion pilus formation. Microbiology 158:Pt. 51334–49 [Google Scholar]
  81. Hassan S, Shevchik VE, Robert X, Hugouvieux-Cotte-Pattat N. 81.  2013. PelN is a new pectate lyase of Dickeya dadantii with unusual characteristics. J. Bacteriol. 195:102197–206 [Google Scholar]
  82. Hausner J, Hartmann N, Lorenz C, Büttner D. 82.  2013. The periplasmic HrpB1 protein from Xanthomonas spp. binds to peptidoglycan and to components of the type III secretion system. Appl. Environ. Microbiol. 79:206312–24 [Google Scholar]
  83. He SY, Jin Q. 83.  2003. The Hrp pilus: learning from flagella. Curr. Opin. Microbiol. 6:115–19 [Google Scholar]
  84. Henrichfreise B, Schiefer A, Schneider T, Nzukou E, Poellinger C. 84.  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. 73:5913–23 [Google Scholar]
  85. Hodak H, Clantin B, Willery E, Villeret V, Locht C, Jacob-Dubuisson F. 85.  2006. Secretion signal of the filamentous haemagglutinin, a model two-partner secretion substrate. Mol. Microbiol. 61:2368–82 [Google Scholar]
  86. Hood RD, Singh P, Hsu F, Güvener T, Carl MA. 86.  et al. 2010. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7:125–37 [Google Scholar]
  87. Houben D, Demangel C, van Ingen J, Perez J, Baldeón L. 87.  et al. 2012. ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria. Cell Microbiol. 14:81287–98 [Google Scholar]
  88. Houben ENG, Bestebroer J, Ummels R, Wilson L, Piersma SR. 88.  et al. 2012. Composition of the type VII secretion system membrane complex. Mol. Microbiol. 86:2472–84 [Google Scholar]
  89. Ieva R, Bernstein HD. 89.  2009. Interaction of an autotransporter passenger domain with BamA during its translocation across the bacterial outer membrane. Proc. Natl. Acad. Sci. USA 106:4519120–25 [Google Scholar]
  90. Jacob-Dubuisson F, Guérin J, Baelen S, Clantin B. 90.  2013. Two-partner secretion: as simple as it sounds?. Res. Microbiol. 164:6583–95 [Google Scholar]
  91. Jeong B-R, Lin Y, Joe A, Guo M, Korneli C. 91.  et al. 2011. Structure function analysis of an ADP-ribosyltransferase type III effector and its RNA-binding target in plant immunity. J. Biol. Chem. 286:5043272–81 [Google Scholar]
  92. Jerse AE, Yu J, Tall BD, Kaper JB. 92.  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 87:207839–43 [Google Scholar]
  93. Jiménez-Soto LF, Kutter S, Sewald X, Ertl C, Weiss E. 93.  et al. 2009. Helicobacter pylori type IV secretion apparatus exploits β1 integrin in a novel RGD-independent manner. PLoS Pathog. 5:12e1000684 [Google Scholar]
  94. Jin Q, He SY. 94.  2001. Role of the Hrp pilus in type III protein secretion in Pseudomonas syringae. Science 294:55512556–58 [Google Scholar]
  95. Jones JDG, Dangl JL. 95.  2006. The plant immune system. Nature 444:7117323–29 [Google Scholar]
  96. Joshi MV, Mann SG, Antelmann H, Widdick DA, Fyans JK. 96.  et al. 2010. The twin arginine protein transport pathway exports multiple virulence proteins in the plant pathogen Streptomyces scabies. Mol. Microbiol. 77:1252–71 [Google Scholar]
  97. Journet L, Agrain C, Broz P, Cornelis GR. 97.  2003. The needle length of bacterial injectisomes is determined by a molecular ruler. Science 302:56511757–60 [Google Scholar]
  98. Kang Y, Huang J, Mao G, He LY, Schell MA. 98.  1994. Dramatically reduced virulence of mutants of Pseudomonas solanacearum defective in export of extracellular proteins across the outer membrane. Mol. Plant-Microbe Interact. 7:3370–77 [Google Scholar]
  99. Kanonenberg K, Schwarz CKW, Schmitt L. 99.  2013. Type I secretion systems: a story of appendices. Res. Microbiol. 164:6596–604 [Google Scholar]
  100. Kaplan-Türköz B, Jiménez-Soto LF, Dian C, Ertl C, Remaut H. 100.  et al. 2012. Structural insights into Helicobacter pylori oncoprotein CagA interaction with β1 integrin. Proc. Natl. Acad. Sci. USA 109:3614640–45 [Google Scholar]
  101. Kay S, Hahn S, Marois E, Hause G, Bonas U. 101.  2007. A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318:5850648–51 [Google Scholar]
  102. Kazemi-Pour N, Condemine G, Hugouvieux-Cotte-Pattat N. 102.  2004. The secretome of the plant pathogenic bacterium Erwinia chrysanthemi. Proteomics 4:103177–86 [Google Scholar]
  103. Kenny B, DeVinney R, Stein M, Reinscheid DJ, Frey EA, Finlay BB. 103.  1997. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91:4511–20 [Google Scholar]
  104. Kimbrel JA, Thomas WJ, Jiang Y, Creason AL, Thireault CA. 104.  et al. 2013. Mutualistic co-evolution of type III effector genes in Sinorhizobium fredii and Bradyrhizobium japonicum. PLoS Pathog. 9:2e1003204 [Google Scholar]
  105. Knowles TJ, Scott-Tucker A, Overduin M, Henderson IR. 105.  2009. Membrane protein architects: the role of the BAM complex in outer membrane protein assembly. Nat. Rev. Microbiol. 7:3206–14 [Google Scholar]
  106. Korotkov KV, Sandkvist M, Hol WGJ. 106.  2012. The type II secretion system: biogenesis, molecular architecture and mechanism. Nat. Rev. Microbiol. 10:5336–51 [Google Scholar]
  107. Koskiniemi S, Lamoureux JG, Nikolakakis KC, t'Kint de Roodenbeke C, Kaplan MD. 107.  et al. 2013. Rhs proteins from diverse bacteria mediate intercellular competition. Proc. Natl. Acad. Sci. USA 110:177032–37 [Google Scholar]
  108. Kudryashov DS, Durer ZAO, Ytterberg AJ, Sawaya MR, Pashkov I. 108.  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 105:4718537–42 [Google Scholar]
  109. Küper U, Meyer C, Müller V, Rachel R, Huber H. 109.  2010. Energized outer membrane and spatial separation of metabolic processes in the hyperthermophilic archaeon Ignicoccus hospitalis. Proc. Natl. Acad. Sci. USA 107:73152–56 [Google Scholar]
  110. Kvitko BH, Park DH, Velásquez AC, Wei C-F, Russell AB. 110.  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. 5:4e1000388 [Google Scholar]
  111. Kvitko BH, Ramos AR, Morello JE, Oh H-S, Collmer A. 111.  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. 189:228059–72 [Google Scholar]
  112. Lacroix B, Tzfira T, Vainstein A, Citovsky V. 112.  2006. A case of promiscuity: Agrobacterium's endless hunt for new partners. Trends Genet. 22:129–37 [Google Scholar]
  113. Lara-Tejero M, Kato J, Wagner S, Liu X, Galán JE. 113.  2011. A sorting platform determines the order of protein secretion in bacterial type III systems. Science 331:60211188–91 [Google Scholar]
  114. Leiman PG, Basler M, Ramagopal UA, Bonanno JB, Sauder JM. 114.  et al. 2009. Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc. Natl. Acad. Sci. USA 106:114154–59 [Google Scholar]
  115. Leo JC, Grin I, Linke D. 115.  2012. Type V secretion: mechanism(s) of autotransport through the bacterial outer membrane. Philos. Trans. R. Soc. Lond. B 367:15921088–101 [Google Scholar]
  116. Létoffé S, Delepelaire P, Wandersman C. 116.  1989. Characterization of a protein inhibitor of extracellular proteases produced by Erwinia chrysanthemi. Mol. Microbiol. 3:179–86 [Google Scholar]
  117. Leyton DL, Rossiter AE, Henderson IR. 117.  2012. From self sufficiency to dependence: mechanisms and factors important for autotransporter biogenesis. Nat. Rev. Microbiol. 10:3213–25 [Google Scholar]
  118. Li J-G, Liu H-X, Cao J, Chen L-F, Gu C. 118.  et al. 2010. PopW of Ralstonia solanacearum, a new two-domain harpin targeting the plant cell wall. Mol. Plant Pathol. 11:3371–81 [Google Scholar]
  119. Li M, Le Trong I, Carl MA, Larson ET, Chou S. 119.  et al. 2012. Structural basis for type VI secretion effector recognition by a cognate immunity protein. PLoS Pathog. 8:4e1002613 [Google Scholar]
  120. Lightbody KL, Ilghari D, Waters LC, Carey G, Bailey MA. 120.  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. 283:2517681–90 [Google Scholar]
  121. Lindgren PB, Peet RC, Panopoulos NJ. 121.  1986. Gene cluster of Pseudomonas syringae pv. “phaseolicola” controls pathogenicity of bean plants and hypersensitivity of nonhost plants. J. Bacteriol. 168:2512–22 [Google Scholar]
  122. Linhartová I, Bumba L, Mašín J, Basler M, Osička R. 122.  et al. 2010. RTX proteins: a highly diverse family secreted by a common mechanism. FEMS Microbiol. Rev. 34:61076–112 [Google Scholar]
  123. Liu J, Elmore JM, Lin Z-JD, Coaker G. 123.  2011. A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe 9:2137–46 [Google Scholar]
  124. Locht C, Coutte L, Mielcarek N. 124.  2011. The ins and outs of pertussis toxin. FEBS J. 278:234668–82 [Google Scholar]
  125. Loper JE, Hassan KA, Mavrodi DV, Davis EW, Lim CK. 125.  et al. 2012. Comparative genomics of plant-associated Pseudomonas spp.: insights into diversity and inheritance of traits involved in multitrophic interactions. PLoS Genet. 8:7e1002784 [Google Scholar]
  126. Lorenz C, Büttner D. 126.  2009. Functional characterization of the type III secretion ATPase HrcN from the plant pathogen Xanthomonas campestris pv. vesicatoria. J. Bacteriol. 191:51414–28 [Google Scholar]
  127. Lorenz C, Büttner D. 127.  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. 79:2447–67 [Google Scholar]
  128. Lorenz C, Hausner J, Büttner D. 128.  2012. HrcQ provides a docking site for early and late type III secretion substrates from Xanthomonas. PLoS ONE 7:11e51063 [Google Scholar]
  129. Lorenz C, Schulz S, Wolsch T, Rossier O, Bonas U, Büttner D. 129.  2008. HpaC controls substrate specificity of the Xanthomonas type III secretion system. PLoS Pathog. 4:6e1000094 [Google Scholar]
  130. Lu YY, Franz B, Truttmann MC, Riess T, Gay Fraret J. 130.  et al. 2013. Bartonella henselae trimeric autotransporter adhesin BadA expression interferes with effector translocation by the VirB/D4 type IV secretion system. Cell Microbiol. 15:5759–78 [Google Scholar]
  131. Luo Z-Q. 131.  2012. Legionella secreted effectors and innate immune responses. Cell Microbiol. 14:119–27 [Google Scholar]
  132. Lycklama A, Nijeholt JA, Driessen AJM. 132.  2012. The bacterial Sec-translocase: structure and mechanism. Philos. Trans. R. Soc. Lond. B 367:15921016–28 [Google Scholar]
  133. Ma AT, McAuley S, Pukatzki S, Mekalanos JJ. 133.  2009. Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe 5:3234–43 [Google Scholar]
  134. Mackey D, Holt BF, Wiig A, Dangl JL. 134.  2002. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:6743–54 [Google Scholar]
  135. Mak AN-S, Bradley P, Bogdanove AJ, Stoddard BL. 135.  2013. TAL effectors: function, structure, engineering and applications. Curr. Opin. Struct. Biol. 23:193–99 [Google Scholar]
  136. Marits R, Kõiv V, Laasik E, Mäe A. 136.  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. 81959–66 [Google Scholar]
  137. Marlovits TC, Kubori T, Sukhan A, Thomas DR, Galán JE, Unger VM. 137.  2004. Structural insights into the assembly of the type III secretion needle complex. Science 306:56981040–42 [Google Scholar]
  138. Matsumoto A, Huston SL, Killiny N, Igo MM. 138.  2012. XatA, an AT-1 autotransporter important for the virulence of Xylella fastidiosa Temecula1. MicrobiologyOpen 1:133–45 [Google Scholar]
  139. Mattinen L, Somervuo P, Nykyri J, Nissinen R, Kouvonen P. 139.  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. 82387–96 [Google Scholar]
  140. Meibom KL, Blokesch M, Dolganov NA, Wu C-Y, Schoolnik GK. 140.  2005. Chitin induces natural competence in Vibrio cholerae. Science 310:57551824–27 [Google Scholar]
  141. Miyata S, Casey M, Frank DW, Ausubel FM, Drenkard E. 141.  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. 71:52404–13 [Google Scholar]
  142. Moscou MJ, Bogdanove AJ. 142.  2009. A simple cipher governs DNA recognition by TAL effectors. Science 326:59591501 [Google Scholar]
  143. Mota LJ. 143.  2006. Type III secretion gets an LcrV tip. Trends Microbiol. 14:5197–200 [Google Scholar]
  144. Nicaise V, Joe A, Jeong B-R, Korneli C, Boutrot F. 144.  et al. 2013. Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7. EMBO J. 32:5701–12 [Google Scholar]
  145. Niederweis M, Danilchanka O, Huff J, Hoffmann C, Engelhardt H. 145.  2010. Mycobacterial outer membranes: in search of proteins. Trends Microbiol. 18:3109–16 [Google Scholar]
  146. Niepold F, Anderson D, Mills D. 146.  1985. Cloning determinants of pathogenesis from Pseudomonas syringae pathovar syringae. Proc. Natl. Acad. Sci. USA 82:2406–10 [Google Scholar]
  147. Nomura K, Debroy S, Lee Y, Pumplin N, Jones J, He S. 147.  2006. A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313:5784220–23 [Google Scholar]
  148. Nomura K, Mecey C, Lee YN, Imboden LA, Chang JH, He SY. 148.  2011. Effector-triggered immunity blocks pathogen degradation of an immunity-associated vesicle traffic regulator in Arabidopsis. Proc. Natl. Acad. Sci. USA 108:2610774–79 [Google Scholar]
  149. Nykyri J, Niemi O, Koskinen P, Nokso-Koivisto J, Pasanen M. 149.  et al. 2012. Revised phylogeny and novel horizontally acquired virulence determinants of the model soft rot phytopathogen Pectobacterium wasabiae SCC3193. PLoS Pathog. 8:11e1003013 [Google Scholar]
  150. Oberhettinger P, Schütz M, Leo JC, Heinz N, Berger J. 150.  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 7:10e47069 [Google Scholar]
  151. Ohol YM, Goetz DH, Chan K, Shiloh MU, Craik CS, Cox JS. 151.  2010. Mycobacterium tuberculosis MycP1 protease plays a dual role in regulation of ESX-1 secretion and virulence. Cell Host Microbe 7:3210–20 [Google Scholar]
  152. Okuda S, Tokuda H. 152.  2011. Lipoprotein sorting in bacteria. Annu. Rev. Microbiol. 65:239–59 [Google Scholar]
  153. Oldani A, Cormont M, Hofman V, Chiozzi V, Oregioni O. 153.  et al. 2009. Helicobacter pylori counteracts the apoptotic action of its VacA toxin by injecting the CagA protein into gastric epithelial cells. PLoS Pathog. 5:10e1000603 [Google Scholar]
  154. Pallen MJ. 154.  2002. The ESAT-6/WXG100 superfamily—and a new Gram-positive secretion system?. Trends Microbiol. 10:5209–12 [Google Scholar]
  155. Palmer T, Berks BC. 155.  2012. The twin-arginine translocation (Tat) protein export pathway. Nat. Rev. Microbiol. 10:7483–96 [Google Scholar]
  156. Park E, Rapoport TA. 156.  2012. Mechanisms of Sec61/SecY-mediated protein translocation across membranes. Annu. Rev. Biophys. 41:21–40 [Google Scholar]
  157. Pavlova O, Peterson JH, Ieva R, Bernstein HD. 157.  2013. Mechanistic link between β barrel assembly and the initiation of autotransporter secretion. Proc. Natl. Acad. Sci. USA 110:10E938–47 [Google Scholar]
  158. Pérez-Mendoza D, Coulthurst SJ, Humphris S, Campbell E, Welch M. 158.  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. 82:3719–33 [Google Scholar]
  159. Pitzschke A, Djamei A, Teige M, Hirt H. 159.  2009. VIP1 response elements mediate mitogen-activated protein kinase 3–induced stress gene expression. Proc. Natl. Acad. Sci. USA 106:4318414–19 [Google Scholar]
  160. Preston GM, Studholme DJ, Caldelari I. 160.  2005. Profiling the secretomes of plant pathogenic Proteobacteria. FEMS Microbiol. Rev. 29:2331–60 [Google Scholar]
  161. Pukatzki S, Ma AT, Revel AT, Sturtevant D, Mekalanos JJ. 161.  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 104:3915508–13 [Google Scholar]
  162. Ray SK, Rajeshwari R, Sonti RV. 162.  2000. Mutants of Xanthomonas oryzae pv. oryzae deficient in general secretory pathway are virulence deficient and unable to secrete xylanase. Mol. Plant-Microbe Interact. 13:4394–401 [Google Scholar]
  163. Records AR. 163.  2011. The type VI secretion system: a multipurpose delivery system with a phage-like machinery. Mol. Plant-Microbe Interact. 24:7751–57 [Google Scholar]
  164. Records AR, Gross DC. 164.  2010. Sensor kinases RetS and LadS regulate Pseudomonas syringae type VI secretion and virulence factors. J. Bacteriol. 192:143584–96 [Google Scholar]
  165. Rees DC, Johnson E, Lewinson O. 165.  2009. ABC transporters: the power to change. Nat. Rev. Mol. Cell Biol. 10:3218–27 [Google Scholar]
  166. Reichow SL, Korotkov KV, Hol WGJ, Gonen T. 166.  2010. Structure of the cholera toxin secretion channel in its closed state. Nat. Struct. Mol. Biol. 17:101226–32 [Google Scholar]
  167. Renshaw PS, Panagiotidou P, Whelan A, Gordon SV, Hewinson RG. 167.  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-6*CFP-10 complex. Implications for pathogenesis and virulence. J. Biol. Chem. 277:2421598–603 [Google Scholar]
  168. Reva O, Tümmler B. 168.  2008. Think big: giant genes in bacteria. Environ. Microbiol. 10:3768–77 [Google Scholar]
  169. Rodriguez F, Rouse SL, Tait CE, Harmer J, De Riso A. 169.  et al. 2013. Structural model for the protein-translocating element of the twin-arginine transport system. Proc. Natl. Acad. Sci. USA 110:12E1092–101 [Google Scholar]
  170. Rodríguez E, Gaggero C, Laviña M. 170.  1999. The structural gene for microcin H47 encodes a peptide precursor with antibiotic activity. Antimicrob. Agents Chemother. 43:92176–82 [Google Scholar]
  171. Rojas CM, Ham JH, Deng W-L, Doyle JJ, Collmer A. 171.  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 99:2013142–47 [Google Scholar]
  172. Römer P, Hahn S, Jordan T, Strauss T, Bonas U, Lahaye T. 172.  2007. Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science 318:5850645–48 [Google Scholar]
  173. Rosch JW, Caparon MG. 173.  2005. The ExPortal: an organelle dedicated to the biogenesis of secreted proteins in Streptococcus pyogenes. Mol. Microbiol. 58:4959–68 [Google Scholar]
  174. Ruhe ZC, Low DA, Hayes CS. 174.  2013. Bacterial contact-dependent growth inhibition. Trends Microbiol. 21:5230–37 [Google Scholar]
  175. Russell AB, Hood RD, Bui NK, LeRoux M, Vollmer W, Mougous JD. 175.  2011. Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475:7356343–47 [Google Scholar]
  176. Salama NR, Hartung ML, Müller A. 176.  2013. Life in the human stomach: persistence strategies of the bacterial pathogen Helicobacter pylori. Nat. Rev. Microbiol. 11:6385–99 [Google Scholar]
  177. Salomon D, Orth K. 177.  2013. What pathogens have taught us about posttranslational modifications. Cell Host Microbe 14:3269–79 [Google Scholar]
  178. Sánchez J, Holmgren J. 178.  2008. Cholera toxin structure, gene regulation and pathophysiological and immunological aspects. Cell. Mol. Life Sci. 65:91347–60 [Google Scholar]
  179. Sánchez-Magraner L, Cortajarena AL, García-Pacios M, Arrondo J-LR, Agirre J. 179.  et al. 2010. Interdomain Ca2+ effects in Escherichia coli α-haemolysin: Ca2+ binding to the C-terminal domain stabilizes both C- and N-terminal domains. Biochim. Biophys. Acta 1798:61225–33 [Google Scholar]
  180. Satchell KJF. 180.  2011. Structure and function of MARTX toxins and other large repetitive RTX proteins. Annu. Rev. Microbiol. 65:71–90 [Google Scholar]
  181. Schraidt O, Marlovits TC. 181.  2011. Three-dimensional model of Salmonella's needle complex at subnanometer resolution. Science 331:60211192–95 [Google Scholar]
  182. Schreiber KJ, Desveaux D. 182.  2011. AlgW regulates multiple Pseudomonas syringae virulence strategies. Mol. Microbiol. 80:2364–77 [Google Scholar]
  183. Schwarz S, West TE, Boyer F, Chiang W-C, Carl MA. 183.  et al. 2010. Burkholderia type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog. 6:8e1001068 [Google Scholar]
  184. Serafini A, Boldrin F, Palù G, Manganelli R. 184.  2009. Characterization of a Mycobacterium tuberculosis ESX-3 conditional mutant: essentiality and rescue by iron and zinc. J. Bacteriol. 191:206340–44 [Google Scholar]
  185. Shneider MM, Buth SA, Ho BT, Basler M, Mekalanos JJ, Leiman PG. 185.  2013. PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 500:7462350–53 [Google Scholar]
  186. Sikora AE. 186.  2013. Proteins secreted via the type II secretion system: smart strategies of Vibrio cholerae to maintain fitness in different ecological niches. PLoS Pathog. 9:2e1003126 [Google Scholar]
  187. Silverman JM, Brunet YR, Cascales E, Mougous JD. 187.  2012. Structure and regulation of the type VI secretion system. Annu. Rev. Microbiol. 66:453–72 [Google Scholar]
  188. Simeone R, Bobard A, Lippmann J, Bitter W, Majlessi L. 188.  et al. 2012. Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death. PLoS Pathog. 8:2e1002507 [Google Scholar]
  189. Simeone R, Bottai D, Brosch R. 189.  2009. ESX/type VII secretion systems and their role in host-pathogen interaction. Curr. Opin. Microbiol. 12:14–10 [Google Scholar]
  190. Simpson AJ, Reinach FC, Arruda P, Abreu FA, Acencio M. 190.  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 406:6792151–59 [Google Scholar]
  191. Smith J, Manoranjan J, Pan M, Bohsali A, Xu J. 191.  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. 76:125478–87 [Google Scholar]
  192. Solomonson M, Huesgen PF, Wasney GA, Watanabe N, Gruninger RJ. 192.  et al. 2013. Structure of the mycosin-1 protease from the mycobacterial ESX-1 protein type VII secretion system. J. Biol. Chem. 288:2417782–90 [Google Scholar]
  193. Sory MP, Cornelis GR. 193.  1994. Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol. Microbiol. 14:3583–94 [Google Scholar]
  194. Soscia C, Hachani A, Bernadac A, Filloux A, Bleves S. 194.  2007. Cross talk between type III secretion and flagellar assembly systems in Pseudomonas aeruginosa. J. Bacteriol. 189:83124–32 [Google Scholar]
  195. Stingl K, Müller S, Scheidgen-Kleyboldt G, Clausen M, Maier B. 195.  2010. Composite system mediates two-step DNA uptake into Helicobacter pylori. Proc. Natl. Acad. Sci. USA 107:31184–89 [Google Scholar]
  196. Stoop EJM, Bitter W, van der Sar AM. 196.  2012. Tubercle bacilli rely on a type VII army for pathogenicity. Trends Microbiol. 20:10477–84 [Google Scholar]
  197. Suarez G, Sierra JC, Erova TE, Sha J, Horneman AJ, Chopra AK. 197.  2010. A type VI secretion system effector protein, VgrG1, from Aeromonas hydrophila that induces host cell toxicity by ADP ribosylation of actin. J. Bacteriol. 192:1155–68 [Google Scholar]
  198. Sun Y-H, Rolán HG, Tsolis RM. 198.  2007. Injection of flagellin into the host cell cytosol by Salmonella enterica serotype Typhimurium. J. Biol. Chem. 282:4733897–901 [Google Scholar]
  199. Szczesny R, Jordan M, Schramm C, Schulz S, Cogez V. 199.  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. 187:4983–1002 [Google Scholar]
  200. Tampakaki AP, Skandalis N, Gazi AD, Bastaki MN, Sarris PF. 200.  et al. 2010. Playing the “Harp”: evolution of our understanding of hrp/hrc genes. Annu. Rev. Phytopathol. 48:347–70 [Google Scholar]
  201. Toth IK, Bell KS, Holeva MC, Birch PRJ. 201.  2003. Soft rot erwiniae: from genes to genomes. Mol. Plant Pathol. 4:117–30 [Google Scholar]
  202. Trachtenberg S. 202.  1998. Mollicutes-wall-less bacteria with internal cytoskeletons. J. Struct. Biol. 124:2–3244–56 [Google Scholar]
  203. Troisfontaines P, Cornelis GR. 203.  2005. Type III secretion: more systems than you think. Physiology Bethesda 20:326–39 [Google Scholar]
  204. Tsugawa H, Suzuki H, Saya H, Hatakeyama M, Hirayama T. 204.  et al. 2012. Reactive oxygen species–induced autophagic degradation of Helicobacter pylori CagA is specifically suppressed in cancer stem-like cells. Cell Host Microbe 12:6764–77 [Google Scholar]
  205. Tzfira T, Vaidya M, Citovsky V. 205.  2001. VIP1, an Arabidopsis protein that interacts with Agrobacterium VirE2, is involved in VirE2 nuclear import and Agrobacterium infectivity. EMBO J. 20:133596–607 [Google Scholar]
  206. Tzfira T, Vaidya M, Citovsky V. 206.  2004. Involvement of targeted proteolysis in plant genetic transformation by Agrobacterium. Nature 431:700487–92 [Google Scholar]
  207. van den Berg B. 207.  2010. Crystal structure of a full-length autotransporter. J. Mol. Biol. 396:3627–33 [Google Scholar]
  208. van der Wel N, Hava D, Houben D, Fluitsma D, van Zon M. 208.  et al. 2007. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 129:71287–98 [Google Scholar]
  209. Veena Jiang H, Doerge RW, Gelvin SB. 209.  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. 35:2219–36 [Google Scholar]
  210. Voegel TM, Warren JG, Matsumoto A, Igo MM, Kirkpatrick BC. 210.  2010. Localization and characterization of Xylella fastidiosa haemagglutinin adhesins. Microbiology 156:Pt. 72172–79 [Google Scholar]
  211. Vojtova J, Kamanová J, Šebo P. 211.  2006. Bordetella adenylate cyclase toxin: a swift saboteur of host defense. Curr. Opin. Microbiol. 9:169–75 [Google Scholar]
  212. Voulhoux R, Ball G, Ize B, Vasil ML, Lazdunski A. 212.  et al. 2001. Involvement of the twin-arginine translocation system in protein secretion via the type II pathway. EMBO J. 20:236735–41 [Google Scholar]
  213. Wagner JM, Evans TJ, Chen J, Zhu H, Houben ENG. 213.  et al. 2013. Understanding specificity of the mycosin proteases in ESX/type VII secretion by structural and functional analysis. J. Struct. Biol. 184:2115–28 [Google Scholar]
  214. Wagner JM, Evans TJ, Korotkov KV. 214.  2014. Crystal structure of the N-terminal domain of EccA1 ATPase from the ESX-1 secretion system of Mycobacterium tuberculosis. Proteins 82:1159–63 [Google Scholar]
  215. Walker D, Lancaster L, James R, Kleanthous C. 215.  2004. Identification of the catalytic motif of the microbial ribosome inactivating cytotoxin colicin E3. Protein Sci. 13:61603–11 [Google Scholar]
  216. Wallden K, Williams R, Yan J, Lian PW, Wang L. 216.  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 109:2811348–53 [Google Scholar]
  217. Weerdenburg EM, Abdallah AM, Mitra S, de Punder K, van der Wel NN. 217.  et al. 2012. ESX-5-deficient Mycobacterium marinum is hypervirulent in adult zebrafish. Cell Microbiol. 14:5728–39 [Google Scholar]
  218. Wei H-L, Chakravarthy S, Worley JN, Collmer A. 218.  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. 15601–18
  219. Wood DW, Setubal JC, Kaul R, Monks DE, Kitajima JP. 219.  et al. 2001. The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294:55502317–23 [Google Scholar]
  220. Wu C-F, Lin J-S, Shaw G-C, Lai E-M. 220.  2012. Acid-induced type VI secretion system is regulated by ExoR-ChvG/ChvI signaling cascade in Agrobacterium tumefaciens. PLoS Pathog. 8:9e1002938 [Google Scholar]
  221. Wu H-Y, Chung P-C, Shih H-W, Wen S-R, Lai E-M. 221.  2008. Secretome analysis uncovers an Hcp-family protein secreted via a type VI secretion system in Agrobacterium tumefaciens. J. Bacteriol. 190:82841–50 [Google Scholar]
  222. Yang J, Zhao Y, Shi J, Shao F. 222.  2013. Human NAIP and mouse NAIP1 recognize bacterial type III secretion needle protein for inflammasome activation. Proc. Natl. Acad. Sci. USA 110:3514408–13 [Google Scholar]
  223. Yokoyama K, Higashi H, Ishikawa S, Fujii Y, Kondo S. 223.  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 102:279661–66 [Google Scholar]
  224. Young GM, Schmiel DH, Miller VL. 224.  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 96:116456–61 [Google Scholar]
  225. Zaltsman A, Krichevsky A, Loyter A, Citovsky V. 225.  2010. Agrobacterium induces expression of a host F-box protein required for tumorigenicity. Cell Host Microbe 7:3197–209 [Google Scholar]
  226. Zechner EL, Lang S, Schildbach JF. 226.  2012. Assembly and mechanisms of bacterial type IV secretion machines. Philos. Trans. R. Soc. Lond. B 367:15921073–87 [Google Scholar]
  227. Zgurskaya HI, Krishnamoorthy G, Ntreh A, Lu S. 227.  2011. Mechanism and function of the outer membrane channel TolC in multidrug resistance and physiology of enterobacteria. Front. Microbiol. 2:189 [Google Scholar]
  228. Zhang Y, Bak DD, Heid H, Geider K. 228.  1999. Molecular characterization of a protease secreted by Erwinia amylovora. J. Mol. Biol. 289:51239–51 [Google Scholar]
  229. Zhao Y, Qi M. 229.  2011. Comparative genomics of Erwinia amylovora and related Erwinia species: What do we learn?. Genes 2:3627–39 [Google Scholar]
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