The type III (Hrp) secretion pathway of plant pathogenic bacteria: Trafficking harpins, Avr proteins, and death

Journal of Bacteriology

Volumn 179, Issue 18, 1997, Pages 5655-5662

  Alfano, James R ^a   Collmer, Alan ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN;

AGRICULTURE; BACTERIUM PILUS; CELL DEATH; ERWINIA; FLAGELLUM; GRAM NEGATIVE BACTERIUM; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN TRANSPORT; PSEUDOMONAS; SHORT SURVEY; XANTHOMONAS;

BACTERIA (MICROORGANISMS); ERWINIA; NEGIBACTERIA; PSEUDOMONAS; XANTHOMONAS;

EID: 0030930294     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.179.18.5655-5662.1997     Document Type: Short Survey

References (89)

1. Alfano, J. R., D. W. Bauer, T. M. Milos, and A. Collmer. 1996. Analysis of the role of the Pseudomonas syringae pv. syringae HrpZ harpin in elicitation of the hypersensitive response in tobacco using functionally nonpolar deletion mutations, truncated HrpZ fragments, and hrmA mutations. Mol. Microbiol. 19:715-728.
2. Alfano, J. R., and A. Collmer. 1996. Bacterial pathogens in plants: life up against the wall. Plant Cell 8:1683-1698.
3. Alfano, J. R., H.-S. Kim, T. P. Delaney, and A. Collmer. 1997. Evidence that the Pseudomonas syringae pv. syringae hrp-linked hrmA gene encodes an Avr-like protein that acts in a hrp-dependent manner within tobacco cells. Mol. Plant-Microbe Interact. 10:580-588.
4. Arlat, M., F. Van Gijsegem, J. C. Huet, J. C. Pernollet, and C. A. Boucher. 1994. PopA1, a protein which induces a hypersensitive-like response on specific Petunia genotypes, is secreted via the Hrp pathway of Pseudomonas solanacearum. EMBO J. 13:543-553.
5. Barny, M.-A. 1995. Erwinia amylovora hrpN mutants, blocked in harpin synthesis, express a reduced virulence on host plants and elicit variable hypersensitive reactions on tobacco. Eur. J. Plant Pathol. 101:333-340.
6. Bauer, D. W., A. J. Bogdanove, S. V. Beer, and A. Collmer. 1994. Erwinia chrysanthemi hrp genes and their involvement in soft rot pathogenesis and elicitation of the hypersensitive response. Mol. Plant-Microbe Interact. 7: 573-581.
7. Ech: an elicitor of the hypersensitive response that contributes to soft-rot pathogenesis. Mol. Plant-Microbe Interact. 8:484-491.
8. Beer, S. V., D. W. Bauer, X. H. Jiang, R. J. Laby, B. J. Sneath, Z.-M. Wei, D. A. Wilcox, and C. H. Zumoff. 1991. The hrp gene cluster of Erwinia amylovora, p. 53-60. In H. Hennecke and D. P. S. Verma (ed.), Advances in molecular genetics of plant-microbe interactions. Kluwer Academic Publishers, Dordrecht, The Netherlands.
9. Bogdanove, A. J., S. V. Beer, U. Bonas, C. A. Boucher, A. Collmer, D. L. Coplin, G. R. Cornelis, H.-C. Huang, S. W. Hutcheson, N. J. Panopoulos, and F. Van Gijsegem. 1996. Unified nomenclature for broadly conserved hip genes of phytopathogenic bacteria. Mol. Microbiol. 20:681-683.
10. Bogdanove, A. J., Z.-M. Wei, L. Zhao, and S. V. Beer. 1996. Erwinia amylovora secretes harpin via a type III pathway and contains a homolog of yopN of Yersinia spp. J. Bacteriol. 178:1720-1730.
11. Bonas, U. 1994. hrp genes of phytopathogenic bacteria. Curr. Top. Microbiol. Immunol. 192:79-98.
12. Boucher, C. A., A. Martinel, P. Barberis, G. Alloing, and C. Zischeck. 1986. Virulence genes are carried by a megaplasmid of the plant pathogen Pseudomonas solanacearum. Mol. Gen. Genet. 205:270-275.
13. Brown, I., J. Mansfield, I. Irlam, J. Conrads-Strauch, and U. Bonas. 1993. Ultrastructure of interactions between Xanthomonas campestris pv. vesicatoria and pepper, including immunocytochemical localization of extracellular polysaccharides and the AvrBs3 protein. Mol. Plant-Microbe Interact. 6:376-386.
14. Carpenter, P. B., and G. W. Ordal. 1993. Bacillus subtilis FlhA: a flagellar protein related to a new family of signal-transducing receptors. Mol. Microbiol. 7:735-743.
15. Charkowski, A. O., H.-C. Huang, and A. Collmer. 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. 179:3866-3874.
16. Chen, Y., M. R. Smith, K. Thirumalai, and A. Zychlinsky. 1996. A bacterial invasion induces macrophage apoptosis by binding directly to ICE. EMBO J. 15:3853-3860.
17. Collazo, C. M., and J. E. Galán. 1997. The invasion-associated type III system of Salmonella typhimurium directs the translocation of Sip proteins into the host cell. Mol. Microbiol. 24:747-756.
18. Cornelis, G. R., and H. Wolf-Watz. 1997. The Yersinia Yop regulon: a bacterial system for subverting eukaryotic cells. Mol. Microbiol. 23:861-867.
19. Ecc and elicit a hypersensitive reaction-like response in tobacco leaves. Mol. Plant-Microbe Interact. 9:565-573.
20. Dangl, J. L. 1994. The enigmatic avirulence genes of phytopathogenic bacteria. Curr. Top. Microbiol. Immunol. 192:99-118.
21. Dangl, J. L., R. A. Dietrich, and M. H. Richberg. 1996. Death don't have no mercy: cell death programs in plant-microbe interactions. Plant Cell 8:1793-1807.
22. Fenselau, S., I. Balbo, and U. Bonas. 1992. Determinants of pathogenicity in Xanthomonas campestris pv. vesicatoria are related to proteins involved in secretion in bacterial pathogens of animals. Mol. Plant-Microbe Interact. 5:390-396.
23. Frederick, R. D., D. R. Majerczak, and D. L. Coplin. 1993. Erwinia stewartii WtsA, a positive regulator of pathogenicity gene expression, is similar to Pseudomonas syringae pv. phaseolicola HrpS. Mol. Microbiol. 9:477-485.
24. Fullner, K. J., J. C. Lara, and E. W. Nester. 1996. Pilus assembly by Agrobacterium T-DNA transfer genes. Science 273:1107-1109.
25. Galán, J. E. 1996. Molecular genetic bases of Salmonella entry into host cells. Mol. Microbiol. 20:263-271.
26. Genin, S., and C. A. Boucher. 1994. A superfamily of proteins involved in different secretion pathways in gram-negative bacteria: modular structure and specificity of the N-terminal domain. Mol. Gen. Genet 243:112-118.
27. Genin, S., C. L. Gough, C. Zischek, and C. A. Boucher. 1992. Evidence that the hrpB gene encodes a positive regulator of pathogenicity genes from Pseudomonas solanacearum. Mol. Microbiol. 6:3065-3076.
28. Gopalan, S., D. W. Bauer, J. R. Alfano, A. O. Loniello, S. Y. He, and A. Collmer. 1996. Expression of the Pseudomonas syringae avirulence protein AvrB in plant cells alleviates its dependence on the hypersensitive response and pathogenicity (Hrp) secretion system in eliciting genotype-specific hypersensitive cell death. Plant Cell 8:1095-1105.
29. Gough, C. L., S. Genin, C. Zischek, and C. A. Boucher. 1992. hrp genes of Pseudomonas solanacearum are homologous to pathogenicity determinants of animal pathogenic bacteria and are conserved among plant pathogenic bacteria. Mol. Plant-Microbe Interact. 5:384-389.
30. He, S. Y., D. W. Bauer, A. Collmer, and S. V. Beer. 1994. Hypersensitive response elicited by Erwinia amylovora harpin requires active plant metabolism. Mol. Plant-Microbe Interact. 7:289-292.
31. Pss: a protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants. Cell 73:1255-1266.
32. Heu, S., and S. W. Hutcheson. 1993. Nucleotide sequence and properties of the hrmA locus associated with the Pseudomonas syringae pv. syringae 61 hrp gene cluster. Mol. Plant-Microbe Interact. 6:553-564.
33. Pss with plant cell walls. Mol. Plant-Microbe Interact. 9:608-616.
34. Huang, H.-C., S. Y. He, D. W. Bauer, and A. Collmer. 1992. The Pseudomonas syringae pv. syringae 61 hrpH product, an envelope protein required for elicitation of the hypersensitive response in plants. J. Bacteriol. 174:6878-6885.
35. Huang, H.-C., S. W. Hutcheson, and A. Collmer. 1991. Characterization of the hrp cluster from Pseudomonas syringae pv. syringae 61 and TnphoA tagging of genes encoding exported or membrane-spanning Hrp proteins. Mol. Plant-Microbe Interact. 4:469-476.
36. Pss secretion that are arranged colinearly with Yersinia ysc homologs. Mol. Plant-Microbe Interact. 8:733-746.
37. Huang, H.-C., R. Schuurink, T. P. Denny, M. M. Atkinson, C. J. Baker, I. Yucel, S. W. Hutcheson, and A. Collmer. 1988. Molecular cloning of a Pseudomonas syringae pv. syringae gene cluster that enables Pseudomonas fluorescens to elicit the hypersensitive response in tobacco plants. J. Bacteriol. 170:4748-4756.
38. Huguet, E., and U. Bonas. 1997. hrpF of Xanthomonas campestris pv. vesicatoria encodes an 87-kDa protein with homology to NoIX of Rhizobium fredii. Mol. Plant-Microbe Interact. 10:488-498.
39. Keen, N. T. 1990. Gene-for-gene complementarity in plant-pathogen interactions. Annu. Rev. Genet. 24:447-463.
40. Keen, N. T., S. Tamaki, D. Kobayashi, D. Gerhold, M. Stayton, H. Shen, S. Gold, J. Lorang, H. Thordal-Christensen, D. Dahlbeck, and B. Staskawicz. 1990. Bacteria expressing avirulence gene D produce a specific elicitor of the soybean hypersensitive reaction. Mol. Plant-Microbe Interact. 3:112-121.
41. Kim, J. F., Z.-M. Wei, and S. V. Beer. 1997. The hrpA and hrpC operons of Erwinia amylovora encode components of a type III pathway that secretes harpin. J. Bacteriol. 179:1690-1697.
42. Klement, Z. 1963. Rapid detection of pathogenicity of phytopathogenic pseudomonads. Nature 199:299-300.
43. Klement, Z. 1982. Hypersensitivity, p. 149-177. In M. S. Mount and G. H. Lacy (ed.), Phytopathogenic prokaryotes, vol. 2. Academic Press, Inc., New York, N.Y.
44. Kobayshi, D. Y., S. J. Tamaki, and N. T. Keen. 1989. Cloned avirulence genes from the tomato pathogen Pseudomonas syringae pv. tomato confer cultivar specificity on soybean. Proc. Natl. Acad. Sci. USA 86:157-161.
45. Laby, R. J., and S. V. Beer. 1995. Degradation of harpin by apoplastic protease activity. Phytopathology 85:1144 (Abstract).
46. Leach, J. E., and F. F. White. 1996. Bacterial avirulence genes. Annu. Rev. Phytopathol. 34:153-179.
47. Leister, R. T., F. M. Ausubel, and F. Katagiri. 1996. Molecular recognition of pathogen attack occurs inside of plant cells in plant disease resistance specified by the Arabidopsis genes RPS2 and RPM1. Proc. Natl. Acad. Sci. USA 93:15497-15502.
48. Li, J., H. Ochman, E. A. Groisman, E. F. Boyd, F. Solomon, K. Nelson, and R. K. Selander. 1995 Relationship between evolutionary rate and cellular location among the Inv/Spa invasion proteins of Salmonella enterica. Proc. Natl. Acad. Sci. USA 92:7252-7256.
49. Lindgren, P. B., R. C. Peet, and N. J. Panopoulos. 1986. Gene cluster of Pseudomonas syringae pv. "phaseolicola" controls pathogenicity of bean plants and hypersensitivity on nonhost plants. J. Bacteriol. 168:512-522.
50. Lonetto, M. A., K. L. Brown, K. E. Rudd, and M. J. Buttner. 1994. Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase sigma factors involved in the regulation of extracytoplasmic functions. Proc. Natl. Acad. Sci. USA 91:7573-7577.
51. Lorang, J. M., and N. T. Keen. 1995. Characterization of avrE from Pseudomonas syringae pv. tomato: a hrp-linked avirulence locus consisting of at least two transcriptional units. Mol. Plant-Microbe Interact. 8:49-57.
52. Macnab, R. M. 1996. Flagella and molility, p. 123-145. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, vol. 1. ASM Press, Washington, D.C.
53. Mansfield, J., C. Jenner, R. Hockenhull, M. A. Bennett, and R. Stewart. 1994. Characterization of avrPphE, a gene for cultivar-specific avirulence from Pseudomonas syringae pv. phaseolicola which is physically linked to hrpY, a new hrp gene identified in the halo-blight bacterium. Mol. Plant-Microbe Interact. 7:726-739.
54. Marenda, M., F. Van Gijsegem, M. Arlat, C. Zischek, P. Barberis, J. C. Camus, P. Castello, and C. A. Boucher. 1996. Genetic and molecular dissection of the hrp regulon of Ralstonia (Pseudomonas) solanacearum, p. 165-172. In G. Stacey, B. Mullin, and P. M. Gresshoff (ed.), Advances in molecular genetics of plant-microbe interactions, vol. 3. APS Press, St. Paul, Minn.
55. Midland, S. L., N. T. Keen, J. J. Sims, M. M. Midland, M. M. Stayton, V. Burton, M. J. Smith, E. P. Mazzola, K. J. Graham, and J. Clardy. 1993. The structures of syringolides 1 and 2: novel C glycosidic elicitors from Pseudomonas syringae pv. tomato. J. Org. Chem. 58:2940-2945.
56. Niepold, F., D. Anderson, and D. Mills. 1985. Cloning determinants of pathogenesis from Pseudomonas syringae pathovar syringae. Proc. Natl. Acad. Sci. USA 82:406-410.
57. Oku, T., A. M. Alvarez, and C. I. Kado. 1995. Conservation of the hypersensitivity-pathogenicity regulatory gene hrpX of Xanthomonas campestris and X. oryzae. DNA Sequence 5:245-249.
58. Pirhonen, M. U., M. C. Lidell, D. L. Rowley, S. W. Lee, S. Jin, Y. Liang, S. Silverstone, N. T. Keen, and S. W. Hutcheson. 1996. Phenotypic expression of Pseudomonas syringae avr genes in E. coli is linked to the activities of the hrp-encoded secretion system. Mol. Plant-Microbe Interact. 9:252-260.
59. Plano, G. V., S. S. Barve, and S. C. Straley. 1991. LcrD, a membrane-bound regulator of the Yersinia pestis low-calcium response. J. Bacteriol. 173:7293-7303.
60. Preston, G., H.-C. Huang, S. Y. He, and A. Collmer. 1995. The HrpZ proteins of Pseudomonas syringae pvs. syringae, glycinea, and tomato are encoded by an operon containing Yersinia ysc homologs and elicit the hypersensitive response in tomato but not soybean. Mol. Plant-Microbe Interact. 8:717-732.
61. Roine, E., W. Wei, J. Yuan, E.-L. Nurmiaho-Lassila, N. Kalkkinen, M. Romantschuk, and S. Y. He. 1997. HrpA, a structural protein of a novel bacterial pilus required for plant-bacterial interaction. Proc. Natl. Acad. Sci. USA 94:3459-3464.
62. Rosqvist, R., K. E. Magnusson, and H. Wolf-Watz. 1994. Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J. 13:964-972.
63. Russel, M. 1995. Moving through membranes with filamentous phages. Trends Microbiol. 3:223-228.
64. Salmeron, J. M., and B. J. Staskawicz. 1993. Molecular characterization and hrp-dependence of the avirulence gene avrPto from Pseudomonas syringae pv. tomato. Mol. Gen. Genet. 239:6-10.
65. Salmond, G. P. C., and P. J. Reeves. 1993. Membrane traffic wardens and protein secretion in gram-negative bacteria. Trends Biochem. Sci. 18:7-12.
66. Scofield, S. R., C. M. Tobias, J. P. Rathjen, J. H. Chang, D. T. Lavelle, R. W. Michelmore, and B. J. Staskawicz. 1996. Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science 274:2063-2065.
67. Sory, M.-P., and G. R. Cornelis. 1994. Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol. Microbiol. 14:583-594.
68. Staskawicz, B. J., F. M. Ausubel, B. J. Baker, J. G. Ellis, and J. D. G. Jones. 1995. Molecular genetics of plant disease resistance. Science 268:661-667.
69. Staskawicz, B. J., D. Dahlbeck, and N. T. Keen. 1984. Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race specific incompatibility on Glycine max (L.) Merr. Proc. Natl. Acad. Sci. USA 81:6024-6028.
70. Tang, X., R. D. Frederick, J. Zhou, D. A. Halterman, Y. Jia, and G. B. Martin. 1996. Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274:2060-2062.
71. Turner, J. G., and A. Novacky. 1974. The quantitative relation between plant and bacterial cells involved in the hypersensitive reaction. Phytopathology 64:885-890.
72. Van den Ackerveken, G., E. Marois, and U. Bonas. 1996. Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell. Cell 87:1307-1316.
73. Van Gijsegem, F., S. Genin, and C. Boucher. 1993. Evolutionary conservation of pathogenicity determinants among plant and animal pathogenic bacteria. Trends Microbiol. 1:175-180.
74. Van Gijsegem, F., C. Gough, C. Zischek, E. Niqueux, M. Arlat, S. Genin, P. Barberis, S. German, P. Castello, and C. Boucher. 1995. The hrp gene locus of Pseudomonas solanacearum, which controls the production of a type III secretion system, encodes eight proteins related to components of the bacterial flagellar biogenesis complex. Mol. Microbiol. 15:1095-1114.
75. Vivian, A., and J. Mansfield. 1993. A proposal for a uniform genetic nomenclature for avirulence genes in phytopathogenic pseudomonads. Mol. Plant-Microbe Interact. 6:9-10.
76. Wattiau, P., S. Woestyn, and G. R. Cornelis. 1996. Customized secretion chaperones in pathogenic bacteria. Mol. Microbiol. 20:255-262.
77. Wei, Z.-M., and S. V. Beer. 1993. HrpI of Erwinia amylovora functions in secretion of harpin and is a member of a new protein family. J. Bacteriol. 175:7958-7967.
78. Wei, Z.-M., and S. V. Beer. 1995. htpL activates Erwinia amylovora hrp gene transcription and is a member of the ECF subfamily of σ factors. J. Bacteriol. 177:6201-6210.
79. Wei, Z.-M., R. J. Laby, C. H. Zumoff, D. W. Bauer, S. Y. He, A. Collmer, and S. V. Beer. 1992. Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science 257:85-88.
80. Wengelnik, K., C. Marie, M. Russel, and U. Bonas. 1996. Expression and localization of HrpA1, a protein of Xanthomonas campestris pv. vesicatoria essential for pathogenicity and induction of the hypersensitive response. J. Bacteriol. 178:1061-1069.
81. Wengelnik, K., G. Van den Ackerveken, and U. Bonas. 1996. HrpG, a key hrp regulatory protein of Xanthomonas campestris pv. vesicatoria, is homologous to two-component response regulators. Mol. Plant-Microbe Interact. 9:704-712.
82. Wengelnik, K., and U. Bonas. 1996. HrpXv, and AraC-type regulator, activates expression of five of the six loci in the hrp cluster of Xanthomonas campestris pv. vesicatoria. J. Bacteriol. 178:3462-3469.
83. Whalen, M. C., R. E. Stall, and B. J. Staskawicz. 1988. Characterization of a gene from a tomato pathogen determining hypersensitive resistance in non-host species and genetic analysis of this resistance in bean. Proc. Natl. Acad. Sci. USA 85:6743-6747.
84. Wood, M. W., R. Rosqvist, P. B. Mullan, M. H. Edwards, and E. E. Galyov. 1996. SopE, a secreted protein of Salmonella dublin, is translocated into the target eukaryotic cell via a sip-dependent mechanism and promotes bacterial entry. Mol. Microbiol. 22:327-338.
85. Xiao, Y., S. Hue, J. Yi, Y. Lu, and S. W. Hutcheson. 1994. Identification of a putative alternate sigma factor and characterization of a multicomponent regulatory cascade controlling the expression of Pseudamonas syringae pv. syringae Pss61 hrp and hrmA genes. J. Bacteriol. 176:1025-1036.
86. Yang, Y., and D. W. Gabriel. 1995. Xanthomonas avirulence/pathogenicity gene family encodes functional plant nuclear targeting signals. Mol. Plant-Microbe Interact. 8:627-631.
87. Young, S. A., F. F. White, C. M. Hopkins, and J. E. Leach. 1994. AvrXa10 protein is in the cytoplasm of Xanthomonas oryzae pv. oryzae. Mol. Plant-Microbe Interact. 7:799-804.
88. Yuan, J., and S. Y. He. 1996. The Pseudomonas syringae Hrp regulation and secretion system controls the production and secretion of multiple extracellular proteins. J. Bacteriol. 178:6399-6402.
89. Zupan, J. R., and P. Zambryski. 1995. Transfer of T-DNA from Agrobacterium to the plant cell. Plant Physiol. 107:1041-1047.