Recognition of the Agrobacterium tumefaciens VirE2 Translocation Signal by the VirB/D4 Transport System Does Not Require VirE1

Plant Physiology

Volumn 133, Issue 3, 2003, Pages 978-988

  Vergunst, Annette C ^a   Van Lier, Miranda C M ^a   Den Dulk Ras, Amke ^a   Hooykaas, Paul J J ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ASSAYS; BACTERIA; GENES; PLANT CELL CULTURE; PROTEINS;

FUSION PROTEINS; MUTANTS;

PLANTS (BOTANY);

AGROBACTERIUM; AGROBACTERIUM TUMEFACIENS; BACTERIA (MICROORGANISMS); VIR;

EID: 0344152245     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.103.029223     Document Type: Article

References (63)

1. Baron C, Callaghan DO, Lanka E (2002) Bacterial secrets of secretion: EuroConference on the biology of type IV secretion processes. Mol Microbiol 43: 1359-1365
2. Beijersbergen A, den Dulk-Ras A, Schilperoort RA, Hooykaas PJJ (1992) Conjugative transfer by the virulence system of Agrobacterium tumefaciens. Science 256: 1324-1327
3. Berks BC, Sargent F, Palmer T (2000) The Tat protein export pathway. Mol Microbiol 35: 260-274
4. Birtalan S, Ghosh P (2001) Structure of the Yersinia type III secretory system chaperone SycE. Nat Struct Biol 8: 974-978
5. Birtalan SC, Phillips RM, Ghosh P (2002) Three-dimensional secretion signals in chaperone-effector complexes of bacterial pathogens. Mol Cell 9: 971-980
6. Boschiroli ML, Ouahrani-Bettache S, Foulongne V, Michaux-Charachon S, Bourg G, Allardet-Servent A, Cazevieille C, Lavigne J, Liautard JP, Ramuz M et al. (2002) Type IV secretion and Brucella virulence. Vet Microbiol 90: 341-348
7. Boyd AP, Lambermont I, Cornelis GR (2000) Competition between the Yops of Yersinia enterocolitica for delivery into eukaryotic cells: role of the SycE chaperone binding domain of YopE. J Bacteriol 182: 4811-4821
8. Buchanon-Wollaston V, Passiatore JE, Cannon F (1987) The mob and oriT mobilization functions of a bacterial plasmid promote its transfer to plants. Nature 328: 172-175
9. Bundock P, den Dulk-Ras A, Beijersbergen A, Hooykaas PJJ (1995) Transkingdom T-DNA transfer from Agrobacterium tumefaciens to Saccharomyces cerevisiae. EMBO J 14: 3206-3214
10. Cabezón E, Sastre JI, de la Cruz F (1997) Genetic evidence of a coupling role for the TraG protein family in bacterial conjugation. Mol Gen Genet 254: 400-406
11. Cambronne ED, Cheng LW, Schneewind O (2000) LcrQ/YscM1, regulators of the Yersinia yop virulon, are injected into host cells by a chaperone-dependent mechanism. Mol Microbiol 37: 263-273
12. Christie PJ (2001) Type IV secretion: intercellular transfer of macromolecules by systems ancestrally related to conjugation machines. Mol Microbiol 40: 294-305
13. Christie PJ, Vogel JP (2000) Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol 8: 354-360
14. Citovsky V, Guralnick B, Simon MN, Wall JS (1997) The molecular structure of Agrobacterium VirE2-single-stranded DNA complexes involved in nuclear import. J Mol Biol 271: 718-727
15. Conover GM, Derré I, Vogel JP, Isberg RR (2003) The Legionella pneumophila LidA protein: a translocated substrate of the Dot/Icm system associated with maintenance of bacterial integrity. Mol Microbiol 48: 305-321
16. Day JB, Plano GV (1998) A complex composed of SycN and YscB functions as a specific chaperone for YopN in Yersinia pestis. Mol Microbiol 30: 777-788
17. de Groot MJA, Bundock P, Hooykaas PJJ, Beijersbergen AGM (1998) Agrobacterium tumefaciens-mediated transformation of filamentous fungi. Nature Biotechnol 16: 839-842
18. Dehio C (2003) Recent progress in understanding Bartonella-induced vascular proliferation. Curr Opin Microbiol 6: 61-65
19. Delahay RM, Frankel G (2002) Coiled-coil proteins associated with type III secretion systems: a versatile domain revisited. Mol Microbiol 45: 905-916
20. den Dulk-Ras A, Hooykaas PJ (1995) Electroporation of Agrobacterium tumefaciens: plant cell electroporation and electrofusion protocols. 55: 63-72
21. Deng WY, Chen LS, Peng WT, Liang XY, Sekiguchi S, Gordon MP, Comai L, Nester EW (1999) VirE1 is a specific molecular chaperone for the exported single-stranded-DNA-binding protein VirE2 in Agrobacterium. Mol Microbiol 31: 1795-1807
22. Dombek P, Ream W (1997) Functional domains of Agrobacterium tumefaciens single-stranded DNA-binding protein virE2. J Bacteriol 179: 1165-1173
23. Dumas F, Duckely M, Pelczar P, Van-Gelder P, Hohn B (2001) An Agrobacterium VirE2 channel for transferred-DNA transport into plant cells. Proc Natl Acad Sci USA 98: 485-490
24. Feldman MF, Cornelis GR (2003) The multitalented type III chaperones: all you can do with 15 kDa. FEMS Microbiol Lett 219: 151-158
25. Feldman MF, Muller S, Wuest E, Cornelis GR (2002) Syc E allows secretion of YopE-DHFR hybrids by the Yersinia enterocolitica type III Ysc system. Mol Micro 46: 1183-1197
26. Gelvin SB (2003) Agrobacterium-mediated plant transformation: the biology behind the "gene-jockeying" tool. Microbiol Mol Biol Rev 67: 16-37
27. Gomis-Rüth F, Moncalian G, de la Cruz F, Coll M (2002) Conjugative plasmid protein TrwB, an integral membrane type IV secretion system coupling protein: detailed structural features and mapping of the active site cleft. J Biol Chem 277: 7556-7566
28. Gomis-Rüth F, Moncalian G, Perez LR, Gonzalez A, Cabezön E, de laCruz F, Coll M (2001) The bacterial conjugation protein TrwB resembles ring helicases and F-1-ATPase. Nature 409: 637-641
29. Hamilton CM, Lee H, Li PL, Cook DM, Piper KR, von-Bodman SB, Lanka E, Ream W, Farrand SK (2000) TraG from RP4 and TraG and VirD4 from Ti plasmids confer relaxosome specificity to the conjugal transfer system of pTiC58. J Bacteriol 182: 1541-1548
30. Hooykaas PJJ, Hofker M, den Dulk-Ras A, Schilperoort RA (1984) A comparison of virulence determinants in an octopine Ti plasmid, a nopaline Ti plasmid, and an Ri plasmid by complementation analysis of Agrobacterium tumefaciens mutants. Plasmid 11: 195-205
31. Hooykaas PJJ, Roobol C, Schilperoort RA (1979) Regulation of the transfer of Ti-plasmids of Agrobacterium tumefaciens. J Gen Microbiol 110: 99-109
32. Koekman BP, Hooykaas PJJ, Schilperoort RA (1982) A functional map of the replicator region of the octopine Ti plasmid. Plasmid 7: 119-132
33. Kunik T, Tzfira T, Kapulnik Y, Gafni Y, Dingwall C, Citovsky V (2000) Genetic transformation of HeLa cells by Agrobacterium. Proc Natl Acad Sci USA 98: 1871-1876
34. Luo Y, Bertero MG, Frey EA, Pfuetzner RA, Wenk MR, Creagh L, Marcus SL, Lim D, Sicheri F, Kay C et al. (2001) Structural and biochemical characterization of the type III secretion chaperones CesT and SigE. Nat Struct Biol 8: 1031-1036
35. McBride KE, Knauf VC (1988) Genetic analysis of the virE operon of the Agrobacterium Ti plasmid pTiA6. J Bacteriol 170: 1430-1437
36. Melchers LS, Maroney MJ, den Dulk-Ras A, Thompson DV, van Vuuren HA, Schilperoort RA, Hooykaas PJ (1990) Octopine and nopaline strains of Agrobacterium tumefaciens differ in virulence; molecular characterization of the virF locus. Plant Mol Biol 14: 249-259
37. Mori H, Ito K (2001) The sec protein-translocation pathway. Trends Microbiol 9: 494-500
38. Nagai H, Kagan JC, Zhu XJ, Kahn RA, Roy CR (2002) A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes. Science 295: 679-682
39. Nagai H, Roy CR (2003) Show me the substrates: modulation of host cell function by type IV secretion systems. Cell Microbiol 5: 373-383
40. Page AL, Parsot C (2002) Chaperones of the type III secretion pathway: jacks of all trades. Mol Microbiol 46: 1-11
41. Pansegrau W, Lanka E (1996) Mechanisms of initiation and termination reactions in conjugative DNA processing. J Biol Chem 271: 13068-13076
42. Ried JL, Collmer A (1987) An nptl-sacB-sacR cartridge for constructing directed, unmarked mutations in Gram-negative bacteria by marker exchange-eviction mutagenesis. Gene 57: 239-246
43. Rossi L, Hohn B, Tinland B (1996) Integration of complete transferred DNA units is dependent on the activity of virulence E2 protein of Agrobacterium tumefaciens. Proc Natl Acad Sci USA 93: 126-130
44. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
45. Schrammeijer B (2001) Functional analysis of the virulence protein VirF from Agrobacterium tumefaciens. PhD thesis. Leiden University, Leiden, The Netherlands
46. Schrammeijer B, den-Dulk-Ras A, Vergunst AC, Jurado Jacome E, Hooykaas PJJ (2003) Analysis of Vir protein translocation from Agrobacterium tumefaciens using Saccharomyces cereuisiae as a model: evidence for transport of a novel effector protein VirE3. Nucleic Acids Res 31: 860-868
47. Schrammeijer B, Risseeuw E, Pansegrau W, Regensburg-Tuïk AJG, Crosby WL, Hooykaas PJJ (2001) Interaction of the virulence protein VirF of Agrobacterium tumefaciens with plant homologs of the yeast Skp1 protein. Curr Biol 11: 258-262
48. Schröder G, Krause S, Zechner EL, Traxler B, Yeo HJ, Lurz R, Waksman G, Lanka E (2002) TraG-like proteins of DNA transfer systems and of the Helicobacter pylori type IV secretion system: inner membrane gate for exported substrates? J Bacteriol 184: 2767-2779
49. Simone M, McCullen CA, Stahl LE, Binns AN (2001) The carboxy-terminus of VirE2 from Agrobacterium tumefaciens is required for its transport to host cells by the virB-encoded type IV transport system. Mol Microbiol 41: 1283-1293
50. Spratt BG, Hedge PJ, te Heesen S, Edelman A, Broome-Smith JK (1986) Kanamycin resistant vectors that are analogues of plasmids pUC8, pUC9, pEMBL8 and pEMBL9. Gene 41: 337-342
51. Stebbins CE, Galan JE (2001) Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature 414: 77-81
52. Sundberg C, Meek L, Carroll K, Das A, Ream W (1996) VirE1 protein mediates export of the single-stranded DNA-binding protein VirE2 from Agrobacterium tumefaciens into plant cells. J Bacteriol 178: 1207-1212
53. Sundberg CD, Ream W (1999) The Agrobacterium tumefaciens chaperone-like protein, VirE1, interacts with VirE2 at domains required for single-stranded DNA binding and cooperative interaction. J Bacteriol 181: 6850-6855
54. Szpirer CY, Faelen M, Couturier M (2000) Interaction between the RP4 coupling protein TraG and the pBHR1 mobilization protein Mob. Mol Microbiol 37: 1283-1292
55. Vergunst AC, De Waal EC, Hooykaas PJJ (1998) Root transformation by Agrobacterium tumefaciens. In J Martinez-Zapater, J Salinas, eds, Arabidopsis Protocols. Meth Mol Biol 82: 227-244
56. Vergunst AC, Schrammeijer B, den-Dulk-Ras A, de-Vlaam CMT, Regensburg TT, Hooykaas PJJ (2000) VirB/D4-dependent protein translocation from Agrobacterium into plant cells. Science 290: 979-982
57. Ward EW, Barnes WM (1988) VirD2 protein of Agrobacterium tumefaciens very tightly linked to the 5′ end of T-strand DNA. Science 242: 927-930
58. Wattiau P, Woestyn S, Corenelis GR (1996) Customized secretion chaperones in pathogenic bacteria. Mol Microbiol 20: 255-262
59. Woestyn S, Sory MP, Boland A, Leguenne O, Cornelis GR (1996) The cytosolic SycE and sycH chaperones of Yersinia protect the region of YopE and YopH involved in translocation across eukaryotic cell membranes. Mol Micro 20: 1261-1271
60. Zhao ZM, Sagulenko E, Ding ZY, Christie PJ (2001) Activities of virE1 and the VirE1 secretion chaperone in export of the multifunctional VirE2 effector via an Agrobacterium type IV secretion pathway. J Bacteriol 183: 3855-3865
61. Zhou XR, Christie PJ (1999) Mutagenesis of the Agrobacterium VirE2 single-stranded DNA-binding protein identifies regions required for self-association and interaction with VirEl and a permissive site for hybrid protein construction. J Bacteriol 181: 4342-4352
62. Ziemienowicz A, Merkle T, Schoumacher F, Hohn B, Rossi L (2001) Import of Agrobacterium T-DNA into plant nuclei: two distinct functions of VirD2 and VirE2 proteins. Plant Cell 13: 369-383
63. Zupan JR, Citovsky V, Zambryski P (1996) Agrobacterium virE2 protein mediates nuclear uptake of single-stranded DNA in plant cells. Proc Natl Acad Sci USA 93: 2392-2397