The Rhizobium leguminosarum prsDE genes are required for secretion of several proteins, some of which influence nodulation, symbiotic nitrogen fixation and exopolysaccharide modification

Molecular Microbiology

Volumn 25, Issue 1, 1997, Pages 135-146

  Finnie, Christine ^a   Hartley, Nigel M ^a   Findlay, Kim C ^a   Downie, J Allan ^a  

^a JOHN INNES CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL POLYSACCHARIDE; BACTERIAL PROTEIN;

ARTICLE; BACTERIAL GENETICS; BACTERIUM MUTANT; NITROGEN FIXATION; NODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; RHIZOBIUM LEGUMINOSARUM;

BACTERIA (MICROORGANISMS); ERWINIA; ERWINIA CHRYSANTHEMI; PISUM SATIVUM; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; RHIZOBIUM; RHIZOBIUM LEGUMINOSARUM; RHIZOBIUM LEGUMINOSARUM BV. VICIAE; VICIA;

EID: 0030747558     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1997.4471803.x     Document Type: Article

References (69)

1. Akatsuka, H., Kawai, E., Omori, K., and Shibatani, T. (1995) The three genes lipB, lipC and lipD involved in the extracellular secretion of the Serratia marcescens lipase which lacks an N-terminal signal peptide. J Bacteriol 177: 6381-6389.
2. Akrim, M., Bally, M., Ball, G., Tommassen, J., Teerink, H., Filloux, A., and Lazdunski, A. (1993) Xcp-mediated protein secretion in Pseudomonas aerugiriosa: identification of two additional genes and evidence for regulation of xcp gene expression. Mol Microbiol 10: 431-443.
3. Altschul, S.F., Gish, W., Miller, W., Meyers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
4. Baumann, U., Wu, S., Flaherty, K.M., and McKay, D.B. (1993) Three-dimensional structure of the alkaline protease of Pseudomonas aeruginosa: a two-domain protein with a calcium binding parallel beta roll motif. EMBO J 12: 3357-3364.
5. Beringer, J.E. (1974) R factor transfer in Rhizobium leguminosarum. J Gen Microbiol 84: 188-198.
6. Beringer, J.E., Johnston, A.W.B., and Wells, B. (1977) The isolation of conditional ineffective mutants of Rhizobium leguminosarum. J Gen Microbiol 98: 339-343.
7. Beringer, J.E., Beynon, J.L., Buchanan-Wollaston, A.V., and Johnston, A.W.B. (1978) Transfer of the drug resistance transposon Tn5 to Rhizobium. Nature 276: 633-634.
8. Beynon, J.L., Beringer, J.E., and Johnston, A.W.B. (1980) Plasmids and host range in Rhizobium leguminosarum and Rhizobium phaseoli. J Gen Microbiol 120: 421-429.
9. Borthakur, D., Barber, C.E., Lamb, J.W., Daniels, M.J., Downie, J.A., and Johnston, A.W.B. (1986) A mutation that blocks exopolysaccharide synthesis prevents nodulation of peas by Rhizobium leguminosarum but not of beans by Rhizobium phaseoli and is corrected by cloned DNA from Rhizobium or the phytopathogen Xanthomonas. Mol Gen Genet 203: 320-323.
10. Bradley, D.J., Wood, E.A., Larkins, A.P., Galfrè, G., Butcher, G.W., and Brewin, N.J. (1988) Isolation of monoclonal antibodies reacting with peribacteroid membranes and other components of pea root nodules containing Rhizobium leguminosarum. Planta 173: 149-160.
11. Buchanan-Wollaston, A.V. (1979) Generalized transduction in Rhizobium leguminosarum. J Gen Microbiol 112: 135-142.
12. 2+-binding proteins. Anal Biochem 188: 123-131.
13. Crank, S.F., and Downie, J.A. (1994) Isolation of a DNA polymerase I (polA) mutant of Rhizobium leguminosarum that has significantly reduced levels of an IncQ-group plasmid. Mol Gen Genet 243: 119-123.
14. Dénarié, J., and Debellé, F. (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: signalling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65: 503-535.
15. Dinh, T., Paulsen, I.T., and Saier, M.H. (1994) A family of extracytoplasmic proteins that allow transport of large molecules across the outer membranes of Gram-negative bacteria. J.Bacteriol 176: 3825-3831.
16. Downie, J.A., and Surin, B.P. (1990) Either of two nod gene loci can complement the nodulation defect of a nod deletion mutant of Rhizobium leguminosarum bv. viciae. Mol Gen Genet 222: 81-86.
17. Downie, J.A., Ma, Q.-S., Knight, C.D., Hombrecher, G., and Johnston, A.W.B. (1983) Cloning of the symbiotic region of Rhizobium leguminosarum: the nodulation genes are between the nitrogenase genes and the nifA-like gene. EMBO J 2: 947-952.
18. Downie, J.A., Knight, C.D., and Johnston, A.W.B. (1985) Identification of genes and gene products involved in nodulation of peas by Rhizobium leguminosarum. Mol Gen Genet 198: 255-262.
19. Dudman, W.F., Franzen, L.E., Darvill, J.E., McNeil, M., Darvill, A.G., and Albersheim, P. (1983) The structure of the acidic polysaccharide secreted by Rhizobium phaseoli strain-127k36. Carbohydr Res 117: 141-156.
20. Duong, F., Lazdunski, A., Cami, B., and Murgier, M. (1992) Sequence of a cluster of genes controlling synthesis and secretion of alkaline protease in Pseudomonas aeruginosa: relationships to other secretory pathways. Gene 121: 47-54.
21. Duong, F., Soscia, C., Lazdunski, A., and Murgier, M. (1994) The Pseudomonas fluorescens lipase has a C-terminal secretion signal and is secreted by a three-component bacterial ABC-exporter system. Mol Microbiol 11: 1117-1126.
22. Duong, F., Lazdunski, A., and Murgier, M. (1996) Protein secretion by heterologous bacterial ABC-transporters: the C-terminus secretion signal of the secreted protein confers high recognition specificity. Mol Microbiol 21: 459-470.
23. 2+-binding protein that is exported without N-terminal cleavage and is homologous to haemolysin and related proteins. EMBO J 9: 349-354.
24. Economou, A., Davies, A.E., Johnson, A.W.B., and Downie, J.A. (1994) The Rhizobium leguminosarum biovar viciae nodO gene can enable a nodE mutant of Rhizobium leguminosarum biovar trifolii to nodulate vetch. Microbiol 140: 2341-2347.
25. Ehrhardt, D.W., Atkinson, E.M., and Long, S.R. (1992) Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors. Science 256: 998-1000.
26. Ehrhardt, D.W., Wais, R., and Long, S.R. (1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85: 673-681.
27. Fath, M.J., and Kolter, R. (1993) ABC transporters: bacterial exporters. Microb Rev 57: 995-1017.
28. Fellé, H.H., Kondorosi, E., Kondorosi, A., and Schultze, M. (1996) Rapid alkalinization in alfalfa root hairs in response to rhizobial lipochitooligosaccharide signals. Plant J 10: 295-301.
29. Felmlee, T., Pellett, S., and Welch, R.A. (1985) Nucleotide sequence of an Escherichia coli chromosomal hernolysin. J Bacteriol 163: 94-105.
30. Geelen, D., Van Montagu, M., and Holsters, M. (1995) Cloning of an Azorhizobium caulinodans endoglucanase gene and analysis of its role in symbiosis. Appl Environ Microbiol 61: 3304-3310.
31. Gilson, L., Mahanty, H.K., and Kolter, R. (1990) Genetic analysis of an MDR-like export system: the secretion of colicin V. EMBO J 9: 3875-3844.
32. Glucksmann, M.A., Reuber, T.L., and Walker, G.C. (1993) Genes needed for the modification, polymerization, export, and processing of succinoglycan by Rhizobium meliloti: a model for succinoglycan biosynthesis. J Bacteriol 175: 7045-7055.
33. Guzzo, J., Duong, F., Wandersman, C., Murgier, M., and Lazdunski, A. (1991) The secretion genes of Pseudomonas aeruginosa alkaline protease are functionally related to those of Erwinia chrysanthemi proteases and Escherichia coli α-haemolysin. Mol Microbiol 5: 477-453.
34. Håvarstein, L.S., Diep, D.B., and Nes, I.F. (1995) A family of bacteriocin ABC transporters carry out proteolytic processing of their substrates concomitant with export. Mol Microbiol 16: 229-240.
35. Hawkes, R., Niday, E., and Gordon, J. (1982) A dot-immuno-binding assay for monoclonal and other antibodies. Anal Biochem 119: 142-147.
36. Hirsch, P.R. (1979) Plasmid-determined bacteriocin production by Rhizobium leguminosarum. J Gen Microbiol 113: 219-228.
37. Kim, J.-B., and Cartita, N.C. (1992) Changes in esterification of the uronic acid groups of cell wall polysaccharides during elongation of maize coleoptiles. Plant Physiol 98: 646-653.
38. Knight, C.D., Rossen, L., Robertson, J.G., Wells, B., and Downie, J.A. (1986) Nodulation inhibition by Rhizobium leguminosarum multicopy nodABC genes and analysis of early stages of plant infection. J Bacteriol 166: 552-558.
39. Krol, J.E., and Skorupska, A.M. (1996) Nucleotide sequence analysis of the gene of Rhizobium leguminosarum bv. trifolii coding for a protein closely related to ATP-binding bacterial transport proteins. EMBL Accession No. X98117.
40. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
41. Lamb, J.W., Hombrecher, G., and Johnston, A.W.B. (1982) Plasmid-determined nodulation and nitrogen-fixation abilities in Rhizobium phaseoli. Mol Gen Genet 186: 449-452.
42. Létoffé, S., and Wandersman, C. (1992) Secretion of CyaA-PrtB and Hlya-PrtB fusion proteins in Escherichia coli: involvement of the glycine-rich repeat domain of Erwinia chrysanthemi protease B. J Bacteriol 174: 4920-4927.
43. Létoffé, S., Delepelaire, P., and Wandersman, C. (1990) Protease secretion by Erwinia chrysanthemi: the specific secretion functions are analogous to those of Escherichia coli haemolysin. EMBO J 9: 1375-1382.
44. Létoffé, S., Ghigo, J.M., and Wandersman, C. (1994) Secretion of the Serratia marcescens HasA protein by an ABC transporter. J Bacteriol 176: 5372-5377.
45. Lever, M. (1972) A new reaction for colorimetric determination of carbohydrates. Analyt Biochem 47: 273-279.
46. Loewus, F.A. (1952) Improvement in the anthrone method for determination of carbohydrates. Anal Chem 24: 219.
47. Mateos, P.F., Jimenez-Zurdo, J.I., Chen, J., Squartini, A.S., Haack, S.K., Martinez-Molina, E., Hubbell, D.H., and Dazzo, F.B. (1992) Cell-associated pectinolytic and cellulolytic enzymes in Rhizobium leguminosarum biovar trifolii. Appl Environ Microbiol 58: 1816-1822.
48. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
49. Morona, R., and Reeves, P. (1982) The tolC locus of Escherichia coli affects the expression of three major outer membrane proteins. J Bacteriol 150: 1016-1023.
50. Rivilla, R., and Downie, J.A. (1994) Identification of a Rhizobium leguminosarum gene homologous to nodT but located outside the symbiotic plasmid. Gene 144: 87-91.
51. Salmond, G.P.C. (1994) Secretion of extracellular virulence factors by plant pathogenic bacteria. Ann Rev Phytopathol 32: 181-200.
52. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
53. Scheu, A.K., Economou, A., Hong, G.-F., Ghelani, S., Johnston, A.W.B., and Downie, J.A. (1992) Secretion of the Rhizobium leguminosarum nodulation protein NodO by haemolysin-type systems. Mol Microbiol 6: 231-238.
54. Sebo, P., and Ladant, D. (1993) Repeat sequences in the Bordetella pertussis adenylate cyclase toxin can be recognised as alternative carboxy-proximal secretion signals by the Escherichia coli α-haemolysin translocator. Mol Microbiol 9: 999-1009.
55. Sherwood, M.T. (1970) Improved synthetic medium for the growth of Rhizobium. J Appl Bacteriol 33: 708-713.
56. Simon, R., Priefer, U., and Pühler, A. (1983) A broad host-range mobilization system for in vivo genetic engineering: transposon mutagenesis of Gram-negative bacteria. Biotechnology 1: 784-791.
57. Staskawicz, B., Dahlbeck, D., Keen, N., and Napoli, C. (1987) Molecular characterization of cloned avirulence genes from race-O and race-1 of Pseudomonas syringae pv. Glycinea. J Bacteriol 169: 5789-5794.
58. Sutton, J.M., Lea, E.J.A., and Downie, J.A. (1994) The nodulation-signaling protein NodO from Rhizobium leguminosarum biovar viciae forms ion channels in membranes. Proc Natl Acad Sci USA 91: 9990-9994.
59. Sutton, J.M., Peart, J., Dean, G., and Downie, J.A. (1996) Analysis of the C-terminal secretion signal of the Rhizobium leguminosarum nodulation protein NodO; a potential system for the secretion of heterologous proteins during nodule invasion. Mol Plant-Microbe Interact 9: 671-680.
60. Teather, R.M., and Wood, P.J. (1982) Use of Congo red-polysaccharide interactions in enumeration and characterization of cellulolytic bacteria from the bovine rumen. Appl Environ Microbiol 43: 777-780.
61. van Rhijn, P., Luyten, E., Vlassak, K., and Vanderleyden, J. (1996) Isolation and characterization of a pSym locus of Rhizobium sp. BR816 that extends nodulation ability of narrow host range Phaseolus vulgaris symbionts to Leucaena leucocephala. Mol Plant-Microbe Interact 9: 74-77.
62. van Workum, W.A.T., Canter Cremers, H.C.J., Wijfjes, A.H.M., van der Kolk, C., Wijffelman, C.A., and Kijne, J.W. (1997) Cloning and characterization of four genes of Rhizobium leguminosarum bv. trifolii involved in exopolysaccharide production and nodulation. Mol Plant-Microbe Interact 10: 290-301.
63. Wandersman, C. (1996) Secretion across the bacterial membrane. In Eschericia coli and Salmonella: Cellular and Molecular Biology. Neidhart, F.C. et al. (ed.). Washington, DC: American Society of Microbiology Press, pp. 955-966.
64. Wandersman, C., and Delepelaire, P. (1990) TolC, an Escherichia coli outer membrane protein required for haemolysin secretion. Proc Natl Acad Sci USA 87: 4776-4780.
65. Wassif, C., Cheek, D., and Belas, R. (1995) Molecular analysis of a metalloprotease from Proteus mirabilis. J Bacteriol 177: 5790-5798.
66. Welch, R.A. (1991) Pore-forming cytolysins of Gram-negative bacteria. Mol Microbiol 5: 521-528.
67. Welters, P., Metz, B., Felix, G., Palme, K., Szczglowski, K., and de Bruijn, F.J. (1993) Interaction of a rhizobial DNA-binding protein with the promoter region of a plant leghemoglobin gene. Plant Physiol 102: 1095.
68. York, G.M., and Walker, G.C. (1997) The Rhizobium meliloti exoK gene and prsD/prsE/exsH genes are components of independent degradative pathways which contribute to production of low molecular weight succinoglycan. Mol Microbiol 25: 117-134.
69. Zevenhuizen, L.P.T.M. (1981) Cellular glycogen, β-1,2-glucan, poly-β-hydroxybutyric acid and extracellular polysaccharides in fast-growing species of Rhizobium. Antonie van Leeuwenhoek 47: 481-497.