The C-terminal domain of the Rhizobium leguminosarum chitin synthase NodC is important for function and determines the orientation of the N-terminal region in the inner membrane

Molecular Microbiology

Volumn 19, Issue 3, 1996, Pages 443-453

  Barny, Marie Anne ^a,b   Schoonejans, Eric ^a,c   Economou, Anastassios ^a,d   Johnston, Andrew W B ^a,e   Downie, J Allan ^a  

^a JOHN INNES CENTRE   (United Kingdom)

^b INRA   (France)

^c INSTITUT DES SCIENCES DU VÉGÉTAL   (France)

^d UNIVERSITY OF CRETE   (Greece)

^e UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHITIN SYNTHASE;

ARTICLE; MEMBRANE STRUCTURE; PRIORITY JOURNAL; PROTEIN DOMAIN; RHIZOBIUM LEGUMINOSARUM;

EID: 0030071780     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1996.382911.x     Document Type: Article

References (63)

1. Atkinson, E.M., Palcic, M.M., Hindsgaul, O., and Long, S.R. (1994) Biosynthesis of Rhizobium meliloti lipo-oligosaccharide Nod factors: NodA is required for an N-acyl transferase activity. Proc Natl Acad Sci USA 91: 8418-8422.
2. Barny, M.A., and Downie, J.A. (1993) Identification of the NodC protein in the inner but not the outer membrane of Rhizobium leguminosarum. Mol Plant-Microbe Interact 6: 669-672.
3. Beringer, J.E. (1974) R factor transfer in Rhizobium leguminosarum. J Gen Microbiol 84: 188-198.
4. Bhuvaneswari, T.V., and Solheim, B. (1985) Root hair deformation in the white clover/Rhizobium trifolii symbiosis. Physiol Plant 63: 25-34.
5. 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.
6. Bulawa, C.E., Slater, M., Cabib, E., Au-Young, J., Sburlati, A., Adair, W.L., and Robbins, P.W. (1986) The S. cerevisiae structural gene for chitin synthase is not required for chitin synthesis in vivo. Cell 46: 213-225.
7. Cao, G., and Dalbey, R.E. (1994) Translocation of N-terminal tails across the plasma membrane. EMBO J 19: 4662-4669.
8. Carlson, R.W., Price, N.P.J., and Stacey, G. (1994) The biosynthesis of rhizobial lipo-oligosaccharide nodulation signal molecules. Mol Plant-Microbe Interact 7: 684-695.
9. Claros, M.G., and von Heijne, G. (1994) TopPred II: an improved software for membrane protein structure predictions. CABIOS Application Notes 10: 685-686.
10. Collins-Emerson, J.M., Terzaghi, E.A., and Scott, D.B. (1990) Nucleotide sequence of Rhizobium loti nodC. Nucl Acids Res 18: 6990.
11. Cubo, T., Economou, A., Murphy, G., Johnston, A.W.B., and Downie, J.A. (1992) Molecular characterization and regulation of the rhizosphere-expressed genes rhiABCR that can influence nodulation by Rhizobium leguminosarum biovar viciae. J Bacteriol 174: 4026-4035.
12. 1 is preceded by nolE, a gene whose product is secreted from the cytoplasm. Mol Microbiol 4: 921-923.
13. DeAngelis, P.L., Papaconstantinou, J., and Weigel, P.H. (1993) Molecular cloning, identification, and sequence of the hyaluronan synthase gene from Group A Streptococcus pyogenes. J Biol Chem 268: 19181-19184.
14. Ditta, G.S., Stanfield, S.W., Corby, H.D.L., and Helinski, D.R. (1980) Broad host range DNA cloning system from Gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proc Natl Acad Sci USA 77: 7347-7351.
15. Downie, J.A. (1994) Signalling strategies for nodulation of legumes by rhizobia. Trends Microbiol 2: 318-324.
16. Downie, J.A., Hombrecher, G., Ma, Q.-S., Knight, C.D., Wells, B., and Johnston, A.W.B. (1983) Cloned nodulation genes of Rhizobium leguminosarum determine host-range specificity. Mol Gen Genet 190: 359-365.
17. 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.
18. Egelhoff, T.T., and Long, S.R. (1986) Rhizobium meliloti nodulation genes: identification of nodDABC gene products, purification of Nod protein, and expression of nodA in Rhizobium meliloti. J Bacteriol. 164: 591-599.
19. Ehrmann, M., Boyd, D., and Beckwith, J. (1990) Genetic analysis of membrane protein topology by a sandwich gene fusion approach. Proc Natl Acad Sci USA 87: 7574-7578.
20. Engelman, D.M., Steitz, T.A., and Goldman, A. (1986) Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins. Annu Rev Biophys Chem 15:321-353.
21. Evans, I.J., and Downie, J.A. (1986) The NodI gene product of Rhizobium leguminosarum is closely related to ATP-binding bacterial transport proteins: nucleotide sequence analysis of the nodI and nodJ genes. Gene 43: 95-101.
22. Figurski, D.H., and Helinski, D.R. (1979) Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in frans. Proc Natl Acad Sci USA 76: 1648-1652.
23. Gafvelin, G., and von Heijne, G. (1994) Topological 'Frustration' in multispanning E. coli inner membrane proteins. Cell 77: 401-412.
24. Geremia, R.A., Mergaert, P., Geelen, D., Van Montagu, M., and Holsters, M. (1994) The NodC protein of Azorhizobium caulinodans is an N-acetylglucosaminyltransferase. Proc Natl Acad Sci USA 91: 2669-2673.
25. Goethals, K., Gao, M., Tomekpe, K., Van Montagu, M., and Holsters, M. (1989) Common nodABC genes in Nod locus 1 of Azorhizobium caulinodans: nucleotide sequence and plant-inducible expression. Mol Gen Genet 219: 289-298.
26. Gutierrez, C., and Devedjian, J.C. (1989) A plasmid facilitating in vitro construction of phoA gene fusions in Escherichia coli. Nucl Acids Res 17: 3999.
27. Hubac, H.C., Guerrier, D., Ferran, J., Tremoliers, A., and Kondorosi, A. (1992) Lipid and protein composition of outer and inner membranes in wild-type strains and nod mutants of Rhizobium meliloti. J Gen Microbiol 138: 1973-1983.
28. Jacobs, T.W., Egelhoff, T.T., and Long, S.R. (1985) Physical and genetic map of a Rhizobium meliloti nodulation gene region and nucleotide sequence of nodC. J Bacteriol 162: 469-476.
29. John, M., Schmidt, J., Wieneke, U., Kondorosi, E., Kondorosi, A., and Schell, J. (1985) Expression of the nodulation gene nodC of Rhizobium meliloti in Escherichia coli: role of the nodC gene product in nodulation. EMBO J 4: 2425-2430.
30. John, M., Schmidt, J., Wieneke, U., Krussmann, H.-D., and Schell, J. (1988) Transmembrane orientation and receptor-like structure of the Rhizobium meliloti common nodulation protein NodC. EMBO J 7: 583-588.
31. John, M., Röhrig, H., Schmidt, J., Wieneke, U., and Schell, J. (1993) Rhizobium NodB protein involved in nodulation signal synthesis is a chitooligosaccharide deacetylase. Proc Natl Acad Sci USA 90: 625-629.
32. Johnson, D., Roth, L.E., and Stacey, G. (1989) Immunogold localization of the NodC and NodA proteins of Rhizobium meliloti. J Bacteriol 171: 4583-4588.
33. 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.
34. Krishnan, H.B., and Pueppke, S.G. (1991) Sequence and analysis of the nodABC region of Rhizobium fredii USDA257, a nitrogen-fixing symbiont of soybean and other legumes. Mol Plant-Microbe Interact 4: 512-520.
35. 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.
36. McKay, I.A., and Djordjevic, M.A. (1993) Production and secretion of Nod metabolites by Rhizobium leguminosarum biovar trifolii are disrupted by the same environmental factors that reduce nodulation in the field. Appl Environ Microbiol 59: 3385-3392.
37. Maharaj, C., May, T.B., Wang, S.-K., and Chakrabarty, A.M. (1993) Sequence of the alg8 and alg44 genes involved in the synthesis of alginate by Pseudomonas aeruginosa. Gene 136: 267-269.
38. Manoil, C., and Beckwith, J. (1985) TnphoA: a transposon probe for protein export signals. Proc Natl Acad Sci USA 82: 8129-8133.
39. Manoil, C., and Beckwith, J. (1986) A genetic approach to analysing membrane protein topology. Science 233: 1403.
40. Rivilla, R., Sutton, J.M., and Downie, J.A. (1995) Rhizobium leguminosarum NodT is related to a family of outer-membrane transport proteins that includes TolC, PrtF, CyaE and AprF. Gene 161: 27-31.
41. Röhrig, H., Schmidt, J., Wieneke, U., Kondorosi, E., Barlier, I., Schell, J., and John, M. (1994) Biosynthesis of lipooligosaccharide modulation factors: Rhizobium NodA protein is involved in N-acylation of the chitooligosaccharide backbone. Proc Natl Acad Sci USA 91: 3122-3126.
42. Rosa, F., Sargent, T.D., Rebbert, M.L., Michaels, G.S., Jamrich, M., Grunz, H., Jonas, E., Winkles, J.A., and David, I.B. (1988) Accumulation and decay of DG42 gene products follow a gradient pattern Xenopus embryogenesis. Devel Biol 129: 114-123.
43. Rossen, L., Johnston, A.W.B., and Downie, J.A. (1984) DNA sequence of the Rhizobium leguminosarum nodulation genes nodA, B and C required for root hair curling. Nucl Acids Res 12: 9497-9508.
44. Rossen, L., Shearman, C.A., Johnston, A.W.B., and Downie, J.A. (1985) The nodD gene of Rhizobium leguminosarum is autoregulatory and in the presence of plant exudate induces the nodABC genes. EMBO J 4: 3369-3373.
45. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning. A Laboratory Manual, 2nd edn. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
46. Saxena, I.M., Chyr Lin, F., and Brown, Jr, R.M. (1990) Cloning and sequencing of the cellulose synthase catalytic subunit gene of Acetobacter xylinum. Plant Mol Biol 15: 673-683.
47. Saxena, I.M., Chyr Lin, F., and Brown, Jr, R.M. (1991) Identification of a new gene in an operon for cellulose biosynthesis in Acetobacter xylinum. Plant Mol Biol 16: 947-954.
48. Saxena, I.M., Kudlicka, K., Okuda, K., and Brown, Jr, R.M. (1994) Characterization of genes in the cellulose-synthesizing operon (acs operon) of Acetobacter xylinum: implications for cellulose crystallization. J Bacteriol 176: 5735-5752.
49. Saxena, I.M., Brown, Jr, R.M., Febre, M., Geremia, R.A., and Henrissat, B. (1995) Multidomain architecture of β-glycosyl transferases: implications for mechanism of action. J Bacteriol 177: 1419-1424.
50. Schlaman, W.R.M. (1992). Regulation of nodulation gene expression in Rhizobium leguminosarum biovar viceae, PhD Thesis, University of Leiden.
51. Schmidt, J., John, M., Wieneke, U., Krussmann, H.-D., and Schell, J. (1986) Expression of the nodulation gene nodA in R. meliloti and localization of the gene product in the cytosol. Proc Natl Acad Sci USA 93: 9581-9585.
52. Schofield, P.R., and Watson, J.M. (1986) DNA sequence of Rhizobium trifolii nodulation genes reveals a reiterated and potentially regulatory sequence preceding nodABC and nodFE. Nucl Acids Res 14: 2891-2903.
53. Scott, K.F. (1986) Conserved nodulation genes from the nonlegume symbiont Bradyrhizobium sp. (Parasponia). Nucl Acids Res 14: 2905-2919.
54. Sherwood, M.T. (1970) Improved synthetic medium for the growth of Rhizobium. J Appl Bacteriol 33: 708-713.
55. Silhavy, T.J., and Beckwith, J.R. (1985) Use of lac fusions for the study of biological problems. Microbiol Rev 49: 398-418.
56. Spaink, H.P., Weinman, J., Djordjevic, M.A., Wijffelman, C.A., Okker, R.J.H., and Lugtenberg, B.J.J. (1989) Genetic analysis and cellular localization of the Rhizobium host specificity-determining NodE protein. EMBO J 8: 2811-2818.
57. Spaink, H.P., Sheeley, D.M., Van Brussel, A.A.N., Glushka, J.N., York, W.S., Tak, T., Geiger, O., Kennedy, E.P., Reinhold, V.N., and Lugtenberg, B.J.J. (1991) A novel, highly unsaturated, fatty acid moeity of lipo-oligosaccharide signals determines host specificity of Rhizobium leguminosarum. Nature 354: 125-130.
58. Spaink, H.P., Wijfjes, A.H.M., van der Drift, K.M.G.M., Haverkamp, J., Thomas-Oates, J.E., and Lugtenberg, B.J.J. (1994) Structural identification of metabolites produced by the NodB and NodC proteins of Rhizobium leguminosarum. Mol Microbiol 13: 821-831.
59. Török, I., Kondorosi, E., Stepkowski, T., Posfai, J., and Kondorosi, A. (1984) Nucleotide sequence of Rhizobium meliloti nodulation genes. Nucl Acids Res 12: 9509-9524.
60. Truchet, G., Roche, P., Lerouge, P., Vasse, J., Camut, S., de Billy, F., Prome, J.-C., and Dénarié, J. (1991) Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351: 670-673.
61. Vázquez, M., Dávalos, A., de las Peñas, A., Sánchez, F., and Quinto, C. (1991) Novel organization of the common nodulation genes in Rhizobium leguminosarum bv. phaseoli strains. J Bacteriol 173: 1250-1258.
62. Vázquez, M., Santana, O., and Quinto, C. (1993) The NodI and NodJ proteins from Rhizobium and Bradyrhizobium strains are similar to capsular polysaccharide secretion proteins from Gram-negative bacteria. Mol Microbiol 8: 369-377.
63. Young, J.P.W., Downer, H.L., and Eardly, B.D. (1991) Phylogeny of the phototrophic Rhizobium strain BTAi1 by polymerase chain reaction-based sequencing of a 16S rRNA gene segment. J Bacteriol 173: 2271-2277.