Novel and complex chromosomal arrangement of Rhizobium loti nodulation genes

Molecular Plant-Microbe Interactions

Volumn 9, Issue 3, 1996, Pages 187-197

  Scott, D Barry ^a   Young, Carolyn A ^a   Collins Emerson, Julie M ^a   Terzaghi, Eric A ^a   Rockman, Eva S ^a,d   Lewis, Pauline E ^b   Pankhurst, Clive E ^b,c  

^a MASSEY UNIVERSITY   (New Zealand)

^b New Zealand Department of Scientific and Industrial Research   (New Zealand)

^c CSIRO   (Australia)

^d Ger Israel Found Sci R and D   (Israel)

Author keywords

Nodulation gene rearrangements

Indexed keywords

ACYLTRANSFERASE; AMIDASE; BACTERIAL DNA; BACTERIAL PROTEIN; NODA PROTEIN, RHIZOBIALES; NODB PROTEIN, BACTERIA; NODD PROTEIN, BACTERIA; PRIMER DNA;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENE; CHROMOSOME MAP; GENE EXPRESSION REGULATION; GENE REARRANGEMENT; GENETIC COMPLEMENTATION; GENETICS; LEGUME; MEDICINAL PLANT; MICROBIOLOGY; MOLECULAR GENETICS; NITROGEN FIXATION; NUCLEOTIDE SEQUENCE; OPERON; RHIZOBIUM; SEQUENCE HOMOLOGY; SYMBIOSIS;

ACYLTRANSFERASES; AMIDOHYDROLASES; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE SEQUENCE; CHROMOSOME MAPPING; CHROMOSOMES, BACTERIAL; DNA PRIMERS; DNA, BACTERIAL; FABACEAE; GENE REARRANGEMENT; GENES, BACTERIAL; GENETIC COMPLEMENTATION TEST; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; NITROGEN FIXATION; OPERON; PLANTS, MEDICINAL; RHIZOBIUM; SEQUENCE HOMOLOGY, AMINO ACID; SYMBIOSIS;

BACTERIA (MICROORGANISMS); MESORHIZOBIUM LOTI; RHIZOBIUM;

EID: 0030131178     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-9-0187     Document Type: Article

References (82)

1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Appelbaum, E. R., Thompson, D. V., Idler, K., and Chartrain, N. 1988. Rhizobium japonicum USDA 191 has two nodD genes that differ in primary structure and function. J. Bacteriol. 170:12-20.
3. Atkinson, E. M., Palcic, M. M., Hindsgaul, O., and Long, S. R. 1994. Biosynthesis of Rhizobium meliloti lipooligosaccharide Nod factors: NodA is required for an N-acyltransferase activity. Proc. Natl. Acad. Sci. USA. 91:8418-8422.
4. Beringer, J. E. 1974. R factor transfer in Rhizobium leguminosarum. J. Gen. Microbiol. 84:118-198.
5. Beringer, J. E., Beynon, J. L., Buchanan-Wollaston, A. V., and Johnston, A. W. B. 1978. Transfer of the drug-resistant transposon Tn5 to Rhizobium. Nature 276:633-634.
6. Bloemberg, G. V., Thomas-Oates, J. E., Lugtenberg, B. J. J., and Spaink, H. P. 1994. Nodulation protein NodL of Rhizobium leguminosarum O-acetylates lipo-oligosaccharides, chitin fragments and N-acetylglucosamine in vitro. Mol. Microbiol. 11:793-804.
7. Bolivar, F., Rodriguez, R., Greene, P. J., Betlach, M., Heyneker, H. L., Boyer, H. W., Crosa, J., and Falkow, S. 1977. Construction and characterisation of new cloning vehicles. II. A multipurpose cloning system. Gene 2:95-113.
8. Boyer, H. W., and Roulland-Dussoix, D. 1969. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J. Mol. Biol. 41:459-472.
9. Bulawa, C. E., and Wasco, W. 1991 Chitin and nodulation. Nature 353:710
10. Chua K.-Y., Pankhurst, C. E., Macdonald, P. E., Hopcroft, D. H., Jarvis, B. D. W., and Scott, D. B. 1985. Isolation and characterisation of Tn5-induced symbiotic mutants of Rhizobium loti. J. Bacteriol. 162:335-343.
11. Clark, C. A., Beltrame, J., and Manning P. A. 1991. The oac gene encoding a lipopolysaccharide O-antigen acetylase maps adjacent to the integrase-encoding gene on the genome of Shigella flexneri bacteriophage Sf6. Gene 107:43-52.
12. Collins-Emerson, J. M., Terzaghi, E. A., and Scott, D. B. 1990. Nucleotide sequence of Rhizobium loti nodC. Nucleic Acids Res. 18:6690.
13. Davis, E. O., Evans, I. J., and Johnston, A. W. B. 1988. Identification of nodX, a gene that allows Rhizobium leguminosarum biovar viciae strain TOM to nodulate Afghanistan peas. Mol. Gen. Genet. 212:531-535.
14. Davis, E. O., and Johnston, A. W. B. 1990. Analysis of three nodD genes in Rhizobium leguminosarum biovar phaseoli; nodD1 is preceded by nolE, a gene whose product is secreted from the cytoplasm. Mol. Microbiol. 4:921-932.
15. de Bruijn, F. J., and Lupski, J. R. 1984. The use of transposon Tn5 mutagenesis in the rapid generation of correlated physical and genetic maps of DNA segments cloned into multicopy plasmids - a review. Gene 27:131-149.
16. Devereux, J., Haeberli, P., and Smithies, O. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12: 387-395.
17. Ditta, G., Stanfield, S., Corbin, D., and Helinski, D. R. 1980. Broad host range DNA cloning system for Gram negative bacteria: Construction of a gene bank of Rhizobium meliloti. Proc. Natl. Acad. Sci. USA 77: 7347-7351.
18. Dixon, R., Cannon, F., and Kondorosi, A. 1976. Construction of a P plasmid carrying nitrogen fixation genes from Klebsiella pneumoniae. Nature 260:268-271.
19. Djordjevic, M. A., Schofield, P. R., and Rolfe, B. G. 1985. Tn5 mutagenesis of Rhizobium trifolii host-specific nodulation genes result in mutants with altered host-range ability. Mol. Gen. Genet. 200: 463-471.
20. Downie, J. A. 1994. Signalling strategies for nodulation of legumes by rhizobia. Trends Microbiol. 2:318-324.
21. Egelhoff, T. T., Fisher, R. F., Jacobs, T. W., Mulligan, J. T., and Long, S. R. 1985. Nucleotide sequence of Rhizobium meliloti 1021 nodulation genes: nodD is read divergently from nodABC. DNA 4:241-248.
22. 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.
23. Firmin, J. L., Wilson, K. E., Carlson, R. W., Davies, A. E., and Downie, J. A. 1993. Resistance to nodulation of cv. Afghanistan peas is overcome by nodX, which mediates an O-acetylation of the Rhizobium leguminosarum lipo-oligosaccharide nodulation factor. Mol. Microbiol. 10:351-360.
24. Firmin, J. L., Wilson, K. E., Rossen, L., and Johnston, A. W. B. 1986. Flavonoid activation of nodulation genes in Rhizobium reversed by other compounds present in plants. Nature 324:90-92.
25. Fisher, R. F., Egelhoff, T. T., Mulligan, J. T., and Long, S. R. 1988. Specific binding of proteins from Rhizobium meliloti cell-free extracts containing NodD to DNA sequences upstream of inducible nodulation genes. Genes & Dev. 2:282-293.
26. Friedman, A. M., Long, S. R., Brown, S. E., Buikema, W. J., and Ausubel, F. M. 1982. Construction of a broad host range cosmid cloning vector and its use in the genetic analysis of Rhizobium mutants. Gene 18:298-296.
27. Goethals, K., Van Montagu, M., and Holsters, M. 1992. Conserved motifs in a divergent nod box of Azorhizobium caulinodans ORS571 reveal a common structure in promoters regulated by LysR-type proteins. Proc. Natl. Acad. Sci. USA 89:1646-1650.
28. Göttfert, M., Horvath, B., Kondorosi, E., Putnoky, P., Rodriguez-Quinones, R., and Kondorosi, A. 1986. At least two nodD genes are necessary for efficient nodulation on alfalfa by Rhizobium meliloti. J. Mol. Biol. 191:411-420
29. Göttfert, M., Lamb, J. W., Gasser, R., Semenza, J., and Hennecke, H. 1989. Mutational analysis of the Bradyrhizobium japonicum common nod genes and further nod box-linked genomic DNA regions. Mol. Gen. Genet. 215:407-415.
30. Györgypal, Z., Iyer, N., and Kondorosi, A. 1988, Three regulatory nodD alleles of diverged flavonoid-specificity are involved in host-dependent nodulation by Rhizobium meliloti. Mol. Gen. Genet. 212:85-92.
31. Györgypal, Z., Kondorosi, E., and Kondorosi, A. 1991. Diverse signal sensitivity of NodD protein homologs from narrow and broad host range rhizobia. Mol. Plant-Microbe Interact. 4:356-364.
32. Handberg, K., and Stougaard, J. 1992. Lotus japonicus an autogamous, diploid legume species for classical and molecular genetics. Plant J. 2:487-496.
33. Henikoff, S., Haughn, G. W., Calvo, J. M., and Wallace, J. C. 1988. A large family of bacterial activator proteins. Proc. Natl. Acad. Sci. USA 85:6602-6606.
34. Hong, G.-F., Burn, J. E., and Johnston, A. W. B. 1987. Evidence that DNA involved in the expression of nodulation (nod) genes in Rhizobium binds to the product of the regulatory gene nodD. Nucleic Acids Res. 15:9677-9691.
35. Honma, M. A., and Ausubel, F. M. 1987. Rhizobium meliloti has three functional copies of the nodD symbiotic regulatory gene. Proc. Natl. Acad. Sci. USA 84:8558-8562.
36. Horvath, B., Bachem, C. W. B., Schell, J., and Kondorosi, A. 1987. Host-specific regulation of nodulation genes in Rhizobium is mediated by a plant-signal, interacting with the nodD gene product. EMBO J. 6: 841-848.
37. Innes, R. W., Kuempel, P. L., Plazinski, J., Canter-Cremers, H., Rolfe, B. G., and Djordjevic, M. A. 1985. Plant factors induce expression of nodulation and host-range genes in Rhizobium trifolii. Mol. Gen. Genet. 201:426-432.
38. 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.
39. 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.
40. Jones, W. T., MacDonald, P. E., Jones, S. D., and Pankhurst, C. E. 1987. Peptidoglycan-bound polysaccharide associated with resistance of Rhizobium loti strain NZP2037 to Lotus pedunculatus root flavolan. J. Gen. Microbiol. 133:2617-2629.
41. Kosslak, R. M., Bookland, R., Barkei, J., Paaren, H. E., and Appelbaum, E. R. 1987. Induction of Bradyrhizobium japonicum common nod genes by isoflavones isolated from Glycine max. Proc. Natl. Acad. Sci. USA 84:7428-7432.
42. Leong, S. A., Ditta, G. S., and Helinski, D. R. 1982. Heme biosynthesis in Rhizobium. Identification of a cloned gene coding for δ-aminolevulinic acid synthesis from Rhizobium meliloti. J. Biol. Chem. 257: 8724-8730.
43. Lerouge, P., Roche, P., Faucher, C., Maillet, F., Truchet, G., Promé, J. C., and Dénarié, J. 1990. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glycosamine oligosaccharide signal. Nature 344:781-784.
44. Long, S. R. 1989. Rhizobium-legume nodulation: Life together in the underground. Cell 56:203-214.
45. - mutants. Nature 298:485-488.
46. López-Lara, I. M., van den Berg J. D. J., Thomas-Oates, J. E., Glushka, J., Lugtenberg, B. J. J., and Spaink, H. P. 1995. Structural identification of the lipo-chitin oligosaccharide nodulation signals of Rhizobium loti. Mol. Microbiol. 15:627-638.
47. McKay, I. A., and Djordjevic, M. A. 1993. Production and excretion of Nod metabolites by Rhizobium leguminosarum bv. trifolii are disrupted by the same environmental factors that reduce nodulation in the field. Appl. Environ. Microbiol. 59:3385-3392.
48. Mergaert, P., van Montagu, M., Promé, J.-C. and Holsters, M. 1993. Three unusual modifications, a D-arabinosyl, an N-methyl, and a carbamoyl group, are present on the Nod factors of Azorhizobium caulinodans strain ORS571. Proc. Natl. Acad. Sci. USA 90:1551-1555.
49. Miller, J. M., ed. 1972. Experiments in Molecular Genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
50. Mulligan, J. T., and Long, S. R. 1985. Induction of Rhizobium meliloti nodC expression by plant exudate requires nodD. Proc. Natl. Acad. Sci USA 82:6609-6613.
51. Norrander, J., Kempe, T., and Messing, J. 1983. Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene 26:101-106.
52. Pankhurst, C. E., Craig, A. S., and Jones, W. T. 1979. Effectiveness of Lotus root nodules. I. Morphology and flavolan content of nodules formed on Lotus pedunculatus by fast-growing Lotus rhizobia. J. Exp. Bot. 30:1085-1093.
53. Pankhurst, C. E., Hopcroft, D. H., and Jones, W. T. 1987. Comparative morphology and flavolan content of Rhizobium loti induced effective and ineffective root nodules on Lotus species, Leuceana leucocephala, Carmichaelia flagelliformis, Ornithopus sativus, and Clianthus puniceus. Can. J. Bot. 65:2676-2685.
54. Peters, K. N., Frost, J. W., and Long, S. R. 1986. A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233:977-980.
55. Poupot, R., Martinez-Romero, E., and Promé, J.-C. 1993. Nodulation factors from Rhizobium tropici are sulfated or nonsulfated chitopentasaccharides containing an N-methyl-N-acylglucosaminyl terminus. Biochemistry 32:10430-10435.
56. Price, N. P. J., Relic, B., Talmont., F., Lewin, A., Promé, D., Pueppke, S. G., Maillet, E., Dénarié, J., Promé, J.-C. and Broughton, W. J. 1992. Broad-host-range Rhizobium species strain NGR234 secretes a family of carbamoylated, and fucosylated, nodulation signals that are O-acetylated or sulphated. Mol. Microbiol. 6:3575-3584.
57. Redmond, J. W., Batley, M., Djordjevic, M. A., Innes, R. W., Kuempel, P. L., and Rolfe, B. G. 1986. Flavones induce expression of nodulation genes in Rhizobium. Nature 323:632-635.
58. Roche, P., Debellé, F, Maillet, F., Lerouge, P., Faucher, C., Truchet, G., Dénarié, J., and Promé, J.-C. 1991. Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals. Cell 67:1131-1143.
59. Röhrig, H., Schmidt, J., Wieneke, U., Kondorosi, E., Barlier, I., Schell, J., and John, M. 1994. Biosynthesis of lipooligosaccharide nodulation factors: Rhizobium NodA protein is involved in N-acylation of the chitooligosaccharide backbone Proc. Natl. Acad. Sci. USA 91:3122-3126.
60. 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 nodA, B, C genes. EMBO J. 4:3369-3373.
61. Rostas, K., Kondorosi, E., Horvath, B., Simoncsits, A., and Kondorosi, A. 1986. Conservation of extended promoter regions of nodulation genes in Rhizobium. Proc. Natl. Acad. Sci. USA 83:1757-1761.
62. Ruvkun, G. B., and Ausubel, F. M. 1981. A general method for site-directed mutagenesis in prokaryotes. Nature 289:85-88.
63. Schofield, P. R., Djordevic, M. A., Rolfe, B. G., Shine, J., and Watson, J. M. 1983. A molecular linkage map of nitrogenase and nodulation genes in Rhizobium trifolii. Mol. Gen. Genet. 192:459-465.
64. 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. Nucleic Acids Res. 14: 2891-2903.
65. Schultze, M., Quiclet-Sire, B., Kondorosi, E., Virelizier, H., Glushka, J. N., Endre, G., Géro, S. D., and Kondorosi, A. 1992. Rhizobium meliloti produces a family of sulfated lipooligosaccharides exhibiting different degrees of plant host specificity Proc. Natl. Acad. Sci. USA 89: 192-196.
66. Schwedock, J., and Long, S. R. 1990. ATP sulphurylase activity of the nodP and nodQ gene products of Rhizobium meliloti. Nature 348:644-647.
67. Scott, D. B., Chua, K.-Y., Jarvis, B. D. W., and Pankhurst, C. E. 1985. Molecular cloning of a nodulation gene from fast- and slow-growing strains of Lotus rhizobia. Mol. Gen. Genet. 201:43-50.
68. Scott, D. B., and Ronson, C. W. 1982. Identification and mobilisation by cointegrate formation of a nodulation plasmid in Rhizobium trifolii. J. Bacteriol. 151:36-43.
69. Scott, K. F., Hughes, J. E., Gresshoff, P. M., Beringer, J. E., Rolfe, B. G., and Shine, J. 1982. Molecular cloning of Rhizobium trifolii genes involved in symbiotic nitrogen fixation. J. Mol. Appl. Genet. 1:315-326.
70. Segovia, L., Young, J. P. W., and Martínez-Romero, E. 1993. Reclassification of American Rhizobium leguminosarum biovar phaseoli Type I strains as Rhizobium etli sp. nov. Int. J. Syst. Bacteriol. 43:374-377.
71. Spaink, H. P., Sheeley, D. M., van Brussel, A. A. N., Glushka, J., 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 moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature 354:125-130.
72. Spaink, H. P., Wijffelman, C. A., Pees, E., Okker, R. J. H., and Lugtenberg, B. J. J. 1987. Rhizobium nodulation gene nodD as a determinant of host specificity. Nature 328:337-340.
73. Stacey, G., Luka, S., Sanjuan, J., Banfalvi, Z., Nieuwkoop, A. J., Chun, J. Y., Forsberg, L. S., and Carlson, R. 1994. NodZ, a unique host-specific nodulation gene, is involved in the fucosylation of the lipooligosaccharide nodulation signal of Bradyrhizobium japonicum. J. Bacteriol. 176:620-633.
74. Truchet, G., Roche, P., Lerouge, P., Vasse, J., Camut, S., de Billy, F., Promé, J.-C., and Dénarié, J. 1991. Sulphated lipo-oligosaccharide signals of Rhizobium meliloti elicit root nodule organogenesis in alfalfa. Nature 351:670-673.
75. 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.
76. Vieira, J., and Messing, J. 1987. Production of single-stranded plasmid DNA. Methods Enzymol. 153:3-11.
77. Vincent, J. M. 1970. A Manual for the Practical Study of the Root-Nodule Bacteria. Blackwell Scientific Publications, Oxford.
78. Wang, L., Romana, L. K., and Reeves, P R. 1992. Molecular analysis of a Salmonella enterica Group E1 rfb gene cluster: O antigen and the genetic basis of the major polymorphism. Genetics 130:429-443.
79. Ward, L. J. H., Rockman, E. S., Ball, P., Jarvis, B. D. W., and Scott, D. B. 1989. Isolation and characterization of a Rhizobium loti gene required for effective nodulation of Lotus pedunculatus. Mol. Plant-Microbe Interact. 2:224-232.
80. Yanisch-Perron, C., Vieira, J., and Messing, J. 1985. Improved M13 phage cloning vectors and host strains: Nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119.
81. Young, C., Collins-Emerson, J. M., Terzaghi, E. A., and Scott, D. B. 1990. Nucleotide sequence of Rhizobium loti nodI. Nucleic Acids Res. 10:6691.
82. Young, J. P. W., and Johnston A. W. B. 1989. The evolution of specificity in the legume-Rhizobium symbiosis. Trends Ecol. & Evol. 4:341-349.