Characterization of Rhizobium tropici CIAT899 nodulation factors: The role of nodH and nodPQ genes in their sulfation

Molecular Plant-Microbe Interactions

Volumn 9, Issue 3, 1996, Pages 151-163

  Folch Mallol, Jorge L ^a,b   Marroquí, Silvia ^a   Sousa, Carolina ^a   Manyani, Hamid ^a   López Lara, Isabel M ^d   Van Der Drift, Koen M G M ^c   Haverkamp, Johan ^c   Quinto, Carmen ^b   Gil Serrano, Antonio ^a   Thomas Oates, Jane ^c   Spaink, Herman P ^d   Megías, Manuel ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

^b INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

^c UTRECHT UNIVERSITY   (Netherlands)

^d LEIDEN UNIVERSITY   (Netherlands)

Author keywords

LCOs; Mass spectrometry; nodHPQ; Sulfation

Indexed keywords

BACTERIAL PROTEIN; MULTIENZYME COMPLEX; NODH PROTEIN, SINORHIZOBIUM MELILOTI; NODP PROTEIN, RHIZOBIUM; NODULATION PROTEIN Q, RHIZOBIUM; OLIGOSACCHARIDE; SULFATE; SULFATE ADENYLYLTRANSFERASE; SULFOTRANSFERASE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; CHEMICAL STRUCTURE; CHEMISTRY; CHROMOSOME MAP; COMPARATIVE STUDY; GENETICS; LEGUME; MEDICINAL PLANT; MICROBIOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; MUTATION; NITROGEN FIXATION; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHENOTYPE; RHIZOBIUM; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CHROMOSOME MAPPING; CLONING, MOLECULAR; FABACEAE; GENES, BACTERIAL; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; MULTIENZYME COMPLEXES; MUTATION; NITROGEN FIXATION; OLIGOSACCHARIDES; OPEN READING FRAMES; PHENOTYPE; PLANTS, MEDICINAL; RHIZOBIUM; SEQUENCE HOMOLOGY, AMINO ACID; SULFATE ADENYLYLTRANSFERASE; SULFATES; SULFOTRANSFERASES;

BACTERIA (MICROORGANISMS); LEUCAENA; RHIZOBIUM; RHIZOBIUM TROPICI;

EID: 0030131172     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/mpmi-9-0151     Document Type: Article

References (50)

1. Beringer, J. E. 1974. R-factor transfer in Rhizobium leguminosarum. J. Gen. Microbiol. 120:421-429.
2. Boyer, H. S., and Roulland-Dussoix, D. 1969. A complementation analysis of the restriction and modification of DNA in E. coli. J. Mol. Biol. 41:459-472.
3. 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.
4. Cervantes, E., Sharma, S. B., Maillet, F., Vasse, J., Truchet, G., and Rosenberg, C. 1989. The Rhizobium meliloti host range nodQ gene encodes a protein which shares homology with translation elongation and initiation factors. Mol. Microbiol. 3:745-755.
5. Debellé, F., and Sharma, S. B. 1986. Nucleotide sequence of Rhizobium meliloti RCR2011 genes involved in host specificity of nodulation. Nucleic Acids Res. 14:7453-7472.
6. Dénarié, J., and Cullimore, J. 1993. Lipo-oligosaccharide Nodulation factors: Minireview. A new class of signalling molecules mediating recognition and morphogenesis. Cell 74:951-954.
7. Devereux, J., Haeberli, P., and Smithies, O. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12:387-395.
8. Ditta, G. S. 1986. Tn5 mapping of Rhizobium nitrogen fixation genes. Methods Enzymol. 118:519-528.
9. Geelen D., Mergaert, P., Geremia, R. A., Goormachtig, S., Van Montagu, M., and Holsters, M. 1993. Identification of nodSUIJ in Nod locus I of Azorhizobium caulinodans: Evidence that nodS encodes a methyl-transferase involved in Nod factor modification. Mol. Microbiol. 9:145-154.
10. Henikoff, S. 1987. Unidirectional digestion with exonuclease III in DNA sequence analysis. Methods. Enzymol. 155:156-165.
11. Horvath, B., Kondorosi, E., John, M., Schmidt, J., Törok, I., Barabas, I., Wieneke, U., Schell, J., and Kondorosi, A. 1986. Organization, structure and symbiotic function of Rhizobium meliloti nodulation genes determining host specificity for alfalfa. Cell 46:335-343.
12. Kondorosi, A., Kondorosi E., Pankhurst, C. E., Broughton, W. J., and Banfalvi, Z. 1982. Mobilization of a Rhizobium meliloti megaplasmid carrying nodulation and nitrogen fixation genes into other rhizobia and Agrobacterium. Mol. & Gen. Genet. 188:433-439.
13. Kozac, M. 1983. Comparison of initiation of protein synthesis in procaryotes, eucaryotes and organelles. Microbiol. Rev. 47:1-45.
14. Kyte, J., and Doolittle, R. F. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
15. Lerouge, P., Roche, P., Faucher, C., Maillet, F., Truchet, G., Promé, J.-C., and Dénarié, J. 1990. Symbiotic host specificity of R. meliloti is determined by a sulphated and acylated glucosamine oligo-saccharide signal. Nature 344:781-784.
16. Leyh, T. S., Suo, Y., and Vogt, T. F. 1992. The DNA sequence of the sulfate activation locus from Escherichia coli K-12. J. Biol. Chem. 267:10405-10410.
17. Maniatis, T. A., Fritsch, E. F., and Sambrook, J. 1982. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
18. Martínez, E., Pardo, M. A., Palacios, R., and Ceballos, M. A. 1985. Reiteration of nitrogen fixation gene sequences and specificity of Rhizobium in nodulation and nitrogen fixation in Phaseolus vulgaris. J. Gen. Microbiol. 131:1779-1786.
19. Martínez, E., Poupot, R., Promé, J.-C., Pardo, M. A., Segovia, L., Truchet, G., and Dénarié, J. 1993. Chemical signalling of Rhizobium nodulating bean. Pages 171-175 in: New Horizons in Nitrogen Fixation. R. Palacios, J. Mora, and W. E. Newton, eds. Kluwer Academic Publishers, Dordrecht, The Netherlands.
20. Martínez, E., Poupot, R., Rogel, M. A., Laeremans, T., Vanderleyden, J., and Hernández-Lucas, I. 1994. Sulfated Nod metabolites from Rhizobium species. IS MPMI, 7th, Edinburgh.
21. Martínez, E., Segovia, L., Martin-Mercante, F., Franco, A. A., Graham, P., and Pardo, M. A. 1991. Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. Int. J. Syst. Bacteriol. 41:417-426.
22. Megías, M., Folch, J. L., and Sousa, C. 1993. Control of the expression of bacterial genes involved in symbiotic nitrogen fixation. World J. Microbiol. Biotechnol. 9:444-454.
23. Miller, J. H. 1972. Experiments in Molecular Genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
24. Petersen, G. B., Stockwell, P. A., and Hill, D. F. 1988. Messenger RNA recognition in E. coli: A possible second site of interaction with 16S ribosomal RNA. EMBO J. 7:3957-3962.
25. Poupot, R., Martinez, E., and Promé, J.-C. 1993. Nodulation factors from R. tropici CIAT899 are sulfated or nonsulfated chitopentasaccharides containing a N-methyl-N-acyl glucosaminyl terminus. Biochemistry 32:10430-10435.
26. Prentki, P., and Krisch, H. M. 1984. In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29:303-313.
27. Price, N. P. J., Relic, B., Talmont, F., Lewin, A., Promé, D., Pueppke, S. G., Maillet, F., Dénarié, J., Promé, J.-C., and Broughton, W. J. 1992. Broad-host-range Rhizobium species strain NGR234 secretes a family of carbamoylated, and fucosilated, nodulation signals that are O-acetylated or sulphated. Mol. Microbiol. 6:3575-3584.
28. Putnoky, P., and Kondorosi, A. 1986. Two gene clusters of Rhizobium meliloti code for early essential nodulation function and a third influences nodulation efficiency. J. Bacteriol. 169:102-106.
29. Quandt, J., and Hynes, M. F. 1993. Versatile suicide vectors which allow direct selection for gene replacement in Gram-negative bacteria. Gene 127:15-21.
30. 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.
31. Ruvkun, G. B., and Ausubel, F. M. 1981. A general method for site directed mutagenesis in procaryotes. Nature 289:85-88.
32. Sanger, F., Nicklen, S., and Coulson, A. R. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
33. Schultze, M., Staehelin, C., Röhrig, H., John, M., Schmidt, J., Kondorosi, E., Schell, J., and Kondorosi, A. 1995. In vitro sulfotransferase activity of Rhizobium meliloti NodH protein: Lipochitooligosaccharide nodulation signals are sulfated after synthesis of the core structure. Proc. Natl. Acad. Sci. USA 92:2706-2709.
34. Schwedock, J., and Long, S. R. 1989. Nucleotide sequence and protein products of two new nodulation genes in Rhizobium meliloti, nodP and nodQ. Mol. Plant-Microbe Interact. 2:181-194.
35. 1 shows nucleotide sequence similarity to an Agrobacterium tumefaciens insertion sequence. Mol. Plant-Microbe Interact. 7:151-153.
36. Schwedock, J. S., Liu, C., Leyh, T. S., and Long, S. R. 1994. Rhizobium meliloti NodP and NodQ form a multifunctional sulfate-activating complex requiring GTP for activity. J. Bacteriol. 176:7055-7064.
37. Schwedock, J. S., and Long, S. R. 1990. ATP sulphurylase activity of the nodP and nodQ gene products of Rhizobium meliloti. Nature 348:644-647.
38. Schwedock, J. S., and Long, S. R. 1992. Rhizobium meliloti genes involved in sulfate activation: the two copies of nodPQ and a new locus, saa. Genetics 132:899-909.
39. Shine, J., and Dalgarno, L. 1974. The 3′-terminal sequence of Escherichia coli 16S ribosomal RNA: Complementarity to nonsense triplets and ribosome binding sites. Proc. Natl. Acad. Sci. USA 71: 1342-1346.
40. Simon, R., Priefer, U., and Pühler, A. 1983. A broad host range mobilization system for in vivo genetic engineering: Transposon mutagenesis in gram negative bacteria. Bio/Technology 1:784-791.
41. Sousa, C., Folch, J. L., Boloix, P., Megías, M., Nava, N., and Quinto, C. 1993. A Rhizobium tropici DNA region carrying the amino-terminal half of a nodD gene and a nod-box like sequence confers host range extension. Mol. Microbiol. 9:1157-1168.
42. Spaink, H. P., Aarts, A., Stacey, G., Bloemberg, G. V., Lugtenberg, B. J. J., and Kennedy, E. P. 1992. Detection and separation of Rhizobium and Bradyrhizobium Nod metabolites using thin-layer chromatography. Mol. Plant-Microbe Interact. 5:72-80.
43. Spaink, H. P., Bloemberg, G. V., van Brussel, A. A. N., Lugtenberg, B. J. J., van der Drift, K. M. G. M., Haverkamp, J., and Thomas-Oates, J. E. 1995. Host specificity of Rhizobium leguminosarum is determined by the hydrophobicity of highly unsaturated fatty acyl moieties of the nodulation factors. Mol. Plant-Microbe Interact. 8:155-164.
44. Spaink, H. P., and Lugtenberg, B. J. J. 1994. Role of rhizobial lipo-chitin oligosaccharide signal molecules in root nodule organogenesis. Plant Mol. Biol. 26:1413-1422.
45. Spaink, H. P., Okker, R. J. H., Wijffelmann, C. A., Tak, T., Goosen de Roo, L., Pees, E., van Brussel, A. A. N., and Lugtenberg, B. J. J. 1989. Symbiotic properties of Rhizobia containing a flavonoid independent hybrid NodD product. J. Bacteriol. 171:4045-4053.
46. 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.
47. Tola, E., Giacomini, A., Ollero, F. J., Squartini, A., and Nuti, M. P. 1994. Rhizobium "hedysari," host-specific symbiont of Hedysarum coronarium, carries a gene highly homologous to nodH of Rhizobium meliloti. IS MPMI, 7th, Edinburgh.
48. Vargas, C., Martinez, L. J., Megías, M., and Quinto, C. 1990. Identification and cloning of nodulation genes and host specificity determinants of the broad host range Rhizobium leguminosarum bv. phaseoli strain CIAT899. Mol. Microbiol. 4:1899-1910.
49. Vieille, C., and Elmerich, C. 1990. Characterization of two Azospirillum brasilense Sp7 plasmid genes homologous to Rhizobium meliloti nodPQ. Mol. Plant-Microbe Interact. 3:389-400.
50. Yanisch-Perron, C., Vieira, J., and Messing, J. 1985. Improved M13phage cloning vectors and hosts strains: nucleotide sequence of the M13mp18 and pUC19 vectors. Gene 33:103-119.