Isolation and characterization of the Rhizobium tropici nod factor sulfation genes

Molecular Plant-Microbe Interactions

Volumn 9, Issue 6, 1996, Pages 492-500

  Laeremans, T ^a,b   Caluwaerts, I ^b   Verreth, C ^b   Rogel, M A ^a   Vanderleyden, J ^b   Martinez Romero E ^a  

^a INSTITUTO DE CIENCIAS FÍSICAS   (Mexico)

^b F A Janssens Lab of Genetics   (Belgium)

Author keywords

APS kinase; ATP sulfurylase; nod genes

Indexed keywords

BACTERIA (MICROORGANISMS); PHASEOLUS (ANGIOSPERM); PHASEOLUS VULGARIS; RHIZOBIUM TROPICI;

EID: 0030220684     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-9-0492     Document Type: Article

References (64)

1. Barrios, H., Fischer, H.-M., Hennecke, H., and Morett, E. 1995. Over-lapping promoters for two different RNA polymerase holoenzymes control Bradyrhizobium japonicum nifA expression. J. Bacteriol. 177: 1760-1765.
2. Beringer, J. E. 1974. R-factor in Rhizobium leguminosarum. J. Gen. Microbiol. 120:421-429.
3. Bono, J.-J., Riond, J., Nicolaou, K. C., Bockovich, N. J., Estevez, V. A., Cullimore, J. V., and Ranjeva, R. 1995. Characterization of a binding site for chemically synthesized lipo-oligosaccharidic NodRm factors in particulate fractions prepared from roots. Plant J. 7:253-260
4. 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.
5. Carlson, R W., Sanjuan, J., Bhat, U. R., Glushka, J., Spaink, H. P., Wijfjes, A. H. M , van Brussel, A. A. N., Stokkermans, T. J. W., Peters, N. K., and Stacey, G. 1993. The structures and biological activities of the lipo-oligosaccharide nodulation signals produced by type I and II strains of Bradyhizobium japonicum. J. Biol. Chem. 268: 18372-18381.
6. 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.
7. Debellé, F., Rosenberg, C , Vasse, J., Maillet, F., Martínez, E., Dénarié, J., and Truchet, G. 1986. Assignment of symbiotic developmental phenotypes to common and specific nodulation (nod) genetic loci of Rhizobium meliloti. J. Bacteriol. 168:1075-1086.
8. 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.
9. Dénarié, J., and Cullimore, J. 1993. Lipo-oligosaccharide nodulation factors: A minireview. New class of signaling molecules mediating recognition and morphogenesis. Cell 74:951-954.
10. Dever, E. T., Glynias, M. J., and Merrick, W. C. 1987. GTP-binding domain: Three consensus sequence elements with distinct spacing. Proc. Natl. Acad. Sci. USA 84:1814-1818.
11. Ehrhardt, D. W., Atkinson, E. M., Faull, K. F., Freedberg, D. I., Sutherlin, D. P., Armstrong, R., and Long, S. R. 1995. In vitro sulfotransferase activity of NodH, a nodulation protein of Rhizobium meliloti required for host-specific nodulation. J. Bacteriol. 177:6237-6245.
12. Faucher, C., Maillet, F., Vasse, J., Rosenberg, C., van Brussel, A. A. N., Truchet, G., and Dénarié, J. 1988. Rhizobium meliloti host range nodH gene determines production of an alfalfa-specific extracellular signal J. Bacteriol. 170:5489-5499.
13. Felle, H. H., Kondorosi, E., Kondorosi, A., and Schultze, M. 1995. Nod signal-induced plasma membrane potential changes in alfalfa root hairs are differentially sensitive to structural modifications of the lipochitooligosaccharide. Plant J. 7:939-947.
14. Figurski, D H., and Helinski, D. R. 1979. Replication of an origin-containing derivative of RK2 dependent on a plasmid function provided in trans. Proc Natl. Acad Sci. USA 76:1648-1652.
15. Fisher, R. F., and Long, S. R. 1992. Rhizobium-plant signal exchange. Nature 357:655-660.
16. Geelen, D., Mergaert, P., Geremia, R. A., Goormachtig, S., Van Montagu, M , and Holsters, M 1993. Identification of nodSUIJ genes in Nod locus 1 of Azorhizobium caulinodans: Evidence that nodS encodes a methyltransferase involved in Nod factor modification. Mol. Microbiol. 9:145-154.
17. Géniaux, E., Flores, M., Palacios, R., and Martínez, E. 1995. Presence of megaplasmids in Rhizobium tropici and further evidence of differences between the two R. tropici subtypes Int. J. Syst. Microbiol. 45:392-394.
18. Horvath, B., Kondorosi, E., John, M., Schmidt, J., Torok, I., Györgypal, Z., 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
19. Hirsch, A. M. 1992. Tansley Review No. 40, Developmental biology of legume nodulation. New Phytol. 122:211-237.
20. Jones, D. Y., and Sneath, P. H. A. 1970. Genetic transfer and bacterial taxonomy. Bactenol. Rev. 34.40-81.
21. 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 glucosamine oligosaccharide signal. Nature 344:781-784.
22. Leyh, T. S., Taylor, J. C., and Markham, G. D. 1988. The sulfate activation locus of Escherichia coli K12: Cloning, genetic, and enzymatic characterization. J. Biol. Chem. 263:2409-2416.
23. Marsh, J. L., Erfle, M., and Wykes, E. J 1984. The plC plasmid and phage vectors with versatile cloning sites for recombinant selection by insertional inactivation. Gene 32:481-485
24. Martínez, E., Laeremans, T., Poupot, R , Rogel, M. A., López, L., García, F., Vanderleyden, J., Promé, J. C., and Lara, F. 1995. Nod metabolites and other compounds excreted by Rhizobium spp. Pages 281-286 in: Nitrogen Fixation: Fundamentals and Applications. I. A. Tikhonovich, N. A. Provorov, V. I. Romanov, and W. E Newton, eds. Kluwer Academic Pub , Dordrecht, The Netherlands.
25. Martínez, E., Pardo, M. A., Palacios, R., and Cevallos, 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.
26. Martínez, E., Romero, D., and Palacios, R. 1990. The Rhizobium genome. Plant Sci. 9:59-93.
27. Martínez-Romero, E. 1994. Recent developments in Rhizobium taxonomy. Plant Soil 161:11-20.
28. Martínez-Romero, E., Segóvia, L., Mercante, F. M., Franco, A. A., Graham, P., and Pardo, M. A 1991. Rhizobium tropict, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. Int. J. Syst. Bacteriol. 41:417-426.
29. Norrander, J., Kempe T., and Messing, J. 1983. Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene 26:101-106.
30. Ogawa, J., Brierley, H. L., and Long, S. R. 1991. Analysis of Rhizobium meliloti nodulation mutant WL131: Novel insertion sequence ISRm3 in nodG and altered nodH protein product. J. Bacteriol. 173:3060-3065.
31. Pardo, M. A., Lagunez, J., Miranda, J , and Martínez, E. 1994. Nodulating ability of Rhizobium tropici is conditioned by a plasmid-encoded citrate synthase. Mol. Microbiol. 11:315-321.
32. Peters, N. K., Frost, J. W., and Long, S. R. 1986. A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233:977-980.
33. Petersen, G. B., Stockwell, P. A., and Hill, D. F. 1988. Messenger RNA recognition in Escherichia coli: A possible second site of interaction with 16S ribosomal RNA. EMBO J. 7:3957-3962.
34. Poupot, R., Martínez-Romero, E., Gautier, N., and Promé, J.-C. 1995a. Wild type Rhizobium etli, a bean symbiont, produces acetyl-fucosylated, N-Methylated, and carbamoylated nodulation factors. J. Biol. Chem. 270:6050-6055.
35. Poupot, R., Martínez-Romero, E., Maillet, F., and Promé, J.-C. 1995b. Rhizobium tropici nodulation factor sulfation is limited by the quantity of activated form of sulfate. FEBS Lett. 368:536-540.
36. Poupot, R., Martínez-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.
37. 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 fucosylated, nodulation signals that are O-acetylated or sulphated. Mol. Microbiol. 6:3575-3584.
38. 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.
39. 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.
40. 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
41. Sanjuan, J , Carlson, R. W., Spaink, H. P., Bhat, U. R., Barbour, W. M , Glushka, J., and Stacey, G. 1992. A 2-O-methylfucose moiety is present in the lipo-oligosaccharide nodulation signal of Bradyrhizobium japonicum. Proc. Natl. Acad. Sci. USA 89:8789-8793.
42. Sambrook, J., Fritsch, E. F., and Maniatis, T. A. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
43. Satishchandran, C., Hickman, Y. N., and Markham, G. D. 1992. Characterization of the phosphorylated enzyme intermediate formed in the adenosine 5′-phosphosulfate kinase reaction. Biochemistry 31:11684-11688.
44. Schultze, M., Kondorosi, E., and Kondorosi, A. 1993. The sulfate group on the reducing end protects Nod signals of Rhizobium meliloti against hydrolysis by medicago chitinases. Pages 159-164 in: New Horizons in Nitrogen Fixation. R. Palacios, J. Mora, and W. E. Newton, eds. Kluwer Academic Pub., Dordrecht, The Netherlands.
45. Schultze, M., Kondorosi, E., Ratet, P., Buiré, M., and Kondorosi, A. 1994. Cell and molecular biology of Rhizobium-plant interactions. Int. Rev. Cytol. 156:1-75.
46. Schultze, M , Staehelin, C., Rohrig, 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.
47. 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.
48. Schwedock, J , and Long, S. R. 1989. Nucleotide sequence and protein products of two new nodulation genes of Rhizobium meliloti, nodP and nodQ. Mol. Plant-Microbe Interact. 2:181-194.
49. Schwedock, J., and Long, S. R. 1990. ATP sulphurylase activity of the nodP and nodQ gene products of Rhizobium meliloti. Nature 348.644-647.
50. 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.
51. Shibuya, N., Kaku, H., Kuchitsu, K., and Maliarik, M. J. 1993. Identification of a novel high-affinity binding site for N-acetylchitooligosaccharide elicitor in the membrane fraction from suspension-cultured rice cells FEBS Lett. 329:75-78
52. Simon, R., Priefer, U., and Pudie;hler, A. 1983. Vector plasmids for in vivo and in vitro manipulation of Gram-negative bacteria. Pages 98-106 in: Molecular Genetics of the Bacteria Plant Interaction. A. Puhler, ed. Springer Verlag, Berlin.
53. Spaink, H. P , Bloemberg, G. V , Wijfjes, A. H. M., Ritsema, T., Geiger, O., López-Lara, I. M., Harteveld, M., Kafetzopoulos, D., van Brussel, A. A. N., Kijne, J. W., Lugtenberg, B. J. J., van der Drift, K. M. G. M., Thomas-Oates, J. E., Potrykus, I., and Sautter, C. 1994. The molecular basis of host specificity in the Rhizobium leguminosarumplant interaction. Pages 91-98 in: Advances in Molecular Genetics of Plant-Microbe Interactions, vol. 3 M. J. Daniels, J. A. Downie, and A. E. Osboum, eds. Kluwer Academic Pub., Dordrecht, The Netherlands.
54. Staehelin, C., Granado, J., Müller, J., Wiemken, A., Mellor, R. B., Felix, G., Regenass, M., Broughton, W. J., and Boller, T. 1994a. Perception of Rhizobium nodulation factors by tomato cells and inactivation by root chitinases Proc. Natl. Acad. Sci. USA 91:2196-2200.
55. Staehelin, C., Schultze, M., Kondorosi, E., Mellor, R. B., Boller, T., and Kondorosi A 1994b. Structural modifications in Rhizobium meliloti Nod factors influence their stability against hydrolysis by root chitinases. Plant J. 5:319-330.
56. Staskawicz, B., Dahlbeck, D., Keen, N., and Napoli, C. 1987. Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv glycinea. J. Bacteriol. 169:5789-5794.
57. Swanson, J. A., Tu, J. K., Ogawa, J., Sanga, R., Fisher, R. F., and Long, S. R. 1987. Extended region of nodulation genes in Rhizobium meliloti 1021. I. Phenotypes of Tn5 insertion mutants. Genetics 117: 181-189.
58. Truchet, G., Debellé, F., Vasse, J., Terzaghi, B., Gamerone, A. M., Rosenberg, C., Batut, J., Maillet, F., and Dénarié, J. 1985. Identification of a Rhizobium meliloti pSym 2011 region controlling the host specificity of root hair curling and nodulation J. Bacteriol. 164:1200-1210.
59. +) bean Rhizobia as Rhizobium tropici. Appl. Environ. Microbiol. 60:554-561.
60. van Rhijn, P., and Vanderleyden, J. 1995. The Rhizobium-plant symbiosis. Microbiol. Rev. 59:124-142.
61. van Rhijn, P. J S., Feys, B., Verreth, C., and Vanderleyden, J. 1993. Multiple copies of nodD in Rhizobium tropici CIAT899 and BR816. J. Bacteriol. 175:438-447.
62. Vargas, C., Martinez, L. J., Megias, M., and Quinto, C. 1990. Identification and cloning of nodulation genes and host specificity determinants of the broad host-range Rhizobium leguminosarum biovar phaseoli strain CIAT899. Mol. Microbiol. 4:1899-1910.
63. 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.
64. Waelkens, F., Voets, T., Vlassak, K., Vanderleyden, J., and van Rhijn, P. 1995. The nodS gene of Rhizobium tropici strain CIAT899 is necessary for nodulation on Phaseolus vulgaris and on Leucaena leucocephala. Mol. Plant-Microbe Interact. 8:147-154.