Toward more productive, efficient, and competitive nitrogen-fixing symbiotic bacteria

Critical Reviews in Plant Sciences

Volumn 15, Issue 3, 1996, Pages 191-234

  Maier, Robert J ^a   Triplett, Eric W ^b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Azorhizobium; Bradyrhizobium; Electron transport; Extracellular polysaccharide synthesis; H2 oxidation; Host restricted nodulation; Hup; Hydrogenase; Nickel enzyme; Nodulation efficiency; Regulation; Rhizobium; Speed of nodulation; Trifolitoxin

Indexed keywords

AZORHIZOBIUM; BACTERIA (MICROORGANISMS); BRADYRHIZOBIUM; BRADYRHIZOBIUM JAPONICUM; FABACEAE; RHIZOBIUM; RHIZOBIUM LEGUMINOSARUM;

EID: 0000572550     PISSN: 07352689     EISSN: None     Source Type: Journal    
DOI: 10.1080/07352689609701941     Document Type: Article

References (211)

1. Ackrell, B. A. C., Johnson, M. K., Gunsalus, R. P., and Cecchini, G., 1992. Structure and function of succinate dehydrogenase and fumarate reductase. In: Chemistry and Biochemistry of Flavoenzymes, Vol. III. pp. 229-297. Muller, F., Ed., CRC Press, Ann Arbor.
2. Albracht, S. P. J., 1994. Nickel hydrogenases: in search of the active site. Blochim. Biophys. Acta 1188: 167-204.
3. Araujo, R. S., Robleto, E. A., and Handelsman, J., 1994. A hydrophobic mutant of Rhizobium etli altered in nodulation competitiveness and growth in the rhizosphere. Appl. Environ. Microbiol. 60: 1430-1436.
4. Arp, D. J., 1992. Hydrogen cycling in symbiotic bacteria. In: Biological Nitrogen Fixation. pp. 432-460. Stacey, G., Burris, R. H., and Evans, H. J., Eds., Chapman and Hall, New York.
5. Bedmar, E. J. and Phillips, D. A., 1984. A transmissable plant shoot factor promotes uptake hydrogenase activity in Rhizobium symbionts. Plant Physiol. 75: 629-633.
6. Bedmar, E. J., Edie, S. A., and Phillips, D. A., 1983. Host plant cultivar effects on hydrogen evolution by Rhizobium leguminosarum. Plant Physiol. 72: 1011-1015.
7. Bezdicek, D. F., Quinn, M. A., Forse, L., Heron, D., and Kahn, M. L., 1994. Insecticidal activity and competitiveness of Rhizobium spp. containing the Bacillus thuringiensis subsp. Tenebrionis γ-endotoxin gene (cryIII) in legume nodules. Soil Biol. Biochem. 26: 1637-1646.
8. Bhagwat, A. A. and Keister, D. L., 1992. Identification and cloning of Bradyrhizobium japonicum genes expressed strain selectively in soil and rhizosphere. Appl. Environ. Microbiol. 58: 1490-1495.
9. Black, L. K., 1995. Transcriptional Regulation of Hydrogenase Expression in Bradyrhizobium japonicum, Ph.D. dissertation, Johns Hopkins University.
10. Black, L. K. and Maier, R. J., 1994. Sequences and characterization of hupU and hupV genes of Bradyrhizobium japonicum encoding a possible nickel-sensing complex involved in hydrogenase expression. J. Bacteriol. 176: 7102-7106.
11. Black, L. K. and Maier, R. J., 1995. IHF- and RpoN-dependent regulation of hydrogenase expression in Bradyrhizobium japonicum. Mol. Microbiol. 16: 405-413.
12. Boivin, C., Camut, S., Malpica, C. A., Truchet, G., and Rosenberg, C., 1990. Rhizobium meliloti genes encoding catabolism of trigonelline are induced under symbiotic conditions. Plant Cell 2: 1157-1170.
13. Bosworth, A. H., Williams, M. K., Albrecht, K. A., Hankinson, T. R., Kwiatkowski, R., Beynon, J., Ronson, C. W., Cannon, F., Wacek, T. J., and Triplett, E. W.. 1994. Alfalfa yield response to inoculation with recombinant strains of Rhizobium meliloti carrying an extra copy of dct and/or modified nifA expression. Appl. Environ. Microbiol 60: 3815-3832.
14. Bosworth, A. H., Breil, B. T., and Triplett, E. W., 1993. Production of the anti-rhizobial peptide, trifolitoxin, in sterile soils by Rhizobium leguminosarum bv. trifolii T24. Soil Biol. Biochem. 25: 829-832.
15. Bottomley, P. J., 1992. Ecology of Bradyrhizobium and Rhizobium. pp. 293-348. Stacey, G., Burris, R. H., and Evans, H. J., Eds., Chapman and Hall, New York.
16. Breil, B. T., Borneman, J., and Triplett, E. W., 1996. A new gene, tfuA, involved in the production of the ribosomally synthesized peptide antibiotic trifolitoxin. J. Bacteriol. (submitted).
17. Ereil, B. T., Ludden, P. W., and Triplett, E. W., 1993. DNA sequence and mutational analysis of genes involved in the production and resistance of the antibiotic peptide trifolitoxin. J. Bacteriol. 175: 3693-3702.
18. Brito, B., Palacios, J.-M., Hidalgo, E., Imperial, J., and Ruiz-Argueso, T., 1994. Nickel availability to pea (Pisum sativum L.) plants limits hydrogenase activity of Rhizobium leguminosarum bv. viciae bacteroids by affecting the processing of the hydrogenase structural subunits. J. Bacteriol. 176: 5297-5303.
19. Brockwell, J. and Bottomley, P. J., 1995. Recent advances in inoculant technology and prospects for the future. Soil Biol. Biochem. 27: 683-697.
20. Brzoska, P. M. and Singer, E. R., 1991. lpsZ, a lipopolysaccharide ngene involved in symbiosis of Rhizobium meliloti. J. Bacteriol. 173: 3235-3237.
21. Buendia, A. M., Enekel, B., Koplin, R., Niehaus, K., Arnold, W., and Pühler, A., 1991. The Rhizobium meliloti exoB/exoZ fragment of megaplasmid 2: ExoB functions as a UDP-glucose 4-epimerase and ExoZ shows homology to NodX of Rhizobium leguminosarum biovar viciae strain TOM. Mol. Microbiol. 5: 1519-1530.
22. Cannon, W., Charlton, W., and Buck, M., 1991. Organization and function of binding sites for the transcriptional activator NifA in Klebsiella pneumoniae nifE and nifU promoters. J. Mol. Biol. 220: 915-931.
23. Canter-Cremers, H. C. J., Batley, M., Redmond, J. W., Eydems, L., Breedveld, M. W., Zevenhuizen, L. P. T. M., Pees, E., Wijffelman, C. A., and Lugtenberg, B. J. J., 1990. Rhizobium leguminosarum exoB mutants are deficient in the synthesis of UDP-glucose 4′-epimerase. J. Biol. Chem. 265: 21122-21127.
24. Cantrell, M. A., Haugland, R. A., and Evans, H. J., 1983. Construction of a Rhizobium japonicum gene bank and use in isolation of a hydrogen uptake gene. Proc. Natl. Acad. Sci. U.S.A. 80: 181-185.
25. Cantrell, M. A., Hickok, R. E., and Evans, J. H., 1982. Identification and characterization of plasmids in hydrogen uptake positive and hydrogen uptake negative strains of Rhizobium japonicum. Arch. Microbiol. 131: 102-106.
26. Cauvin, B., Colbeau, A., and Vignais, P. M., 1991. The hydrogenase structural operon in Rhodobacter capsulatus contains a third gene, hupM, necessary for the formation of a physiologically competent hydrogenase. Mol. Microbiol. 5: 2519-2527.
27. Chen, H., Batley, M., Redmond, J., and Rolfe, B. G., 1985. Alteration of the effective nodulation properties of a fast-growing broad host range Rhizobium due to changes in exopolysaccharide synthesis. J. Plant Physiol. 120: 331-349.
28. Chen, J. C. and Mortenson, L. E., 1992a. Identification of six open reading frames from a region of the Azotobacter vinelandii genome likely involved in dihydrogen metabolism. Biochem. Biophys. Acta 131: 199-202.
29. Chen, J. C. and Mortenson, L. E., 1992b. Two open reading frames (ORFs) identified near the hydrogenase structural genes in Azotobacter vinelandii, the first ORF may encode for a polypeptide similar to rubredoxins. Biochim. Biophys. Acta 1131: 122-124.
30. Chun, J. Y. and Stacey, G., 1994. A Bradyrhizobium japonicum gene essential for root nodulation competitiveness is differentially regulated from two promoters. Mol. Plant-Microbe Interact. 7: 248-255.
31. Clover, R. H., Keiber, J., and Signer, E. R., 1989. Lipopolysaccharide mutants of Rhizobium meliloti are not defective in symbiosis. J. Bacteriol. 171: 3961-3967.
32. 2. J. Bacteriol. 174: 4258-4264.
33. Colbeau, A., Richaud, P., Toussaint, B., Caballero, J. F., Elster, C., Delphi, C., Smith, R., Chart, J., and Vignais, P. M., 1993. Organization of the genes necessary for hydrogenase expression in Rhodobacter capsulatus: sequence analysis and identification of two hypE regulatory mutants. Mol. Microbiol. 8: 15-29.
34. Cole, S. T., 1987. Nucleotide sequence and comparative analysis of the frd operon encoding the fumarate reductase of Proteus vulgaris. Eur. J. Biochem., 167: 481-488.
35. Cregan, P. B., Keyser, H. H., and Sadowsky, M. F., 1989a. Soybean genotype restricting nodulation of a previously unrestricted serocluster 123 bradyrhizobia. Crop Sci. 29: 307-312.
36. Cregan, P. B., Keyser, H. H., and Sadowsky, M. F., 1989b. A soybean genotype that restricts nodulation of a previously unrestricted isolate of Bradyrhizobium japonicum serocluster 123. Crop Sci. 29: 307-312.
37. Dean, D. R., Bolin, J. T., and Zheng, L., 1993. Nitrogenase metalloclusters: structures, organization, and synthesis. J. Bacteriol. 175: 6737-6744.
38. 2 inhibition of nitrogenase activity in attached soybean nodules. Plant Physiol. 100: 1863-1868.
39. Dixon, R. O. D., 1972. Hydrogenase in legume root nodule bacteroids: occurrence and properties. Arch. Microbiol. 85; 193-201.
40. Dockendorff, T. C., Sanjuan, J., Grob, P., and Stacey, G., 1994. NolA represses nod gene expression in Bradyrhizobium japonicum. Mol. Plant-Microbe Interact. 7: 596-602.
41. Dowling, D. N. and Broughton, W. J., 1986. Competition for nodulation of legumes. Annu. Rev. Microbiol. 40: 131-157.
42. Dross, G., Geisler, V., Lenger, R., Theis, F., Krafft, T., Fahrenholz, F., Kojro, E., Duchene, A., Tripier, D., Juvenal, K., and Kroger, J. A., 1992. The quinone-reactive Ni/Fe-hydrogenase of Wolinella succinogenes. Eur. J. Biochem. 206: 93-102.
43. Dunigan, E. P., Bollicj, P. K., Hutchinson, R. L., Hicks, P. M., and Zaunbrecher, F. C., et al., 1984. Introduction and survival of an inoculant strain of Rhizobium japonicum in soil. Agron. J. 76: 463-466.
44. Eberz, G. and Friedrich, B., 1991. Three transacting regulatory functions control hydrogenase synthesis in Alcaligenes eutrophus. J. Bacteriol. 173: 1845-1854.
45. Eitcnger, T. and Friedrich, B., 1991. Cloning, sequence, and heterologous expression of a high-affinity nickel transport gene from Alcaligenes eutrophus. J. Biol. Chem. 266: 3222-3227.
46. Elsen, S., Richaud, P., Colbeau, A., and Vignais, P. M., 1993. Sequence analysis and interposon mutagenesis of the hupT gene, which encodes a sensor protein involved in repression of hydrogenase synthesis in Rhodobacter capsulatus. J. Bacteriol. 175: 7404-7412.
47. Emerich, D. W., Ruiz-Argueso, T., Ching, T. M., and Evans, H. J., 1979. Hydrogen-dependent nitrogenase activity and ATP formation in Rhizobium japonicum bacteroids. J. Bacteriol. 137: 153-160.
48. Evans, H. J., Hanus, F. J., Haugland, R. A., Cantrell, M. A., Xu, L. S., Russell, F. J., Lambert, G. R., and Harker, A. R., 1985. Hydrogen recycling in nodules affects nitrogen fixation and growth of soybeans. In: World Soybean Research Conference III Proceedings, pp. 935-942. Shibles, R., Ed., Boulder, Westview Press.
49. Evans, H. J., Harker, A. R., Papen, H., Russell, F. J., Hanus, F. J., and Zuber, M., 1987. Physiology, biochemistry, and genetics of the uptake hydrogenase in rhizobia. Annu. Rev. Microbiol. 41: 335-361.
50. Ferber, D. M. and Maier, R. J., 1993. Hydrogen-ubiquinone oxidoreductase activity by the Bradyrhizobium japonicum membrane-bound hydrogenase. FEMS Microbiol. Lett. 110: 257-264.
51. Ferber, D. M., Moy, B., and Maier, R. J., 1995. Bradyrhizobium japonicum hydrogen-ubiquinone oxidoreductase activity: quinone specificity, inhibition by quinone analogs, and evidence for separate sites of electron acceptor reactivity. Biochim. Biophys. Acta 1229: 334-346.
52. Fred, E. B., Baldwin, I. L., and McCoy, E., 1932. Root Nodule Bacteria and Leguminous Plants. University of Wisconsin Press, 343 pp.
53. Freundlich, M. N., Ramani, N., Mathew, E., Sirko, A., and Tsui, P., 1992. The role of integration host factor in gene expression in E. coli. Mol. Microbiol. 6: 2557-2563.
54. Friedrich, B. and Schwartz, E., 1993. Molecular biology of hydrogen utilization in aerobic chemolithotrophs. Annu. Rev. Microbiol. 47: 351-383.
55. Fu, C. and Maier, R. J., 1991. Identification of a locus within the hydrogenase gene cluster involved in intracellular nickel metabolism in Bradyrhizobium japonicum. Appl. Environ. Microbiol. 57: 3502-3510.
56. c mutants and direct evidence for a nickel metabolism locus involved in nickel incorporation into the enzyme. Arch. Microbiol. 157: 493-498.
57. Fu, C. and Maier, R. J., 1993. A genetic region downstream from the hydrogenase structural genes of Bradyrhizobium japonicum that is required for hydrogenase processing. J. Bacteriol. 175: 295-298.
58. Fu, C. and Maier, R. J., 1994a. Nucleotide sequences of two hydrogenase related genes (hypA and hypB) from Bradyrhizobium japonicum, one of which (hypB) encodes an extremely histidine-rich region and guanine nucleotide-binding domains. Biochim. Biophys. Acta 1184: 135-138.
59. Fu, C. and Maier, R. J., 1994b. Sequence and characterization of three genes within the hydrogenase gene cluster of Bradyrhizobium japonicum. Gene 141: 47-52.
60. Fu, C. and Maier, R. J., 1994c. Organization of the hydrogenase gene cluster from Bradyrhizobium japonicum: sequences and analysis of five more hydrogenase-related genes. Gene 145: 91-96.
61. Fu, C., Javedan, S., Moshiri, F., and Maier, R. J., 1994. Bacterial genes involved in incorporation of nickel into a hydrogenase enzyme. Proc. Natl. Acad. Sci. U.S.A. 91: 5099-5103.
62. Fu, C., Olson, J. W., and Maier, R. J., 1995. HypB protein of Bradyrhizobium japonicum is a metalbinding GTPase capable of binding 18 divalent nickel ions per dimer. Proc. Natl. Acad. Sci. U.S.A. 92: 2333-2337.
63. Gibson, A. H., Dreyfus, B. L., Lawn, R. J., Sprent, J. I., and Turner, G. L., 1981. Host and environmental factors affecting hydrogen evolution and uptake. In: Current Perspectives in Nitrogen Fixation. p. 373. Gibson, A. H. and Newton, W. E., Eds., Australian Academy of Sciences, Canberra, Australia.
64. Glucksman, M. A., Reuber, T. L., and Walker, G. C., 1993a. Family of glycosyl transferases needed for the synthesis of succinoglycan by Rhizobium meliloti: a model for succinoglycan biosynthesis. J. Bacteriol. 175: 7033-7044.
65. Glucksman, M. A., Reuber, T. L., and Walker, G. C., 1993b. Genes needed for the modification, polymerization, export, and processing of succinoglycan by Rhizobium meliloti: a model for succinoglycan biosynthesis. J. Bacteriol. 175: 7045-7055.
66. Goldman, A., Boivin, C., Fleury, V., Message, B., Lecoeur, L., Maille, M., and Tepfer, D., 1991. Betaine use by rhizosphere bacteria: genes essential for trigonelline, stachydrine, and carnitine catabolism in Rhizobium meliloti are located on pSym in the symbiotic region. Mol. Plant-Microbe Interact. 4: 571-578.
67. Ham, G. E., Caldwell, V. B., and Johnson, H. W., 1971a. Evaluation of Rhizobium japonicum inoculants in soils containing naturalized populations of rhizobia. Agron. J. 63: 301-303.
68. Ham, G. E., Frederick, L. R., and Anderson, I. C., 1971b. Serogroups of Rhizobium japonicum in soybean nodules sampled in Iowa. Agron. J. 63: 69-72.
69. Handelsman, U., Ugalde, R. A., and Brill, W. J., 1984. Rhizobium meliloti competitiveness and the alfalfa agglutinin. J. Bacteriol. 157: 703-707.
70. Haugland, R. A., Cantrell, M. A., Beaty, J. S., Hanus, F. J., Russell, S. A., and Evans, H. J., 1984. Characterization of Rhizobium japonicum hydrogen uptake genes. J. Bacteriol. 159: 1006-1012.
71. Hellreigel, H. and Wilfarth, H., 1888. Unterrsuchungenn über die Stickstoffnahrung der Gramineen und Leguminosen. Beilageheft zu der Ztschr. Ver. Rübenzucker-Industrie Deutschen Reichs, 234 pp.
72. Hennecke, H., 1990. Regulation of bacterial gene expression by metal-protein complexes. Mol. Microbiol. 4: 1621-1628.
73. Hemando, Y., Palacios, J.-M., Imperial, J., and Ruiz-Argueso, T., 1995. The hypBFCDE operon from Rhizobium leguminosarum biovar viciae is expressed from an FNR-type promoter that escapes mutagenesis of the fnrN gene. J. Bacteriol. 177: 5661-5669.
74. Hidalgo, E., Leyva, A., and Ruiz-Argueso, T., 1990. Nucleotide sequence of the hydrogenase structural genes from Rhizobium leguminosarum. Plant Mol. Biol. 15: 367-370.
75. Hidalgo, E., Palacios, J. M., Murillo, J., and Ruiz-Argueso, T., 1992. Nucleotide sequence and characterization of four additional genes of the hydrogenase structural operon from Rhizobium leguminosarum bv. viciae. J. Bacteriol. 174: 4130-4139.
76. Hochuli, E., Bannwarth, W., Dobeli, H., Gentz, R., and Stuber, D., 1988. Genetic approach to facilitate purification of recombinant proteins with a novel metal chelate adsorbent. Biotechnology 6: 1321-1325.
77. Horn, S. S. M., Graham, L. A., and Maier, R. J., 1985. Isolation of genes (nif/hup Cosmids) involved in hydrogenase and nitrogenase activities in Rhizobium japonicum. J. Bacteriol. 161: 882-887.
78. 2. Appl. Environ. Microbiol. 54: 358-363.
79. Hoover, T. R., Santero, E., Porter, S., and Kustsu, S., 1990. The integration host factor stimulates interaction of RNA polymerase with NifA. the transcriptional activator for nitrogen fixation operons. Cell 63: 11-22.
80. Hungria, M., Neves, M. C. P., and Dobereiner, J., 1989. Relative efficiency, ureide transport and harvest index in soybeans inoculated with isogenic HUP mutants of Bradyrhizobium japonicum. Biol. Fertil. Soils 7: 325-329.
81. Hunter, W. J. and Kuykendall, L. D., 1990. Enhanced nodulation and nitrogen fixation by a revertant of a nodulation-defective Bradyrhizobium japonicum tryptophan mutant. Appl. Environ. Microbiol. 56: 2399-2403.
82. Imperial, J., Rey, L., Palacios, J. M., and Ruiz-Argueso, T., 1993. Microcorrespondence. Mol. Microbiol. 9: 1305-1306.
83. Jacobi, A., Rossmann, R., and Bock, A., 1992. The hyp operon gene products are required for the maturation of catalytically active hydrogenase isoenzymes in E. coli. Arch. Microbiol. 158: 444-451.
84. Jiménez-Zurdo, J. I., van Dillewijn, P., Soto, M. J., de Felipe, M. R., Olivares, J., and Toro, N., 1995. Characterization of a Rhizobium meliloti proline dehydrogenase mutant altered in nodulation efficiency and competitiveness on alfalfa roots. Mol. Plant-Microbe Interact. 8: 492-498.
85. Johnson, H. W. and Means, U. M., 1963. Serological groups of Rhizobium japonicum recovered from nodules of soybeans (Glycine max) in field soils. Agron. J. 55: 239-271.
86. Judd, A. K., Sadowsky, M. J., Bhagwat, A. A., and Cregan, P. B., 1993. Isolation of a Bradyrhizobium japonicum serogroup 123 mutant which has an extended host range for nodulation-restricting soybean genotypes. FEMS Microbiol. Lett. 106: 205-210.
87. Keyser, H. H. and Cregan, P. B., 1987. Modulation and competition for nodulation of selected soybean genotypes among Bradyrhizobium japonicum serogroup 123 isolates. Appl. Environ. Microbiol. 53: 2631-2635.
88. Keyser, H. H. and Li, F., 1992. Potential for increasing biological nitrogen fixation in soybean. Plant Soil 141: 119-135.
89. Keyser, H. H., Weber, D. F., and Uratsu, S. L., 1984. Rhizobium japonicum serogroup and hydrogenase phenotype distribution in 12 states. Appl. Environ. Microbiol. 47: 613-615.
90. Kim, H. and Maier, R. J., 1990. Transcriptional regulation of hydrogenase synthesis by nickel in Bradyrhizobium japonicum. J. Biol. Chem. 265: 18729-18732.
91. Kim, H., Yu, C., and Maier, R. J., 1991. Common cis-acting region responsible for transcriptional regulation of Bradyrhizobium japonicum hydrogenase by nickel, oxygen, and hydrogen. J. Bacteriol. 173: 3993-3999.
92. c Strains of Bradyrhizobium japonicum. Arch. Microbiol. 160: 43-50.
93. Kosslak, R. M. and Bohlool, B. B., 1985. Influence of environmental factors on interstrain competition in Rhizobium japonicum. Appl. Environ. Microbiol. 49: 1128-1133.
94. Kosslak, R. M., Bohlool, B. B., Dowdle, S. F., and Sadowsky, M. J., 1983. Competition of Rhizobium japonicum strains in early stages of soybean nodulation. Appl. Environ. Microbiol. 46: 870-873.
95. Kroger, A., Dadak, V., Klingenberg, M., and Diemer, F., 1971. On the role of quinones in bacterial electron transport. Differential roles of ubiquinone and menquinone in Proteus rettgeri. Eur. J. Biochem., 21: 322-333.
96. Labandera, C. A. and Vincent, J. M., 1975. Competition between an introduced strain and native Uruguayan strains of Rhizobium trifolii. Plant Soil 42: 327-347.
97. Lagares, A., Caetano-Anollés, G., Niehaus, K., Lorenzen, J., Ljunggren, H. D., Pühler, A., and Favelukes, G., 1992. A Rhizobium meliloti lipopolysaccharide mutant altered in competitiveness for nodulation of alfalfa. J. Bacteriol. 174: 5941-5952.
98. Lambert, G. R., Harker, A. R., Cantrell, M. A., Hanus, F. J., Russell, S. A., Haugland, R. A., and Evans, H. J., 1987. Symbiotic expression of cosmid-borne Bradyrhizobium japonicum hydrogenase genes. Appl. Environ. Microbiol. 53: 422-428.
99. Lee, M. H., Mulrooney, B. S. B., Renver, M. J., Markowicz, Y., and Hausinger, R. P., 1992. Klebsiella aerogenes urease gene cluster: sequence of ureD and demonstration that four accessory genes (ureD, ureE, urel, and ureG) are involved in nickel metallocenter biosynthesis. J. Bacteriol. 174: 4324-4330.
100. Lee, M. H., Pankratz, H. S., Wang, S., Scott, R. A., Finnegan, M. G., Johnson, M. K., Ippolito, J. A., Christianson, D. W., and Hausinger, R. P., 1993. Purification and characterization of Klebsiella aerogenes UreE protein: a nickel-binding protein that functions in urease metallocenter assembly. Protein Sci. 2: 1042-1052.
101. Leigh, J. A. and Coplin, D. L., 1992. Exopolysaccharides in plant-bacterial interactions. Annu. Rev. Microbiol. 46: 307-346.
102. Leigh, J. A., Signer, E. R., and Walker, G. C., 1985. Exopolysaccharide-deficient mutants of R. meliloti that form ineffective nodules. Proc. Natl. Acad. Sci. U.S.A. 82: 6231-6235.
103. Leigh, J. A. and Walker, G. C., 1994. Exopolysaccharides of Rhizobium: synthesis, regulation and symbiotic function. Trends Genet. 10: 63-67.
104. + Rhizobium leguminosarum strains. Appl. Environ. Microbiol. 53: 2539-2543.
105. Leyva, A., Palacios, J. M., Mozo, T., and Ruiz-Argueso, T., 1987b. Cloning and characterization of hydrogen uptake genes from Rhizobium leguminosarum. J. Bacteriol. 169:4929-4934.
106. Leyva, A., Palacios, J. M., Murillo, J., and Ruiz-Argueso, T., 1990. Genetic organization of the hydrogen uptake (hup) cluster from Rhizobium leguminosarum. J. Bacteriol. 172: 1647-1655.
107. Lochhead, A. G., 1929. Cultures for the inoculation of legume seed. Canada Experimental Farms, Rpt. Dominion Agr. Bact for 1927-28, pp. 15-16.
108. Lochhead, A. G., 1931. Cultures for the inoculation of legume seed. Canada Experimental Farms, Rpt. Dominion Agr. Bact for 1929-30, pp. 26-27.
109. Long, S., Reed, J. W., Himawan, J., and Walker, G. C., 1988. Genetic analysis of a cluster of genes required for synthesis of the calcofluor-binding exopolysaccharide for Rhizobium meluoti. J. Bacteriol. 170: 4239-4248.
110. Lutz, S., Bohm, R., Beier, A., and Bock, A., 1990. Characterization of divergent ntrA-dependent promoters in the anaerobically expressed gene cluster coding for hydrogenase 3 components of Escherichia coli. Mol. Microbiol. 4: 13-20.
111. Lutz, S., Jacobi, A., Schlensog, V., Bohm, R., Sawers, G., and Bock, A., 1991. Molecular characterization of an operon (hyp) necessary for the activity of the three hydrogenase isoenzymes in Escherichia coli. Mol. Microbiol. 5: 123-135.
112. Maier, R. J., 1986. Biochemistry, regulation, and genetics of hydrogen oxidation in Rhizobium. CRC Crit. Rev. Biotechnol. 3: 17-38.
113. Maier, R. and Brill, W. J., 1978. Mutant strains of Rhizobium japonicum with increased ability to fix nitrogen for soybean. Science 201: 448-450.
114. Maier, T., Jacobi, A., Sauter, M., and Bock, A., 1993. The product of the hypB gene, which is required for nickel incorporation into hydrogenases, is a novel guanine nucleotide-binding protein. J. Bacteriol. 175: 630-635.
115. Maier, T., Lottspeich, F., and Bock, A., 1995. GTP hydrolysis by HypB is essential for nickel insertion into hydrogenases of Escherichia coli. Eur. J. Biochem. 230: 133-138.
116. Martensson, A. M., 1990. Competitiveness of inoculant strains of Rhizobium leguminosarum bv. trifolii in red clover using repeated inoculation and increased inoculum levels. Can. J. Microbiol. 36: 136-139.
117. McDermott, T. R. and Graham, P. H., 1990. Competitive ability and efficiency in nodule formation of strains of Bradyrhizobium japonicum. Appl. Environ. Microbiol. 56: 3035-3039.
118. Menon, N. K., Peck, Jr., H. D., LeGall, J., and Przybyla, A. E., 1987. Cloning and sequencing of the genes encoding the large and small subunits of the periplasmic (NiFeSe) hydrogenase from Desulfovibrio baculatus. J. Bacteriol. 169: 5401-5407. (Published erratum appears in J. Bacteriol. 170: 4429, 1988.)
119. Menon, A. L., Stults, L. W., Robson, R. L., and Mortenson, L. E., 1990. Cloning, sequencing and characterization of the (NiFe) hydrogenase-encoding structural genes (hoxK and hoxG) from Azotobacter vinelandii. Gene 96: 67-74.
120. Menon, N. K., Robbins, J., Wendt, J. C., Shanmugan, K. T., and Przybla, A. E., 1991. Mutational analysis and characterization of the E. coli hya operon, which encodes NiFe hydrogenase-1. J. Bacteriol. 173: 4851-4861.
121. Merberg, D. and Maier, R. J., 1983. Mutants of Rhizobium japonicum with increased hydrogenase activity. Science 220: 1064-1065.
122. Merberg, D., O'Hara, E. B., and Maier, R. J., 1983. Regulation of hydrogenase in Rhizobium japonicum: analysis of mutants altered in regulation by carbon substrates and oxygen. J. Bacteriol. 156: 1236-1242.
123. N). Mol. Microbiol. 10: 903-909.
124. Michiels, J., Pelemans, H., Vlassak, K., Verreth, C., and Vanderleyden, J., 1995. Identification and characterization of a Rhizobium leguminosarum bv. phaseoli gene that is important for nodulation competitiveness and shows structural homology to a Rhizobium fredii host-inducible gene. Mol. Plant-Microbe Interact. 8: 468-472.
125. Milner, J. L., Araujo, R. S., and Handelsman, J., 1992. Molecular and symbiotic characterization of exopolysaccharide-deficient mutants of Rhizobium tropici strain CIAT899. Mol. Microbiol. 6: 3137-3147.
126. Minamisawa, K., Fukai, K., and Asami, T., 1990. Rhizobitoxine inhibition of hydrogenase synthesis in free-living Bradyrhizobium japonicum. J. Bacteriol. 172: 4505-4509.
127. Moloney, A. H., Guy, R. D., and Layzell, D. B., 1994. A model of the regulation of nitrogenase electron allocation in legume nodules. II. Comparison of empirical and theoretical studies in soybean. Plant Physiol. 104: 541-550.
128. Müller, P., Keller, M., Weng, W.-M., Quandt, J., Arnold, W., and Pühler, A., 1993. Genetic analysis of the Rhizobium meliloti exoYFQ operon: ExoY is homologous to sugar transferases and ExoQ represents a transmembrane protein. Mol. Plant Microbe Interact. 6: 55-65.
129. Müller, P., Hynes, M., Kapp, D., Niehaus, K., and Pühler, A., 1988. Two classes of Rhizobium meliloti infection mutants differ in exopolysaccharide production and in coinoculation properties with nodulation mutants. Mol. Gen. Genet. 211: 17-26.
130. Mulrooney, S. B. and Hausinger, R. P., 1990. Sequence of the Klebsiella aerogenes urease genes and evidence for accessory proteins facilitating nickel incorporation. J. Bacteriol. 172: 5837-5843.
131. Murphy, P. J., Trenz, S. P., Grzemski, W., de Bruijn, F. J., and Schell, J., 1993. The Rhizobium meliloti rhizopine mos locus is a mosaic structure facilitating its symbiotic regulation. J. Bacteriol. 175: 5193-5204.
132. Murphy, P. J., Wexler, W., Grzemski, W., Rao, J. P., and Gordon, D., 1995. Rhizopines - their role in symbiosis and competition. Soil Biol. Biochem. 27: 525-529.
133. Nautiyal, C. S., Hedge, S. V., and Van Berkum, P., 1988. Nodulation, nitrogen fixation, and hydrogen oxidation by pigeon pea Bradyrhizobium spp. in symbiotic association with pigeon pea, cowpea and soybean. Appl. Environ. Microbiol. 54: 94-97.
134. Navarro, R. B., Vargas, A. T., Schroder, and van Berkum, P., 1993. Uptake hydrogenase (Hup) in common bean (Phaseolus vulgaris) symbioses. Appl. Environ. Microbiol. 59: 4161-4165.
135. Nelson, L. M., Grosskopf, E., Tichy, H. V., and Lotz, W., 1985. Characterization of hup-specific DNA in Rhizohium leguminosarum strains of different origin. FEMS Microbiol. Lett. 30: 53-58.
136. Nelson, L. M. and Salminen, S. O., 1982. Uptake hydrogenase activity and ATP formation in Rhizobium leguminosarum bacteroids. J. Bacteriol. 151: 989-995.
137. Neves, M. C. P. and Hungria, M., 1987. The physiology of nitrogen fixation in tropical grain legumes. CRC Crit. Rev. Plant Sci. 6: 267-321.
138. Nobbe, F. and Hiltner, L., 1896. Inoculation of the Soil for Cultivating Leguminous Plants. U.S. Patent No. 570,813.
139. Noel, K. D., 1993. Rhizobium leguminosarum CE3 lipopolysaccharide structure required in symbiosis with bean. In: New Horizons in Nitrogen Fixation. pp. 213-216. Palacios, R., Mora, J., and Newton, W. E., Eds., Kluwer, Dordrecht.
140. Novak, P. D. and Maier, R. J., 1989. Identification of a locus upstream from the hydrogenase structural genes that is involved in hydrogenase expression in Bradyrhizobium japonicum. Appl. Environ. Microbiol. 55: 3051-3057.
141. O'Brian, M. R. and Maier, R. J., 1985. Expression of cytochrome o in hydrogen uptake constitutive mutants of Rhizobium japonicum. J. Bacteriol. 161: 507-514.
142. O'Brian, M. R. and Maier, R. J., 1988. Hydrogen metabolism in Rhizobium: energetics, regulation, enzymology and genetics. Advances in Microbial. Physiology 29: 1-52.
143. O'Brian, M. R. and Maier, R. J., 1989. Molecular aspects of the energetics of nitrogen fixation in Rhizohium-legume symbioses. Biochim. Biophys. Acta 974: 229-246.
144. Ollero, F. J., Valverde, M. A., Sánchez-Palazón, L., Villalobo, E., Espuny, M. R., and Bellogín, R. A., 1994. An exoB mutant of Rhizobium sp. is effective in indeterminant nodules of Hedysarum coronarium. Microbiology 140: 1389-1394.
145. Oliveira, L. A. and Graham, P. H., 1989. Speed of nodulation and competitive ability among strains of Rhizobium leguminosarum bv. Phaseoli. Arch. Microbiol. 153: 311-315.
146. Ozawa, T. and Yamiguchi, M., 1986. Enhancement of symbiotic nitrogen fixation of Bradyrhizobium japonicum by acridine orange. Agric. Biol. Chem. 50: 1061-1062.
147. Paau, A. S., 1989. Improvement of Rhizobium inoculants. Appl. Environ. Microbiol. 55: 862-865.
148. Palacios, J., Murillo, M. J., Leyva, A., and Ruiz-Argueso, T., 1990. Differential expression of hydrogen uptake (hup) genes in vegetative and symbiotic cells of Rhizobium leguminosarum. Mol. Gen. Genet. 221: 363-370.
149. Parniske, M., Kosch, K., Werner, D., and Muller, P., 1993. ExoB mutants of Bradyrhizobium japonicum with reduced competitiveness for nodulation of glycine max. Mol. Plant-Microbe Interact. 6: 99-106.
150. Phillips, D. A., Kapulnik, Y., Bedmar, E. J., and Joseph, C. M., 1990. Development and partial characterization of nearly isogenic pea lines (Pisum sativum L.) that alter hydrogenase activity in symbiotic Rhizobium. Plant Physiol. 92: 983-989.
151. Phillips, D. A., Joseph, C. M., and Maxwell, C. A., 1992. Trigonelline and stacyhydrine released from alfalfa seeds activate NodD2 protein in Rhizobium meliloti. Plant Physiol. 99: 1526-1531.
152. Przybyla, A. E., Robbins, J., Menon, N., and Peck, Jr., H. D., 1992. Structure-function relationships among the nickel-containing hydrogenases. FEMS Microbiol. Rev. 88: 109-136.
153. Rasche, M. E. and Arp, D. J., 1989. Hydrogen inhibition of nitrogen reduction by nitrogenase in isolated soybean nodule bacteroids. Plant Physiol. 91: 663-668.
154. 2-uptake gene cluster from Rhizobium leguminosarum bv. viciae containing a rubredoxin-like gene and four additional open reading frames. J. Mol. Biol. 228: 998-1002.
155. Rey, L., Imperial, J., Palacios, J.-M., and Ruiz-Argueso, T., 1994. Purification of Rhizobium leguminosarum HypB, a nickel-binding protein required for hydrogenase synthesis. J. Bacteriol. 176: 6066-6073.
156. Rey, L., Murillo, J., Hernando, Y., Hidalgo, E., Cabrera, E., Imperial, J., and Ruiz-Argueso, T., 1993. Molecular analysis of a microaerobically induced operon required for hydrogenase synthesis in Rhizobium leguminosarum biovar viciae. Mol. Microbiol. 8: 471-481.
157. Richaud, P., Colbeau, A., Toussaint, B., and Vignais, P. M., 1991. Identification and sequence analysis of the hupR gene, which encodes a response regulator of the NtrC family required for hydrogenase expression in Rhodobacter capsulatus. J. Bacteriol. 173: 5928-5932.
158. Römermann, D., Warrelmann, J., Bender, R. A., and Friedrich, B., 1989. An rpoN-like Gene of Acaligenes eutrophus and Pseudomonas facilis controls expression of diverse metabolic pathways, including hydrogen oxidation. J. Bacteriol. 171: 1093-1099.
159. Rossbach, S., Kulpa, D. A., Rossbach, U., and de Bruijn, F. J., 1994. Molecular and genetic characterization of the rhizopine catabolism (mocABRC) genes of Rhizobium meliloti L5-50. Mol. Gen. Genet. 245: 11-24.
160. Rossbach, S., Rasul, G., Schneider, M., Eardley, B., and de Bruijn, F. J., 1995. Structural and functional conservation of the rhizopine catabolism (moc) locus is limited to selected Rhizobium meliloti strains and unrelated to their geographic origin. Mol. Plant-Microbe Interact. 8: 549-559.
161. Rossman, R., Maier, T., Lottspeich, F., and Bock, A., 1995. Characterization of a protease from Escherichia coli involved in hydrogenase maturation. Eur. J. Biochem. 227: 545-550.
162. Rynne, F. G., Glenn, A. R., and Dilworth, M. J., 1994. Effect of mutations in aromatic catabolism on the persistence and competitiveness of Rhizobium leguminosarum bv. trifolii. Soil Biol. Biochem. 26: 703-710.
163. Sadowsky, M. J. and Cregan, P. B., 1992. The soybean Rj4 allele restricts nodulation by Bradyrhizobium japonicum serogroup 123 strains. Appl. Environ. Microbiol. 58: 720-723.
164. Sadowsky, M. J., Cregan, P. B., Gottfert, M., Sharma, A., Gerhold, D., Rodriguez-Quinones, F., Keyser, H. H., Hennecke, H., and Stacey, G., 1991. The Bradyrhizobium japonicum nolA gene and its involvement in the genotype-specific nodulation of soybeans. Proc. Natl. Acad. Sci. U.S.A. 88: 637-641.
165. Sadowsky, M. J., Kosslak, R. M., Madrzak, C. J., Golinska, B., and Cregan, P. B., 1995. Restriction of nodulation by Bradyrhizobium japonicum is mediated by factors present in the roots of glycine max. Appl. Environ. Microbiol. 61: 832-836.
166. Sadowsky, M. J., Tully, R. E., Cregan, P. B., and Keyser, H. H., 1987. Genetic diversity in Bradyrhizobium japonicum serogroup 123 and its relation to genotype-specific nodulation of soybean. Appl. Environ. Microbiol. 53: 2624-2630.
167. Salzwedel, J. L. and Van Berkum, P., 1992. Cloning of the host-regulated uptake hydrogenase genes in Bradyrhizobium japonicum. In: Sixth International Symposium on Molecular PlantMicrobe Interactions, July 11-16, 1992. Seattle, Washington.
168. Sanjuan, J. and Olivares, J., 1991. NifA-NtrA regulatory system activates transcription of nfe, a gene locus involved in nodulation competitiveness of Rhizobium meliloti. Arch. Microbiol. 155: 543-548.
169. 54-dependent nifH promoter. J. Mol. Biol. 227: 602-620.
170. Sayavedra-Soto, L. A., Powell, G. K., Evans, H. J., and Morris, R. O., 1988. Nucleotide sequence of the genetic loci encoding subunits of Bradyrhizobium japonicum uptake hydrogenase. Proc. Natl. Acad. Sci. U.S.A. 85: 8395-8399.
171. Sayavedra-Soto, L. A. and Arp, D. J., 1992. The hoxZ gene of the Azotobacter vinelandii hydrogenase operon is required for activation of hydrogenase. J. Bacteriol. 174: 5295-5301.
172. Schlensog, V. and Böck, A., 1990. Identification and sequence analysis of the gene encoding the transcriptional activator of the formate hydrogenlyase system of E. coll. Mol. Microbiol. 4: 1319-1329.
173. Schneider, C. G., Schmitt, H. J., Schild, C., Tichy, H. V., and Lotz, W., 1990. DNA sequence encoding the two structural genes for uptake hydrogenase of Rhizobium leguminosarum bv. viciae B10. Nucleic Acids Res. 18: 5285.
174. Scott, D. B., Hennecke, H., and Lim, S. T., 1979. The biosynthesis of nitrogenase MoFe protein polypeptides in free-living cultures of Rhizobium japonicum. Biochim. Biophys. Acta 565: 365-378.
175. Simpson, F. B. and Burris, R. H., 1984. A nitrogen pressure of 50 atmospheres does not prevent evolution of hydrogen by nitrogenase. Science 224: 1095-1097.
176. Soedarjo, M., Hemscheidt, T. K., and Borthakur, D., 1994. Mimosine, a toxin present in leguminous trees (Leucaena spp.), induces a mimosine-degrading enzyme activity in some Rhizobium strains. Appl. Environ. Microbiol. 60: 4268-4272.
177. Soto, M. J., Zorzano, A., Mercado-Blanco, J., Lepek, V., Olivares, J., and Toro, N., 1993. Nucleotide sequence and characterization of Rhizobium meliloti nodulation competitiveness genes nfe. J. Mol. Biol. 229: 570-576.
178. Soto, M. J., Zorzano, A., Olivares, J., and Toro, N., 1992. Nucleotide sequence of Rhizobium meliloti GR4 insertion sequence ISRm3 linked to the nodulation competitiveness locus nfe. Plant Mol. Biol. Int. J. Mol. Biol. Biochem. Genet. Eng. 20: 307-309.
179. Soto, M. J., Zorzano, A., Garcia-Rodriguez, F. M., Mercado-Blanco, J., Lopez-Lara, I. M., Olivares, J., and Toro, N., 1994. Identification of a novel Rhizobium meliloti nodulation efficiency nfe gene homolog of Agrobacterium ornithine cyclodeaminase. Mol. Plant-Microbe Interact. 7: 703-707.
180. Stephens, P. M. and Cooper, J. E., 1988. Variation in speed of infection of "no root hair zone" of white clover and nodulating competitiveness among strains of Rhizobium trifolii. Soil Biol. Biochem., 20: 465-470.
181. Stevens, F. D., 1915. Labor efficiency of field inoculation. The Wisconsin Agriculturalist, March 4, 1915.
182. Stoker, K., Reijnders, W. N. M., Oltmann, L. F., and Stouthamer, A. H., 1989. Initial cloning and sequencing of hydHG, and operon homologous to ntrBC and regulating the labile hydrogenase activity in Escherichia coli K-12. J. Bacteriol. 171: 4448-4456.
183. Streeter, J. G., 1994. Failure of inoculant rhizobia to overcome the dominance of indigenous strains for nodule formation. Can. J. Microbiol. 40: 513-522.
184. Stults, L., Sray, W. A., and Maier, R. J., 1986. Regulation of hydrogenase biosynthesis by nickel in B. japonicum. Arch. Microbiol. 146: 280-283.
185. Surpin, M. A., Moshiri, F., Murphy, A. M., and Maier, R. J., 1994. Genetic evidence for a fourth terminal oxidase in Bradyrhizobium japonicum. Gene 143: 73-77.
186. Toussaint, B., Bosc, C., Richaud, P., Colbeau, A., and Vignais, P. M., 1991. A mutation in Rhodobacter capsulatus gene encoding an integration host factor-like protein impairs in vivo hydrogenase expression. Proc. Natl. Acad. Sci. U.S.A. 88: 10749-10753.
187. Toussaint, B., Delic-Attree, I., d'Aspremont, R. D. S., David, L., Venin, M., and Vignais, P. M., 1993. Purification of the integration host factor homolog of Rhodobacter capsulatus: cloning and sequencing of the hip gene, which encodes the β subunit. J. Bacteriol. 175: 6499-6504.
188. Trinick, M. J. and Hadobas, P. A., 1989. Competition by Bradyrhizobium strains for nodulation of the nonlegume Parasponia andersonii. Appl. Environ. Microbiol. 55: 1242-1248.
189. Triplett, E. W., 1988. Isolation of genes involved in nodulation competitiveness from Rhizobium leguminosarum bv. trifolii T24. Proc. Natl. Acad. Sci. U.S.A. 85: 3810-3814.
190. Triplett, E. W., 1990a. The molecular genetics of nodulation competitiveness in Rhizobium and Bradyrhizobium. Mol. Plant-Microbe Interact. 3: 199-206.
191. Triplett, E. W., 1990b. Construction of a symbiotically effective strain of Rhizobium leguminosarum bv. trifolii with increased nodulation competitiveness. Appl. Environ. Microbiol. 56: 98-103.
192. Triplett, E. W. and Barta, T. M., 1987. Trifolitoxin production and nodulation are necessary for the expression of superior nodulation competitiveness by Rhizobium leguminosarum bv. trifolii T24. Plant Physiol. 85: 335-342.
193. Triplett, E. W., Breil, B. T., and Splitter, G. A., 1994. Expression of tfx and sensitivity to the rhizobial peptide antibiotic trifolitoxin in a taxonomically distinct group of α-proteobacteria including the animal pathogen Brucella abortus. Appl. Environ. Microbiol. 60: 4163-4166.
194. Triplett, E. W. and Sadowsky, M. J., 1992. Genetics of competition for nodulation of legumes. Annu. Rev. Microbiol. 46: 399-428.
195. Unden, G., Böcher, R., Knecht, J., and Kroger, A., 1982. Hydrogenase from Vibrio succinogenes, a nickel protein. FEBS Lett. 145: 230-234.
196. Uratsu, S. L., Keyser, H. H., Weber, D. F., and Lim, S. T., 1982. Hydrogen uptake (HUP) activity of Rhizobium japonicum from major U.S. soybean production areas. Crop Sci. 22: 600-602.
197. Uttaro, A. D., Cangelosi, G. A., Geremia, R. A., Nester, E. W., and Ugalde, R. A., 1990. Biochemical characterization of avirulent exoC mutants of Agrobacterium tumefaciens. J. Bacteriol. 172: 1640-1646.
198. Van Berkum, P., 1990. Evidence for a third uptake hydrogenase phenotype among the soybean bradyrhizobia. Appl. Environ. Microbiol. 56: 3835-3841.
199. Van Rensburg, J. and Strijdom, B. W., 1982. Root surface association in relation to nodulation of Medicago sativa. Appl. Environ. Microbiol. 44: 93-97.
200. Van Soom, C., Browaeys, J., Verreth, C., and Vanderleyden, J., 1993a. Nucleotide sequence analysis of four genes, hupC, hupD, hupF and hupG, downstream of the hydrogenase structural genes in Bradyrhizobium japonicum. J. Mol. Biol. 234: 508-512.
201. Van Soom, C., Rumjanek, N., Vanderleyden, J., and Neves, M. C. P., 1993b. Hydrogenase in Bradyrhizobium japonicum: genetics, regulation and effect on plant growth. World J. Microbiol. Biotechnol. 9: 615-624.
202. Van Soom, C., Verreth, C., Sampaio, M. J., and Vanderleyden, J., 1993c. Identification of a potential transcriptional regulator of hydrogenase activity in free-living Bradyrhizobium japonicum strains. Mol. Gen. Genet. 239: 235-240.
203. 2-uptake hydrogenases. Arch. Microbiol. 161: 1-10.
204. Volbeda, A., Charon, M.-H., Piras, C., Hatchikian, E. C., Frey, M., and Fontecilla-Camps, J. C., 1995. Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas. Nature 373: 580-587.
205. Voordouw, G., Menon, N. K., LeGall, J., Choi, E. S., Peck, Jr., H. D., and Przybyla, A. E., 1989. Analysis and comparison of nucleotide sequences encoding the genes for [NiFe] hydrogenases from Desulfovibrio gigas and Desulfovibrio baculalus. J. Bacteriol. 171: 2894-2899.
206. Weber, D. F., Keyser, H. H., and Uratsu, S. L., 1989. Serological distribution of Bradyrhizobium japonicum from U.S. soybean production areas. Agron. J. 81: 786-789.
207. Weinstein, M., Roberts, R. C., and Helinski, D. R., 1992. A region of the broad-host-range plasmid RK2 causes stable in planta inheritance of plasmids in Rhizobium meliloti cells isolated from alfalfa in root nodules. J. Bacteriol. 174: 7486-7489.
208. Williams, L. F. and Phillips, D. A., 1983. Increased soybean productivity with a Rhizobium japonicum mutant. Crop Sci. 23: 246-250.
209. Williams, M. N., Hollingsworth, R. I., Brzoska, P. M., and Signer, E. R., 1990. Rhizobium meliloti chromosomal loci required for suppression of exopolysaccharide mutations by lipopolysaccharide. J. Bacteriol. 172: 6596-6598.
210. Witty, J. F., 1991. Microelectrode measurements of hydrogen concentrations and gradients in legume nodules. J. Exp. Bot. 42: 765-771.
211. Wu, L.-F. and Mandrand, M. A., 1993. Microbial hydrogenases: primary structure, classification, signatures and phylogeny. FEMS Microbiol. Rev. 104: 243-247.