Biological Nitrogen Fixation in Cereals Crops: A Bacterial Perspective

  • S. GarchaEmail author
  • P. K. Maan
Part of the Microorganisms for Sustainability book series (MICRO, volume 4)


Nitrogen (N2) is one of the essential requirements of all living forms. The crop requirement is generally met by cheaply available chemical fertilizers. Endophytic bacteria of cereal crops as rice, wheat, etc. have the natural ability to fix atmospheric nitrogen. A few of them have established a mutually beneficial association with the plants. This chapter lists commonly encountered endophytic microbes of rice and wheat and the major enzymes catalyzing N2 fixation, an energy intensive reaction. Nitrogenase enzyme is sensitive to the presence of oxygen. Microbial cells have devised a method to lower oxygen concentration for optimal performance of the enzyme. Further, genetic control of nitrogen fixation is explained mentioning the genes and their respective functions. Quality assurance and longer shelf life of such biological products can go a long way in consolidating market share of biofertilizers. Engineering plant microbe communication can facilitate manipulation for greater efficacy of nitrogen fixation.


Biological nitrogen fixation Cereal crops Associative nitrogen fixation Nitrogen-fixing enzymes Genetics of nitrogen fixation Bio-inoculants 


  1. Adesemoye AO, Torbert HA, Kloepper JW (2008) Enhanced plant nutrient use efficiency with PGPR and AMF in an integrated nutrient management system. Can J Microbiol 54:876–886PubMedCrossRefGoogle Scholar
  2. Ahmed M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci 26:1–20CrossRefGoogle Scholar
  3. Allen RM, Chatterjee R, Madden MS, Ludden PW, Shah VK (1994) Biosynthesis of the iron-molybdenum cofactor of nitrogenase. Crit Rev Biotechnol 14:225–249PubMedCrossRefGoogle Scholar
  4. Al-Mallah MK, Davey MR, Cocking EC (1990) Nodulation of oilseed rape (Brassica napus) by rhizobia. J Exp Bot 41:1567–1572CrossRefGoogle Scholar
  5. Aly MM, Ahmed El Sayed H, Jastaniah SD (2012) Synergistic effect between Azotobacter vinelandii and Streptomyces sp isolated from saline soil on seed germination and growth of wheat plant. J Am Sci 8:667–676Google Scholar
  6. Anastasia V, Dimon M, Pergalis P, Kefalogianni I, Chatzipavlidis I, Katinakis P (2011) The genetic diversity of culturable nitrogen fixing bacteria in the rhizophere of wheat. Microb Ecol 61:277–285CrossRefGoogle Scholar
  7. Arnold W, Rump A, Klipp W, Priefer UB, Puihler A (1988) Nucleotide sequence of a 24,206-base-pair DNA fragment carrying the entire nitrogen fixation gene cluster of Klebsiella pneumoniae. J Mol Biol 203:715–738PubMedCrossRefGoogle Scholar
  8. Axelsson R, Lindblad P (2002) Transcriptional regulation of Nostoc hydrogenases: effects of oxygen, hydrogen, and nickel. Appl Environ Microbiol 68:444–447PubMedPubMedCentralCrossRefGoogle Scholar
  9. Balandreau J (2002) The spermosphere model to select for plant growth promoting rhizobacteria. In: Kennedy IR, Choudhury ATMA (eds) Biofertilisers in action. Rural Industries Research and Development Corporation, Canberra, pp 55–63Google Scholar
  10. Baldani VLD, Döbereiner J (1980) Host-plant specificity in the infection of cereals with Azospirillum spp. Soil Biol Biochem 12:433–439CrossRefGoogle Scholar
  11. Baldani VLD, de Alvarez BMA, Baldani JI, Dobereiner J (1986) Establishment of inoculated Azospirillum spp in the rhizosphere and in the roots of field grown wheat and sorghum. Plant Soil 90:35–46CrossRefGoogle Scholar
  12. Baldani VLD, Baldani JI, Dobereiner J (2000) Inoculation of rice plants with the endophytic diazotrophs Herbaspirillum seropedicae and Burkholderia spp. Biol Fertil Soils 30:485–491CrossRefGoogle Scholar
  13. Batut J, Daveran-Mingot ML, David M, Jacobs J, Garnerone AM, Kahn D (1989) fixK, a gene homologous with fnr and crp from Escherichia coli, regulates nitrogen fixation genes both positively and negatively in Rhizobium meliloti. EMBO J 8:1279–1286PubMedPubMedCentralGoogle Scholar
  14. Beringer JE, Hirsch PR (1984) Genetic engineering and nitrogen fixation. Biotechnol Genet Eng Rev 1:65–88CrossRefGoogle Scholar
  15. Bishop PE, Jarlenski DML, Hetherington DR (1980) Evidence for an alternative nitrogen fixation system in Azotobacter vinelandii. Proc Natl Acad Sci U S A 77:7342–7346PubMedPubMedCentralCrossRefGoogle Scholar
  16. Biswas JC, Ladha JK, Dazzo FB (2000) Rhizobia inoculation improves nutrient uptake and growth of lowland rice. Soil Sci Soc Am J 64:1644–1650CrossRefGoogle Scholar
  17. Bogdanovic D, Jarak M, Milosev D, Šeremesic S (2005) Effect of N-fertilizer inoculation interaction on wheat yields (in Serbian). Letopis naučnih radova 29(1):50Google Scholar
  18. Boistard P, Batut J, David M, Fourment J, Garnerone AM, Kahn D, de Philip P, Reyrat JM, Waelkens F (1991) Regulation of nitrogen fixation genes in Rhizobium meliloti. In: Hennecke H, Verma DPS (eds) Advances in molecular genetics of plant-microbe interactions. Kluwer, Dordrecht, pp 195–202CrossRefGoogle Scholar
  19. Brigle KE, Weiss MC, Newton WE, Dean DR (1987) Products of the iron-molybdenum cofactor-specific biosynthetic genes, nifE and nifN, are structurally homologous to the products of the nitrogenase molybdenum-iron protein genes, nifD and nifK. J Bacteriol 169:1547–1553PubMedPubMedCentralCrossRefGoogle Scholar
  20. Burgess BK, Lowe DJ (1996) Mechanism of molybdenum nitrogenase. Chem Rev 96:2983–3011PubMedCrossRefGoogle Scholar
  21. Burris RH, Roberts GP (1993) Biological nitrogen fixation. Annu Rev Nutr 13:317–335PubMedCrossRefGoogle Scholar
  22. Chen J, Christiansen J, Tittsworth RC, Hales BJ, George SJ, Coucouvanis D, Cramer SP (1993) Characterization of a gene, glnL, whose product is involved in the regulation of nitrogen utilization in Escherichia coli. J Am Chem Soc 115:5509CrossRefGoogle Scholar
  23. Cheng Q (2008) Perspectives in biological nitrogen fixation research. J Integr Plant Biol 50(7):784–796CrossRefGoogle Scholar
  24. Choudhury ATMA, Kennedy IR (2004) Prospects and potentials for system of biological nitrogen fixation in sustainable rice production. Biol Fertil Soils 39:219–227CrossRefGoogle Scholar
  25. Conn VM, Franco CMM (2004) Analysis of the endophytic actinobacterial population in the roots of wheat (Triticum aestivum L.) by terminal restriction fragment length polymorphism and sequencing of 16rRNA clones. Appl Environ Microbiol 69:4915–4926Google Scholar
  26. David M, Domergue O, Pognonec P, Kahn D (1987) Transcription patterns of Rhizobium meliloti symbiotic plasmid pSym; identification of nifA-independent fix genes. J Bacteriol 169:2239–2244PubMedPubMedCentralCrossRefGoogle Scholar
  27. David M, Daveran ML, Batut J, Dedieu A, Domergue O, Ghai J, Hertig C, Boistard P, Kahn D (1988) Cascade regulation of nif gene expression in Rhizobium meliloti. Cell 54:671–683PubMedCrossRefGoogle Scholar
  28. de Philip P, Boistard P, Schluter A, Patschkowski T, Priefer UB, O’Gara F, Boesten B, Noonan B, Puihler A (1992) Developmental and metabolic regulation of nitrogen fixation gene expression in Rhizobium meliloti. Can J Microbiol 38:467–474CrossRefGoogle Scholar
  29. Dean DR, Jacobson MR (1992) Biochemical genetics of nitrogenase. In: Stacey G, Burris RH, Evans HJ (eds) Biological nitrogen fixation. Chapman and Hall, New York, pp 763–834Google Scholar
  30. Dean DR, Bolin JT, Zheng L (1993) Nitrogenase metalloclusters: structures, organization, and synthesis. J Bacteriol 175:6737–6744PubMedPubMedCentralCrossRefGoogle Scholar
  31. Dixon R (1998) The oxygen-responsive NIFL-NIFA compG12 lex: a novel two-component regulatory system contolling nitrogenase synthesis in J-Proteobacteria. Arch Microbiol 169:371–380PubMedCrossRefGoogle Scholar
  32. Dobereiner J (1997) Biological nitrogen fixation in the tropics: social and economic contributions. Soil Biol Biochem 29:771–774CrossRefGoogle Scholar
  33. Dong Y, Iniguez AL, Triplett EW (2003) Quantitative assessments of the host range and strain specificity of endophytic colonization by Klebsiella pneumonia 342. Plant Soil 257:49–59CrossRefGoogle Scholar
  34. Eady RR (1996) Structure-function relationships of alternative nitrogenases. Chem Rev 96:3013–3030PubMedCrossRefGoogle Scholar
  35. Earl CD, Ronson CW, Ausubel FM (1987) Genetic and structural analysis of the Rhizobium meliloti fixA, fixB, fixC, and fixX genes. J Bacteriol 169:1127–1136PubMedPubMedCentralCrossRefGoogle Scholar
  36. Ebeling S, Noti JD, Hennecke H (1988) Identification of a new Bradyrhizobium japonicum gene (fix4) encoding a ferredoxin-like protein. J Bacteriol 170:1999–2001PubMedPubMedCentralCrossRefGoogle Scholar
  37. Elbadry M, El-Bassel A, Elbanna K (1999) Occurrence and dynamics of phototrophic purple nonsulphur bacteria compared with other asymbiotic nitrogen fixers in rice fields of Egypt. World J Microbiol Biotechnol 15:359–362CrossRefGoogle Scholar
  38. Elbeltagy A, Nishioka K, Suzuki H, Sato T, Sato Y, Morisaki H, Mitsui H, Minamisawa K (2000) Isolation and characterization of endophytic bacteria from wild and traditionally cultivated rice varieties. Soil Sci Plant Nutr 46:617–629CrossRefGoogle Scholar
  39. Elmerich C, Zimmer W, Vieille C (1992) Associative nitrogen-fixing bacteria. In: Stacey G, Burris RH, Evans HJ (eds) Biological nitrogen fixation. Chapman and Hall, New York, pp 212–258Google Scholar
  40. Engerhard M, Hurek T, Reinhold-Hurek B (2000) Preferential occurrence of diazotrophic endophytes, Azoarcus spp in wild rice species and land races of Oryza sativa in comparison with modern races. Environ Microbiol 2:131–141CrossRefGoogle Scholar
  41. Enon AL, Mortenson LE, Robson RL (1992) Nucleotide sequences and genetic analysis of hydrogen oxidation (hox) genes in Azotobacter vinelandii. J Bacteriol 174:4549–4557CrossRefGoogle Scholar
  42. Estrada-de los Santos P, Bustilios-Cristales R, Caballero-Mellado J (2001) Burkholderia, a genus rich in plant-associated nitrogen fixers with wide environmental and geographic distribution. Appl Environ Microbiol 67:2790–2798PubMedPubMedCentralCrossRefGoogle Scholar
  43. Fallik E, Robson RL (1990) Completed sequence of the region encoding the structural genes for the vanadium nitrogenase of Azotobacter chroococcum. Nucleic Acids Res 18:15CrossRefGoogle Scholar
  44. Gottfert M (1993) Regulation and function of rhizobial nodulation genes. FEMS Microbiol Rev 104:39–63CrossRefGoogle Scholar
  45. Gronger P, Manian SS, Reilander H, O’Connell M, Priefer UB, Piihler A (1987) Organisation and partial sequence of a DNA region of the Rhizobium leguminosarum symbiotic plasmid pRL6JI containing the genes fixABC, nifA, nifB and a novel open reading frame. Nucleic Acids Res 15:31–49PubMedPubMedCentralCrossRefGoogle Scholar
  46. Grunwald SK, Lies DP, Roberts GP, Ludden PW (1995) Posttranslational regulation of nitrogenase in Rhodospirillum rubrum strains overexpressing the regulatory enzymes dinitrogenase reductase ADP-ribosyltransferase and dinitrogenase reductase activating glycohydrolase. J Bacteriol 177:628–635PubMedPubMedCentralCrossRefGoogle Scholar
  47. Gubler M, Hennecke H (1986) fixs, B and C genes are essential for symbiotic and free-living, microaerobic nitrogen fixation. FEBS Lett 200:186–192CrossRefGoogle Scholar
  48. Gubler M, Zurcher T, Hennecke H (1989) The Bradyrhizobium japonicum fixBCX operon: identification of fixX and of a 5′ mRNA region affecting the level of the fixBCX transcript. Mol Microbiol 3:141–148PubMedCrossRefGoogle Scholar
  49. Gutierrez-Zamora ML, Martinez-Romero E (2001) Natural endophytic association between Rhizobium etli and maize (Zea mays L.) J Biotechnol 91:117–126PubMedCrossRefGoogle Scholar
  50. Gyaneshwar P, James EK, Reddy PM, Ladha JK (2002) Herbaspirillum colonization increases growth and nitrogen accumulation in aluminium-tolerant rice varieties. New Phytol 154:131–145CrossRefGoogle Scholar
  51. Halbleib CM, Zhang Y, Ludden PW (2000) Regulation of dinitrogenase reductase ADP-ribosyltransferase and dinitrogenase reductase activating glycohydrolase by a redox-dependent conformational change of nitrogenase Fe protein. J Biol Chem 275:3493–3500PubMedCrossRefGoogle Scholar
  52. Hanson D (1996) Biotechnology is future path for crop protection. Chem Eng 13:22Google Scholar
  53. Happe T, Schütz K, Böhme H (2000) Transcriptional and mutational analysis of the uptake hydrogenase of the filamentous cyanobacterium Anabaena variabilis ATCC 29413. J Bacteriol 182:1624–1631PubMedPubMedCentralCrossRefGoogle Scholar
  54. Hardoim PR, Van Overbeek LS, Van Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471PubMedCrossRefGoogle Scholar
  55. Haselkorn R, Buikema WJ (1992) Nitrogen fixation in cyanobacteria. In: Stacey G, Burris RH, Evans HJ (eds) Biological nitrogen fixation. Chapman and Hall, New York, pp 166–190Google Scholar
  56. Hawkes T, McLean PA, Smith BE (1984) Nitrogenase from nifV mutants of Klebsiella pneumoniae contains an altered form of the iron-molybdenum cofactor. Biochem J 217:317–321PubMedPubMedCentralCrossRefGoogle Scholar
  57. Hecht-Buchholz C (1998) The apoplast-habitat of endophytic dinitrogen-fixing bacteria and their significance for the nitrogen nutrition of nonleguminous plants. J Plant Nutr Soil Sci 161:509–520Google Scholar
  58. Herrero A, Flores E (2008) The cyanobacteria: molecular biology, genomics and evolution. Caister Academic Press, Norfolk. ISBN 978-1-904455-15-8Google Scholar
  59. Hill S, Austin S, Eydmann T, Jones T, Dixon R (1996) Azotobacter vinelandii NIFL is a flavoprotein that modulates transcriptional activation of nitrogen-fixation genes via a redox-sensitive switch. Proc Natl Acad Sci 93:2143–2148PubMedPubMedCentralCrossRefGoogle Scholar
  60. Homer MJ, Paustian TD, Shah VK, Roberts GP (1993) The nifY product of Klebsiella pneumoniae is associated with apo dinitrogenase and dissociates upon activation with the iron molybdenum cofactor. J Bacteriol 175:4907–4910PubMedPubMedCentralCrossRefGoogle Scholar
  61. Honeycutt RJ, McClelland M, Sobra BWS (1993) Physical map of the genome of Rhizobium meliloti 1021. J Bacteriol 175:6945–6952PubMedPubMedCentralCrossRefGoogle Scholar
  62. Hoover TR, Robertson AD, Cerny RL, Hayes RN, Imperial J, Shah VK (1987) Identification of the V factor needed for synthesis of the iron-molybdenum cofactor of nitrogenase as homocitrate. Nature 329:855–857PubMedCrossRefGoogle Scholar
  63. Howard JB, Rees DC (1996) Structural basis of biological nitrogen fixation. Chem Rev 96:2965–2982PubMedCrossRefGoogle Scholar
  64. Hu Y, Fay AW (2007) P-cluster maturation on nitrogenase MoFe protein. Proc Natl Acad Sci 104(25):10424–10429PubMedPubMedCentralCrossRefGoogle Scholar
  65. Hynes MF, Quandt J, Schiuter A, Paschkowski T, Weidner S, Priefer UB (1992) In Abstracts of the ninth international congress of nitrogen fixation, FEMS, pp 464Google Scholar
  66. Iismaa SE, Ealing PM, Scott KF, Watson JM (1989) Molecular linkage of the nifl fix and nod gene regions in Rhizobium leguminosarum biovar trifolii. Mol Microbiol 3:1753–1764PubMedCrossRefGoogle Scholar
  67. Imperial J, Ugalde RA, Shah VK, Brill WJ (1984) Role of the nifQ gene product in the incorporation of molybdenum into nitrogenase in Klebsiella pneumoniae. J Bacteriol 158:187–194PubMedPubMedCentralGoogle Scholar
  68. Iniguez AL, Dong Y, Triplett EW (2004) Nitrogen fixation in wheat is provided by Klebsiella pneumonia 342. Mol Plant Microbiol Interact 17:1078–1085CrossRefGoogle Scholar
  69. Inoue A, Shigematsu T, Hidaka M, Masaki H, Uozumi T (1996) Cloning, sequencing and transcriptional regulation of the draT and draG genes of Azospirillum lipoferum. FS Gene 170:101–106PubMedCrossRefGoogle Scholar
  70. Islam N, Bora LC (1998) Biological management of bacterial leaf blight of rice (Oryza sativa) with plant growth promoting rhizobacteria. Indian J Agric Sci 68:798–800Google Scholar
  71. Jain V, Gupta K (2003) The flavonoid naringen enhances intercellular colonization of rice roots by Azorhizobium caulinodans. Biol Fertil Soils 38:119–123CrossRefGoogle Scholar
  72. James EK (2000) Nitrogen fixation in endopytic and associative symbiosis. Field Crops Res 65:197–209CrossRefGoogle Scholar
  73. James EK, Gyaneshwar P, Mathan N, Barraquio WL, Reddy PM, Iannetta PPM, Olivares FL, Ladha JK (2002) Infection and colonization of rice seedlings by the plant growth-promoting bacteria Herbaspirillum seropedicae Z67. Mol Plant Microbe Interact 15:894–906PubMedCrossRefGoogle Scholar
  74. Kahn D, David M, Domergue O, Daveran ML, Ghai J, Hirsch PR, Batut J (1989) Rhizobium meliloti fixGHI sequence predicts involvement of a specific cation pump in symbiotic nitrogen fixation. J Bacteriol 171:929–939PubMedPubMedCentralCrossRefGoogle Scholar
  75. Kaminski PA, Norel F, Desnoues N, Kush A, Salzano G, Elmerich C (1988) Characterization of the JixABC region of Azorhizobium caulinodans ORS571 and identification of a new nitrogen fixation gene. Mol Gen Genet 214:496–502PubMedCrossRefGoogle Scholar
  76. Kanemoto RH, Ludden PW (1987) Amino acid concentrations in Rhodospirillum rubrum during expression and switch-off of nitrogenase activity. J Bacteriol 169:3035–3043PubMedPubMedCentralCrossRefGoogle Scholar
  77. Kanungo PK, Ramakrishnan B, Rao VR (1997) Placement effect of organic sources on nitrogenase activity and nitrogen-fixing bacteria in flooded rice soils. Biol Fertil Soils 25:103–108CrossRefGoogle Scholar
  78. Kennedy IR, Pereg-Gerk LL, Wood C, Deaker R, Gilchrist K, Katupitiya S (1997) Biological nitrogen fixation in non-leguminous field crops: facilitating the evolution of an effective association between Azospirillum and wheat. Plant Soil 194:65–79CrossRefGoogle Scholar
  79. Khandan T, Namvar A (2013) Response of wheat to mineral nitrogen fertilizer and biofertilizer (Azotobacter sp. and Azospirillum sp.) inoculation under different levels of weed interference. Ekologia 59:85–94Google Scholar
  80. Kim S, Burgess BK (1996) Evidence for the direct interaction of the nifW gene product with the MoFe protein. J Biol Chem 271:9764–9770PubMedCrossRefGoogle Scholar
  81. Klipp W, Paschen A (1998) Duplication of a transcriptional regulator as a mechanism for genetic control: NifAI and NifAII from Rhodobacter capsulatus differ in their susceptibility to ammonium control. In: Elmerich C, Kondorosi A, Newton WE (eds) Biological nitrogen fixation for the 21st century. Kluwer, Dordrecht, p 131Google Scholar
  82. Kondorosi A, Kondorosi E, John M, Schmidt J, Schell J (1991) The role of nodulation genes in bacterium-plant communication. Genet Eng 13:115–136CrossRefGoogle Scholar
  83. Krey R, Pu¨hler A, Klipp W (1992) A defined amino acid exchange close to the putative nucleotide binding site is responsible for an oxygen-tolerant variant of the Rhizobium meliloti NifA protein. Mol Gen Genet 234:433–441PubMedCrossRefGoogle Scholar
  84. Ladha JK, Baraquio WL, Watanabe I (1982) Immunological techniques to identify Azospirillum associated with rice. Can J Microbiol 28:478–485PubMedCrossRefGoogle Scholar
  85. Ladha JK, Tirol AC, Daroy MLG, Caldo G, Ventura W, Watanabe I (1986) Plant-associated N2fixation (C2H2-reduction) by five rice varieties, and relationship with plant growth characters as affected by straw incorporation. Soil Sci Plant Nutr 32:91–106CrossRefGoogle Scholar
  86. Ladha JK, So RB, Watanabe I (1987) Composition of Azospirillum species associated with wetland rice plant grown in different soils. Plant Soil 102:127–129CrossRefGoogle Scholar
  87. Liang JH, Nielsen GM, Lies DP, Burris RH, Roberts GP, Ludden PW (1991) Mutations in the draT and draG genes of Rhodospirillum rubrum result in loss of regulation of nitrogenase by reversible ADP-ribosylation. J Bacteriol 173:6903–6909PubMedPubMedCentralCrossRefGoogle Scholar
  88. Lobo AL, Zinder SH (1992) Nitrogen fixation by methanogenic bacteria. In: Stacey G, Burris RH, Evans HJ (eds) Biological nitrogen fixation. Chapman and Hall, New York, pp 191–211Google Scholar
  89. Long SR (1989) Rhizobium-legume nodulation: life together in the underground. Cell 56:203–214PubMedCrossRefGoogle Scholar
  90. Ludden PW, Roberts GP (1989) Regulation of nitrogenase activity by reversible ADP ribosylation. Curr Top Cell Regul 30:23–56PubMedCrossRefGoogle Scholar
  91. Lyons EM, Thiel T (1995) Characterization of nifB, nifS, and nifU genes in the cyanobacterium Anabaena variabilis: NifB is required for the vanadium-dependent nitrogenase. J Bacteriol 177:1570–1575PubMedPubMedCentralCrossRefGoogle Scholar
  92. Malarvizhi P, Ladha JK (1999) Influence of available nitrogen and rice genotype on associative dinitrogen fixation. Soil Sci Soc Am J 63:93–99CrossRefGoogle Scholar
  93. Malik KA, Mirza MS, Hassan U, Mehnaz S, Rasul G, Haurat J, Bally R, Normand P (2002) The role of plant-associated beneficial bacteria in rice-wheat cropping system. In: Kennedy IR, Choudhury ATMA (eds) Biofertilisers in action. Rural Industries Research and Development Corporation, Canberra, pp 73–83Google Scholar
  94. Mandon K, Hillebrand H, Mougel C, Desnoues N, Dreyfus B, Kaminski PA, Elmerich C (1993) Characterization of fixK-regulated Azorhizobium caulinodans genes. In: Palacios R, Mora J, Newton WE (eds) New horizons in nitrogen fixation. Kluwer, Dordrecht, p 478Google Scholar
  95. Mano H, Morisaki H (2008) Endophytic bacteria in rice plant. Microbes Environ 23:109–117PubMedCrossRefGoogle Scholar
  96. Martinez-Toledo MV (1985) Isolation and characterization of Azotobacter chroococcum from the roots of Zea mays. FEMS Microbiol Lett 31:4CrossRefGoogle Scholar
  97. Masepohl B, Krey R, Klipp W (1993) The draTG gene region of Rhodobacter capsulatus is required for post-translational regulation of both the molybdenum and the alternative nitrogenase. J Gen Microbiol 139:2667–2675PubMedCrossRefGoogle Scholar
  98. Mavingui P, Laguerre G, Berge O, Henlin T (1992) Genetic and phenotypic diversity of Bacillus polymyxa in soil and in the wheat rhizosphere. Appl Environ Microbiol 58:1894–1903PubMedPubMedCentralGoogle Scholar
  99. Merrick MJ (1992) Regulation of nitrogen fixation genes in free living and symbiotic bacteria. In: Stacey G, Burris RH, Evans HJ (eds) Biological nitrogen fixation. Chapman and Hall, New York, pp 835–876Google Scholar
  100. Michiels J, Vanderleyden J (1993) Cloning and sequence of the Rhizobium leguminosarum biovar phase of fix4 gene. Biochim Biophys Acta 1144:232–233PubMedCrossRefGoogle Scholar
  101. Milosevic N, Jarak M (2005) Značaj azotofiksacije u snabdevanju biljaka azotom (in Serbian). In: Kastori R (ed) Nitrogen-agrochemical, cultural practice, physiological and ecological aspects. Institute of Field and Vegetable Crops, Novi Sad, pp 305–352Google Scholar
  102. Mirza MS, Rasul G, Mehnaz S, Ladha JK, So RB, Ali S, Malik KA (2000) Beneficial effects of inoculated nitrogen-fixing bacteria on rice. In: Ladha JK, Reddy PM (eds) The quest for nitrogen fixation in rice. International Rice Research Institute, Los Baños, pp 191–204Google Scholar
  103. Mirza MS, Ahmad W, Latif F, Haurat J, Bally R, Normand P, Malik KA (2001) Isolation, partial characterization, and effect of plant growth promoting bacteria (PGPB) on micropropagated sugarcane in vitro. Plant Soil 237:47–54CrossRefGoogle Scholar
  104. Murty MG, Ladha JK (1988) Influence of Azospirillum inoculation on the mineral uptake and growth of rice under hydroponic conditions. Plant Soil 108:281–285CrossRefGoogle Scholar
  105. Nakas JP, Hagedorn C (1990) Biotechnology of plant-microbe interactions. McGraw-Hill, New YorkGoogle Scholar
  106. Nakata PA (2002) The generation of a transposon-mutagenized Burkholderia glumae library to isolate novel mutants. Plant Sci 162:267–271CrossRefGoogle Scholar
  107. Norén A, Soliman A, Nordlund S (1997) The role of NAD+ as a signal during nitrogenase switch-off in Rhodospirillum rubrum. Biochem J 322:829–832PubMedPubMedCentralCrossRefGoogle Scholar
  108. Pandey A, Kumar S (1989) Potential of Azotobacters and Azospirilla as biofertilizers for upland agriculture: a review. J Sci Ind Res 48:134–144Google Scholar
  109. Pereira JAR, Cavalcante VA, Baldani JI, Döbereiner J (1988) Field inoculation of sorghum and rice with Azospirillum spp. and Herbaspirillum seropedicae. Plant Soil 110:269–274CrossRefGoogle Scholar
  110. Peters JW, Stowell MH, Soltis SM, Finnegan MG, Johnson MK, Rees DC (1997) Redox-dependent structural changes in the nitrogenase P-cluster. Biochemistry 36:1181–1187PubMedCrossRefGoogle Scholar
  111. Postgate J (1998) Nitrogen fixation, 3rd edn. Cambridge University Press, CambridgeGoogle Scholar
  112. Preisig UO, Anthamatten D, Hennecke H (1993) Genes for a microaerobically induced oxidase complex in Bradyrhizobium japonicum are essential for a nitrogen-fixing endosymbiosis. Proc Natl Acad Sci 90:3309–3313PubMedPubMedCentralCrossRefGoogle Scholar
  113. Rees DC, Schindelin H, Kisker C, Schlessman JL, Peters JW, Seefeldt LC, Howard JB (1998) Complex structures of nitrogenase. In: Elmerich C, Kondorosi A, Newton WE (eds) Biological nitrogen fixation for the 21st century. Kluwer, Dordrecht/London/Boston, pp 11–16CrossRefGoogle Scholar
  114. Renalier MH, Batut J, Ghai J, Terzaghi B, Gherardi M, David M, Garnerone AM, Vasse J, Truchet G, Huguet T, Boistard P (1987) A new symbiotic cluster on the pSym megaplasmid of Rhizobium meliloti 2011 carries a functional fix gene repeat and a nod locus. J Bacteriol 169:2231–2238PubMedPubMedCentralCrossRefGoogle Scholar
  115. Roberts GP, Ludden PW (1992) Nitrogen fixation by photosynthetic bacteria. In: Stacey G, Burris RH, Evans HJ (eds) Biological nitrogen fixation. Chapman and Hall, New York, pp 135–165Google Scholar
  116. Roper MM, Ladha JK (1995) Biological N2 fixation by heterotrophic and phototrophic bacteria in association with straw. Plant Soil 174:211–224CrossRefGoogle Scholar
  117. Salamone de Garcia IE, Di Salvo LP, Escobar Ortega JS, Boa Sorte PMF, Urquiaga S, Teixeira KRS (2010) Field response of rice paddy crop to Azospirillum inoculation: physiology of rhizosphere bacterial communities and the genetic diversity of endophytic bacteria in different parts of the plants. Plant Soil 336:351–362CrossRefGoogle Scholar
  118. Salamone de Garcia IE, Funes JM, Di Salvo LP, Escobar-Ortega JS, Auria FD, Ferrando L, Scavino AF (2012) Inoculation of paddy rice with Azospirillum brasilense and Pseudomonas fluorescens: impact of plant genotypes on rhizosphere microbial communities and field crop production. Appl Soil Ecol 61:196–204CrossRefGoogle Scholar
  119. Schindelin H, Kisker C, Schlessman JL, Howard JB, Rees DC (1997) Structure of ADP x AlF4(-)-stabilized nitrogenase complex and its implications for signal transduction. Nature 387:370–376PubMedCrossRefGoogle Scholar
  120. Schlessman JL, Woo D, Joshua-Tor L, Howard JB, Rees DC (1998) Conformational variability in structures of the nitrogenase iron proteins from Azotobacter vinelandii and Clostridium pasteurianum. J Mol Biol 280:669–685PubMedCrossRefGoogle Scholar
  121. Shah VK, Hoover TR, Imperial J, Paustian TD, Roberts GP, Ludden PW (1988) Role of nif gene products and homocitrate in the biosynthesis of iron-molybdenum cofactor. In: Bothe H, deBruijn FJ, Newton WE (eds) Nitrogen fixation: hundred years after. Gustav Fischer, Stuttgart, pp 115–120Google Scholar
  122. Shah VK, Rangara P, Chatterjee R, Allen RM, Roll JT, Roberts GP (1999) Requirement of NifX and other nif proteins for in vitro biosynthesis of the iron-molybdenum cofactor of nitrogenase. J Bacteriol 181:2797–2801PubMedPubMedCentralGoogle Scholar
  123. Shrestha RK, Ladha JK (1996) Genotypic variation in promotion of rice dinitrogen fixation as determined by nitrogen-15 dilution. Soil Sci Soc Am J 60:1815–1821CrossRefGoogle Scholar
  124. Singh S (2014) A review on possible elicitor molecules of cyanobacteria: their role in improving plant growth and providing tolerance against biotic or abiotic stress. J Appl Microbiol 117:1221–1244PubMedCrossRefGoogle Scholar
  125. Singh RK, Mishra RPN, Jaiswal HK, Kumar V, Pandey SP, Rao SB, Annapurna K (2006) Isolation and identification of natural endophytic rhizobia from rice (Oryza sativa L.) through r DNA PCR-RFLP and sequence analysis. Curr Microbiol 52:117–122PubMedCrossRefGoogle Scholar
  126. Steinshamn H, Thuen E, Bleken MA, Brenoe UT, Ekerholt G, Yri C (2004) Utilization of nitrogen (N) and phosphorus (P) in an organic dairy farming system in Norway. Agric Ecosyst Environ 104:509–522CrossRefGoogle Scholar
  127. Suarez-Moreno Z, Caballero-Mellado J, Continho B, Mendonca-Previato L, James E, Venturio V (2012) Common features of environmentally and potentially beneficial plant-associated Burkholderia. Microb Ecol 63:249–266Google Scholar
  128. Thiel T, Lyons EM, Thielemier J (1998) Organization and regulation of two clusters of nif genes in the cyanobacterium Anabaena variabilis. In: Peschek LW, Schmetterer G (eds) Phototrophic prokaryotes. Plenum Press, New York, pp 517–521Google Scholar
  129. Thony B (1989) Structure and genetic control of a regulatory operon (fixRnifA) essential for symbiotic nitrogen fixation in Bradyrhizobium japonicum. Ph.D. dissertation ETH 8859. Eidgenossische Technische Hochschule, ZurichGoogle Scholar
  130. Thony B, Fischer HM, Anthamatten D, Bruderer T, Hennecke H (1987) The symbiotic nitrogen fixation regulatory operon (fixRnifA) of Bradyrhizobium japonicum is expressed aerobically and is subject to a novel, nifA-independent type of activation. Nucleic Acids Res 15:8479–8499PubMedPubMedCentralCrossRefGoogle Scholar
  131. Thorneley RN, Abell C, Ashby GA, Drummond MH, Eay RR, Huff S (1992) Posttranslational modification of Klebsiella pneumoniae flavodoxin by covalent attachment of coenzyme A, shown by 31P NMR and electrospray mass spectrometry, prevents electron transfer from the nifJ protein to nitrogenase. A possible new regulatory mechanism for biological nitrogen fixation. Biochemistry 31:1216–1224PubMedCrossRefGoogle Scholar
  132. Tittsworth RC, Hales BJ (1996) Oxidative titration of nitrogenase VFe protein from Azotobacter vinelandii: an example of redox-gated electron flow. Biochemistry 35:479PubMedCrossRefGoogle Scholar
  133. Tran Van V, Berge O, Ke SN, Balandreau J, Heulin T (2000) Repeated beneficial effects of rice inoculation with a strain of Burkholderia vietnamiensis on early and late yield components in low fertility sulphate acid soils of Vietnam. Plant Soil 218:273–284CrossRefGoogle Scholar
  134. Urquiaga S, Botteon PBL, Boddey RM (1989) Selection of sugarcane cultivars for associated biological nitrogen fixation using 15N-labelled soils. In: Skinner A (ed) Nitrogen fixation with non-legumes. Kluwer, Dordrecht, pp 311–319CrossRefGoogle Scholar
  135. Vance CP, Graham PH (1995) Nitrogen fixation in agriculture: applications and perspectives. In: Tikhonovich IA, Provorov NA, Romanov VI, Newton WE (eds) Nitrogen fixation: fundamentals and applications, current plant science and biotechnology in agriculture, vol 27. Kluwer, Dordrecht, pp 77–86CrossRefGoogle Scholar
  136. Vandamme P, Goris J, Chen Wen-Ming, de Vos P, Willems A (2002) Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Syst Appl Microbiol 25:507–512PubMedCrossRefGoogle Scholar
  137. Vargas L, Carvalho TLGD, Ferreira PCG, Baldani VLD, Baldani JI, Hemerly AS (2012) Early responses of rice (Oryza sativa L.) seedlings to inoculation with beneficial diazotrophioc bacteria are dependent on plant and bacteria genotypes. Plant Soil 356:127–137CrossRefGoogle Scholar
  138. Wani SP (1990) Inoculation with associstave nitrogen fixing bacteria: role in cereal grain production. Ind J Microbiol 30:363–393Google Scholar
  139. Webster G, Jain V, Davey MR, Gough C, Vasse J, Denarie J, Cocking EC (1998) The flavonoid naringenin stimulates the intercellular colonization of wheat roots by Azorhizobium caulinodans. Plant Cell Environ 21:373–383CrossRefGoogle Scholar
  140. Wu P, Zhang G, Ladha JK, McCouch SR, Huang N (1995) Molecular-marker-facilitated investigation on the ability to stimulate N2 fixation in the rhizosphere by irrigated rice plants. Theor Appl Genet 91:1177–1183PubMedCrossRefGoogle Scholar
  141. Xie CH, Yokota A (2005) Azospirillum oryzae sp nov., a nitrogen fixing bacterium isolated from the roots of the rice plant Oryza sativa. Int J Syst Evol Microbiol 55:1435–1438PubMedCrossRefGoogle Scholar
  142. Yanni YG, El-Fattah FKA (1999) Towards integrated biofertilization management with free living and associative dinitrogen fixers for enhancing rice performance in the Nile delta. Symbiosis 27:319–331Google Scholar
  143. Yanni YG, Rizk RY, Corich V, Squartini A, Ninke K, Philip-Hollingsworth S, Orgambide G, de Bruijn F, Stoltzfus J, Buckley D, Schmidt TM, Mateos PF, Ladha JK, Dazzo FB (1997) Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice and assessment of its potential to promote rice growth. Plant Soil 194:99–114CrossRefGoogle Scholar
  144. Yates MG, Campbell F (1989) The effect of nutrient limitation on the competition between an H2-uptake, hydrogenase-positive recombinant strain of Azotobacter chroococcum and the Hup-mutant parent in mixed populations. J Gen Microbiol 135:221–226Google Scholar
  145. Yuvaniyama P, Agar JN, Cash VL, Johnson MK, Dean DR (2000) NifS-directed assembly of a transient [2Fe-2S] cluster within the NifU protein. Proc Natl Acad Sci 97:599–604PubMedPubMedCentralCrossRefGoogle Scholar
  146. Zhang Y, Burris RH, Roberts GP (1992) Cloning, sequencing, mutagenesis, and functional characterization of draT and draG genes from Azospirillum brasilense. J Bacteriol 174:3364–3369PubMedPubMedCentralCrossRefGoogle Scholar
  147. Zhang Y, Cummings AD, Burris RH, Ludden PW, Roberts GP (1995) Effect of an ntrBC mutation on the posttranslational regulation of nitrogenase activity in Rhodospirillum rubrum. J Bacteriol 177:5322–5326PubMedPubMedCentralCrossRefGoogle Scholar
  148. Zheng L, White RH, Cash VL, Jack RF, Dean DR (1993) Cysteine desulfurase activity indicates a role for NIFS in metallocluster biosynthesis. Proc Natl Acad Sci 90:2754–2758PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  1. 1.Department of MicrobiologyPunjab Agricultural UniversityLudhianaIndia

Personalised recommendations