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Endophytic Nitrogen-Fixing Bacteria as Biofertilizer

  • Garima Gupta
  • Jitendra PanwarEmail author
  • Mohd Sayeed AkhtarEmail author
  • Prabhat N. JhaEmail author
Chapter
Part of the Sustainable Agriculture Reviews book series (SARV, volume 11)

Abstract

Nitrogen is the most limiting nutritional factor for the growth of plants. Since plants cannot reduce atmospheric N2, they require exogenously fixed nitrogen for growth and development. Atmospheric N2 must be first reduced to ammonia to be used by plants. In practice, chemical N fertilizers are used to provide nitrogen nutrition to plants. However, manufacture and use of N fertilizers are associated with environmental hazards that include release of greenhouse gases at the time of manufacture, as well as contamination of underground and surface water due to leaching out of nitrates. Moreover, manufacture of chemical fertilizers requires non-renewable resources like coal and petroleum products. Excess and continuous use of chemical fertilizers to improve the yield of commercial crops has negative effect on soil fertility and reduces their agricultural sustainability. All these concerns necessitate the search for an alternative strategy that can provide nitrogen nutrition to the plants in an efficient and sustainable manner. Here biological nitrogen fixation has immense potential and can be used as an alternate to chemical fertilizers. Biological nitrogen fixation has been reported to be exclusively carried out by few members of the prokaryotic organisms. Biological nitrogen fixation is a process where atmospheric N2 is reduced to NH3. This process is catalyzed by microbial enzyme nitrogenase. Microorganisms having the capacity to fix atmospheric N2 can be used as efficient biofertilizer.

In this chapter, we review application, properties, ecology, and advances in biology of nitrogen fixing bacteria with reference to endophytic bacteria that colonize the interior of plant without exerting any substantive harm to their host plant. Nitrogen-fixing endophytic bacteria have edge over its rhizospheric counterparts because, being sheltered inside plant tissues, they face less competition and can make available the fixed nitrogen directly to plants. Moreover, the partial pressure of oxygen inside the plant tissue is more acquiescent for efficient nitrogen fixation. Nitrogen fixing endophytic bacteria have been isolated from several plant species and found to contribute upto 47% of nitrogen derived from air, which in turn enhance plant growth. Nitrogen fixing ability of bacteria can be evaluated by total nitrogen difference method, acetylene reduction assay, analysis of nitrogen solutes in xylem and other plant parts and N-Labeling Methods. Furthermore, molecular approaches such as amplification, analysis of nitrogen-fixing genes (nif genes), and qualitative and quantitative estimation of their products can be used for evaluation of nitrogen fixing ability of the bacteria.In addition to nitrogen-fixation ability, these bacteria can influence plant growth through one or more properties. These include production of phytohormones, siderophores, induced systemic tolerance through production of 1-aminocyclopropane-1-carboxylase deaminase, induced systemic resistance and antagonistic activities. The make-up of endophytic bacterial communities depends on various factors such as soil type, soil composition, soil environment, plant genotype and physiological status, bacterial colonization traits, and agricultural management regimes. Colonization and abundance of different bacterial species varies widely with host plants. Endophytic bacterial community can be analyzed employing stable isotope probing as well as various modern molecular approaches which are based on analysis of 16S ribosomal deoxyribonucleic acid (DNA), gene encoding products for nitrogen fixation and repetitive DNAs. Moreover, metagenomic approaches allow estimation and analysis of unculturable bacteria at genomic as well as functional genomic level. Colonization process of an endophytic bacterium involves various steps which include migration towards root surface, attachment and microcolony formation on plant surface, distribution along root and growth and survival of the population inside plant tissue. Ongoing progress towards in-depth analysis of genomic and whole protein profile of some of the potential endophytic bacteria such as Azoarcus sp., Gluconoacetobacter diazotrophicus, Herbaspirillum seropedicae, Serratia marcesens can help understand mechanism involved in plant-endophyte interaction which in turn will be deterministic in use of suitable formulations of endophytic bacteria to be used as biofertilizer for sustainable agriculture.

Keywords

1-aminocyclopropane-1-carboxylase deaminase Biofertilizer Diazotrophic Endophytic Nitrogen Reverse transcription-polymerase chain reaction 

Abbreviations

CO2

Carbon dioxide

DNA

Deoxyribonucleic acid

gfp

gfp is a gene which encodes for green fluorescent protein

gus

gus is a gene which encodes for β-glucuronidase

HCN

Hydrogen cyanide

mRNA

messenger RNA which is used as template for protein synthesis.

N

Nitrogen

N2

Atmospheric Nitrogen

NO2

Nitric oxide

nifHDK

These are set of genes which encodes structural part of nitrogenase, an enzyme which catalyzes nitrogen fixation.

PCR

Polymerase chain reaction

PGPB

Plant growth promoting bacteria

r DNA

ribosomal DNA encodes for rRNA, a structural component of ribosome

References

  1. Abeysingha NS, Weerarathne CS (2010) A preliminary study on quantification of biological nitrogen fixation in sugarcane grown in Sevanagala in Sri Lanka. J Nat Sci Found Sri Lanka 38:207–210. doi: 10.4038/jnsfsr.v38i3.2311 Google Scholar
  2. Abreu-Tarazi MF, Navarrete AA, Andreote FD, Almeida CV, Tsai SM, Almeida M (2010) Endophytic bacteria in long-term in vitro cultivated “axenic” pineapple microplants revealed by PCR-DGGE. World J Microbiol Biotechnol 26:555–560. doi: 10.1007/s11274-009-0191-3 CrossRefGoogle Scholar
  3. Akhtar MS, Siddiqui ZA (2010) Role of Plant growth promoting rhizobacteria in biocontrol of plant diseases and sustainable agriculture. In: Maheshwari DK (ed) Plant growth and health promoting bacteria, vol 18, Microbiology monographs. Springer, Berlin/Heidelberg, pp 157–196. doi: 10.1007/978-3-642-13612-2_7 CrossRefGoogle Scholar
  4. Ali SKZ, Sandhya V, Grover M, Kishore N, Rao LV, Venkateswarlu B (2009) Pseudomonas sp. strain AKM-P6 enhances tolerance of sorghum seedlings to elevated temperatures. Biol Fertil Soils 46:45–55. doi: 10.1007/s00374-009-0404-9 CrossRefGoogle Scholar
  5. America AHP, Cordewener JHG (2008) Comparative LC-MS: a landscape of peaks and valleys. Proteomics 8:731–749. doi: 10.1002/pmic.200700694 PubMedCrossRefGoogle Scholar
  6. Andreote FD, Rocha UN, Araujo WL, Azevedo JL, van Overbeek LS (2010) Effect of bacterial inoculation, plant genotype and developmental stage on root-associated and endophytic bacterial communities in potato (Solanum tuberosum). Antonie van Leeuwen 97:389–399. doi: 10.1007/s10482-010-9421-9 CrossRefGoogle Scholar
  7. Araujo WL, Marcon J, Maccheroni WJ, van Elsas JD, van Vuurde JWL, Azevedo JL (2002) Diversity of endophytic bacterial populations and their interaction with Xylella fastidiosa in citrus plants. Appl Environ Microbiol 68:4906–4914. doi: 10.1128/AEM.68.10.4906-4914.2002 PubMedCrossRefGoogle Scholar
  8. Audenaert K, Pattery T, Comelis P, Hofte M (2002) Induction of systemic resistance to Botrytis cinerea in tomato by Pseudomonas aeruginosa 7NSK2: role of salicylic acid, pyochelin, and pyocyanin. Mol Plant Microbe Interact 15:1147–1156. doi: 10.1094/MPMI.2002.15.11.1147 PubMedCrossRefGoogle Scholar
  9. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266. doi: 10.1146/annurev.arplant.57.032905.105159 PubMedCrossRefGoogle Scholar
  10. Baldani VLD, Baldani JI, Dobereiner J (2000) Inoculation of rice plants with the endophytic diazotrophs Herbaspirillum seropedicae and Burkholderia spp. Biol Fertil Soils 30:485–491. doi: 10.1007/s003740050027 CrossRefGoogle Scholar
  11. Bertalan M, Albano R, de Padua V, Rouws L, Rojas C, Hemerly A, Teixeira K, Schwab S, Araujo J, Oliveira A, França L, Magalhaes V, Alqueres S, Cardoso A, Almeida W, Loureiro MM, Nogueira E, Cidade D, Oliveira D, Simao T, Macedo J, Valadao A, Dreschsel M, Freitas F, Vidal M, Guedes H, Rodrigues E, Meneses C, Brioso P, Pozzer L, Figueiredo D, Montano H, Junior J, de Souza FG, Flores VMQ, Ferreira B, Branco A, Gonzalez P, Guillobel H, Lemos M, Seibel L, Macedo J, Alves-Ferreira M, Sachetto-Martins G, Coelho A, Santos E, Amaral G, Neves A, Pacheco AB, Carvalho D, Lery L, Bisch P, Rossle SC, Urmenyi T, Pereira AR, Silva R, Rondinelli E, von Kruger W, Martins O, Baldani JI, Ferreira PC (2009) Complete genome sequence of the sugarcane nitrogen-fixing endophyte Gluconacetobacter diazotrophicus Pal5. BMC Genomics 10:450. doi: 10.1186/1471-2164-10-450 PubMedCrossRefGoogle Scholar
  12. Bhatia S, Maheshwari DK, Dubey RC, Arora DS, Bajpai VK, Kang SC (2008) Beneficial effects of fluorescent Pseudomonads on seed germination, growth promotion, and suppression of charcoal rot in groundnut (Arachis hypogea L.). J Microbiol Biotechnol 18:1578–1583Google Scholar
  13. Bhattacharjee RB, Singh A, Mukhopadhyay SN (2008) Use of nitrogen-fixing bacteria as biofertiliser for non-legumes: prospects and challenges. Appl Microbiol Biotechnol 80:199–209. doi: 10.1007/s00253-008-1567-2 PubMedCrossRefGoogle Scholar
  14. Bilal R, Rasul G, Arshad M, Malik KA (1993) Attachment, colonization and proliferation of Azospirillum brasilense and Enterobacter spp. on root surface of grasses. World J Microbiol Biotechnol 9:63–69. doi: 10.1007/BF00656519 CrossRefGoogle Scholar
  15. Biswas JC, Ladha JK, Dazzo FB, Yanni YG, Rolfe BG (2000) Rhizobial inoculation influences seedling vigor and yield of rice. Agron J 92:880–886CrossRefGoogle Scholar
  16. Bohm M, Hurek T, Reinhold-Hurek B (2007) Twitching motility is essential for endophytic rice colonization by the N2-fixing endophyte Azoarcus sp. strain BH72. Mol Plant Microbe Interact 20:526–533. doi: 10.1094/MPMI-20-5-0526 PubMedCrossRefGoogle Scholar
  17. Borneman J, Skroch PW, O’Sullivan KM, Palus JM, Rumjanek NG, Jansen J, Nienhuis J, Triplett EW (1996) Molecular microbial diversity of an agricultural soil in Wisconsin. Appl Environ Microbiol 62:1935–1943PubMedGoogle Scholar
  18. Bothe H, Schmitz O, Yates MG, Newton WE (2010) Nitrogen fixation and hydrogen metabolism in cyanobacteria. Microbiol Mol Boil Rev 74:529–551. doi: 10.1128/MMBR.00033-10 CrossRefGoogle Scholar
  19. Bottini R, Cassan F, Piccoli P (2004) Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl Microbiol Biotechnol 65:497–503. doi: 10.1007/s00253-004-1696-1 PubMedCrossRefGoogle Scholar
  20. Burbano CS, Reinhold-Hurek B, Hurek T (2010) LNA-substituted degenerate primers improve detection of nitrogenase gene transcription in environmental samples. Environ Microbiol Rep 2:251–257. doi: 10.1111/j.1758-2229.2009.00107.x CrossRefGoogle Scholar
  21. Burdman S, Jurkevitch E, Okon Y (2000) Recent advances in the use of plant growth promoting rhizobacteria (PGPR) in agriculture. In: Rao NS, Dommergues YR (eds) Microbial interactions in agriculture and forestry. Science Publishers, Plymouth, pp 29–250Google Scholar
  22. Cartieaux F, Contesto C, Gallou A, Desbrosses G, Kopka J, Taconnat L, Renou JP, Touraine B (2008) Simultaneous interaction of Arabidopsis thaliana with Bradyrhizobium sp. Strain ORS278 and Pseudomonas syringae pv. tomato DC3000 leads to complex transcriptome changes. Mol Plant Microbe Interact 21:244–259. doi: 10.1094/MPMI-21-2-0244 PubMedCrossRefGoogle Scholar
  23. Castillo UF, Strobel GA, Ford EJ, Hess WM, Porter H, Jensen JB, Albert H, Robison R, Condron MAM, Teplow DB (2002) Munumbicins, wide-spectrum antibiotics produced by Streptomyces NRRL 30562, endophytic on Kennedia nigriscans. Microbiology 148:2675–2685PubMedGoogle Scholar
  24. Cazorla FM, Duckett SB, Bergstrom ET (2006) Biocontrol of Avocado dematophora root rot by the antagonistic Pseudomonas fluorescens PCL1606 correlates with the production of 2-hexyl 5-propyl resorcinol. Mol Plant Microbe Interact 19:418–428. doi: 10.1094/MPMI-19-0418 PubMedCrossRefGoogle Scholar
  25. Chaves DFS, Ferrer PP, de Souza EM, Gruz LM, Monteriro RA, de Oliveira PF (2007) A two-dimensional proteome reference map of Herbaspirillum seropedicae proteins. Proteomics 7:3759–3763. doi: 10.1002/pmic.200600859 PubMedCrossRefGoogle Scholar
  26. Chelius MK, Triplett EW (2000) Immunolocalization of dinitrogenase reductase produced by Klebsiella pneumoniae in association with Zea mays L. Appl Environ Microbiol 66:783–787. doi: 10.1128/AEM.66.2.783-787.2000 PubMedCrossRefGoogle Scholar
  27. Chen C, Belanger R, Benhamou N, Paulitz TC (2000) Defence enzymes induced in cucumber roots by treatment with plant growth-promoting rhizobacteria (PGPR) and Pythium aphanidermatum. Physiol Mol Plant Pathol 56:13–23. doi: 10.1006/pmpp.1999.0243 CrossRefGoogle Scholar
  28. Chen XH, Koumoutsi A, Scholz R, Eisenreich A, Schneider K, Heinemeyer I, Morgenstern B, Voss B, Hess WR, Reva O, Junge H, Voigt B, Jungblut PR, Vater J, Sussmuth R, Liesegang H, Strittmatter A, Gottschalk G, Borriss R (2007) Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nat Biotechnol 25:1007–1014. doi: 10.1038/nbt1325 PubMedCrossRefGoogle Scholar
  29. Cheng Z, Woody OZ, Song J, Glick BR, McConkey BJ (2009) Proteome reference map for the plant growth-promoting bacterium Pseudomonas putida UW4. Proteomics 9:4271–4274. doi: 10.1002/pmic.200900142 PubMedCrossRefGoogle Scholar
  30. Chi F, Shen SH, Cheng HP, Jing YX, Yanni YG, Dazzo FB (2005) Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Appl Environ Microbiol 71:7271–7278. doi: 10.1128/AEM.71.11.7271-7278.2005 PubMedCrossRefGoogle Scholar
  31. Chowdhury SP, Schmid M, Hartmann A, Tripathi AK (2007) Identification of diazotrophs in the culturable bacterial community associated with roots of Lasiurus sindicus, a perennial grass of Thar desert, India. Microb Ecol 54:82–90. doi: 10.1007/s00248-006-9174-1 PubMedCrossRefGoogle Scholar
  32. Cocking EC (2003) Endophytic colonization of plant roots by nitrogen-fixing bacteria. Plant Soil 252:169–175. doi: 10.1023/A:1024106605806 CrossRefGoogle Scholar
  33. Compant S, Duffy B, Nowak J, Clement C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959. doi: 10.1128/AEM.71.9.4951-4959.2005 PubMedCrossRefGoogle Scholar
  34. Compant S, Kaplan H, Sessitsch A, Nowak J, Barka EA, Clement C (2008) Endophytic colonization of Vitis vinifera L. by Burkholderia phytofirmans strain PsJN: from the rhizosphere to inflorescence tissues. FEMS Microbiol Ecol 63:84–93. doi: 10.1111/j.1574-6941.2007.00410.x PubMedCrossRefGoogle Scholar
  35. Compant S, Clement C, Sessitsch A (2010a) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678. doi: 10.1016/j.soilbio.2009.11.024 CrossRefGoogle Scholar
  36. Compant S, van der Heijden MGA, Sessitsch A (2010b) Climate change effects on beneficial plant microorganism interactions. FEMS Microbiol Ecol 73:197–214. doi: 10.1111/j.1574-6941.2010.00900.x PubMedGoogle Scholar
  37. Compant S, Mitter B, Colli-Mull JG, Gangl H, Sessitsch A (2011) Endophytes of grapevine flowers, berries, and seeds: identification of cultivable bacteria, comparison with other plant parts, and visualization of niches of colonization. Microb Ecol 62:188–197. doi: 10.1007/s00248-011-9883-y PubMedCrossRefGoogle Scholar
  38. Croes CL, Moens S, van Bastelaere E, Vanderleyden J, Michiels KW (1993) The polar flagellum mediates Azospirillum brasilense adsorption to wheat roots. J Gen Microbiol 139:960–967. doi: 10.1099/00221287-139-9-2261 Google Scholar
  39. de Lorenzo V (1994) Designing microbial system for gene expression in the field. Trends Biotechnol 12:365–371. doi: 10.1016/0167-7799(94)90037-X PubMedCrossRefGoogle Scholar
  40. de Morais RF, Quesada DM, Reis VM, Urquiaga S, Alves BJR, Boddey RM (2012) Contribution of biological nitrogen fixation to elephant grass (Pennisetum purpureum Schum.). Plant Soil 356:23–34. doi: 10.1007/s11104-011-0944-2 CrossRefGoogle Scholar
  41. de Salamone IEG, Salvo LPD, Ortega JSE, Sorte PMFB, 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 336:351–362. doi: 10.1007/s11104-010-0487-y CrossRefGoogle Scholar
  42. Deng Y, Zhu Y, Wang P, Zhu L, Zheng J, Li R, Ruan L, Peng D, Sun M (2011) Complete Genome Sequence of Bacillus subtilis BSn5, an endophytic bacterium of Amorphophallus konjac with antimicrobial activity to plant pathogen Erwinia carotovora subsp. carotovora. J Bacteriol 193:2070–2071. doi: 10.1128/JB.00129-11 PubMedCrossRefGoogle Scholar
  43. Deslippe JR, Egger KN (2006) Molecular diversity of nifH genes from bacteria associated with high arctic dwarf shrubs. Microb Ecol 51:516–525. doi: 10.1007/s00248-006-9070-8 PubMedCrossRefGoogle Scholar
  44. Diallo MD, Reinhold-Hurek B, Hurek T (2008) Evaluation of PCR primers for universal nifH gene targeting and for assessment of transcribed nifH pools in roots of Oryza longistaminata with and without low nitrogen input. FEMS Microbiol Ecol 65:220–228. doi: 10.1111/j.1574-6941.2008.00545.x CrossRefGoogle Scholar
  45. Dobereiner J, Reis VM, Paula MA, Olivares F (1993) Endophytic diazotrophs in sugarcane cereals and tuber crops. In: Palacios R, Moor J, Newton WE (eds) New horizons in nitrogen fixation. Kluwer, Dordrecht, pp 671–674Google Scholar
  46. Dong Y, Iniguez AL, Ahmer BMM, Triplett EW (2003) Kinetics and strain specificity of rhizosphere and endophytic colonization by enteric bacteria on seedlings of Medicago sativa and Medicago truncatula. Appl Environ Microbiol 69:1783–1790. doi: 10.1128/AEM.69.3.1783-1790.2003 PubMedCrossRefGoogle Scholar
  47. Dorr J, Hurek T, Reinhold-Hurek B (1998) Type IV pili are involved in plant-microbe and fungus-microbe interactions. Mol Microbiol 30:7–17. doi: 10.1046/j.1365-2958.1998.01010.x PubMedCrossRefGoogle Scholar
  48. dos Reis FB Jr, Reis VM, Urquiaga S, Dobereiner J (2000) Influence of fertilization on the population of diazotrophic bacteria Herbaspirillum spp. and Acetobacter diazotrophicus in sugar cane (Saccharum spp.). Plant Soil 219:153–159. doi: 10.1023/A:1004732500983 CrossRefGoogle Scholar
  49. Duijff BJ, Gianinazzi-Pearson V, Lemanceau P (1997) Involvement of the outer membrane lipopolysaccharides in the endophytic colonization of tomato roots by biocontrol Pseudomonas fluorescens strain WCS417r. New Phytol 135:325–334. doi: 10.1046/j.1469-8137.1997.00646.x CrossRefGoogle Scholar
  50. Eckert B, Weber OB, Kirchhof G, Halbritter A, Stoffels M, Hartmann A (2001) Azospirillum doebereinerae sp. nov., a nitrogen-fixing bacterium associated with the C4-grass Miscanthus. Int J Syst Evol Microbiol 51:17–26PubMedGoogle Scholar
  51. Egamberdieva D (2009) Alleviation of salt stress by plant growth regulators and IAA producing bacteria in wheat. Acta Physiol Plant 31:861–864. doi: 10.1007/s11738-009-0297-0 CrossRefGoogle Scholar
  52. Egener T, Martin DE, Sarkar A, Reinhold-Hurek B (2001) Role of a ferredoxin gene cotranscribed with the nifHDK operon in N2 fixation and nitrogenase “switch-off” of Azoarcus sp. strain BH72. J Bacteriol 183:3752–3760. doi: 10.1128/JB.183.12.3752-3760.2001 PubMedCrossRefGoogle Scholar
  53. Feng Y, Shen D, Song W (2006) Rice endophyte Pantoea agglomerans YS19 promotes host plant growth and affects allocations of host photosynthates. J Appl Microbiol 100:938–945. doi: 10.1111/j.1365-2672.2006.02843.x PubMedCrossRefGoogle Scholar
  54. Figueiredo MVB, Martinez CR, Burity HA, Chanway CP (2008) Plant growth-promoting rhizobacteria for improving nodulation and nitrogen fixation in the common bean (Phaseolus vulgaris L.). World J Microbiol Biotechnol 24:1187–1193. doi: 10.1007/s11274-007-9591-4 CrossRefGoogle Scholar
  55. Forchetti G, Masciarelli O, Izaguirre MJ, Alemano S, Alvarez D, Abdala G (2010) Endophytic bacteria improve seedling growth of sunflower under water stress, produce salicylic acid, and inhibit growth of pathogenic fungi. Curr Microbiol 61:485–493. doi: 10.1007/s00284-010-9642-1 PubMedCrossRefGoogle Scholar
  56. Fouts DE, Tyler HL, DeBoy RT, Daugherty S, Ren Q, Badger JH, Durkin AS, Huot H, Srivastava S, Kothari S, Dodson RJ, Mohamoud Y, Khouri H, Roesch LFW, Krogfelt KA, Struve C, Triplett EW, Mathe BA (2008) Complete Genome sequence of the N2-fixing broad host range endophyte Klebsiella pneumoniae 342 and virulence predictions verified in mice. PLoS Genet 4:e1000141. doi: 10.1371/journal.pgen.1000141 PubMedCrossRefGoogle Scholar
  57. Franche C, Lindstrom K, Elmerich C (2009) Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321:35–59. doi: 10.1007/s11104-008-9833-8 CrossRefGoogle Scholar
  58. Fridlender M, Inbar J, Chet I (1993) Biological control of soilborne plant pathogens by a β-1,3-glucanase-producing Pseudomonas cepacia. Soil Biol Biochem 25:1211–1221. doi: 10.1016/0038-0717(93)90217-Y CrossRefGoogle Scholar
  59. Fuentes-Ramirez LE, Caballero-Mellado J, Sepulveda J, Martinez-Romero E (1999) Colonization of sugarcane by Acetobacter diazotrophicus is inhibited by high N-fertilization. FEMS Microbiol Lett 29:117–128. doi: 10.1111/j.1574-6941.1999.tb00603.x Google Scholar
  60. Glick BR, Cheng Z, Czarny J, Duan J (2007) Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur J Plant Pathol 119:329–339. doi: 10.1007/s10658-007-9162-4 CrossRefGoogle Scholar
  61. Godfrey SAC, Mansfield JW, Corry DS, Lovell HC, Jackson RW, Arnold DL (2010) Confocal imaging of Pseudomonas syringae pv. phaseolicola colony development in bean reveals reduced multiplication of strains containing the genomic island PPHGI-1. Mol Plant Microbe Interact 23:1294–1302. doi: 10.1094/MPMI-05-10-0114 PubMedCrossRefGoogle Scholar
  62. Gong W, He K, Covington M, Dinesh-Kumar SP, Snyder M, Harmer SL, Zhu YX, Deng XW (2008) The development of protein microarrays and their applications in DNA-protein and protein-protein interaction analyses of Arabidopsis transcription factors. Mol Plant 1:27–41. doi: 10.1093/mp/ssm009 PubMedCrossRefGoogle Scholar
  63. Gough C, Galera C, Vasse J, Webster G, Cocking EC, Denarie J (1997) Specific flavonoids promote intercellular root colonization of Arabidopsis thaliana by Azorhizobium caulinodans ORS571. Mol Plant Microbe Interact 10:560–570. doi: 10.1094/MPMI.1997.10.5.560 PubMedCrossRefGoogle Scholar
  64. Govindarajan M, Balandreau J, Kwon SW, Weon HY, Lakshminarasimhan C (2008) Effects of the inoculation of Burkholderia vietnamiensis and related endophytic diazotrophic bacteria on grain yield of rice. Microb Ecol 55:21–37. doi: 10.1007/s00248-007-9247-9 PubMedCrossRefGoogle Scholar
  65. Grange L, Hungria M (2004) Genetic diversity of indigenous common bean (Phaseolus vulgaris) rhizobia on two Brazilian ecosystem. Soil Biol Biochem 36:1389–1398. doi: 10.1016/j.soilbio.2004.03.005 CrossRefGoogle Scholar
  66. Gyaneshwar P, James EK, Reddy PM, Ladha JK (2002) Herbaspirillum colonization increases growth and nitrogen accumulation in aluminium-tolerant rice varieties. New Phytol 154:131–145. doi: 10.1046/j.1469-8137.2002.00371.x CrossRefGoogle Scholar
  67. Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914. doi: 10.1139/m97-131 CrossRefGoogle Scholar
  68. Han J, Choi HK, Lee SW, Orwin PM, Kim J, LaRoe SL, Kim TG, O’Neil J, Leadbetter JR, Lee SY, Hur CG, Spain JC, Ovchinnikova G, Goodwin L, Han C (2011) Complete genome sequence of the metabolically versatile plant growth-promoting endophyte Variovorax paradoxus S110. J Bacteriol 193:1183–1190. doi: 10.1128/JB.00925-10 PubMedCrossRefGoogle Scholar
  69. Hardoim PR, van Overbeek LS, Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471. doi: 10.1016/j.tim.2008.07.008 PubMedCrossRefGoogle Scholar
  70. Hartmann A, Stoffels M, Eckert B, Kirchhof G, Schloter M (2000) Analysis of the presence and diversity of diazotrophic endophytes. In: Triplett EW (ed) Prokaryotic nitrogen fixation: a model system for the analysis of a biological process. Horizon Scientific Press, Wymondham, UK, pp 727–736Google Scholar
  71. Hawes MC, Brigham LA, Wen F, Woo HH, Zhu Y (1998) Function of root border cells in plant health: pioneers in the rhizosphere. Annu Rev Phytopathol 36:311–327. doi: 10.1146/annurev.phyto.36.1.311 PubMedCrossRefGoogle Scholar
  72. Hoflich G, Wiehe W, Hecht-Buchholz C (1995) Rhizosphere colonization of different crops with growth promoting Pseudomonas and Rhizobium bacteria. Microbiol Res 150:139–147. doi: 10.1016/S0944-5013(11)80048-0 CrossRefGoogle Scholar
  73. Hurek T, Reinhold-Hurek B (2003) Azoarcus sp. strain BH72 as a model for nitrogen-fixing grass endophytes. J Biotechnol 106:169–178. doi: 10.1016/j.jbiotec.2003.07.010 PubMedCrossRefGoogle Scholar
  74. Hurek T, Wagner B, Reinhold-Hurek B (1997) Identification of N2-fixing plant and fungus associated Azoarcus species by PCR-based genomic fingerprints. Appl Environ Microbiol 63:4331–4339PubMedGoogle Scholar
  75. Iniguez AL, Dong Y, Triplett EW (2004) Nitrogen fixation in wheat provided by Klebsiella pneumoniae 342. Mol Plant Microbe Interact 17:1078–1085. doi: 10.1094/MPMI.2004.17.10.1078 PubMedCrossRefGoogle Scholar
  76. Iniguez AL, Dong Y, Carter HD, Ahmer BMM, Stone JM, Triplett EW (2005) Regulation of enteric endophytic bacterial colonization by plant defenses. Mol Plant Microbe Interact 18:169–178. doi: 10.1094/MPMI-18-0169 PubMedCrossRefGoogle Scholar
  77. Islam R, Trivedi P, Madhaiyan M, Seshadri S, Lee G, Yang J, Kim Y, Kim M, Han G, Chauhan PS, Sa T (2010) Isolation, enumeration, and characterization of diazotrophic bacteria from paddy soil sample under long-term fertilizer management experiment. Biol Fertil Soils 46:261–269. doi: 10.1007/s00374-009-0425-4 CrossRefGoogle Scholar
  78. Izquierdo JA, Nusslein K (2006) Distribution of extensive nifH gene diversity across physical soil microenvironments. Microb Ecol 51:441–452. doi: 10.1007/s00248-006-9044-x PubMedCrossRefGoogle Scholar
  79. James EK, Olivares FL (1998) Infection and colonization of sugarcane and other gramineous plants by endophytic diazotrophs. Crit Rev Plant Sci 17:77–119. doi: 10.1080/07352689891304195 CrossRefGoogle Scholar
  80. James EK, Olivares FL, de Oliveira ALM, dos Reis Jr FB, da Silva LG, Reis M (2001) Further observations on the interaction between sugarcane and Gluconoacetobacter diazotrophicus under laboratory and greenhouse conditions. J Exp Bot 52:747–760. doi: 10.1093/jexbot/52.357.747 PubMedGoogle Scholar
  81. Jha PN, Kumar A (2007) Endophytic colonization of Typha australis by a plant growth-promoting bacterium Klebsiella oxytoca strain GR-3. J Appl Microbiol 103:1311–1320. doi: 10.1111/j.1365-2672.2007.03383.x PubMedCrossRefGoogle Scholar
  82. Jha P, Kumar A (2009) Characterization of novel plant growth promoting endophytic bacterium Achromobacter xylosoxidans from wheat plant. Microb Ecol 58:179–188. doi: 10.1007/s00248-009-9485-0 PubMedCrossRefGoogle Scholar
  83. Jousset A, Rochat L, Lanoue A, Bonkowski M, Keel C, Scheu S (2011) Plants respond to pathogen infection by enhancing the antifungal gene expression of root-associated bacteria. Mol Plant Microbe Interact 24:352–358. doi: 10.1094/MPMI-09-10-0208 PubMedCrossRefGoogle Scholar
  84. Kaneko T, Minamisawa K, Isawa T, Nakatsukasa H, Mitsui H, Kawaharada Y, Nakamura Y, Watanabe A, Kawashima K, Ono A, Shimizu Y, Takahashi C, Minami C, Fujishiro T, Kohara M, Katoh M, Nakazaki N, Nakayama S, Yamada M, Tabata S, Sato S (2010) Complete genomic structure of the cultivated rice endophyte Azospirillum sp. B510. DNA Res 17:37–50. doi: 10.1093/dnares/dsp026 PubMedCrossRefGoogle Scholar
  85. Kannan V, Sureendar R (2009) Synergistic effect of beneficial rhizosphere microflora in biocontrol and plant growth promotion. J Basic Microbiol 49:158–164. doi: 10.1002/jobm.200800011 PubMedCrossRefGoogle Scholar
  86. Kaur R, Macleod J, Foley W, Nayudu M (2006) Gluconic acid: an antifungal agent produced by Pseudomonas species in biological control of take-all. Phytochemistry 67:595–604. doi: 10.1016/j.phytochem.2005.12.011 PubMedCrossRefGoogle Scholar
  87. Khammas KM, Kaiser P (1991) Characterization of a pectinolytic activity in Azospirillum irakense. Plant Soil 137:75–79. doi: 10.1007/BF02187435 CrossRefGoogle Scholar
  88. Kiely PD, Haynes JM, Higgins CH, Franks A, Mark GL, Morrissey JP, O’Gara F (2006) Exploiting new systems-based strategies to elucidate plant-bacterial interactions in the rhizosphere. Microb Ecol 51:257–266. doi: 10.1007/s00248-006-9019-y PubMedCrossRefGoogle Scholar
  89. King RJ, Short KA, Seidler RJ (1991) Assay for detection and enumeration of genetically engineered microorganisms which is based on the activity of a deregulated 2,4-dichlorophenoxyacetate monooxygenase. Appl Environ Microbiol 57:1790–1792PubMedGoogle Scholar
  90. Kirchhof G, Reis VM, Baldani JI, Eckert B, Dobereiner J, Hartmann A (1997) Occurrence, physiological and molecular analysis of endophytic diazotrophic bacteria in gramineous energy plants. Plant Soil 194:45–55. doi: 10.1023/A:1004217904546 CrossRefGoogle Scholar
  91. Kirk JL, Beaudette LA, Hart M, Moutoglis P, Klironomos JN, Lee H, Trevors JT (2004) Methods of studying soil microbial diversity. J Microbiol Methods 58:169–188. doi: 10.1016/j.mimet.2004.04.006 PubMedCrossRefGoogle Scholar
  92. Knauth S, Hurek T, Brar D, Reinhold-Hurek B (2005) Influence of different Oryza cultivars on expression of nifH gene pools in roots of rice. Environ Microbiol 7:1725–1733. doi: 10.1111/j.1462-2920.2005.00841.x PubMedCrossRefGoogle Scholar
  93. Kohler J, Hernandez JA, Caravaca F, Roldan A (2008) Plant-growth-promoting rhizobacteria and arbuscular mycorrhizal fungi modify alleviation biochemical mechanisms in water-stressed plants. Funct Plant Biol 35:141–151. doi: 10.1071/FP07218 CrossRefGoogle Scholar
  94. Kovach ME, Phillips RW, Elzer PH, Roop RM, Peterson KM (1994) pBBR1MCS: a broad-host-range cloning vector. Biotechniques 16:800–802PubMedGoogle Scholar
  95. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, Roop RM, Peterson KM (1995) Four new derivatives of the broad-host range cloning vector pBBR1MCS, carrying antibiotic-resistance cassettes. Gene 166:175–176. doi: 10.1016/0378-1119(95)00584-1 PubMedCrossRefGoogle Scholar
  96. Kraepiel AML, Bellenge JP, Wichard T, Morel FMM (2009) Multiple roles of siderophores in free-living nitrogen-fixing bacteria. Biometals 22:573–581. doi: 10.1007/s10534-009-9222-7 PubMedCrossRefGoogle Scholar
  97. Krause A, Ramakumar A, Bartels D, Battistoni F, Bekel T, Bosh J, Bohm M, Friedrich F, Hurek T, Krause L, Linke B, McHardy AC, Sarkar A, Schneiker S, Syed AA, Thauer R, Vorholter FJ, Weinder S, Puhler A, Reinhold-Hurek B, Kaiser O, Goesmann A (2006) Complete genome of the mutualistic, N2-fixing grass endophyte Azoarcus sp. strain BH72. Nat Biotechnol 24:1385–1391. doi: 10.1038/nbt1243 PubMedCrossRefGoogle Scholar
  98. Ladha JK, Reddy PM (2000) The quest for nitrogen fixation in rice. In: Proceeding of the third working group meeting on assessing opportunities for nitrogen fixation in rice, 9–12 Aug 1999. International Rice Research Institute, Makati City, pp 354Google Scholar
  99. Lery LMS, Coelho A, von Kruger WMA, Goncalves MSM, Santos MF, Valente RH, Santos EO, Rocha SLG, Perales J, Domont GB, Teixeira KRS, Bisch PM (2008) Protein expression profile of Gluconacetobacter diazotrophicus PAL5, a sugarcane endophytic plant growth-promoting bacterium. Proteomics 8:1631–1644. doi: 10.1002/pmic.200700912 PubMedCrossRefGoogle Scholar
  100. Li CH, Zhao MW, Tang CM, Li SP (2010) Population dynamics and identification of endophytic bacteria antagonistic toward plant-pathogenic fungi in cotton root. Microb Ecol 59:344–356. doi: 10.1007/s00248-009-9570-4 PubMedCrossRefGoogle Scholar
  101. Lin L, Guo W, Xing Y, Zhang X, Li Z, Hu C, Li S, Li Y, An Q (2012) The actinobacterium Microbacterium sp. 16SH accepts pBBR1-based pPROBE vectors, forms biofilms, invades roots, and fixes N2 associated with micropropagated sugarcane plants. Appl Microbiol Biotechnol 93:1185–1195. doi: 10.1007/s00253-011-3618-3 PubMedCrossRefGoogle Scholar
  102. Lopez-Bucio J, Campos-Cuevas JC, Hernandez-Calderon E, Velasquez-Becerra C, Farias-Rodriguez R, Macias-Rodriguez LI, Valencia-Cantero E (2007) Bacillus megaterium rhizobacteria promote growth and alter root-system architecture through an auxin- and ethylene-independent signaling mechanism in Arabidopis thaliana. Mol Plant Microbe Interact 20:207–217. doi: 10.1094/MPMI-20-2-0207 PubMedCrossRefGoogle Scholar
  103. Lovell CR, Piceno YM, Quattro JM, Bagwell CE (2000) Molecular analysis of diazotroph diversity in the rhizosphere of the smooth Cordgrass, Spartina alterniflora. Appl Environ Microbiol 66:3814–3822. doi: 10.1128/AEM.66.9.3814-3822.2000 PubMedCrossRefGoogle Scholar
  104. Lucy M, Reed E, Glick BR (2004) Applications of free living plant growth promoting rhizobacteria. Antonie Van Leeuwenhoek 86:1–25. doi: 10.1023/B:ANTO.0000024903.10757.6e PubMedCrossRefGoogle Scholar
  105. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting Rhizobacteria. Annu Rev Microbiol 63:541–556. doi: 10.1146/annurev.micro.62.081307.162918 PubMedCrossRefGoogle Scholar
  106. Lugtenberg BJJ, Dekkers LC, Bloemberg GV (2001) Molecular determinants of rhizosphere colonization by Pseudomonas. Annu Rev Phytopathol 39:461–490. doi: 10.1146/annurev.phyto.39.1.461 PubMedCrossRefGoogle Scholar
  107. Manefield M, Whiteley AS, Griffiths RI, Bailey MJ (2002) RNA stable isotope probing, a novel means of linking microbial community function to phylogeny. Appl Environ Microbiol 68:5367–5373. doi: 10.1128/AEM.68.11.5367-5373.2002 PubMedCrossRefGoogle Scholar
  108. Marulanda A, Barea JM, Azcon R (2009) Stimulation of plant growth and drought tolerance by native microorganisms (AM fungi and bacteria) from dry environments: mechanisms related to bacterial effectiveness. J Plant Growth Regul 28:115–124. doi: 10.1007/s00344-009-9079-6 CrossRefGoogle Scholar
  109. Miche L, Battistoni F, Gernmer S, Belghazi M, Reinhold-Hurek B (2006) Upregulation of jasmonate-inducible defense proteins and differential colonization of roots of Oryza sativa cultivars with the endophyte Azoarcus sp. Mol Plant Microbe Interact 19:502–511. doi: 10.1094/MPMI-19-0502 PubMedCrossRefGoogle Scholar
  110. 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, Manila, pp 191–204Google Scholar
  111. Muthukumarasamy R, Cleenwerck I, Revathi G, Vadivelu M, Janssens D, Hoste B, Gum KU, Park K, Son CY, Sa T, Caballero-Mellado J (2005) Natural association of Gluconoacetobacter diazotrophicus and diazotrophic Acetobacter peroxydans with wetland rice. Syst Appl Microbiol 28:277–286. doi: 10.1016/j.syapm.2005.01.006 PubMedCrossRefGoogle Scholar
  112. Muthukumarasamy R, Kang UG, Park KD, Jeon WT, Park CY, Cho YS, Kwon SW, Song J, Roh DH, Revathi G (2007) Enumeration, isolation and identification of diazotrophs from Korean wetland rice varieties grown with long-term application of N and compost and their short-term inoculation effect on rice plants. J Appl Microbiol 102:981–991. doi: 10.1111/j.1365-2672.2006.03157.x PubMedGoogle Scholar
  113. Nishizawa T, Tago K, Oshima S, Hattori M, Ishii S, Otsuka S, Senoo K (2012) Complete genome sequence denitrifying and N2O-reducing bacterium Azoarcus sp. strain KH32C. J Bacteriol 194:1255. doi: 10.1128/JB.06618-11 PubMedCrossRefGoogle Scholar
  114. Niu DD, Liu HX, Jiang CH, Wang YP, Jin HL, Guo JH (2011) The plant growth-promoting rhizobacterium Bacillus cereus AR156 induces systemic resistance in Arabidopsis thaliana, by simultaneously activating salicylate- and jasmonate/ethylene-dependent signaling pathways. Mol Plant Microbe Interact 24:533–542. doi: 10.1094/MPMI-09-10-0213 PubMedCrossRefGoogle Scholar
  115. Nogales B, Moore ERB, Llobet-Brossa E, Rossello-Mora R, Amann R, Timmis KN (2001) Combined use of 16S ribosomal DNA and 16S rRNA to study the bacterial community of polychlorinated biphenyl-polluted soil. Appl Environ Microbiol 67:1874–1884. doi: 10.1128/AEM.67.4.1874-1884.2001 PubMedCrossRefGoogle Scholar
  116. O’Callaghan KJ, Stone PJ, Hu X, Griffiths DW, Davey MR, Cocking EC (2000) Effects of glucosinolates and flavonoids on colonization of the roots of Brassica napus by Azorhizobium caulinodans ORS571. Appl Environ Microbiol 66:2185–2191. doi: 10.1128/AEM.66.5.2185-2191.2000 PubMedCrossRefGoogle Scholar
  117. Ordentlich A, Elad Y, Chet I (1988) The role of chitinase of Serratia marcescens in biocontrol of Sclerotium rolfsii. Phytopathology 78:84–88. doi: 10.1094/Phyto-78-84 Google Scholar
  118. Ovreas L, Torsvik VV (1998) Microbial diversity and community structure in two different agricultural soil communities. Microb Ecol 36:303–315. doi: 10.1007/s002489900117 PubMedCrossRefGoogle Scholar
  119. Pandey A, Mann M (2000) Proteomics to study genes and genomes. Nature 405:837–846. doi: 10.1038/35015709 PubMedCrossRefGoogle Scholar
  120. Pedrosa FO, Monteiro RA, Wassem R, Cruz LM, Ayub RA, Colauto NB, Fernandez MA, Fungaro MHP, Grisard EC, Hungria M, Madeira HMF, Nodari RO, Osaku CA, Petzl-Erler ML, Terenzi H, Vieira LGE, Steffens MBR, Weiss VA, Pereira LFP, Almeida MIM, Alves LR, Marin A, Araujo LM, Balsanelli E, Baura VA, Chubatsu LS, Faoro H, Favetti A, Friedermann G, Glienke C, Karp S, Kava-Cordeiro V, Raitzz RT, Ramos HJO, Ribeiro EMSF, Rigo LU, Rocha SN, Schwab S, Silva AG, Souza EM, Tadra-Sfeir MZ, Torres RA, Dabul ANG, Soares MAM, Gasques LS, Gimenes CCT, Valle JS, Ciferri RR, Correa LC, Murace NK, Pamphile JA, Patussi EV, Prioli AJ, Prioli SMA, Rocha CLMSC, Arantes OMN, Furlaneto MC, Godoy LP, Oliveira CEC, Satori D, Vilas-Boas LA, Watanabe MAE, Dambros BP, Guerra MP, Mathioni SM, Santos KL, Steindel M, Vernal J, Barbellos FG, Campo RJ, Chueira LMO, Nicholas MF, Pereira-Ferrari L, da Conceicao Silva JL, Gioppa NMR, Margarido VP, Menck-Soares MA, Pinto FGS, Simao RDCG, Takahashi EK, Yates MG, Souza EM (2011) Genome of Herbaspirillum seropedicae strain SmR1, a specialized diazotrophic endophyte of tropical grasses. PLoS Genet 7:e1002064. doi: 10.1371/journal.pgen.1002064 PubMedCrossRefGoogle Scholar
  121. Pilhofer M, Pavlekovic M, Lee NM, Ludwig W, Schleifer KH (2009) Fluorescence in situ hybridization for intracellular localization of nifH mRNA. Syst Appl Microbiol 32:186–192. doi: 10.1016/j.syapm.2008.12.007 PubMedCrossRefGoogle Scholar
  122. Pleban S, Chernin L, Chet I (1997) Chitinolytic activity of an endophytic strain of Bacillus cereus. Lett Appl Microbiol 25:284–288. doi: 10.1046/j.1472-765X.1997.00224.x PubMedCrossRefGoogle Scholar
  123. Preston GM, Bertrand N, Rainey PB (2001) Type III secretion in plant growth-promoting Pseudomonas fluorescens SBW25. Mol Microbiol 41:999–1014. doi: 10.1046/j.1365-2958.2001.02560.x PubMedCrossRefGoogle Scholar
  124. Prieto P, Schiliro E, Maldonado-Gonzalez MM, Valderrama R, Barroso-Albarracin JB, Mercado-Blanco J (2011) Root hairs play a key role in the endophytic colonization of olive roots by Pseudomonas spp. with biocontrol activity. Microb Ecol 62:435–445. doi: 10.1007/s00248-011-9827-6 PubMedCrossRefGoogle Scholar
  125. Rabus R, Kube M, Heider J, Beck A, Heitmann K, Widdel F, Reinhardt R (2005) The genome sequence of an anaerobic aromatic-degrading denitrifying bacterium strain EbN1. Arch Microbiol 183:27–36. doi: 10.1007/s00203-004-0742-9 PubMedCrossRefGoogle Scholar
  126. Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149. doi: 10.1016/j.tibtech.2009.12.002 PubMedCrossRefGoogle Scholar
  127. Ramos HJO, Roncato-Maccari LDB, Souza EM, Soares-Ramos JR, Hungria M, Pedrosa FO (2002) Monitoring Azospirillum-wheat interactions using the gfp and gusA genes constitutively expressed from a new broad-host range vector. J Biotechnol 97:243–252. doi: 10.1016/S0168-1656(02)00108-6 PubMedCrossRefGoogle Scholar
  128. Rasche F, Lueders T, Schloter M, Schaefer S, Buegger F, Gattinger A, Hood-Nowotny RC, Sessitsch A (2009) DNA-based stable isotope probing enables the identification of active bacterial endophytes in potatoes. New Phytol 181:802–807. doi: 10.1111/j.1469-8137.2008.02744.x PubMedCrossRefGoogle Scholar
  129. Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Mol Biol Evol 21:541–554. doi: 10.1093/molbev/msh047 PubMedCrossRefGoogle Scholar
  130. Reinhold-Hurek B, Hurek T (1998) Interactions of gramineous plants with Azoarcus spp. and other diazotrophs: identification, localization and perspectives to study their function. Crit Rev Plant Sci 17:29–54. doi: 10.1080/07352689891304186 CrossRefGoogle Scholar
  131. Reinhold-Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Curr Opin Plant Biol 14:435–443. doi: 10.1016/j.pbi.2011.04.004 PubMedCrossRefGoogle Scholar
  132. Reinhold-Hurek B, Maes T, Gemmer S, Montagu MV, Hurek T (2006) An endoglucanase is involved in infection of rice roots by the not-cellulose-metabolizing endophyte Azoarcus Sp. strain BH72. Mol Plant Microbe Interact 19:181–188. doi: 10.1094/MPMI-19-01810 PubMedCrossRefGoogle Scholar
  133. Reuber TL, Long S, Walker GC (1991) Regulation of Rhizobium meliloti exo genes in free-living cells and in planta examined by using TnphoA fusions. J Bacteriol 173:426–434PubMedGoogle Scholar
  134. Rochat L, Pechy-Tarr M, Baehler E, Maurhofer M, Keel C (2010) Combination of fluorescent reporters for simultaneous monitoring of root colonization and antifungal gene expression by a biocontrol Pseudomonad on cereals with Flow cytometry. Mol Plant Microbe Interact 23:949–961. doi: 10.1094/MPMI-23-7-0949 PubMedCrossRefGoogle Scholar
  135. Roe MR, Griffin TJ (2006) Gel-free mass spectrometry-based high throughput proteomics: tools for studying biological response of proteins and proteomes. Proteomics 6:4678–4687. doi: 10.1002/pmic.200500876 PubMedCrossRefGoogle Scholar
  136. Rosado AS, Duarte GF, Seldin L, Elsas JDV (1998) Genetic Diversity of nifH gene sequences in Paenibacillus azotofixans strains and soil samples analyzed by Denaturing gradient gel electrophoresis of PCR-amplified gene fragments. Appl Environ Microbiol 64:2770–2779PubMedGoogle Scholar
  137. Rosenblueth M, Martinez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact 19:827–837. doi: 10.1094/MPMI-19-0827 PubMedCrossRefGoogle Scholar
  138. Rothballer M, Eckert B, Schmid M, Fekete A, Schloter M, Lehner A, Pollmann S, Hartmann A (2008) Endophytic root colonization of gramineous plants by Herbaspirillum frisingense. FEMS Microbiol Ecol 66:85–95. doi: 10.1111/j.1574-6941.2008.00582.x PubMedCrossRefGoogle Scholar
  139. Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9. doi: 10.1111/j.1574-6968.2007.00918.x PubMedCrossRefGoogle Scholar
  140. Ryu RJ, Patten CL (2008) Aromatic amino acid-dependent expression of indole-3-pyruvate decarboxylase is regulated by TyrR in Enterobacter cloacae UW5. J Bacteriol 190:7200–7208. doi: 10.1128/JB.00804-08 PubMedCrossRefGoogle Scholar
  141. Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Pare PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026. doi: 10.1104/pp.103.026583 PubMedCrossRefGoogle Scholar
  142. Saleh SS, Glick BR (2001) Involvement of gacS and rpoS in enhancement of the plant growth-promoting capabilities of Enterobacter cloacae CAL2 and UW4. Can J Microbiol 47:698–705. doi: 10.1139/cjm-47-8-698 PubMedGoogle Scholar
  143. Schloss PD, Handelsman J (2003) Biotechnological prospects from metagenomics. Curr Opin Biotechnol 14:303–310. doi: 10.1016/S0958-1669(03)00067-3 PubMedCrossRefGoogle Scholar
  144. Schmidt MA, Souza EM, Baura V, Wassem R, Yates MG, Pedrosa FO, Monteiro RA (2011) Evidence for the endophytic colonization of Phaseolus vulgaris (common bean) roots by the diazotroph Herbaspirillum seropedicae. Braz J Med Biol Res 44:182–185. doi: 10.1590/S0100-879X2011007500004 PubMedCrossRefGoogle Scholar
  145. Schwab S, Ramos HJ, Souza EM, Pedrosa FO, Yates MG, Chubatsu LS, Rigo LU (2007) Identification of NH4+-regulated genes of Herbaspirillum seropedicae by random insertional mutagenesis. Arch Microbiol 187:379–386. doi: 10.1007/s00203-006-0202-9 PubMedCrossRefGoogle Scholar
  146. Serrato RV, Sassaki GL, Cruz LM, Carlson RW, Muszynski A, Monteiro RA, Pedrosa FO, Souza EM, Iacomini M (2010) Chemical composition of lipopolysaccharides isolated from various endophytic nitrogen-fixing bacteria of the genus Herbaspirillum. Can J Microbiol 56:342–347. doi: 10.1139/W10-011 PubMedCrossRefGoogle Scholar
  147. Setubal JC, dos Santos P, Goldman BS, Ertesvag H, Espin G, Rubio LM, Valla S, Almeida NF, Balasubramanian D, Cromes L, Curatti L, Du Z, Godsy E, Goodner B, Hellner-Burris K, Hernandez JA, Houmiel K, Imperial J, Kennedy C, Larson TJ, Latreille P, Ligon LS, Lu J, Marek M, Miller NM, Norton S, O’Carroll IP, Paulsen I, Raulfs EC, Roemer R, Rosser J, Segura D, Slater S, Stricklin SL, Studholme D, Sun J, Viana CJ, Wallin E, Wang B, Wheller C, Zhu H, Dean DR, Dixon R, Wood D (2009) Genome sequence of Azotobacter vinelandii, an obligate aerobe specialized to support diverse anaerobic metabolic processes. J Bacteriol 191:4534–4545. doi: 10.1128/JB.00504-09 PubMedCrossRefGoogle Scholar
  148. Sevilla M, Kennedy C (2000) Genetic analysis of nitrogen fixation and plant-growth stimulating properties of Acetobacter diazotrophicus, an endophyte of sugarcane. In: Triplett EW (ed) Prokaryotic Nitrogen fixation: a model system for the analysis of biological process. Horizon Scientific Press, Wymondham, UK, pp 737–760Google Scholar
  149. Singh MK, Singh DP, Mesapogu S, Babu BK, Bontemps C (2011) Concomitant colonization of nifH positive endophytic Burkholderia sp. in rice (Oryza sativa L.) promotes plant growth. World J Microbiol Biotechnol 27:2023–2031. doi: 10.1007/s11274-011-0664-z CrossRefGoogle Scholar
  150. Somers E, Srinivasan M, Vanderleyden J (2004) Rhizosphere bacterial signalling: a love parade beneath our feet. Crit Rev Microbiol 30:205–240PubMedCrossRefGoogle Scholar
  151. Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448. doi: 10.1111/j.1574-6976.2007.00072.x PubMedCrossRefGoogle Scholar
  152. Sprent JI, de Faria SM (1988) Mechanisms of infection of plants by nitrogen fixing organisms. Plant Soil 110:157–165. doi: 10.1007/BF02226795 CrossRefGoogle Scholar
  153. Strobel G (2006) Harnessing endophytes for industrial microbiology. Curr Opin Microbiol 9:240–244. doi: 10.1016/j.mib.2006.04.001 PubMedCrossRefGoogle Scholar
  154. Tadra-Sfeir MZ, Souza EM, Faoro H, Muller-Santos M, Baura VA, Tuleski TR, Rigo L, Yates MG, Waseem R, Pedrosa FO, Monteiro RA (2011) Naringenin regulates expression of genes involved in cell wall synthesis in Herbaspirillum seropedicae. Appl Environ Microbiol 77:2180–2183. doi: 10.1128/AEM.02071-10 PubMedCrossRefGoogle Scholar
  155. Taghavi S, van der Lelie D, Hoffman A, Zhang YB, Walla MD, Vangronsveld J, Newman L, Monchy S (2010) Genome sequence of the plant growth promoting endophytic bacterium Enterobacter sp. 638. PLoS Genet 6:e1000943. doi: 10.1371/journal.pgen.1000943 PubMedCrossRefGoogle Scholar
  156. Taule C, Mareque C, Barlocco C, Hackembruch F, Reis VM, Sicardi M, Battistoni F (2012) The contribution of nitrogen fixation to sugarcane (Saccharum officinarum L.), and the identification and characterization of part of the associated diazotrophic bacterial community. Plant Soil 356:35–49. doi: 10.1007/s11104-011-1023-4 CrossRefGoogle Scholar
  157. Terakado-Tonooka J, Ohwaki Y, Yamakawa H, Tanaka F, Yoneyama T, Fujihara S (2008) Expressed nifH genes of endophytic bacteria detected in field-grown sweet potatoes (Ipomoea batatas L.). Microbes Environ 23:89–93. doi: 10.1264/jsme2.23.89 PubMedCrossRefGoogle Scholar
  158. Tjamos SE, Flemetakis E, Paplomatas EJ, Katinakis P (2005) Induction of resistance to Verticillium dahlia in Arabidopsis thaliana by the biocontrol agent K-165 and pathogenesis-related proteins gene expression. Mol Plant Microbe Interact 18:555–561. doi: 10.1094/MPMI-18-0555 PubMedCrossRefGoogle Scholar
  159. Ueda T, Suga Y, Yahiro N, Matsuguchi T (1995a) Remarkable N2-fixing bacterial diversity detected in rice roots by molecular evolutionary analysis of nifH gene sequences. J Bacteriol 177:1414–1417PubMedGoogle Scholar
  160. Ueda T, Suga Y, Yahiro N, Matsuguchi T (1995b) Genetic diversity of N2-fixing bacteria associated with rice roots by molecular evolutionary analysis of nifD library. Can J Microbiol 41:235–240PubMedCrossRefGoogle Scholar
  161. Urquiaga S, Xavier RP, de Morais RF, Batista RB, Schultz N, Leite JM, Sa JM, Barbosa KP, de Resende AS, Alves BJR, Boddey RM (2012) Evidence from field nitrogen balance and 15N natural abundance data for the contribution of biological N2-fixation to Brazilian sugarcane varieties. Plant Soil. doi: 10.1007/s11104-011-1016-3
  162. van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–254. doi: 10.1007/s10658-007-9165-1 CrossRefGoogle Scholar
  163. van West P, Morris BM, Reid B, Appiah AA, Osborne MC, Campbell TA, Shepherd SJ, Gow NAR (2002) Oomycete plant pathogens use electric fields to target roots. Mol Plant Microbe Interact 15:790–798. doi: 10.1094/MPMI.2002.15.8.790 PubMedCrossRefGoogle Scholar
  164. Venieraki A, Dimou M, Pergalis P, Chatzipavlidis I, Katinakis P (2011) The genetic diversity of culturable nitrogen-fixing bacteria in the rhizosphere of wheat. Microb Ecol 61:277–285. doi: 10.1007/s00248-010-9747-x PubMedCrossRefGoogle Scholar
  165. Verhagen BW, Trotel-Aziz P, Couderchet M, Hofte M, Aziz A (2010) Pseudomonas spp. induced systemic resistance to Botrytis cinerea is associated with induction and priming of defence responses in grapevine. J Exp Bot 61:249–260. doi: 10.1093/jxb/erp295 PubMedCrossRefGoogle Scholar
  166. Verma SC, Singh A, Chowdhury SP, Tripathi AK (2004) Endophytic colonization ability of two deep-water rice endophytes, Pantoea sp. and Ochrobactrum sp. using green fluorescent protein reporter. Biotechnol Lett 26:425–429. doi: 10.1023/B:BILE.0000018263.94440.ab PubMedCrossRefGoogle Scholar
  167. Voorhorst WGB, Eggen RIL, Luesink EJ, de Vos WM (1995) Characterization of the celB gene coding for b-glucosidase from the hyperthermophilic archaeon Pyrococcus furiosus and its expression and site-directed mutation in Escherichia coli. J Bacteriol 177:7105–7111PubMedGoogle Scholar
  168. Webster G, Gough C, Vasse J, Bathchelor CA, O’Callaghan KJ, Kothari SL, Davey MR, Denarie J, Cocking EC (1997) Interactions of rhizobia with rice and wheat. Plant Soil 194:115–122. doi: 10.1023/A:1004283819084 CrossRefGoogle Scholar
  169. Weilharter A, Mitter B, Shin MV, Chain PSG, Nowak J, Sessitsch A (2011) Complete genome sequence of the plant growth-promoting endophyte Burkholderia phytofirmans strain PsJN. J Bacteriol 193:3383–3384. doi: 10.1128/JB.05055-11 PubMedCrossRefGoogle Scholar
  170. West ER, Cother EJ, Steel CC, Ash GJ (2010) The characterization and diversity of bacterial endophytes of grapevine. Can J Microbiol 56:209–216. doi: 10.1139/W10-004 PubMedCrossRefGoogle Scholar
  171. Widmer F, Shaffer BT, Porteous LA, Seidler RJ (1999) Analysis of nifH gene pool complexity in soil and little at Douglas fir forest sites of the Orgegon cascade mountain range. Appl Environ Microbiol 65:374–380PubMedGoogle Scholar
  172. Winstanley C, Morgan JA, Pickup RW, Saunders JR (1991) Use of a xylE marker gene to monitor survival of recombinant Pseudomonas putida populations in lake water by culture on nonselective media. Appl Environ Microbiol 57:1905–1913PubMedGoogle Scholar
  173. Xing T, Quellet T, Miki BL (2004) Towards genomic and proteomic studies of protein phosphorylation in plant-pathogen interactions. Trends Plant Sci 7:224–230. doi: 10.1016/S1360-1385(02)02255-0 CrossRefGoogle Scholar
  174. Yan Y, Yang J, Dou Y, Chen M, Ping S, Peng J, Lu W, Zhnag W, Yao Z, Li H, Liu W, He S, Geng L, Zhnag X, Yang F, Yu H, Zhan Y, Li D, Lin Z, Wang Y, Elmerich C, Lin M, Jin Q (2008) Nitrogen fixation island and rhizosphere competence traits in the genome of root-associated Pseudomonas stutzeri A1501. Proc Natl Acad Sci 105:7564–7569. doi: 10.1073/pnas.0801093105 PubMedCrossRefGoogle Scholar
  175. Yang J, Kloepper JW, Ryu C (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4. doi: 10.1016/j.tplants.2008.10.004 PubMedCrossRefGoogle Scholar
  176. Yanni YG, Rizk RY, Corich V, Squartini A, Ninke K, Phillip-Hollingswoth 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 roots and assessment of its potential to promote rice growth. Plant Soil 194:99–114. doi: 10.1023/A:1004269902246 CrossRefGoogle Scholar
  177. Yanni YG, Rizk RY, Abd El-Fattah FK, Squartini A, Corich V, Giacomini A, de Bruijn F, Rasemaker J, Maya-Flores J, Ostrom P, Vega-Hernandez M, Hollingsworth RI, Martinez-Molina E, Mateos P, Velazequez E, Wopereis J, Triplett E, Umali-Gracia M, Anarna JA, Rolfe BG, Ladha JK, Hill J, Mujoo R, Ng PK, Dazzo FB (2001) The beneficial plant growth-promoting association of Rhizobium leguminosarum bv. trifolii with rice roots. Aust J Plant Physiol 28:845–870. doi: 10.1071/PP01069 Google Scholar
  178. Zehr JP, Mellon MT, Zani S (1998) New nitrogen-fixing microorganisms detected in oligotrophic oceans by amplification of nitrogenase (nifH) genes. Appl Environ Microbiol 64:3444–3450PubMedGoogle Scholar
  179. Zehr JP, Jenkins BD, Short SM, Steward GF (2003) Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 5:539–554. doi: 10.1046/j.1462-2920.2003.00451.x PubMedCrossRefGoogle Scholar
  180. Zeyaullah M, Kamli MR, Islam B, Atif M, Benkhayal FA, Nehal M, Rizvi MA, Ali A (2009) Metagenomics-an advanced approach for noncultivable micro-organisms. Biotechnol Mol Biol Rev 4:49–54Google Scholar
  181. Zhang X, Candas M, Griko NB, Taussig R, Bulla LA Jr (2006) A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis. Proc Natl Acad Sci 103:9897–9902. doi: 10.1073/pnas.0604017103 PubMedCrossRefGoogle Scholar
  182. Zhang H, Xie X, Kim MS, Kornyeyev DA, Holaday S, Pare PW (2008) Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J 56:264–273. doi: 10.1111/j.1365-313X.2008.03593.x PubMedCrossRefGoogle Scholar
  183. Zhu B, Liu H, Tian WX, Fan XY, Li B, Zhou XP, Jin GL, Xie GL (2012) Genome sequence of Stenotrophomonas maltophilia RR-10, isolated as an endophyte from rice root. J Bacteriol 194:1280–1281. doi: 10.1128/JB.06702-11 PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  1. 1.Centre for Biotechnology, Department of Biological SciencesBirla Institute of Technology and SciencePilaniIndia
  2. 2.Department of Biology, College of Natural SciencesJimma UniversityJimmaEthiopia

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