Advertisement

Azospirillum: A Biofertilizer for Every Crop

  • Samina Mehnaz
Chapter

Abstract

Azospirillum is known for its nitrogen-fixing and phytohormone production ability. It is one of very well-studied plant growth-promoting rhizobacteria, at lab scale to field. None of its species or strain is reported as human or plant pathogen. It is considered as safest bacteria which can be used as a biofertilizer at commercial level for several crops, especially cereals or grasses including wheat and rice which are of economic importance for the whole world. Some of its species are reported for phosphate-solubilizing ability and high salt tolerance. Fifteen of its species have been isolated from variety of hosts and environmental sources; however, a majority have been reported from plants. There are several reviews available on this organism; in this chapter, an overview of this organism covering its plant growth-promoting abilities, used as inoculum in lab and field experiments and used as a commercial biofertilizer for different crops, is provided.

Keywords

Indole Acetic Acid Plant Growth Promotion Phosphate Solubilization Siderophore Production Biological Nitrogen Fixation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Alen’kina SA, Payusova OA, Nikitina VE (2006) Effect of Azospirillum lectins on the activities of wheat-root hydrolytic enzymes. Plant Soil 283:147–151Google Scholar
  2. Ayrault G (2002) Seed germinability and plant establishment of Lactuca sativa and Daucus carota inoculated with Azospirillum and exposed to salt stress. MSc dissertation, University of Mar del Plata, Argentina, p 90Google Scholar
  3. Babu RS, Sankaranarayanan C, Jothi G (1998) Management of Pratylenchus zeae on maize by biofertilizers and VAM. Ind J Nematol 28:77–80Google Scholar
  4. Bacilio M, Vazquez P, Bashan Y (2003) Alleviation of noxious effects of cattle ranch composts on wheat seed germination by inoculation with Azospirillum spp. Biol Fertil Soils 38:261–266Google Scholar
  5. Bacilio M, Rodriguez H, Moreno M, Hernandez JP, Bashan Y (2004) Mitigation of salt stress in wheat seedlings by a gfp-tagged Azospirillum lipoferum. Biol Fertil Soils 40:188–193Google Scholar
  6. Bansal RK, Dahiya RS, Lakshminarayana K, Suneja S, Anand RC, Narula N (1999) Effect of rhizospheric bacteria on plant growth of wheat infected with Heterodera avenae. Nematol Mediterr 27:311–314Google Scholar
  7. Barassi CA, Ayrault G, Creus CM, Sueldo RJ, Sobrero MT (2006) Seed inoculation with Azospirillum mitigates NaCl effects on lettuce. Sci Hortic 109:8–14Google Scholar
  8. Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58Google Scholar
  9. Bashan Y (1990) Short exposure to Azospirillum brasilense Cd inoculation enhanced proton efflux in intact wheat roots. Can J Microbiol 36:419–425Google Scholar
  10. Bashan Y (1991) Changes in membrane potential of intact soybean root elongation zone cells induced by Azospirillum brasilense. Can J Microbiol 37:958–963Google Scholar
  11. Bashan Y, de-Bashan LE (2002) Protection of tomato seedlings against infection by Pseudomonas syringae pv. tomato by using the plant growth-promoting bacterium Azospirillum brasilense. Appl Environ Microbiol 68:2637–2643PubMedPubMedCentralGoogle Scholar
  12. Bashan Y, de-Bashan LE (2010) How the plant growth promoting bacterium Azospirillum promotes plant growth – a critical assessment. Adv Agron 108:77–136Google Scholar
  13. Bashan Y, Levanony H (1990) Current status of Azospirillum inoculation technology: Azospirillum as a challenge for agriculture. Can J Microbiol 36:591–608Google Scholar
  14. Bashan Y, Levanony H (1991) Alterations in membrane potential and in proton efflux in plant roots induced by Azospirillum brasilense. Plant Soil 137:99–103Google Scholar
  15. Bashan Y, Alcaraz-Melendez L, Toledo G (1992) Responses of soybean and cowpea root membranes to inoculation with Azospirillum brasilense. Symbiosis 13:217–228Google Scholar
  16. Bashan Y, Holguin G, de-Bashan LE (2004) Azospirillum-plant relationships: physiological, molecular, agricultural and environmental advances (1997–2003). Can J Microbiol 50:521–577PubMedGoogle Scholar
  17. Bashan Y, Bustillos JJ, Leyva LA, Hernandez JP, Bacilio M (2006) Increase in auxiliary photoprotective photosynthetic pigments in wheat seedlings induced by Azospirillum brasilense. Biol Fertil Soils 42:279–285Google Scholar
  18. Belimov A, Dietz KJ (2000) Effect of associative bacteria on element composition of barley seedlings grown in solution culture at toxic cadmium concentrations. Microbiol Res 155:113–121PubMedGoogle Scholar
  19. Belimov AA, Kunakova AM, Safronova VI, Stepanok VV, Yudkin LY, Alekseev YV, Kozhemyakov AP (2004) Employment of rhizobacteria for the inoculation of barley plants cultivated in soil contaminated with lead and cadmium. Microbiology (Moscow) 73:99–106Google Scholar
  20. Bottini R, Cassan F, Piccoli P (2004) Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl Microbiol Biotechnol 65:497–503PubMedGoogle Scholar
  21. Bouillant ML, Miché L, Ouedraogo O, Alexandre G, Jacoud C, Sallé G, Bally R (1997) Inhibition of Striga seed germination associated with sorghum growth promotion by soil bacteria. C R Acad Sci Paris-Sciences de la vie 320:159–162Google Scholar
  22. Boyer M, Bally R, Perrotto S, Chaintreuil C, Wisniewski-Dye F (2008) A quorum quenching approach to identify quorum-sensing regulated functions in Azospirillum lipoferum. Res Microbiol 20:72–77Google Scholar
  23. Brasil MS, Baldani VLD, Baldani JI, Souto SM (2005) Effects of inoculation of diazotrophs in grasses Pantanal. Pasturas Tropicales 27:22–33Google Scholar
  24. Cacciari I, Lippi D, Pietrosanti T, Pietrosanti W (1989) Phytohormone-like substances produced by single and mixed diazotrophic cultures of Azospirillum spp. and Arthrobacter. Plant Soil 115:151–153Google Scholar
  25. Carrillo AE, Li CY, Bashan Y (2002) Increased acidification in the rhizosphere of cactus seedlings induced by Azospirillum brasilense. Naturwissenschaften 89:428–432PubMedGoogle Scholar
  26. Carrozzi LE (2005) Lactuca sativa (L.) seed priming and Azospirillum inoculations a tool for improving germination rate. MSc dissertation, University of Mar del Plata, ArgentinaGoogle Scholar
  27. Casanovas EM, Barassi CA, Sueldo RJ (2002) Azospirillum inoculation mitigates water stress effects in maize seedlings. Cer Res Commun 30:343–350Google Scholar
  28. Cassan F, Maiale S, Masciarelli O, Vidal A, Luna V, Ruiz O (2009a) Cadaverine production by Azospirillum brasilense and its possible role in plant growth promotion and osmotic stress mitigation. Eur J Soil Biol 45:12–19Google Scholar
  29. Cassan F, Perrig D, Sgroy V, Masciarelli O, Penna C, Luna V (2009b) Azospirillum brasilense Az39 and Bradyrhizobium japonicum E109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L.) and soybean (Glycine max L.). Eur J Soil Biol 45:28–35Google Scholar
  30. Chang TT, Li CY (1998) Weathering of limestone, marble, and calcium phosphate by ecto-mycorrhizal fungal and associated microorganisms. Taiwan J Sci 13:8590Google Scholar
  31. Cohen AC, Bottini R, Piccoli PN (2008) Azospirillum brasilense Sp 245 produces ABA in chemically-defined culture medium and increases ABA content in Arabidopsis plants. Plant Growth Regul 54:97–103Google Scholar
  32. Cohen AC, Travaglia CN, Bottini R, Piccoli PN (2009) Participation of abscisic acid and gibberellins produced by endophytic Azospirillum in the alleviation of drought effects in maize. Botany 87:455–462Google Scholar
  33. Correa-Aragunde N, Graziano M, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905PubMedGoogle Scholar
  34. Costacurta A, Vanderleyden J (1995) Synthesis of phytohormones by plant-associated bacteria. Crit Rev Microbiol 21:1–18PubMedGoogle Scholar
  35. Costacurta A, Keijers V, Vanderleyden J (1994) Molecular cloning and sequence analysis of an Azospirillum brasilense indole-3-pyruvate decarboxylase gene. Mol Gen Genet 243:463–472PubMedGoogle Scholar
  36. Creus CM, Sueldo RJ, Barssi CA (1997) Shoot growth and water status in Azospirillum inoculated wheat seedlings grown under osmotic and salt stresses. Plant Physiol Biochem 35:939–944Google Scholar
  37. Creus CM, Suelda RJ, Barassi CA (2004) Water relations and yield in Azospirillum-inoculated wheat exposed to drought in the field. Can J Bot 82:273–281Google Scholar
  38. Creus CM, Graziano M, Casanovas EM, Pereyra MA, Simontacchi M, Puntarulo S, Barassi CA, Lamattina L (2005) Nitric oxide is involved in the Azospirillum brasilense-induced lateral root formation in tomato. Planta 221:297–303PubMedGoogle Scholar
  39. Crozier A, Arruda P, Jasmin JM, Monteiro AM, Sandberg G (1988) Analysis of indole-3-acetic acid and related indoles in culture medium from Azospirillum lipoferum and Azospirillum brasilense. Appl Environ Microbiol 54:2833–2837PubMedPubMedCentralGoogle Scholar
  40. Dadon T, Bar Nun N, Mayer AM (2004) A factor from Azospirillum brasilense inhibits germination and radicle growth of Orobanche aegyptiaca. Isr J Plant Sci 52:83–86Google Scholar
  41. Dalla Santa OR, Hernandez RF, Alvarez GLM, Ronzelli JP, Soccol CR (2004) Azospirillum sp. inoculation in wheat, barley and oats seeds greenhouse experiments. Braz Arch Biol Tech 47:843–850Google Scholar
  42. de-Bashan LE, Bashan Y (2008) Joint immobilization of plant growth-promoting bacteria and green microalgae in alginate beads as an experimental model for studying plant–bacterium interactions. Appl Environ Microbiol 74:6797–6802PubMedPubMedCentralGoogle Scholar
  43. de-Bashan LE, Antoon H, Bashan Y (2005) Cultivation factors and population size control uptake of nitrogen by the microalgae Chlorella vulgaris when interacting with the microalgae growth-promoting bacterium Azospirillum brasilense. FEMS Microbiol Ecol 54:197–203PubMedGoogle Scholar
  44. Deubel A, Gransee A, Merbach W (2000) Transformation of organic rhizodepositions by rhizosphere bacteria and its influence on the availability of tertiary calcium phosphate. J Plant Nutr Soil Sci 163:387–392Google Scholar
  45. Diaz-Zorita M, Fernandez-Canigia MV (2009) Field performance of a liquid formulation of Azospirillum brasilense on dryland wheat productivity. Eur J Soil Biol 45:3–11Google Scholar
  46. Didonet AD, Didonet CCGM, Gomes GF (2003) Evaluation of strains of upland rice inoculated with Azospirillum lipoferum Sp59b and A. brasilense Sp24. Comunicado Tecnico EMBRAPA, p 69Google Scholar
  47. Dobbelaere S, Croonenborghs A, Thys A, Vande Broek A, Vanderleyden J (1999) Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil 212:155–164Google Scholar
  48. El-Khawas H, Adachi K (1999) Identification and quantification of auxins in culture media of Azospirillum and Klebsiella and their effect on rice roots. Biol Fertil Soils 28:377–381Google Scholar
  49. El-Komy HM, Hamdia MA, El-Baki GKA (2003) Nitrate reductase in wheat plants grown under water stress and inoculated with Azospirillum spp. Biol Plant 46:281–287Google Scholar
  50. Fallik E, Okon Y, Epstein E, Goldman A, Fischer M (1989) Identification and quantification of IAA and IBA in Azospirillum brasilense inoculated maize roots. Soil Biol Biochem 21:147–153Google Scholar
  51. Ferreira MCB, Fernandes MS, Dobereiner J (1987) Role of Azospirillum brasilense nitrate reductase in nitrate assimilation by wheat plants. Biol Fertil Soils 4:47–53Google Scholar
  52. Garcia de Salamone IE, Dobereiner J, Urquiaga S, Boddey RM (1997) Biological nitrogen fixation in Azospirillum strain–maize genotype associations as evaluated by the 15N isotope dilution technique. Biol Fertil Soils 23:249–256Google Scholar
  53. Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E, Avarre JC, Jaubert M, Simon D, Cartieaux F, Prin Y, Bena G, Hannibal L, Fardoux J, Kojadinovic M, Vuillet L, Lajus A, Cruveiller S, Rouy Z, Mangenot S, Segurens B, Dossat C, Franck WL, Chang WS, Saunders E, Bruce D, Richardson P, Normand P, Dreyfus B, Pignol D, Stacey G, Emerich D, Vermeglio A, Medigue C, Sadowsky M (2007) Legumes symbioses: absence of genes in nod in photosynthetic bradyrhizobia. Science 316:1307–1312PubMedGoogle Scholar
  54. Glick BR, Patten CL, Holguin G, Penrose DM (1999) Biochemical and genetic mechanisms used by plant growth promoting bacteria. Imperial College Press, London, pp 125–140Google Scholar
  55. Goncalves AFS, de Oliveira RGB (1998) Cyanide production by Brazilian strains of Azospirillum. Rev Microbiol 29:36–39Google Scholar
  56. Hamaoui B, Abbadi JM, Burdman S, Rashid A, Sarig S, Okon Y (2001) Effects of inoculation with Azospirillum brasilense on chickpeas (Cicer arietinum) and faba beans (Vicia faba) under different growth conditions. Agronomie 21:553–560Google Scholar
  57. Hartmann A, Zimmer W (1994) Physiology of Azospirillum. In: Okon Y (ed) Azospirillum/plant association. CRC Press, Boca Raton, pp 15–39Google Scholar
  58. Hartmann A, Singh M, Klingmuller W (1983) Isolation and characterization of Azospirillum mutants excreting high amounts of indole acetic acid. Can J Microbiol 29:916–923Google Scholar
  59. Hassouna MG, El-Saedy MAM, Saleh HMA (1998) Biocontrol of soil-borne plant pathogens attacking cucumber (Cucumis sativus) by rhizobacteria in a semiarid environment. Arid Soil Res Rehabil 12:345–357Google Scholar
  60. Hernandez JP, de-Bashan LE, Bashan Y (2006) Starvation enhances phosphorus removal from wastewater by the microalga Chlorella spp. co-immobilized with Azospirillum brasilense. Enzyme Microb Technol 38:190–198Google Scholar
  61. Holguin G, Bashan Y (1996) Nitrogen-fixing by Azospirillum brasilense Cd is promoted when co-cultured with a mangrove rhizosphere bacterium (Staphylococcus sp.). Soil Biol Biochem 28:1651–1660Google Scholar
  62. Horemans S, De Koninck K, Neuray J, Hermans R, Vlassak K (1986) Production of plant growth substances by Azospirillum sp. and other rhizosphere bacteria. Symbiosis 2:341–346Google Scholar
  63. 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(1):37–50PubMedPubMedCentralGoogle Scholar
  64. Kasim WA, Osman ME, Omar MN, Abd-Eldeim IA, Bejai S, Meijer J (2013) Control of drought stress in wheat using plant growth promoting bacteria. J Plant Growth Regul 32:122–130Google Scholar
  65. Kavitha K, Meenakumari KS, Sivaprasad P (2003) Effect of dual inoculation of native arbuscular mycorrhizal fungi and Azospirillum on suppression of damping off in chilli. Ind Phytopathol 56:112–113Google Scholar
  66. Kennedy IR, Choudhry ATMA, Kecskes ML (2004) Non-symbiotic bacterial diazotrophs in crop-farming systems: can their potential for plant growth promotion be better explored. Soil Biol Biochem 36:1229–1244Google Scholar
  67. Khan MR, Kounsar K (2000) Effect of seed treatment with certain bacteria and fungi on the growth of mung bean and reproduction of Meloidogyne incognita. Nematol Mediterr 28:221–226Google Scholar
  68. Kishore P (1998) Response of sorghum variety Pusa chari-121 to carrier based inoculants (Azotobacter and Azospirillum), fermented residue and shootfly (Atherigona soccata Rondani) under field conditions. J Entomol Res 22:101–105Google Scholar
  69. Kyungseok P, Kloepper JW, Ryu CM (2008) Rhizobacterial exopolysaccharides elicit induced resistance on cucumber. J Microbiol Biotechnol 18:1095–1100Google Scholar
  70. Lavrinenko K, Chernousova E, Gridneva E, Dubinina G, Akimov V, Kuever J, Lysenko A, Grabovich M (2010) Azospirillum thiophilum sp. nov., a novel diazotrophic bacterium isolated from a sulfide spring. Int J Syst Evol Microbiol 60:2832–2837PubMedGoogle Scholar
  71. Lin SY, Young CC, Hupfer H, Siering C, arun AB, Chen WM, Lai WA, Shen FT, Rekha PD, Yasin AF (2009) Azospirillum picis sp. nov., isolated from discarded tar. Int J Syst Evol Microbiol 59:761–765PubMedGoogle Scholar
  72. Lombardo MC, Graziano M, Polacco JC, Lamattina L (2006) Nitric oxide functions as a positive regulator of root hair development. Plant Signal Behav 1:28–33PubMedPubMedCentralGoogle Scholar
  73. Lucangeli C, Bottini R (1997) Effects of Azospirillum spp. on endogenous gibberellin content and growth of maize (Zea mays L.) treated with uniconazole. Symbiosis 23:63–72Google Scholar
  74. Lucy M, Reed E, Glick BR (2004) Application of free living plant growth promoting rhizobacteria. Antonie van Leeuwenhoek Int J Gen Mol Biol 86:1–25Google Scholar
  75. Lyubun YV, Fritzsche A, Chernyshova MP, Dudel EG, Fedorov EE (2006) Arsenic transformation by Azospirillum brasilense Sp245 in association with wheat (Triticum aestivum L.) roots. Plant Soil 286:219–227Google Scholar
  76. Malhotra M, Srivastava S (2006) Targeted engineering of Azospirillum brasilense SM with indole acetamide pathway for indole acetic acid over-expression. Can J Microbiol 52:1078–1084PubMedGoogle Scholar
  77. Malhotra M, Srivastava S (2008) An ipdc gene knock out of Azospirillum brasilense strain SM and its implications on indole 3-acetic acid biosynthesis and plant growth promotion. Antonie van Leeuwenhoek J Gen 93:425–433Google Scholar
  78. Malhotra M, Srivastava S (2009) Stress responsive indole-3-acetic acid biosynthesis by Azospirillum brasilense SM and its ability to modulate plant growth. Eur J Soil Biol 45:73–80Google Scholar
  79. Manivannan M, Tholkappian P (2013) Prevalence of Azospirillum isolates in tomato rhizosphere soils of coastal areas of Cuddalore District, Tamil Nadu. Int J Recent Sci Res 4:1610–1613Google Scholar
  80. Mehnaz S, Lazarovits G (2006) Inoculation effects of Pseudomonas putida, Gluconacetobacter azotocaptans and Azospirillum lipoferum on corn plant growth under green house conditions. Microb Ecol 51:326–335PubMedGoogle Scholar
  81. Mehnaz S, Weselowski B, Lazarovits G (2007a) Azospirillum canadense sp. nov., a nitrogen fixing bacterium isolated from corn rhizosphere. Int J Syst Evol Microbiol 57(3):620–624PubMedGoogle Scholar
  82. Mehnaz S, Weselowski B, Lazarovits G (2007b) Azospirillum zeae sp. nov., diazotrophic bacteria isolated from rhizosphere soil of Zea mays. Int J Syst Evol Microbiol 57(12):2805–2809PubMedGoogle Scholar
  83. Miché L, Bouillant ML, Rohr R, Sallé G, Bally R (2000) Physiological and cytological studies on the inhibition of Striga seed germination by the plant growth-promoting bacterium Azospirillum brasilense. Eur J Plant Pathol 106:347–351Google Scholar
  84. Molina-Favero C, Creus CM, Lanteri ML, Correa-Aragunde N, Lombardo MC, Barassi CA, Lamattina L (2007) Nitric oxide and plant growth promoting rhizobacteria: common features influencing root growth and development. Adv Bot Res 46:1–33Google Scholar
  85. Molina-Favero C, Creus CM, Simontacchi M, Puntarulo S, Lamattina L (2008) Aerobic nitric oxide production by Azospirillum brasilense Sp245 and its influence on root architecture in tomato. Mol Plant Microbe Interact 21:1001–1009PubMedGoogle Scholar
  86. Molla AH, Shamsuddin ZH, Saud HM (2001) Mechanism of root growth and promotion of nodulation in vegetable soybean by Azospirillum brasilense. Commun Soil Sci Plant Anal 32:2177–2187Google Scholar
  87. Moutia YJF, Saumtally S, Spaepen S, Vanderleyden J (2010) Plant growth promotion by Azospirillum sp. in sugarcane is influenced by genotype and drought stress. Plant Soil 337:233–242Google Scholar
  88. Nikitina VE, Bogomolova NV, Ponomareva EG, Sokolov OI (2004) Effect of azospirilla lectins on germination capacity of seeds. Biol Bull (Moscow) 31:354–357Google Scholar
  89. Okon Y (1985) Azospirillum as a potential inoculants for agriculture. Trends Biotechnol 3:223–228Google Scholar
  90. Okon Y, Vanderleyden J (1997) Root-associated Azospirillum species can stimulate plants. Appl Environ Microbiol 63:366–370Google Scholar
  91. Okumura RS, Mariano DC, Dallacort R, Nogueira de Albuquerque A, Lobato AKS, Guedes EMS, Neto CFO, Oliveira da Conceicao HE, Alves GAR (2013) Azospirillum: a new and efficient alternative to biological nitrogen fixation in grasses. J Food Agric Environ 2(1):1142–1146Google Scholar
  92. Oliveira RGB, Drozdowicz A (1987) Inhibition of bacteriocin producing strains of Azospirillum lipoferum by their own bacteriocin. Zentralblatt fur Mikrobiologie 142:387–391Google Scholar
  93. Ona O, Smets I, Gysegom P, Bernaerts K, Impe JV, Prinsen E, Vanderleyden J (2003) The effect of pH on indole-3-acetic acid biosynthesis of Azospirillum brasilense Sp7. Symbiosis 35:199–208Google Scholar
  94. Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L (2002) Nitric oxide is required for root organogenesis. Plant Physiol 129:954–956PubMedPubMedCentralGoogle Scholar
  95. Pagnussat GC, Lanteri ML, Lamattina L (2003) Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol 132:1241–1248PubMedPubMedCentralGoogle Scholar
  96. Pedraza RO, Motok J, Tortora ML, Salazar SM, Dı’az Ricci JC (2007) Natural occurrence of Azospirillum brasilense in strawberry plants. Plant Soil 295:169–178Google Scholar
  97. Pereyra MA, Zalazar CA, Barassi CA (2006) Root phospholipids in Azospirillum inoculated wheat seedlings exposed to water stress. Plant Physiol Biochem 44:873–879PubMedGoogle Scholar
  98. Perrig D, Boiero ML, Masciarelli OA, Penna C, Ruiz OA, Cassan FD, Luna MV (2007) Plant-growth-promoting compounds produced by two agronomically important strains of Azospirillum brasilense, and implications for inoculant formulation. Appl Microbiol Biotechnol 75:1143–1150PubMedGoogle Scholar
  99. Piccoli P, Masciarelli O, Bottini R (1999) Gibberellin production by Azospirillum lipoferum cultured in chemically defined medium as affected by oxygen availability and water status. Symbiosis 27:135–145Google Scholar
  100. Prigent-Combaret C, Blaha D, Pothier JF, Vial L, Poirier MA, Wisniewski-Dyé F, Moe¨nne-Loccoz Y (2008) Physical organization and phylogenetic analysis of acdR as leucine-responsive regulator of the 1-aminocyclopropane-1-carboxylate deaminase gene acdS in phytobeneficial Azospirillum lipoferum 4B and other proteobacteria. FEMS Microbiol Ecol 65:202–219PubMedGoogle Scholar
  101. Puente ME, Bashan Y, Li CY, Lebsky VK (2004) Microbial populations and activities in the rhizoplane of rock-weathering desert plants I. Root colonization and weathering of igneous rocks. Plant Biol 6:629–642PubMedGoogle Scholar
  102. Ramakrishnan S, Gunasekaran CR, Vadivelu S (1997) Effect of bio-fertilizers Azolla and Azospirillum on root-knot nematode, Meloidogyne incognita and plant growth of okra. Ind J Nematol 26:127–130Google Scholar
  103. Reis VM, Teixeira KRS, Pedraza RO (2011) What is expected from the genus Azospirillum as a plant growth promoting bacteria? In: Maheshwari DK (ed) Bacteria in agrobiology: plant growth responses. Springer, Berlin/Heidelberg, pp 123–138Google Scholar
  104. Remans R, Beebe S, Blair M, Manrique G, Tovar E, Rao I, Croonenborghs A, Torres-Gutierrez R, El-Howeity M, Michiels J, Vanderleyden J (2008) Physiological and genetic analysis of root responsiveness to auxin-producing plant growth-promoting bacteria in common bean (Phaseolus vulgaris L.). Plant Soil 302:149–161Google Scholar
  105. Reynders L, Vlassak K (1979) Conversion of tryptophan to indole acetic acid by Azospirillum brasilense. Soil Biol Biochem 11:547–548Google Scholar
  106. Rodrigues EP, Rodrigues LS, de Oliveira ALM, Baldani VLD, Teixeira KRD, Urquiaga S, Reis VM (2008) Azospirillum amazonense inoculation: effects on growth, yield and N2-fixation of rice (Oryza sativa L.). Plant Soil 302:249–261Google Scholar
  107. Rodriguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339PubMedGoogle Scholar
  108. Rodriguez H, Gonzalez T, Goire I, Bashan Y (2004) Gluconic acid production and phosphate solubilization by the plant growth-promoting bacterium Azospirillum spp. Naturwissenschaften 91:552–555PubMedGoogle Scholar
  109. Rodriguez-Salazar J, Suarez R, Caballero-Mellado J, Iturriaga G (2009) Trehalose accumulation in Azospirillum brasilense improves drought tolerance and biomass in maize plants. FEMS Microbiol Lett 296:52–59PubMedGoogle Scholar
  110. Rueda-Puente EO, Castellanos T, Troyo-Dieguez E, Diaz de Leon-Avarez JL (2004) Effect of Klebsiella pneumonia and Azospirillum halopraeferens on the growth and development of two Salicornia bigelovii genotypes. Aust J Exp Agric 44:65–74Google Scholar
  111. Saikia SP, Jain V, Khetarpal S, Aravind S (2007) Dinitrogen fixation activity of Azospirillum brasilense in maize (Zea mays). Curr Sci 93:1296–1300Google Scholar
  112. Sala VMR, Freitas SS, Donzeli VP, Freitas JG, Gallo PB, Silveira APD (2005) Occurrence and effect of diazotrophic bacteria in wheat genotypes. Revista Brasileira de Ciencia do Solo 29:345–352Google Scholar
  113. Sala VMR, Cardoso EJBN, Freitas JG, Silveira APD (2007) Wheat genotypes response to inoculation of diazotrophic bacteria in field conditions. Pesq Agrop Brasileira 42:833–842Google Scholar
  114. Sankari JU, Dinakar S, Sekar C (2011) Dual effect of Azospirillum exo-polysaccharides (EPS) on the enhancement of plant growth and biocontrol of blast (Pyricularia oryzae) disease in upland rice (var. ASD-19). J Phytol 3(10):16–19Google Scholar
  115. Sant’Anna FH, Almeida LGP, Cecagno R, Reolon LA, Siqueira FM, Machado MRS, Vasconcelos ATR, Schrank IS (2011) Genomics insight into the versatility of the plant growth promoting bacterium Azospirillum amazonense. BMC Genomics 12:409PubMedPubMedCentralGoogle Scholar
  116. Sarig S, Okon Y, Blum A (1990) Promotion of leaf area development and yield in Sorghum bicolor inoculated with Azospirillum brasilense. Symbiosis 9:235–245Google Scholar
  117. Saubidet MI, Barneix AJ (1998) Growth stimulation and nitrogen supply to wheat plants inoculated with Azospirillum brasilense. J Plant Nutr 21:2565–2577Google Scholar
  118. Saubidet MI, Fatta N, Barneix AJ (2002) The effect of inoculation with Azospirillum brasilense on growth and nitrogen utilization by wheat plants. Plant Soil 245:215–222Google Scholar
  119. Seshadri S, Muthukumuramasamy R, Lakshiminarasami C, Ignacimuthu S (2000) Solubilization of inorganic phosphates by Azospirillum halopraeferans. Curr Sci 79:565–567Google Scholar
  120. Sgroy V, Cassan F, Masciarelli O, Del Papa MF, Lagares A, Luna V (2009) Isolation and characterization of endophytic plant growth-promoting (PGPB) or stress homeostasis-regulating (PSHB) bacteria associated to the halophyte Prosopis strombulifera. Appl Microbiol Biotechnol 85:371–381PubMedGoogle Scholar
  121. Shah S, Karkhanis V, Desai A (1992) Isolation and characterization of siderophore, with antimicrobial activity, from Azospirillum lipoferum. Curr Microbiol 25:347–351Google Scholar
  122. Somers E, Ptacek D, Gysegom P, Srinivasan M, Vanderleyden J (2005) Azospirillum brasilense produces the auxin like phenylacetic acid by using the key enzyme for indole 3-acetic acid biosynthesis. Appl Environ Microbiol 71:1803–1810PubMedPubMedCentralGoogle Scholar
  123. Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448PubMedGoogle Scholar
  124. Spaepen S, Vanderleyden J, Okon Y (2009) Plant growth promoting actions of rhizobacteria. Adv Bot Res 51:283–320Google Scholar
  125. Steenhoudt O, Vanderleyden J (2000) Azospirillum, a free living nitrogen fixing bacterium closely associated with grasses: genetic, biochemistry and ecological aspects. FEMS Microbiol Rev 24:487–506PubMedGoogle Scholar
  126. Strzelczyk E, Kampert M, Li CY (1994) Cytokinin-like substances and ethylene production by Azospirillum in media with different carbon sources. Microbiol Res 149:55–60Google Scholar
  127. Sudhakar P, Chattopadhyay GN, Gangwar SK, Ghosh JK (2000) Effect of foliar application of Azotobacter, Azospirillum and Beijerinckia on leaf yield and quality of mulberry (Morus alba). J Agric Sci 134:227–234Google Scholar
  128. Tahir M, Mirza MS, Zaheer A, Dimitrov MR, Smidt H, Hameed S (2013) Isolation and identification of phosphate solubilizer Azospirillum, Bacillus and Enterobacter strain by 16S rRNA sequence analysis and their effect on growth of wheat (Triticum aestivum L.). Aust J Crop Sci 7(9):1284–1292Google Scholar
  129. Tapia-Hernandez A, Mascarua-Esparza M, Caballero-Mellado J (1990) Production of bacteriocins and siderophore-like activity by Azospirillum brasilense. Microbios 64:73–83PubMedGoogle Scholar
  130. Tarrand JJ, Kreig NR, Dobereiner J (1978) A taxonomic study of the Spirillum lipoferum group with description of a new genus Azospirillum gen.nov., and two species, Azospirillum lipoferum (Beijerinck) com nov. and Azospirillum brasilense sp. nov. Can J Microbiol 24:967–980PubMedGoogle Scholar
  131. Thuler DS, Floh EIS, Handro W, Barbosa HR (2003) Plant growth regulators and amino acids released by Azospirillum sp in chemically defined media. Lett Appl Microbiol 37:174–178PubMedGoogle Scholar
  132. Tien TM, Gaskins MH, Hubell DH (1979) Plant growth substances produced by Azospirillum brasilense and their effect on the growth of pearl millet (Pennisetum americanum L). Appl Environ Microbiol 37:1016–1024PubMedPubMedCentralGoogle Scholar
  133. Tortora ML, Diaz-Ricci JC, Pedraza RO (2011) Azospirillum brasilense siderophores with antifungal activity against Colletotrichum acutatum. Arch Microbiol 193:275–286PubMedGoogle Scholar
  134. Walker V, Bertrand C, Bellvert F, Moenne-Loccoz Y, Bally R (2011) Host plant secondary metabolite profiling shows a complex strain dependent response of maize to plant growth promoting rhizobacteria of the genus Azospirillum. New Phytol 189:494–506PubMedGoogle Scholar
  135. Wisniewski-Dye F, Lozano L, Acosta-Cruz E, Borland S, Drogue B, Prigent-Combaret C, Rouy Z, Barbe V, Herrera AM, Gonzalez B, Mavingui P (2012) Genome sequence of Azospirillum brasilense CBG497 and comparative analysis of Azospirillum core and accessory genomes provide insight into niche adaptation. Genes 3:576–602PubMedPubMedCentralGoogle Scholar
  136. Yahalom E, Okon Y, Dovrat A (1990) Possible mode of action of Azospirillum brasilense strain Cd on the root morphology and nodule formation in burr medic (Medicago polymorpha). Can J Microbiol 36:10–14Google Scholar
  137. Yasuda M, Isawa T, Shinozaki S, Minamisawa K, Nakashita H (2009) Effects of colonization of a bacterial endophyte, Azospirillum sp. B510, on disease resistance in rice. Biosci Biotechnol Biochem 73:2595–2599PubMedGoogle Scholar
  138. Zakharova E, Shcherbakov A, Brudnik V, Skripko N, Bulkhin N, Ignatov V (1999) Biosynthesis of indole-3-acetic acid in Azospirillum brasilense. Insights from quantum chemistry. Eur J Biochem 259:572–576PubMedGoogle Scholar
  139. Zakharova EA, Iosipenko AD, Ignatov VV (2000) Effect of water soluble vitamins on the production of indole-3-acetic acid by Azospirillum brasilense. Microbial Res 155:209–214Google Scholar
  140. Zhou Y, Wei W, Wang X, Xu L, Lai R (2009) Azospirillum palatum sp. nov. isolated from forest soil in Zhejiang province, China. J Gen Appl Microbiol 55:1–7PubMedGoogle Scholar
  141. Zimmer W, Roeben K, Bothe H (1988) An alternative explanation for plant growth promotion by bacteria of the genus Azospirillum. Planta 176:333–342PubMedGoogle Scholar

Copyright information

© Springer India 2015

Authors and Affiliations

  1. 1.Department of Biological SciencesForman Christian College (A Chartered University)LahorePakistan

Personalised recommendations