Journal of Plant Growth Regulation

, Volume 33, Issue 2, pp 440–459 | Cite as

Physiological and Agronomical Aspects of Phytohormone Production by Model Plant-Growth-Promoting Rhizobacteria (PGPR) Belonging to the Genus Azospirillum

  • Fabricio Cassán
  • Jos Vanderleyden
  • Stijn Spaepen


The functional analysis of phytohormone production, interaction, and regulation in higher plants has re-emerged in the past 10 years due to spectacular advances in integrative study models. However, plants are not axenic in natural conditions and are usually colonized or influenced directly by different microorganisms such as rhizobacteria of which many have the ability to produce phytohormones. This review summarizes information related to the biosynthesis, metabolism, regulation, physiological role, and agronomical impact of phytohormones produced by the model plant-growth-promoting rhizobacteria (PGPR) belonging to the genus Azospirillum, considered to be one of the most representative PGPR. We include exhaustive information about the phytohormones auxins, gibberellins, cytokinins, ethylene, and abscisic acid, as well as the plant growth regulators polyamines and nitric oxide. We deal with their metabolism by Azospirillum sp. in chemically defined medium, in plant–microbe interactions, or in the context of the agronomical use of Azospirillum sp.


Auxins Gibberellins Cytokinins Abscisic acid Ethylene Inoculants 



The review was written in the framework of a bilateral FWO-Vlaanderen-MINCyT research project (VS.011.11N) granted to FC and JV. FC is a researcher of Consejo Nacional de Investigaciones Científico-Tecnológicas (CONICET) and Universidad Nacional de Río Cuarto (UNRC) and SS is a recipient of a postdoctoral fellowship grant from Research Foundation Flanders (FWO-Vlaanderen). Special thanks to Yoav Bashan (CBNOR) and Cecilia Creus (INTA-UNMdP) for providing information to complete the phytohormonal model of Azospirillum sp.

Conflict of interest

The authors have no conflict of interest to disclose.


  1. Arshad M, Frankenberger R Jr (1993) Microbial production of plant growth regulators. In: Meeting B (ed) Soil microbial ecology. Marcel Dekker, New York, pp 307–347Google Scholar
  2. Aziz A, Martin-Tanguy J, Larher F (1997) Plasticity of polyamine metabolism associated with high osmotic stress in rape leaf discs and with ethylene treatment. Plant Growth Regul 21:153–163CrossRefGoogle Scholar
  3. Baca B, Soto-Urzua L, Xochiua-Corona Y, Cuervo-García A (1994) Characterization of two aromatic amino acid aminotransferases and production of indoleacetic acid in Azospirillum strains. Soil Biol Biochem 26:57–63CrossRefGoogle Scholar
  4. Baldani V, Alvarez M, Baldani J, Döbereiner J (1986) Establishment of inoculated Azospirillum spp. in the rhizosphere and in roots of field grown wheat and sorghum. Plant Soil 90:35–46CrossRefGoogle Scholar
  5. Bally R, Thomas-Bauzon D, Heulin T, Balandreau J (1983) Determination of the most frequent N2 fixing bacteria in the rice rhizosphere. Can J Microbiol 29:881–887CrossRefGoogle Scholar
  6. Bar T, Okon Y (1993) Tryptophan conversion to indole-3-acetic acid via indole-3-acetamide in Azospirillum brasilense Sp7. Can J Microbiol 39:81–86CrossRefGoogle Scholar
  7. Barbieri P, Bernardi A, Galli E, Zanetti G (1988) Effects of inoculation with different strains of A. brasilense on wheat roots development. In: Klingmüller W (ed) Azospirillum IV. Genetics, physiology, ecology. Springer, Berlin, pp 181–188Google Scholar
  8. Barea J, Navarro M, Montoya E (1976) Production of plant growth regulators by rhizosphere phosphate-solubilizing bacteria. J Appl Bacteriol 40:129–134PubMedCrossRefGoogle Scholar
  9. Bashan Y, de Bashan L (2010) How the plant growth-promoting bacterium Azospirillum promotes plant growth: a critical assessment. Adv Agron 108:77–136CrossRefGoogle Scholar
  10. Bashan Y, Holguín G (1998) Proposal for the division of plant growth-promoting rhizobacteria into two classifications: biocontrol-PGPB (plant growth promoting bacteria) and PGPB. Soil Biol Biochem 30:1225–1228CrossRefGoogle Scholar
  11. Bashan Y, Levanony H (1990) Current status of Azospirillum inoculation technology: Azospirillum as a challenge for agriculture. Can J Microbiol 36:591–608Google Scholar
  12. Baudoin E, Lerner A, Mirza MS, El Zemrany H, Prigent-Combaret C, Jurkevich E, Spaepen S, Vanderleyden J, Nazaret S, Okon Y et al (2010) Effects of Azospirillum brasilense with genetically modified auxin biosynthesis gene ipdC upon the diversity of the indigenous microbiota of the wheat rhizosphere. Res Microbiol 161:219–226PubMedCrossRefGoogle Scholar
  13. Bergersen F (1971) Biochemistry of symbiotic nitrogen fixation in legumes. Ann Rev Plant Physiol 22:121–140CrossRefGoogle Scholar
  14. Blaha D, Prigent-Combaret C, Mirza M, Möenne-Loccoz Y (2006) Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminase-encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. FEMS Microbiol Ecol 56:455–470PubMedCrossRefGoogle Scholar
  15. Bothe H, Körsgen H, Lehmaher T, Hundeshagen B (1992) Differential effects of Azospirillum, auxin and combined nitrogen on the growth of the roots of wheat. Symbiosis 13:167–179Google Scholar
  16. Bottini R, Fulchieri M, Pearce D, Pharis R (1989) Identification of gibberellins A1, A3, and Iso-A3 in cultures of A. lipoferum. Plant Physiol 90:45–47PubMedCentralPubMedCrossRefGoogle Scholar
  17. Bottini R, Cassán F, Piccoli P (2004) Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl Microbiol Biotechnol 65(5):497–503PubMedGoogle Scholar
  18. Burdman S, Volpin H, Kigel J, Kapulnik Y, Okon Y (1996) Promotion of nod gene inducers and nodulation in common bean (Phaseolus vulgaris) roots inoculated with Azospirillum brasilense Cd. Appl Environ Microbiol 62:3030–3033PubMedCentralPubMedGoogle Scholar
  19. Burg S (1962) The physiology of ethylene formation. Ann Rev Plant Physiol 13:265–302CrossRefGoogle Scholar
  20. Burg S, Burg P (1968) Ethylene formation in pea seedlings: its relation to the inhibition of bud growth caused by indole-3-acetic acid. Plant Physiol 43:1069–1073PubMedCentralPubMedCrossRefGoogle Scholar
  21. Cacciari I, Lippi D, Pietrosanti T (1989) Phytohormone-like substances produced by single and mixed diazotrophic cultures of Azospirillum spp. and Arthrobacter. Plant Soil 115:151–153CrossRefGoogle Scholar
  22. Carreño-López R, Campos-Reales C, Elmerich C, Baca B (2000) Physiological evidence for differently regulated tryptophan-dependent pathways for indole-3-acetic acid synthesis in Azospirillum brasilense. Mol Gen Genet 264:521–530PubMedCrossRefGoogle Scholar
  23. Cassán F, Bottini R, Piccoli P (2001a) In vivo gibberellin A9 metabolism by Azospirillum sp. in dy dwarf rice mutants seedlings. PGRSA Q 28:124–129Google Scholar
  24. Cassán F, Bottini R, Schneider G, Piccoli P (2001b) Azospirillum brasilense and Azospirillum lipoferum hydrolize conjugates of GA20 and metabolize the resultant aglycones to GA1 in seedlings of rice dwarf mutants. Plant Physiol 125:2053–2058PubMedCentralPubMedCrossRefGoogle Scholar
  25. Cassán F, Lucangelli C, Bottini R, Piccoli P (2001c) Azospirillum spp. metabolize [17,17-2H2]gibberellin A20 to [17,17-2H2] gibberellin A1 in vivo in dy rice mutant seedlings. Plant Cell Physiol 42:763–767PubMedCrossRefGoogle Scholar
  26. Cassán 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 45:12–19CrossRefGoogle Scholar
  27. Cassán F, Perrig D, Sgroy V, Masciarelli O, Penna C, Luna V (2009b) Azospirillum brasilense Az39 and Bradyrhizobium japonicum E 109 promote seed germination and early seedling growth, independently or co-inoculated in maize (Zea mays L.) and soybean (Glycine max L.). Eur J Soil Biol 45:28–35CrossRefGoogle Scholar
  28. Castro-Guerrero J, Romero A, Aguilar J, Xiqui M, Sandoval J, Baca B (2012) The hisC1 gene, encoding aromatic amino acid aminotransferase-1 in Azospirillum brasilense Sp7, expressed in wheat. Plant Soil 356:139–150CrossRefGoogle Scholar
  29. Charyulu P, Fourcassie F, Barbouche A, Rondro Harisoa L, Omar A, Weinhard P, Marie R, Balandreau J (1985) Field inoculation of rice using in vitro selected bacterial and plant genotypes. In: Klingmüller W (ed) Azospirillum III: genetics, physiology, ecology. Springer, Berlin, pp 163–179CrossRefGoogle Scholar
  30. Cohen A, Bottini R, Piccoli P (2008) Azospirillum brasilense Sp 245 produces ABA in chemically-defined culture medium and increases ABA content in Arabidopsis plants. Plant Growth Regul 54:97–103CrossRefGoogle Scholar
  31. Cohen A, Travaglia C, Bottini R, Piccoli P (2009) Participation of abscisic acid and gibberellins produced by endophytic Azospirillum in the alleviation of drought effects in maize. Botany 87:455–462CrossRefGoogle Scholar
  32. Combes-Meynet E, Pothier JF, Moënne-Loccoz Y, Prigent-Combaret C (2011) The Pseudomonas secondary metabolite 2,4-diacetylphloroglucinol is a signal inducing rhizoplane expression of Azospirillum genes involved in plant-growth promotion. Mol Plant Microbe Interact 24:271–284PubMedCrossRefGoogle Scholar
  33. Conney T, Nonhebel H (1991) Biosynthesis of indole-3-acetic acid in tomato shoots: measurement, mass-spectral identification and incorporation of 2H from 2H2O into indole-3-acetic acid, d- and l-tryptophan, indole-3-pyruvate and tryptamine. Planta 184:368–376Google Scholar
  34. Cooper J (2007) Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. J Appl Microbiol 103:1355–1365PubMedCrossRefGoogle Scholar
  35. Correa-Aragunde N, Graziano M, Chevalier C, Lamattina L (2006) Nitric oxide modulates the expression of cell cycle regulatory genes during lateral root formation in tomato. J Exp Bot 57:581–588PubMedCrossRefGoogle Scholar
  36. Costacurta A, Keijers V, Vanderleyden J (1994) Molecular cloning and sequence analysis of an Azospirillum brasilense indole-3-pyruvate deccarboxylase. Mol Gen Genet 243:463–472PubMedGoogle Scholar
  37. Creus C, Graziano M, Casanovas E, Pereyra A, Simontacchi M, Puntarulo S, Barassi C, Lamattina L (2005) Nitric oxide is involved in the Azospirillum brasilense-induced lateral root formation in tomato. Planta 221:297–303PubMedCrossRefGoogle Scholar
  38. Crozier A, Arruda P, Jasmim 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 54:2833–2837PubMedCentralPubMedGoogle Scholar
  39. Dardanelli M, Fernandez de Cordoba F, Espuny M, Rodriguez Carvajal M, Soria Diaz M, Gil Serrano A, Okon Y, Megias M (2008) Effect of Azospirillum brasilense coinoculated with Rhizobium on Phaseolus vulgaris flavonoids and Nod factor production under salt stress. Soil Biol Biochem 40:2713–2721CrossRefGoogle Scholar
  40. Davies P (1995) Plant hormones. physiology, biochemistry and molecular biology. Kluwer Academic, Dordrecht, p 833Google Scholar
  41. Díaz-Zorita M, Fernández Canigia M (2009) Field performance of a liquid formulation of Azospirillum brasilense on dryland wheat productivity. Eur J Soil Biol 45(1):3–11CrossRefGoogle Scholar
  42. 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 212:155–164CrossRefGoogle Scholar
  43. Esquivel-Cote R, Ramírez-Gama R, Tsuzuki-Reyes G, Orozco-Segovia A, Huante P (2010) Azospirillum lipoferum strain AZm5 containing 1-aminocyclopropane-1-carboxylic acid deaminase improves early growth of tomato seedlings under nitrogen deficiency. Plant Soil 337:65–75CrossRefGoogle Scholar
  44. Falik 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 21:147–153CrossRefGoogle Scholar
  45. Ford Y, Taylor J, Blake P, Marks P (2002) Gibberellin A3 stimulates adventitious rooting of cuttings from cherry (Prunus avium). Plant Growth Regul 37:127–133CrossRefGoogle Scholar
  46. Frankenberger W, Arshad M (1995) Phytohormones in soil. Marcel Dekker, New York, p 503Google Scholar
  47. Fulchieri M, Lucangelli C, Bottini R (1993) Inoculation with A. lipoferum affects growth and gibberellin status of corn seedlings roots. Plant Cell Physiol 34:1305–1309Google Scholar
  48. Gamarnik A, Frydman R (1991) Cadaverine, an essential diamine for the normal root development of germinating soybean (Glycine max) seeds. Plant Physiol 97:778–785PubMedCentralPubMedCrossRefGoogle Scholar
  49. Ge SM, Chen SF (2009) Expression and functional analysis of aminotransferase involved in indole-3-acetic acid biosynthesis in Azospirillum brasilense Yu62. Biochemistry (Moscow) 74(1):81–84CrossRefGoogle Scholar
  50. Glick B, Karaturovic D, Newell P (1995) A novel procedure for rapid isolation of plant growth promoting pseudomonads. Can J Microbiol 41:533–536CrossRefGoogle Scholar
  51. Glick B, Patten C, Holguin G, Penrose D (1999) Biochemical and genetic mechanisms used by plant growth promoting bacteria. Imperial College Press, London, p 267CrossRefGoogle Scholar
  52. Goris J, Kersters K, De Vos P (1998) Polyamines distribution among authentic Pseudomonads and Azotobacteraceae. Syst Appl Microbiol 21:285–290CrossRefGoogle Scholar
  53. Hamana K, Matsuzaki K, Sakakibara M (1988) Distribution of sym-homospermidine in eubacteria, cyanobacteria, algae and ferns. FEMS Microbiol Lett 50:11–16CrossRefGoogle Scholar
  54. Hamana K, Minamisawa K, Matsuzaki S (1990) Polyamines in Rhizobium, Bradyrhizobium, Azorhizobium and Agrobacterium. FEMS Microbiol Lett 71:71–76CrossRefGoogle Scholar
  55. Hartmann A, Singh M, Klingmüller W (1983) Isolation and characterization of Azospirillum mutants excreting high amounts of indoleacetic acid. Can J Microbiol 29:916–923CrossRefGoogle Scholar
  56. Hartmann A, Rothballer M, Schmid M (2008) Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant Soil 312:7–14CrossRefGoogle Scholar
  57. Hedden P, Phillips AL (2000) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5:523–530PubMedCrossRefGoogle Scholar
  58. Holguín G, Glick BR (2001) Expression of the ACC deaminase gene from Enterobacter cloacae UW4 in Azospirillum brasilense. Microb Ecol 41:281–288PubMedCrossRefGoogle Scholar
  59. Horemans S, Koninck K, Neuray J, Hermans R, Vlassak K (1986) Production of plant growth substances by Azospirillum sp. and other rhizophere bacteria. Symbiosis 2:341–346Google Scholar
  60. Hubbell D, Tien T, Gaskins M, Lee J (1979) Physiological interaction in the Azospirillum-grass root association. In: Vose P, Ruschel A (eds) Associative N2-fixation. CRC Press, Boca Raton, pp 1–6Google Scholar
  61. Inada S, Shimmen T (2000) Regulation of elongation growth by gibberellin in root segments of Lemna minor. Plant Cell Physiol 41:932–939PubMedCrossRefGoogle Scholar
  62. Janzen R, Rood S, Dormaar J, McGill W (1992) Azospirillum brasilense produces gibberellins in pure culture on chemically-defined medium and in co-culture on straw. Soil Biol Biochem 24:1061–1064CrossRefGoogle Scholar
  63. Kaneko T, Minamisawa K, Isawa T, Nakatsukasa H, Mitsui H et al (2010) Complete genomic structure of the cultivated rice endophyte Azospirillum sp. B510. DNA Res 17:37–50PubMedCentralPubMedCrossRefGoogle Scholar
  64. Klee H, Montoya A, Horodyski F, Lichenstein C, Garfinkel D, Fuller S, Flores C, Peschon J, Nester E, Gordon M (1984) Nucleotide sequence of the tms genes of the pTiANC octopine C plasmid: two genes products involved in plants tumorogenesis. P Natl Acad Sci USA 81:1728–1732CrossRefGoogle Scholar
  65. Kloepper J, Schroth M (1978) Plant growth-promoting rhizobacteria in radish. In Proceedings of the 4th international conference on plant pathogenic bacteria, vol 2. Angers, INRA, France, pp 879-882Google Scholar
  66. Kloepper J, Lifshitz R, Schroth M (1989) Pseudomonas inoculants to benefit plant production. ISI Atlas Sci Anim Plant Sci 8:60–64Google Scholar
  67. Kobayashi M, Sakurai A, Saka A, Takahashi N (1989) Quantitative analysis of endogenous gibberellins in normal and dwarf cultivars of rice. Plant Cell Physiol 30:963–969Google Scholar
  68. Kolb W, Martin P (1985) Response of plant roots to inoculation with Azospirillum brasilense and to application of indoleacetic acid. In: Klingmüller W (ed) Azospirillum III: genetics, physiology, ecology. Springer, Berlin, pp 215–221CrossRefGoogle Scholar
  69. Korasick DA, Enders TA, Strader LC (2013) Auxin biosynthesis and storage forms. J Exp Bot 64:2541–2555PubMedCentralPubMedCrossRefGoogle Scholar
  70. Krumpholz E, Ribaudo C, Cassán F, Bottini R, Cantore M, Curá A (2006) Azospirillum sp. promotes root hair development in tomato plants through a mechanism that involves ethylene. J Plant Growth Regul 25:175–185CrossRefGoogle Scholar
  71. Kucey R (1988) Alteration of size of wheat root systems and nitrogen fixation by associative nitrogen-fixing bacteria measured under field conditions. Can J Microbiol 34:735–739CrossRefGoogle Scholar
  72. Kuznetsov V, Radyukina N, Shevyakova N (2006) Polyamines and stress: biological role, metabolism, and regulation. Russ J Plant Physiol 53:583–604CrossRefGoogle Scholar
  73. Lamattina L, Polacco J (2007) Nitric oxide in plant growth development and stress physiology. Springer, Berlin, p 283CrossRefGoogle Scholar
  74. Lambrecht M, Vande Broek A, Dosselaere F, Vanderleyden J (1999) The ipdC promoter auxin-responsive element of Azospirillum brasilense, a prokaryotic ancestral form of the plant AusxRE? Mol Microbiol 32:889–890PubMedCrossRefGoogle Scholar
  75. Lambrecht M, Okon Y, Vande Broek A, Vanderleyden J (2000) Indole-3-acetic acid: a reciprocal signalling molecule in bacteria-plant interactions. Trends Microbiol 8:298–300PubMedCrossRefGoogle Scholar
  76. Letham D (1963) Zeatin, a factor inducing cell division from Zea mays. Life Sci 8:569–573PubMedCrossRefGoogle Scholar
  77. Liu K, Fu H, Bei Q, Luan S (2000) Inward potassium channel in guard cells as a target for polyamine regulation of stomatal movements. Plant Physiol 124:1315–1325PubMedCentralPubMedCrossRefGoogle Scholar
  78. Lucangelli 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
  79. Magalhães F, Baldani J, Souto S, Kuykendall J, Döbereiner J (1983) A new acid-tolerant Azospirillum species. An Acad Bras Ciênc 55:417–430Google Scholar
  80. Malhotra M, Srivastava S (2008) Organization of the ipdC region regulates IAA levels in different Azospirillum brasilense strains: molecular and functional analysis of ipdC in strain SM. Environ Microbiol 10:1365–1373PubMedCrossRefGoogle Scholar
  81. 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 45:73–80CrossRefGoogle Scholar
  82. Martínez-Morales L, Soto-Urzua L, Baca B, Sanchez-Ahedo J (2003) Indole-3-butyric acid (IBA) production in culture medium by wild strain Azospirillum brasilense. FEMS Microbiol Lett 228:167–173PubMedCrossRefGoogle Scholar
  83. Mathesius U, Shalaman H, Meijer D, Lugtenberg B, Spaink H, Weinman J, Rodam L, Sautter C, Rolfe B, Djordjevic M (1997) New tools for investigating nodule initiation and ontogeny: spot inoculation and microtargeting of transgenic withe clover roots shows auxin involvement and suggest a role for flavonoids. In: Stacey G, Mullin B, Gresshoff P (eds) Advances in molecular genetics of plant–microbe interactions. Kluwer Academic, DordrechtGoogle Scholar
  84. Miller C, Skoog F, Von Saltza M, Strong F (1955) Kinetin, a cell division factor from deoxyribonucleic acid. J Am Chem Soc 77:1392CrossRefGoogle Scholar
  85. Molina-Favero C, Creus C, Lanteri M, Correa-Aragunde N, Lombardo M, Barassi C, Lamattina L (2007) Nitric oxide and plant growth promoting rhizobacteria: common features influencing root growth and development. Adv Bot Res 46:1–33CrossRefGoogle Scholar
  86. Molina-Favero C, Creus C, 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 21:1001–1009PubMedCrossRefGoogle Scholar
  87. Murakami Y (1968) A new rice seedling bioassay for gibberellins, microdrop method and its use for testing extracts of rice and morning glory. Bot Mag 81:3–43Google Scholar
  88. Murakami Y (1972) Dwarfing genes in rice and their relation to gibberellin biosynthesis. In: Carr D (ed) Plant growth substances 1970. Springer, Berlin, pp 164–174Google Scholar
  89. Muralidhara R, Rai P (1986) Plant growth regulators produced by diazotrophic bacteria. National seminar on microbial ecology, January 23-24, 1986, Tamil Nadu Agricultural University, Tamil Nadu, India, pp 18-23Google Scholar
  90. Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185PubMedCrossRefGoogle Scholar
  91. Niemi K, Haggman H, Sarjala T (2001) Effects of exogenous diamines on the interaction between ectomycorrhizal fungi and adventitious root formation in Scots pine in vitro. Tree Physiol 22:373–381CrossRefGoogle Scholar
  92. Nonhebel H, Cooney T, Simpson R (1993) The route, control and compartmentation of auxin synthesis. Aust J Plant Physiol 20:527–539CrossRefGoogle Scholar
  93. Okon Y, Labandera-González C (1994) Agronomic applications of Azospirillum: an evaluation of 20 years worlwide field inoculation. Soil Biol Biochem 26:1591–1601CrossRefGoogle Scholar
  94. Omay S, Schmidt W, Martin P, Bangerth F (1993) Indoleacetic acid production by the rhizosphere bacterium Azospirillum brasilense Cd under in vitro conditions. Can J Microbiol 39:187–192CrossRefGoogle Scholar
  95. Ona O, Smets I, Gysegom P, Bernaerts K, Impe J, Prinsen E, Vanderleyden J (2003) The effect of pH on indole-3-acetic acid (IAA) biosynthesis of Azospirillum brasilense sp7. Symbiosis 35:199–208Google Scholar
  96. Ona O, van Impe J, Prinsen E, Vanderleyden J (2005) Growth and indole-3-acetic acid biosynthesis of Azospirillum brasilense Sp245 is environmentally controlled. FEMS Microbiol Lett 246:125–132PubMedCrossRefGoogle Scholar
  97. Patten C, Glick B (1996) Bacterial biosynthesis of indole 3-acetic acid. Can J Microbiol 42:207–220PubMedCrossRefGoogle Scholar
  98. Pearce D, Koshioka M, Pharis R (1994) Chromatography of gibberellins. J Chromatogr A 658:91–122CrossRefGoogle Scholar
  99. Pedraza R, Ramirez-Mata A, Xiqui M, Baca B (2004) Aromatic amino acid aminotransferase activity and indole-3-acetic acid production by associative nitrogen-fixing bacteria. FEMS Microbiol Lett 233:15–21PubMedCrossRefGoogle Scholar
  100. Perley J, Stowe B (1966) On the ability of Taphrina deformans to produce indole acetic acid from tryptophan by way of tryptamine. Plant Physiol 41:234–237PubMedCentralPubMedCrossRefGoogle Scholar
  101. Perrig D, Boiero L, Masciarelli O, Penna C, Cassán F, Luna V (2007) Plant growth promoting compounds produced by two agronomically important strains of Azospirillum brasilense, and their implications for inoculant formulation. Appl Microbiol Biotechnol 75:1143–1150PubMedCrossRefGoogle Scholar
  102. Phinney B, Spray C (1988) Dwarf mutants of maize-research tools for the analysis of growth. In: Pharis R, Rood S (eds) Plant growth substances 1988. Springer, Berlin, pp 65–73Google Scholar
  103. Piccoli P, Bottini R (1994a) Metabolism of 17,17-[2H2]-gibberellin A20 to 17,17-[2H2]-gibberellin A1 by A. lipoferum cultures. AgriScientiae 11:13–15Google Scholar
  104. Piccoli P, Bottini R (1994b) Effect of C/N ratio, N content, pH and incubation time on growth and gibberellin production by Azospirillum lipoferum cultures. Symbiosis 21:263–264Google Scholar
  105. Piccoli P, Bottini R (1996) Gibberellins production in A. lipoferum cultures and enhanced by light. Biocell 20:185–190Google Scholar
  106. Piccoli P, Lucangelli C, Schneider G, Bottini R (1997) Hydrolisis of 17,17-[2H2]-gibberellin A20-glucoside and 17,17-[2H2]-gibberellin A20-glucosyl ester by Azospirillum lipoferum cultured in nitrogen-free biotin-based chemycally-definded medium. Plant Growth Regul 23:179–182CrossRefGoogle Scholar
  107. 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 27:135–146Google Scholar
  108. Piotrowski M (2008) Primary or secondary? Versatile nitrilases in plant metabolism. Phytochemistry 69:2655–2667PubMedCrossRefGoogle Scholar
  109. Primrose S, Dilworth M (1976) Ethylene production by bacteria. J Gen Microbiol 93:177–181PubMedCrossRefGoogle Scholar
  110. Prinsen E, Costacurta A, Michiels K, Vanderleyden J, Van Onckelen H (1993) Azospirillum brasilense indole-3-acetic acid biosynthesis: evidence for a non-tryptophan dependent pathway. Mol Plant Microbe Interact 6:609–615CrossRefGoogle Scholar
  111. Rademacher W (2000) Growth retardants: effects on gibberellin biosynthesis and other metabolic pathways. Ann Rev Plant Physiol Plant Mol Biol 51:501–531CrossRefGoogle Scholar
  112. Rahman A, Hosokawa S, Oono Y, Amakawa T, Goto N, Tsurumi S (2002) Auxin and ethylene response interactions during Arabidopsis root hair development diss. Plant Physiol 130:1908–1917PubMedCentralPubMedCrossRefGoogle Scholar
  113. Remans R, Beebe S, Blair M, Marique G, Tovar E, Rao I, Croonenbarghs A, Torres-Gutierrez R, El-Idoweity M, Michiels J, Vanderlyden J (2008a) Physiological and genetic analysis of root responsiveness to auxin-producing plant growth promoting bacteria in common bean (Phaseolus vulgaris L.). Plant Soil 302:149–161CrossRefGoogle Scholar
  114. Remans R, Schelkens S, Hernandez G, Garcia A, Luis Reyes J, Mendez N, Toscano V, Mulling M, Galvez L, Vanderleyden J (2008b) Effect of RihzobiumAzospirillum coinoculation on nitrogen fixation and yield of two contrasting Phaseolus vulgaris L. genotypes cultivated across different environments in cube. Plant Soil 312:25–37CrossRefGoogle Scholar
  115. Rodrigues E, Rodrigues L, de Oliveira A, Baldani V, Teixeira K, Urquiaga S, Reis V (2008) Azospirillum amazonense inoculation: effects on growth, yield and N2 fixation of rice (Oryza sativa L.). Plant Soil 302:249–261CrossRefGoogle Scholar
  116. Rood S, Pharis R (1987) Evidence for reversible conjugation of gibberellins in higher plants. In: Schreiber H, Schutte H, Semder G (eds), Conjugated plant hormones. Structure, metabolism and function. In Proceedings of the international symposium conjugated plant hormones: structure, metabolism and function held in Gera, Germany. Berlin, VEB Deustcher Verlag der Wissenschaften, pp 183-190Google Scholar
  117. Ross J, O’Neill D (2001) New interactions between classical plant hormones. Trends Plant Sci 6:2–4Google Scholar
  118. Rothballer M, Schmid M, Fekete A, Hartmann A (2005) Comparative in situ analysis of ipdC-gfpmut3 promoter fusions of Azospirillum brasilense Sp7 and Sp245. Environ Microbiol 7:1839–1846PubMedCrossRefGoogle Scholar
  119. Ruckäschel E, Klingmüller W (1992) Analysis of IAA biosynthesis in Azospirillum lipoferum and Tn5 induced mutants. Symbiosis 13:123–131Google Scholar
  120. Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57:431–449Google Scholar
  121. Sant’Anna F, Almeida L, Cecagno R, Reolon L, Siqueira F, Machado M, Vasconcelos A, Schrank I (2011) Genomic insights into the versatility of the plant growth-promoting bacterium Azospirillum amazonense. BMC Genomics 12:409PubMedCentralPubMedCrossRefGoogle Scholar
  122. Schmidt W, Martin P, Omay H, Bangerth F (1988) Influence of Azospirillum brasilense on nodulation of legumes. In: Klingmüller W (ed) Azospirillim IV. Genetics, physiology, ecology. Springer, Heidelberg, pp 92–100Google Scholar
  123. Sembder G, Gross D, Liebisch H, Schneider G (1980) Biosynthesis and metabolism of plant hormones. In: MacMillan J (ed) Encyclopedia of plant physiology, new series. Springer, Berlin, pp 281–444Google Scholar
  124. 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 Microb 71:1803–1810CrossRefGoogle Scholar
  125. Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448PubMedCrossRefGoogle Scholar
  126. Spaepen S, Dobbelaere S, Croonenborghs A, Vanderleyden J (2008) Effects of Azospirillum brasilense indole-3-acetic acid production on inoculated wheat plants. Plant Soil 312:15–23CrossRefGoogle Scholar
  127. Strzelczyk E, Kamper M, Li C (1994) Cytokinin-like substances and ethylene production by Azospirillum in media with different carbon sources. Microbiol Res 149:55–60CrossRefGoogle Scholar
  128. Teale W, Paponov I, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859PubMedCrossRefGoogle Scholar
  129. Thiman K (1936) On the physiology of the formation of nodule in legumes roots. Proc Natl Acad Sci USA 22:511–514CrossRefGoogle Scholar
  130. Thuler D, Floh E, Handro W, Barbosa H (2003a) Beijerinckia derxii releases plant growth regulators and amino acids in synthetic media independent of nitrogenase activity. J Appl Microbiol 95:799–806PubMedCrossRefGoogle Scholar
  131. Thuler D, Floh E, Handro W, Barbosa H (2003b) Plant growth regulators and amino acids released by Azospirillum sp. in chemically defined media. Lett Appl Microbiol 37:174–178PubMedCrossRefGoogle Scholar
  132. Tien T, Gaskins M, Hubbell D (1979) Plant growth substances produced by Azsopirillum brasilense and their effect on the growth of pearl millet (Pennisetum americanum L.). Appl Environ Microbiol 37:1016–1024PubMedCentralPubMedGoogle Scholar
  133. Van Laer S (2003) PhD thesis, University of Antwerpen, BelgiumGoogle Scholar
  134. Van Puyvelde S, Cloots L, Engelen K, Das F, Marchal K, Vanderleyden J, Spaepen S (2011) Transcriptome analysis of the rhizosphere bacterium Azospirillum brasilense reveals an extensive auxin response. Microb Ecol 61:723–728PubMedCrossRefGoogle Scholar
  135. Vande Broek A, Lambrecht M, Eggermont K, Vanderleyden J (1999) Auxins upregulate expression of the indole-3-pyruvate decarboxylase gene in Azospirillum brasilense. J Bacteriol 181:1338–1342PubMedCentralPubMedGoogle Scholar
  136. Vande Broek A, Gysegom P, Ona O, Hendrickx N, Prinsen E, Van Impe J, Vanderleyden J (2005) Transcriptional analysis of the Azospirillum brasilense indole-3-pyruvate decarboxylase gene and identification of a cis-acting sequence involved in auxin responsive expression. Mol Plant Microbe Interact 18(4):311–323PubMedCrossRefGoogle Scholar
  137. Vorwerk S, Biernacki S, Hillebrand H, Janzik I, Muller A, Weiler E, Piotrowski M (2001) Enzymatic characterization of the recombinant Arabidopsis thaliana nitrilase subfamily encoded by the NIT2/NIT1/NIT3-gene cluster. Planta 212:508–516PubMedCrossRefGoogle Scholar
  138. Wisniewski-Dyé F, Borziak K, Khalsa-Moyers G, Alexandre G, Sukharnikov L et al (2011) Azospirillum genomes reveal transition of bacteria from aquatic to terrestrial environments. PLoS Genet 7(12):e1002430PubMedCentralPubMedCrossRefGoogle Scholar
  139. Wisniewski-Dyé F, Lozano L, Acosta-Cruz E, Borland S, Drogue B, Prigent-Combaret et al (2012) Genome sequence of Azospirillum brasilense CBG497 and comparative analyses of Azospirillum core and accessory genomes provide insight into niche adaptation. Genes 3:576–602PubMedCentralPubMedCrossRefGoogle Scholar
  140. Yahalom E, Okon Y, Dovrat A (1990) Possible mode of action of Azospirillum brasilense strain Cd on the roots morphology and nodule formation in burr medic (Medicago polymorpha). Can J Microbiol 36:10–14CrossRefGoogle Scholar
  141. Yaxley J, Ross J, Sherriff L, Reid J (2001) Gibberellin biosynthesis mutations and root development in pea. Plant Physiol 125:627–633PubMedCentralPubMedCrossRefGoogle Scholar
  142. Zeevaart J (1999) Abscisic acid metabolism and its regulation. In: Hooykaas P, Hall M, Libbenga K (eds) Biochemistry and molecular biology of plant hormones. Elsevier Science, Amsterdam, pp 189–207CrossRefGoogle Scholar
  143. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273PubMedCentralPubMedCrossRefGoogle Scholar
  144. Zimmer W, Roeben K, Bothe H (1988) An alternative explanation for plant growth promotion by bacteria of the genus Azospirillum. Planta 176:333–342PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Fabricio Cassán
    • 1
  • Jos Vanderleyden
    • 2
  • Stijn Spaepen
    • 2
  1. 1.Laboratorio de Fisiología Vegetal y de la Interacción planta-microorganismoUniversidad Nacional de Río CuartoRío CuartoArgentina
  2. 2.Centre of Microbial and Plant GeneticsKU LeuvenHeverleeBelgium

Personalised recommendations