Everything you must know about Azospirillum and its impact on agriculture and beyond

Abstract

Azospirillum is one of the most studied plant growth-promoting bacteria (PGPB); it represents a common model for plant-bacterial interactions. While Azospirillum brasilense is the species that is most widely known, at least 22 species, including 17 firmly validated species, have been identified, isolated from agricultural soils as well as habitats as diverse as contaminated soils, fermented products, sulfide springs, and microbial fuel cells. Over the last 40 years, studies on Azospirillum-plant interactions have introduced a wide array of mechanisms to demonstrate the beneficial impacts of this bacterium on plant growth. Multiple phytohormones, plant regulators, nitrogen fixation, phosphate solubilization, a variety of small-sized molecules and enzymes, enhanced membrane activity, proliferation of the root system, enhanced water and mineral uptake, mitigation of environmental stressors, and competition against pathogens have been studied, leading to the concept of the Multiple Mechanisms Hypothesis. This hypothesis is based on the assumption that no single mechanism is involved in the promotion of plant growth; it posits that each case of inoculation entails a combination of a few or many mechanisms. Looking specifically at the vast amount of information about the stimulatory effect of phytohormones on root development and biological nitrogen fixation, the Efficient Nutrients Acquisition Hypothesis model is proposed. Due to the existence of extensive agriculture that covers an area of more than 60 million hectares of crops, such as soybeans, corn, and wheat, for which the bacterium has proven to have some agronomic efficiency, the commercial use of Azospirillum is widespread in South America, with over 100 products already in the market in Argentina, Brazil, and Uruguay. Studies on Azospirillum inoculation in several crops have shown positive and variable results, due in part to crop management practices and environmental conditions. The combined inoculation of legumes with rhizobia and Azospirillum (co-inoculation) has become an emerging agriculture practice in the last several years, mainly for soybeans, showing high reproducibility and efficiency under field conditions. This review also addresses the use of Azospirillum for purposes other than agriculture, such as the recovery of eroded soils or the bioremediation of contaminated soils. Furthermore, the synthetic mutualistic interaction of Azospirillum with green microalgae has been developed as a new and promising biotechnological application, extending its use beyond agriculture.

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References

  1. Amavizca E, Bashan Y, Ryu C-M, Farag MA, Bebout BM, de-Bashan LE (2017) Enhanced performance of the microalga Chlorella sorokiniana remotely induced by the plant growth-promoting bacteria Azospirillum brasilense and Bacillus pumilus. Sci Rep-Nature 7:41310. https://doi.org/10.1038/srep41310

    Article  CAS  Google Scholar 

  2. Anandham R, Heo J, Krishnamoorthy R, SenthilKumar M, Gopal NO, Kim SJ, Kwon SW (2019) Azospirillum ramasamyi sp. nov. a novel diazotrophic bacterium isolated from fermented bovine products. Int J Syst Evol Microbiol 69:1369–1375. https://doi.org/10.1099/ijsem.0.003320

    Article  PubMed  CAS  Google Scholar 

  3. Arora K, Sharma S, Monti A (2016) Bio-remediation of Pb and Cd polluted soils by switchgrass: a case study in India. Int J Phytoremediat 18:704–709. https://doi.org/10.1080/15226514.2015.1131232

    Article  CAS  Google Scholar 

  4. Baldani J, Baldani V (2005) History on the biological nitrogen fixation research in graminaceous plants: special emphasis on the Brazilian experience. An Acad Bras Cienc 77:549–579. https://doi.org/10.1590/S0001-37652005000300014

    Article  PubMed  CAS  Google Scholar 

  5. Baldani JI, Krieg NR, Baldani VLD, Hartmannand A, Dobereiner J (2005) Genus II. Azospirillum. In: Brenner DJ, Krieg NR, Staley JT (eds) Bergey’s manual of systematic bacteriology, vol 2C. Springer, New York, pp 7–26

    Google Scholar 

  6. Barea JM, Bonis AF, Olivares J (1983) Interactions between Azospirillum and VA mycorrhiza and their effects on growth and nutrition of maize and ryegrass. Soil Biol Biochem 15:705–709. https://doi.org/10.1016/0038-0717(83)90036-6

    Article  Google Scholar 

  7. Bashan Y, de-Bashan LE (2010) How the plant growth-promoting bacterium Azospirillum promotes plant growth—a critical assessment. Adv Agron 108:77–136. https://doi.org/10.1016/S0065-2113(10)08002-8

    Article  CAS  Google Scholar 

  8. Bashan Y, Holguin G (1997) Azospirillum–plant relationships: environmental and physiological advances (1990–1996). Can J Microbiol 43:103–112. https://doi.org/10.1139/m97-015

    Article  CAS  Google Scholar 

  9. Bashan Y, Levanony H (1990) Current status of Azospirillum inoculation technology: Azospirillum as a challenge for agriculture. Can J Microbiol 36:591–608. https://doi.org/10.1139/m90-105

    Article  CAS  Google Scholar 

  10. Bashan Y, Rojas A, Puente ME (1999) Improved establishment and development of three cactus species inoculated with Azospirillum brasilense transplanted into disturbed urban soil. Can J Microbiol 45:441–451. https://doi.org/10.1139/w99-043

    Article  CAS  Google Scholar 

  11. Bashan Y, Holguin G, de-Bashan LE (2004) Azospirillum-plant relationships: physiological, molecular, agricultural and environmental advances (1997-2003). Can J Microbiol 50:521–577. https://doi.org/10.1139/w04-035

    Article  PubMed  CAS  Google Scholar 

  12. Bashan Y, Salazar BG, Moreno M, Lopez BR, Linderman RG (2012) Restoration of eroded soil in the Sonoran Desert with native leguminous trees using plant growth-promoting microorganisms and limited amounts of compost and water. J Environ Manag 102:26–36. https://doi.org/10.1016/j.jenvman.2011.12.032

    Article  CAS  Google Scholar 

  13. Beijerinck MW (1925) Uber ein Spirillum welches frei en Stick-stoff binden kann? Zentralbl Bakteriol 63:353–359

    CAS  Google Scholar 

  14. Ben Dekhil S, Cahill M, Stackebrt E, Sly LI (1997) Transfer of Conglomeromonas largomobilis subsp. largomobilis to the genus Azospirillum as Azospirillum largimobile comb. nov. and elevation of Conglomeromonas largomobilis subsp. parooensis to the new type species of Conglomeromonas Conglomeromonas parooensis sp. nov. Syst Appl Microbiol 20:72–77. https://doi.org/10.1016/S0723-2020(97)80050-1

    Article  Google Scholar 

  15. Benintende S, Uhrich W, Herrera M, Gangge F, Sterren M, Benintende M (2010) Comparación entre coinoculación con Bradyrhizobium japonicum y Azospirillum brasilense e inoculación simple con Bradyrhizobium japonicum en la nodulación, crecimiento y acumulación de N en el cultivo de soja. Agriscientia 27:71–77. https://doi.org/10.31047/1668.298x.v27.n2.2768

    Article  Google Scholar 

  16. Boddey R, Knowles R (1987) Methods for quantification of nitrogen fixation associated with gramineae. Crit Rev Plant Sci 6:209–266. https://doi.org/10.1080/07352688709382251

    Article  CAS  Google Scholar 

  17. Bottini R, Fulchieri M, Pearce D, Pharis RP (1989) Identification of gibberellins A1, A3 and iso-A3 in cultures of Azospirillum lipoferum. Plant Physiol 90:45–47. https://doi.org/10.1104/pp.90.1.45

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Broek AV, Lambrecht M, Eggermont K, Vanderleyden J (1999) Auxins upregulate expression of the indole-3-pyruvate decarboxylase gene in Azospirillum brasilense. J Bacteriol 181:1338–1342. https://doi.org/10.1128/JB.181.4.1338-1342.1999

    Article  Google Scholar 

  19. Cassán F, Diaz-Zorita M (2016) Azospirillum sp. in current agriculture: from the laboratory to the field. Soil Biol Biochem 103:117–130. https://doi.org/10.1016/j.soilbio.2016.08.020

    Article  CAS  Google Scholar 

  20. Cassán F, Perrig D, Sgroy V, Masciarelli O, Penna C, Luna V (2009) 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 45:28–35. https://doi.org/10.1016/j.ejsobi.2008.08.005

    Article  CAS  Google Scholar 

  21. Cassán F, Vanderleyden J, Spaepen S (2014) Physiological and agronomical aspects of phytohormone production by model plant-growth-promoting rhizobacteria (PGPR) belonging to the genus Azospirillum. J Plant Growth Regul 33:440–459. https://doi.org/10.1007/s00344-013-9362-4

    Article  CAS  Google Scholar 

  22. Cerezini P, Kuwano BH, dos Santos MB, Terassi F, Hungria M, Nogueira MA (2016) Strategies to promote early nodulation in soybean under drought. Field Crop Res 196:160–167. https://doi.org/10.1016/j.fcr.2016.06.017

    Article  Google Scholar 

  23. Chibeba AM, Guimarães MD, Brito OR, Nogueira MA, Araujo RS, Hungria M (2015) Co-inoculation of soybean with Bradyrhizobium and Azospirillum promotes early nodulation. Am J Plant Sci 6:1641–1649. https://doi.org/10.4236/ajps.2015.610164

    Article  Google Scholar 

  24. Choix FJ, de-Bashan LE, Bashan Y (2012a) Enhanced accumulation of starch and total carbohydrates in alginate-immobilized Chlorella spp. induced by Azospirillum brasilense. I. Autotrophic conditions. Enzyme Microb Tech 51:294–299. https://doi.org/10.1016/j.enzmictec.2012.07.012

    Article  CAS  Google Scholar 

  25. Choix FJ, de-Bashan LE, Bashan Y (2012b) Enhanced accumulation of starch and total carbohydrates in alginate-immobilized Chlorella spp. induced by Azospirillum brasilense. II. Heterotrophic conditions. Enzyme Microb Tech 51:300–309. https://doi.org/10.1016/j.enzmictec.2012.07.012

    Article  CAS  Google Scholar 

  26. Choix FJ, Bashan Y, Mendoza A, de-Bashan LE (2014) Enhanced activity of ADP glucose pyrophosphorylase and formation of starch induced by Azospirillum brasilense in Chlorella vulgaris. J Biotechnol 177:22–34. https://doi.org/10.1016/j.jbiotec.2014.02.014

    Article  PubMed  CAS  Google Scholar 

  27. Choix FJ, Lopez-Cisneros CG, Mendez-Acosta HO (2018) Azospirillum brasilense increases CO2 fixation on microalgae Scenedesmus obliquus, Chlorella vulgaris, and Chlamydomonas reinhardtii cultured on high CO2 concentrations. Microb Ecol 76:430–442. https://doi.org/10.1007/s00248-017-1139-z

    Article  PubMed  CAS  Google Scholar 

  28. Christiansen-Weniger C (1997) Ammonium-excreting Azospirillum brasilense C3:gusA inhabiting induced tumors along stem and roots of rice. Soil Biol Biochem 29:943–950. https://doi.org/10.1016/S0038-0717(96)00224-6

    Article  CAS  Google Scholar 

  29. Christiansen-Weniger C, van Veen JA (1991) NH4+-excreting Azospirillum brasilense mutants enhance the nitrogen supply of a wheat host. Appl Environ Microbiol 57:3006–3012. https://doi.org/10.1128/AEM.57.10.3006-3012.1991

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Costacurta A, Keijers V, Vanderleyden J (1994) Molecular cloning and sequence analysis of an Azospirilium brasilense indole-3-pyruvate decarboxylase gene. Mol Gen Genet 243:463–472. https://doi.org/10.1007/BF00280477

    Article  PubMed  CAS  Google Scholar 

  31. Creus CM, Graziano M, Casanovas EM, Pereyra MA, Simontacchi M, Puntarulo S, Barassi C, Lamattina L (2005) Nitric oxide is involved in the Azospirillum brasilense-induced lateral root formation in tomato. Planta 221:297–303. https://doi.org/10.1007/s00425-005-1523-7

    Article  PubMed  CAS  Google Scholar 

  32. 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 54:2833–2837. https://doi.org/10.1128/AEM.54.11.2833-2837.1988

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Day JM, Döbereiner J (1976) Physiological aspects of N,-fixation by a Spirillum from Digitaria roots. Soil Biol Biochem 8:45–50. https://doi.org/10.1016/0038-0717(76)90020-1

    Article  CAS  Google Scholar 

  34. 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 74:6797–6802. https://doi.org/10.1128/AEM.00518-08

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. de-Bashan LE, Bashan Y, Moreno M, Lebsky VK, Bustillos JJ (2002) Increased pigment and lipid content, lipid variety, and cell and population size of the microalgae Chlorella spp. when co-immobilized in alginate beads with the microalgae-growth-promoting bacterium Azospirillum brasilense. Can J Microbiol 48:514–521. https://doi.org/10.1139/w02-051

    Article  PubMed  CAS  Google Scholar 

  36. de-Bashan LE, Antoun H, Bashan Y (2008a) Involvement of indole-3-acetic-acid produced by the growth-promoting bacterium Azospirillum spp. in promoting growth of Chlorella vulgaris. J Phycol 44:938–947. https://doi.org/10.1111/j.1529-8817.2008.00533.x

    Article  PubMed  CAS  Google Scholar 

  37. de-Bashan LE, Magallon P, Antoun H, Bashan Y (2008b) Role of glutamate dehydrogenase and glutamine synthetase in Chlorella vulgaris during assimilation of ammonium when jointly immobilized with the microalgae-growth-promoting bacterium Azospirillum brasilense. J Phycol 44:1188–1196. https://doi.org/10.1111/j.1529-8817.2008.00572.x

    Article  PubMed  CAS  Google Scholar 

  38. de-Bashan LE, Hernandez JP, Nelson KN, Bashan Y, Maier RM (2010) Growth of quailbush in acidic, metalliferous desert mine tailings: effect of Azospirillum brasilense Sp6 on biomass production and rhizosphere community structure. Microb Ecol 60:915–927. https://doi.org/10.1007/s00248-010-9713-7

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. de-Bashan LE, Hernandez J-P, Bashan Y (2012) The potential contribution of plant growth-promoting bacteria to reduce environmental degradation—a comprehensive evaluation. Appl Soil Ecol 61:171–189. https://doi.org/10.1016/j.apsoil.2011.09.003

    Article  Google Scholar 

  40. de-Bashan LE, Mayali X, Bebout BM, Weber PK, Detweiler A, Hernandez J-P, Prufert-Bebout L, Bashan Y (2016) Establishment of stable synthetic mutualism without co-evolution between microalgae and bacteria demonstrated by mutual transfer of metabolites (NanoSIMS isotopic imaging) and persistent physical association (fluorescent in situ hybridization). Algal Res 15:179–186. https://doi.org/10.1016/j.algal.2016.02.019

    Article  Google Scholar 

  41. de Souza E, Pedrosa F (2015) Inorganic nitrogen metabolism in Azospirillum spp. In: Cassan F, Okon Y, Creus C (eds) Handbook for Azospirillum: technical issues and protocols. Springer International Publishing Switzerland, pp 139–153. https://doi.org/10.1007/978-3-319-06542-7_8

  42. Díaz-Zorita M (2012) Avaliacao da producao de milho (Zea mays L.) inoculado com Azospirillum brasilense na Argentina. In: Paterniani MEAGZ, Duarte AP, Tsunechiro A (eds) Diversidade e Innovações na Cadeia Produtiva de Milho e Sorgo na Era dos Transgênicos. Instituto Agronômico-Associação Brasileira de Milho e Sorgo Campinas (SP Brazil), pp 529–536

  43. Díaz-Zorita M, Fernández-Canigia MV (2009) Field performance of a liquid formulation of Azospirillum brasilense on dryland, wheat productivity. Eur J Soil Biol 45:3–11. https://doi.org/10.1016/j.ejsobi.2008.07.001

    Article  Google Scholar 

  44. Díaz-Zorita M, Fernández-Canigia MV, Bravo OA, Berger A, Satorre EH (2015) Field evaluation of extensive crops inoculated with Azospirillum sp. In: Cassan FD, Okon Y, Creus CM (eds) Handbook for Azospirillum Technical issues and protocols. Springer International Publishing, Switzerland, pp 435–445. https://doi.org/10.1007/978-3-319-06542-7_24

    Google Scholar 

  45. Dobbelaere S, Croonenborghs A, Thys A, Broek AV, Vanderleyden J (1999) Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil 212:153–162. https://doi.org/10.1023/A:1004658000815

    Article  Google Scholar 

  46. Döbereiner J, Marriel IE, Nery M (1976) Ecological distribution of Spirillum lipoferum Beijerinck. Can J Microbiol 22:1464–1473. https://doi.org/10.1139/m76-217

    Article  PubMed  Google Scholar 

  47. Dubrovsky JG, Puente ME, Bashan Y (1994) Arabidopsis thaliana as a model system for the study of the effect of inoculation by Azospirillum brasilense Sp-245 on root hair growth. Soil Biol Biochem 26:1657–1664. https://doi.org/10.1016/0038-0717(94)90318-2

    Article  CAS  Google Scholar 

  48. 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 51:17–26. https://doi.org/10.1099/00207713-51-1-17

    Article  PubMed  CAS  Google Scholar 

  49. Falk EC, Döbereiner J, Johnson JL, Krieg NR (1985) Deoxyribonucleic acid homology of Azospirillum amazonense Magalhaes et al. 1984 and emendation of the description of the genus Azospirillum. Int J Syst Evol Microbiol 35:117–118. https://doi.org/10.1099/00207713-35-1-117

    Article  CAS  Google Scholar 

  50. Fallik E, Sarig S, Okon Y (1994) Morphology and physiology of plant roots associated with Azospirillum. In: Okon Y (ed) Azospirillum/plant associations. CRC Press, Boca Raton, pp 77–85

    Google Scholar 

  51. Ferraris G, Couretot L (2011) Interacción entre microorganismos fijadores de nitrógeno y promotores de crecimiento (PGPM) en soja. I. Bradyrhizobium japonicum y Azospirillum brasilense: efectos sobre la nodulación el rendimiento y su interacción con prácticas de manejo. INTA EEA Pergamino Desarrollo Rural-Unidad Territorial Agricola. Campaña 2010/11

  52. Ferraris G, Couretot L (2013) Evaluación de tratamientos biológicos con Bradyrhizobium japonicum y Azospirillum brasilense en soja: efectos sobre la fijación de nitrógeno y el rendimiento. INTA EEA Pergamino Desarrollo Rural-Unidad Territorial Agricola. Campaña 2012/13

  53. Fipke GM, Conceição GM, Grando LFT, Ludwig RL, Nunes UR, Martin TN (2016) Co-inoculation with diazotrophic bacteria in soybeans associated to urea topdressing. Cienc Agrotec 40:522–533. https://doi.org/10.1590/1413-70542016405001316

    Article  CAS  Google Scholar 

  54. Fomenkov A, Vincze T, Grabovich M, Anton BP, Dubinina G, Orlova M, Belousova E, Roberts RJ (2016) Complete genome sequence of a strain of Azospirillum thiophilum isolated from a sulfide spring. Genome Announc 4:e01521–e01515. https://doi.org/10.1128/genomeA.01521-15

    Article  PubMed  PubMed Central  Google Scholar 

  55. Fontana CA, Salazar SM, Bassi D, Puglisi E, Lovaisa N, Toffoli LM, Pedraza R, Cocconcelli PS (2018) Genome sequence of Azospirillum brasilense REC3, isolated from strawberry plants. Genome Announc 6:e00089–e00018. https://doi.org/10.1128/genomeA.00089-18

    Article  PubMed  PubMed Central  Google Scholar 

  56. Fukami J, Nogueira MA, Araujo RS, Hungria M (2016) Accessing inoculation methods of maize and wheat with Azospirillum brasilense. AMB Express 6(3):13. https://doi.org/10.1186/s13568-015-0171-y

    Article  CAS  Google Scholar 

  57. Galindo FS, Teixeira Filho M, Buzetti S, Ludkiewicz MG, Rosa PA, Tritapepe CA (2018) Technical and economic viability of co-inoculation with Azospirillum brasilense in soybean cultivars in the Cerrado. Rev Bras Eng Agr Amb 22:51–56. https://doi.org/10.1590/1807-1929/agriambi.v22n1p51-56

    Article  Google Scholar 

  58. Gonzalez LE, Bashan Y (2000) Increased growth promotion of the microalgae Chlorella vulgaris when coimmobilized and cocultured in alginate beads with the plant growth-promoting bacteria Azospirillum brasilense. Appl Environ Microbiol 66:1527–1531. https://doi.org/10.1128/AEM.66.4.1527-1531.2000

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Grouzdev DS, Tikhonova EN, Krutkina MS, Kravchenko IK (2018) Genome sequence of methylotrophic Azospirillum sp. strain B2, isolated from a raised Sphagnum bog. Genome Announc 6:e00492–e00418. https://doi.org/10.1128/genomeA.00492-18

    Article  PubMed  PubMed Central  Google Scholar 

  60. Gualpa J, Lopez G, Nievas S, Coniglio A, Halliday N, Cámara M, Cassán F (2019) Azospirillum brasilense Az39, a model rhizobacterium with AHL quorum-quenching capacity. J Appl Microbiol 126:1850–1860. https://doi.org/10.1111/jam.14269

    Article  PubMed  CAS  Google Scholar 

  61. Hadas R, Okon Y (1987) Effect of Azospirillum brasilense inoculation on root morphology and respiration in tomato seedlings. Biol Fertil Soils 5:241–247. https://doi.org/10.1007/BF00256908

    Article  Google Scholar 

  62. Hartmann A, Singh M, Klingmüller W (1983) Isolation and characterization of Azospirillum mutants excreting high amounts of indoleacetic acid. Can J Microbiol 29:916–923. https://doi.org/10.1139/m83-147

    Article  CAS  Google Scholar 

  63. Horemans S, de Koninck K, Neuray J, Hermans R, Valassak K (1986) Production of plant growth substances by Azospirillum sp. and other rhizosphere bacteria. Symbiosis 2:341–346

  64. Hungria M, Nogueira MA, Araujo RS (2013) Co-inoculation of soybeans and common beans with rhizobia and azospirilla: strategies to improve sustainability. Biol Fertil Soils 49:791–801. https://doi.org/10.1007/s00374-012-0771-5

    Article  Google Scholar 

  65. Hungria M, Nogueira MA, Araujo RS (2015) Soybean seed co-inoculation with Bradyrhizobium spp. and Azospirillum brasilense: a new biotechnological tool to improve yield and sustainability. Am J Plant Sci 6:811–817. https://doi.org/10.4236/ajps.2015.66087

    Article  CAS  Google Scholar 

  66. Hungria M, Nogueira MA, Araujo RS (2016) Inoculation of Brachiaria spp. with the plant growth-promoting bacterium Azospirillum brasilense: an environment-friendly component in the reclamation of degraded pastures in the tropics. Agric Ecosyst Environ 221:125–131. https://doi.org/10.1016/j.agee.2016.01.024

    Article  CAS  Google Scholar 

  67. Hungria M, Ribeiro RA, Nogueira MA (2018) Draft genome sequences of Azospirillum brasilense strains Ab-V5 and Ab-V6, commercially used in inoculants for grasses and legumes in Brazil. Genome Announc 6:e00393–e00318. https://doi.org/10.1128/genomeA.00393-18

    Article  PubMed  PubMed Central  Google Scholar 

  68. Iruthayathas EE, Gunasekaran S, Vlassak K (1983) Effect of combined inoculation of Azospirillum and Rhizobium on nodulation and N2-fixation of winged bean and soybean. Sci Hortic 20:231–240. https://doi.org/10.1016/0304-4238(83)90003-1

    Article  Google Scholar 

  69. Jain DK, Patriquin DG (1985) Characterization of a substance produced by Azospirillum which causes branching of wheat root hairs. Can J Microbiol 31:206–210. https://doi.org/10.1139/m85-039

    Article  Google Scholar 

  70. Janzen RA, Rood SB, Dormaar JF, McGill WB (1992) Azospirillum brasilense produces gibberellin in pure culture on chemically-defined medium and in co-culture on straw. Soil Biol Biochem 24:1061–1064. https://doi.org/10.1016/0038-0717(92)90036-W

    Article  CAS  Google Scholar 

  71. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282. https://doi.org/10.1093/bioinformatics/8.3.275

    Article  PubMed  CAS  Google Scholar 

  72. 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 (2010) Complete genomic structure of the cultivated rice endophyte Azospirillum sp. B510. DNA Res 17:37–50. https://doi.org/10.1093/dnares/dsp026

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  73. Kapulnik Y, Kigel J, Okon Y, Nur I, Henis Y (1981) Effect of Azospirillum inoculation on some growth parameters and N content of wheat, sorghum and panicum. Plant Soil 61:65–70. https://doi.org/10.1007/BF02277363

    Article  Google Scholar 

  74. Katupitiya S, New PB, Elmerich C, Kennedy IR (1995) Improved N2 fixation in 2, 4-D treated wheat roots associated with Azospirillum lipoferum: studies of colonization using reporting genes. Soil Biol Biochem 27:447–452. https://doi.org/10.1016/0038-0717(95)98617-W

    Article  CAS  Google Scholar 

  75. Kazi N, Deaker R, Wilson N, Muhammad K, Trethowan R (2016) The response of wheat genotypes to inoculation with Azospirillum brasilense in the field. Field Crop Res 196:368–378. https://doi.org/10.1016/j.fcr.2016.07.012

    Article  Google Scholar 

  76. Kennedy IR, Pereg-Gerk LL, Wood C, Deaker R, Gilchrist K, Katupitiya S (1997) Biological nitrogen fixation in nonleguminous field crops: facilitating the evolution between Azospirillum and wheat. Plant Soil 194:65–79. https://doi.org/10.1007/BF00011312

    Article  CAS  Google Scholar 

  77. Kennedy IR, Choudhury ATMA, Kecskes ML (2004) Non-symbiotic bacterial diazotrophs in crop-farming systems: can their potential for plant growth promotion be better exploited? Soil Biol Biochem 36:1229–1244. https://doi.org/10.1016/j.soilbio.2004.04.006

    Article  CAS  Google Scholar 

  78. Khammas KM, Ageron E, Grimont PAD, Kaiser P (1989) Azospirillum irakense sp. nov., a nitrogen-fixing bacterium associated with rice roots and rhizosphere soil. Res Microbiol 140:679–693. https://doi.org/10.1016/0923-2508(89)90199-X

    Article  PubMed  CAS  Google Scholar 

  79. Kolb W, Martin P (1985) Response of plant roots to inoculation with Azospirillum brasilense and to application of indole acetic acid. In: Klingmuller W (ed) Azospirillum III. Springer, Berlin, Heidelberg, pp 215–221. https://doi.org/10.1007/978-3-642-70791-9_20

  80. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Kwak Y, Shin JH (2015) A. brasilense Sp7 genome sequence and assembly. Accession: PRJNA293508. NCBI. https://www.ncbi.nlm.nih.gov/bioproject/293508

  82. Lavrinenko K, Chernousova E, Gridneva E, Dubinina G, Akimov V, Kuever J, Lysenko A, Grabovich M (2010) Azospirillum thiophilum sp. nov. a diazotrophic bacterium isolated from a sulfide spring. Int J Syst Evol Microbiol 60:2832–2837. https://doi.org/10.1099/ijs.0.018853-0

    Article  PubMed  CAS  Google Scholar 

  83. Leyva L, Bashan Y (2008) Activity of two catabolic enzymes of the phosphogluconate pathway in mesquite roots inoculated with Azospirillum brasilense Cd. Plant Physiol Bioch 46(10):898–904. https://doi.org/10.1016/j.plaphy.2008.05.011

  84. Leyva LA, Bashan Y, Mendoza A, de-Bashan LE (2014) Accumulation of fatty acids in Chlorella vulgaris under heterotrophic conditions in relation to activity of acetyl-CoA carboxylase, temperature, and co-immobilization with Azospirillum brasilense. Naturwissenschaften 101:819–830. https://doi.org/10.1007/s00114-014-1223-x

    Article  PubMed  CAS  Google Scholar 

  85. Leyva LA, Bashan Y, de-Bashan LE (2015) Activity of acetyl-CoA carboxylase is not directly linked to accumulation of lipids when Chlorella vulgaris is co-immobilised with Azospirillum brasilense in alginate under autotrophic and heterotrophic conditions. Ann Microbiol 65:339–349. https://doi.org/10.1007/s13213-014-0866-3

    Article  CAS  Google Scholar 

  86. Lin SY, Young CC, Hupfer H, Siering C, Arun AB, Chen W, Lai W, Shen F, Rekha P, Yassin AF (2009) Azospirillum picis sp. nov. isolated from discarded tar. Int J Syst Evol Microbiol 59:761–765. https://doi.org/10.1099/ijs.0.65837-0

    Article  PubMed  CAS  Google Scholar 

  87. Lin SY, Shen FT, Young CC (2011) Rapid detection and identification of the free-living nitrogen fixing genus Azospirillum by 16S rRNA-gene-targeted genus-specific primers. A Van Leeuw J 99:837–844. https://doi.org/10.1007/s10482-011-9558-1

    Article  CAS  Google Scholar 

  88. Lin SY, Shen FT, Young LS, Zhu ZL, Chen WM, Young CC (2012) Azospirillum formosense sp. nov. a diazotroph from agricultural soil. Int J Syst Evol Microbiol 62:1185–1190. https://doi.org/10.1099/ijs.0.030585-0

    Article  PubMed  CAS  Google Scholar 

  89. Lin SY, Liu YC, Hameed A, Hsu YH, Lai WA, Shen FT, Young CC (2013) Azospirillum fermentarium sp. nov. a nitrogen-fixing species isolated from a fermenter. Int J Syst Evol Microbiol 63:3762–3768. https://doi.org/10.1099/ijs.0.050872-0

    Article  PubMed  CAS  Google Scholar 

  90. Lin SY, Hameed A, Shen FT, Liu YC, Hsu YH, Shahina M, Lai W, Young CC (2014) Description of Niveispirillum fermenti gen. nov. sp. nov. isolated from a fermentor in Taiwan transfer of Azospirillum irakense (1989) as Niveispirillum irakense comb. nov., and reclassification of Azospirillum amazonense (1983) as Nitrospirillum amazonense gen. nov. A Van Leeuw J 105:1149–1162. https://doi.org/10.1007/s10482-014-0176-6

    Article  CAS  Google Scholar 

  91. Lin SY, Hameed A, Liu YC, Hsu YH, Lai WA, Shen FT, Young CC (2015) Azospirillum soli sp. nov. a nitrogen-fixing species isolated from agricultural soil. Int J Syst Evol Microbiol 65:4601–4607. https://doi.org/10.1099/ijsem.0.000618

    Article  PubMed  CAS  Google Scholar 

  92. Lin SY, Liu YC, Hameed A, Hsu YH, Huang HI, Lai WA, Young CC (2016) Azospirillum agricola sp. nov. a nitrogen-fixing species isolated from cultivated soil. Int J Syst Evol Microbiol 66:1453–1458. https://doi.org/10.1099/ijsem.0.000904

    Article  PubMed  CAS  Google Scholar 

  93. Lopez BR, Bashan Y, Trejo A, de-Bashan LE (2013) Amendment of degraded desert soil with wastewater debris containing immobilized Chlorella sorokiniana and Azospirillum brasilense significantly modifies soil bacterial community structure, diversity, and richness. Biol Fertil Soils 49:1053–1063. https://doi.org/10.1007/s00374-013-0799-1

    Article  CAS  Google Scholar 

  94. Lopez BR, Palacios OA, Bashan Y, Hernandez-Sandoval FE, de-Bashan LE (2019) Riboflavin and lumichrome exuded by the bacterium Azospirillum brasilense promote growth and changes in metabolites in Chlorella sorokiniana under autotrophic conditions. Algal Res. https://doi.org/10.1016/j.algal.2019.101696, https://doi.org/10.1016/j.algal.2019.101696

  95. Machado HB, Funayama S, Rigo LU, Pedrosa FO (1991) Excretion of ammonium by Azospirillum brasilense. Can J Microbiol 37:549–553

  96. Martin-Didonet CC, Chubatsu LS, Souza EM, Kleina M, Rego FG, Rigo LU, Yates M, Pedrosa FO (2000) Genome structure of the genus Azospirillum. J Bacteriol 182:4113–4116. https://doi.org/10.1128/JB.182.14.4113-4116.2000

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  97. 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 228:167–173. https://doi.org/10.1016/S0378-1097(03)00694-3

    Article  PubMed  CAS  Google Scholar 

  98. Mehnaz S, Weselowski B, Lazarovits G (2007a) Azospirillum canadense sp. nov. a nitrogen-fixing bacterium isolated from corn rhizosphere. Int J Syst Evol Microbiol 57:620–624. https://doi.org/10.1099/ijs.0.64804-0

    Article  PubMed  CAS  Google Scholar 

  99. Mehnaz S, Weselowski B, Lazarovits G (2007b) Azospirillum zeae sp. nov. a diazotrophic bacterium isolated from rhizosphere soil of Zea mays. Int J Syst Evol Microbiol 57:2805–2809. https://doi.org/10.1099/ijs.0.65128-0

    Article  PubMed  CAS  Google Scholar 

  100. Meza B, de-Bashan LE, Bashan Y (2015) Involvement of indole-3-acetic acid produced by Azospirillum brasilense in accumulating intracellular ammonium in Chlorella vulgaris. Res Microbiol 166:72–83. https://doi.org/10.1016/j.resmic.2014.12.010

    Article  PubMed  CAS  Google Scholar 

  101. Molina R, Rivera D, Mora V, López G, Rosas S, Spaepen S, Vanderleyden J, Cassán F (2018) Regulation of IAA biosynthesis in Azospirillum brasilense under environmental stress conditions. Curr Microbiol 75:1408–1418. https://doi.org/10.1007/s00284-018-1537-6

    Article  PubMed  CAS  Google Scholar 

  102. 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 In 21:1001–1009. https://doi.org/10.1094/MPMI-21-7-1001

    Article  CAS  Google Scholar 

  103. Morais TPD, Brito CHD, Brandão AM, Rezende WS (2016) Inoculation of maize with Azospirillum brasilense in the seed furrow. Rev Ciênc Agron 47:290–298. https://doi.org/10.5935/1806-6690.20160034

    Article  Google Scholar 

  104. Moreno M, de-Bashan LE, Hernandez JP, Lopez BR, Bashan Y (2017) Success of long-term restoration of degraded arid land using native trees planted 11 years earlier. Plant Soil 421:83–92. https://doi.org/10.1007/s11104-017-3438-z

    Article  CAS  Google Scholar 

  105. Morla FD, Cerioni GA, Giayetto O, Tello RD, Pelizza NA, Baliña R (2019) Evaluación de la co-inoculación en soja con Bradyrhizobium japonicum y Azospirillum brasilense. 7° Congreso de la Soja del MERCOSUR (MERCOSOJA 2019)

  106. Murty M, Ladha J (1988) Influence of Azospirillum inoculation on the mineral uptake and growth of rice under hydroponic conditions. Plant Soil 108:281–285. https://doi.org/10.1007/BF02375660

    Article  Google Scholar 

  107. Nogueira MA, Prando AM, de Oliveira AB, de Lima D, Conte O, Harger N, Teixeira de Oliveira F, Hungria M (2018) Ações de transferência de tecnologia em inoculação/coinoculação com Bradyrhizobium e Azospirillum na cultura da soja na safra 2017/18 no estado do Paraná. Embrapa Soja-Circular Técnica (INFOTECA-E)

  108. Okon Y (1982) Azospirillum: physiological properties, mode of association with roots and its application for the benefit of cereal and forage grass crops. Israel J Bot 31:214–220. https://doi.org/10.1080/0021213X.1982.10676945

    Article  Google Scholar 

  109. Okon Y, Kapulnik Y (1986) Development and function of Azospirillum-inoculated roots. Plant Soil 90:3–16. https://doi.org/10.1007/BF02277383

    Article  CAS  Google Scholar 

  110. Okon Y, Labandera-Gonzalez CA (1994) Agronomic applications of Azospirillum: an evaluation of 20 years worldwide field inoculation. Soil Biol Biochem 26:1591–1601. https://doi.org/10.1016/0038-0717(94)90311-5

    Article  CAS  Google Scholar 

  111. Okon Y, Heytler PG, Hardy RWF (1983) N2 fixation by Azospirillum brasilense and its incorporation into host Setaria italica. Appl Environ Microbiol 46:694–697. https://doi.org/10.1128/AEM.46.3.694-697.1983

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  112. Okon YC, Labandera-Gonzales C, Lage M, Lage P (2015) Agronomic applications of Azospirillum and other PGPR. In: de Bruijn FJ (ed) Biological nitrogen fixation, vol 2. John Wiley & Sons Inc, New York, pp 925–936. https://doi.org/10.1002/9781119053095

  113. Oliveira RG, Drozdowicz A (1981) Bacteriocins in the genus Azospirillum. Rev Microbiol 12:42–47

    Google Scholar 

  114. Ona O, Smets I, Gysegom P, Bernaerts K, Van Impe J, Prinsen E, Vanderleyden J (2003) The effect of pH on indole-3-acetic acid (IAA) biosynthesis of Azospirillum brasilense Sp7. Symbiosis 35:199–208

    CAS  Google Scholar 

  115. Ozturk A, Caglar O, Sahin F (2003) Yield response of wheat and barley to inoculation of plant growth promoting rhizobacteria at various levels of nitrogen fertilization. J Plant Nutr Soil Sci 166:262–266. https://doi.org/10.1002/jpln.200390038

    Article  CAS  Google Scholar 

  116. Palacios OA, Bashan Y, Schmid M, Hartmann A, de-Bashan LE (2016) Enhancement of thiamine release during synthetic mutualism between Chlorella sorokiniana and Azospirillum brasilense growing under stress conditions. J Appl Phycol 28:1521–1531. https://doi.org/10.1007/s10811-015-0697-z

    Article  CAS  Google Scholar 

  117. Pankievicz VCS, Do Amaral FP, Santos KFDN, Agtuca B, Xu Y, Schueller MJ, Arisi ACM, Steffens MBR, de Souza EM, Pedrosa FO, Stacey G, Ferrieri RA (2015) Robust biological nitrogen fixation in a model grass-bacterial association. Plant J 81:907–919. https://doi.org/10.1111/tpj.12777

    Article  PubMed  CAS  Google Scholar 

  118. Pedrosa FO, Oliveira ALM, Guimarães VF, Etto RM, Souza EM, Furmam FG, Gonçalves DRP, Santos OJAP, Gonçalves LSA, Battistus AG, Galvão CW (2019) The ammonium excreting Azospirillum brasilense strain HM053: a new alternative inoculant for maize. Plant Soil:1–12. https://doi.org/10.1007/s11104-019-04124-8

  119. Peng G, Wang H, Zhang G, Hou W, Liu Y, Wang ET, Tan Z (2006) Azospirillum melinis sp. nov. a group of diazotrophs isolated from tropical molasses grass. Int J Syst Evol Microbiol 56:1263–1271. https://doi.org/10.1099/ijs.0.64025-0

    Article  PubMed  CAS  Google Scholar 

  120. Perez-Garcia O, de-Bashan LE, Hernandez J-P, Bashan Y (2010) Efficiency of growth and nutrient uptake from wastewater by heterotrophic, autotrophic, and mixotrophic cultivation of Chlorella vulgaris immobilized with Azospirillum brasilense. J Phycol 46:800–812. https://doi.org/10.1111/j.1529-8817.2010.00862.x

    Article  CAS  Google Scholar 

  121. Perrig D, Boiero ML, Masciarelli OA, Penna C, Ruiz OA, Cassán 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 75:1143–1150. https://doi.org/10.1007/s00253-007-0909-9

    Article  PubMed  CAS  Google Scholar 

  122. Prando AM, de Oliveira AB, Hungría M, de Oliveira FT, Harger N (2016) Transferência de tecnologia sobre inoculação em soja em parceria entre Embrapa e Emater. In: 27 RELAR Londrina. Fortalecendo as parcerias Sul-Sul: anais. Curitiba: SBCS-NEPAR 2016. p. 308

  123. Prando AM, de Oliveira AB, Lima D, Conte O, Harger N, Teixeira FT, Nogueira MA, Hungría M (2018). Ações de transferência de tecnologia sobre inoculação em soja em parceria entre EMATER Paraná e Embrapa. In: 8 Congresso Brasileiro de soja Goiânia. Inovação Tecnologias

  124. 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 In 6:609–609

    Article  CAS  Google Scholar 

  125. Puente ME, Bashan Y (1993) Effect of inoculation with Azospirillum brasilense strains on the germination and seedlings growth of the giant columnar cardon cactus (Pachycereus pringlei). Symbiosis 15:49–60

    Google Scholar 

  126. Puente M, Gualpa J, Lopez G, Molina R, Carletti S, Cassan F (2017) The benefits of foliar inoculation with Azospirillum brasilense in soybean are explained by an auxin signaling model. Symbiosis 76:41–49. https://doi.org/10.1007/s13199-017-0536-x

    Article  CAS  Google Scholar 

  127. Puente M, Zawoznik M, López de Sabando M, Perez G, Gualpa J, Carletti S, Cassán F (2018) Improvement of soybean grain nutritional quality under foliar inoculation with Azospirillum brasilense strain Az39. Symbiosis 77:41–47. https://doi.org/10.1007/s13199-018-0568-x

    Article  CAS  Google Scholar 

  128. Reinhold B, Hurek T, Fendrik I, Pot B, Gillis M, Kersters K, Thielemans S, De Ley J (1987) Azospirillum halopraeferens sp. nov. a nitrogen-fixing organism associated with roots of Kallar grass (Leptochloa fusca (L.) Kunth). Int J Syst Evol Microbiol 37:43–51. https://doi.org/10.1099/00207713-37-1-43

    Article  Google Scholar 

  129. Reis VM, Baldani VLD, Baldani JI (2015) Isolation, identification and biochemical characterization of Azospirillum spp., and other nitrogen-fixing bacteria. In: Cassán FD, Okon Y, Creus CM (eds) Handbook for Azospirillum. Springer, International Publishing, Switzerland, pp 3–26. https://doi.org/10.1007/978-3-319-06542-7_1

    Google Scholar 

  130. Reynders L, Vlassak K (1979) Conversion of tryptophan to indoleacetic-acid by Azospirillum-brasilense. Soil Biol Biochem 11:547–548. https://doi.org/10.1016/0038-0717(79)90016-6

    Article  CAS  Google Scholar 

  131. Reynders L, Vlassak K (1982) Use of Azospirillum brasilense as biofertilizer in intensive wheat cropping. Plant Soil 66:217–223. https://doi.org/10.1007/BF02183980

    Article  Google Scholar 

  132. Rivera Botia D, Revale S, Molina R, Gualpa J, Puente M, Maroniche G, Paris G, Baker D, Clavijo B, McLay K, Spaepen S, Perticari A, Vazquez M, Wisniewski-Dyé F, Watkins C, Martínez-Abarca Pastor F, Vanderleyden J, Cassán F (2014) Complete genome sequence of the model rhizosphere strain Azospirillum brasilense Az39, successfully applied in agriculture. Genome Announc 2:0683–0614. https://doi.org/10.1128/genomeA.00683-14

    Article  Google Scholar 

  133. Rivera D, Mora V, Lopez G, Rosas S, Spaepen S, Vanderleyden J, Cassan F (2018) New insights into indole-3-acetic acid metabolism in Azospirillum brasilense. J Appl Microbiol 125:1774–1785. https://doi.org/10.1111/jam.14080

    Article  CAS  Google Scholar 

  134. Rodriguez Caceres EA (1982) Improved medium for isolation of Azospirillum spp. Appl Environ Microbiol 44:990–991

    Article  Google Scholar 

  135. Rodriguez H, Gonzalez T, Goire I, Bashan Y (2004) Gluconic acid production and phosphate solubilization by the plant growth-promoting bacterium Azospirillum spp. Naturwissenschaften 91:552–555. https://doi.org/10.1007/s00114-004-0566-0

    Article  PubMed  CAS  Google Scholar 

  136. Saikia SP, Srivastava GC, Jain V (2004) Nodule-like structures induced on the roots of maize seedlings by the addition of synthetic auxin 2, 4-D and its effects on growth and yield. Cereal Res Commun 32:83–89. https://doi.org/10.1007/BF03543284

    Article  CAS  Google Scholar 

  137. Saikia SP, Jain V, Khetarpal S, Aravind S (2007) Dinitrogen fixation activity of Azospirillum brasilense in maize (Zea mays). Curr Sci 93:1296–1300

    CAS  Google Scholar 

  138. Santos KFDN, Moure VR, Hauer V, Santos ARS, Donatti L, Galvão CW, Pedrosa FO, Souza EM, Wassem R, Steffens MBR (2017) Wheat colonization by an Azospirillum brasilense ammonium-excreting strain reveals upregulation of nitrogenase and superior plant growth promotion. Plant Soil 415:245–255. https://doi.org/10.1007/s11104-016-3140-6

    Article  CAS  Google Scholar 

  139. Sarig S, Kapulnik Y, Nur I, Okon Y (1984) Response of non-irrigated Sorghum bicolor to Azospirillum inoculation. Exp Agric 20:59–66. https://doi.org/10.1017/S0014479700017592

    Article  Google Scholar 

  140. Saubidet M, Fatta IN, Barneix AJ (2002) The effect of inoculation with Azospirillum brasilense on growth, nitrogen utilization by wheat plants. Plant Soil 245:215–222. https://doi.org/10.1023/A:1020469603941

    Article  CAS  Google Scholar 

  141. 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 71:1803–1810. https://doi.org/10.1128/AEM.71.4.1803-1810.2005

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  142. Spaepen S, Versées W, Gocke D, Pohl M, Steyaert J, Vanderleyden J (2007) Characterization of phenylpyruvate decarboxylase, involved in auxin production of Azospirillum brasilense. J Bacteriol 189:7626–7633. https://doi.org/10.1128/JB.00830-07

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  143. Spaepen S, Bossuyt S, Engelen K, Marchal K, Vanderleyden J (2014) Phenotypical and molecular responses of Arabidopsis thaliana roots as a result of inoculation with the auxin-producing bacterium Azospirillum brasilense. New Phytol 201:850–861. https://doi.org/10.1111/nph.12590

    Article  PubMed  CAS  Google Scholar 

  144. Strzelczyk E, Kampert M, Li CY (1994) Cytokinin-like substances and ethylene production by Azospirillum in media with different carbon sources. Microbiol Res 149:55–60. https://doi.org/10.1016/S0944-5013(11)80136-9

    Article  CAS  Google Scholar 

  145. Tarrand JJ, Krieg NR, Döbereiner J (1978) A taxonomic study of the Spirillum lipoferum group with descriptions of a new genus Azospirillum gen. nov. and two species Azospirillum lipoferum (Beijerinck) comb. nov. and Azospirillum brasilense sp. nov. Can J Microbiol 24:967–980. https://doi.org/10.1139/m78-160

    Article  PubMed  CAS  Google Scholar 

  146. Tchan YT, Zeman AMM, Kennedy IR (1991) Nitrogen fixation in para-nodules of wheat roots by introduced free-living diazotrophs. Plant Soil 137:43–47. https://doi.org/10.1007/BF02187430

    Article  CAS  Google Scholar 

  147. Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859. https://doi.org/10.1038/nrm2020

    Article  PubMed  CAS  Google Scholar 

  148. Thuler DS, Floh EIS, Handro W, Barbosa HR (2003) Plant growth regulators, amino acids released by Azospirillum sp. in chemically defined media. Lett Appl Microbiol 37:174–178. https://doi.org/10.1046/j.1472-765X.2003.01373.x

    Article  PubMed  CAS  Google Scholar 

  149. Tien TM, Gaskins MH, Hubbell D (1979) Plant growth substances produced by Azospirillum brasilense and their effect on the growth of pearl millet (Pennisetum americanum L.). Appl Environ Microbiol 37:1016–1024. https://doi.org/10.1128/AEM.37.5.1016-1024.1979

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  150. Tikhonova EN, Grouzdev DS, Kravchenko IK (2019) Azospirillum palustre sp. nov., a methylotrophic nitrogen-fixing species isolated from raised bog. Int J Syst Evol Microbiol 69:2787–2793. https://doi.org/10.1099/ijsem.0.003560

    Article  PubMed  CAS  Google Scholar 

  151. Trejo A, de Bashan LE, Hartmann A, Hernandez J-P, Rothballer M, Schmid M, Bashan Y (2012) Recycling waste debris of immobilized microalgae and plant growth-promoting bacteria from wastewater treatment as a resource to improve fertility of eroded desert soil. Environ Exp Bot 75:65–73. https://doi.org/10.1016/j.envexpbot.2011.08.007

    Article  Google Scholar 

  152. Tugarova AV, Vetchinkina EP, Loshchinina EA, Shchelochkov AG, Nikitina VE, Kamnev AA (2013) The ability of the rhizobacterium Azospirillum brasilense to reduce selenium (IV) to selenium (0). Microbiology 82:352–355. https://doi.org/10.1134/S0026261713030120

    Article  CAS  Google Scholar 

  153. Tyagi S, Singh DK (2014) Azospirillum himalayense sp. nov. a nifH bacterium isolated from Himalayan valley soil India. Ann Microbiol 64:259–266. https://doi.org/10.1007/s13213-013-0658-1

    Article  CAS  Google Scholar 

  154. Van Dommelen A, Croonenborghs A, Spaepen S, Vanderleyden J (2009) Wheat growth promotion through inoculation with an ammonium-excreting mutant of Azospirillum brasilense. Biol Fertil Soils 45:549–553. https://doi.org/10.1007/s00374-009-0357-z

    Article  CAS  Google Scholar 

  155. Vanbleu E, Marchal K, Lambrecht M, Mathys J, Vanderleyden J (2004) Annotation of the pRhico plasmid of Azospirillum brasilense reveals its role in determining the outer surface composition. FEMS Microbiol Lett 232:165–172. https://doi.org/10.1016/S0378-1097(04)00046-1

    Article  PubMed  CAS  Google Scholar 

  156. Veresoglou SD, Menexes G (2010) Impact of inoculation with Azospirillum spp. on growth properties and seed yield of wheat: a meta-analysis of studies in the ISI Web of Science from 1981 to 2008. Plant Soil 337:469–480. https://doi.org/10.1007/s11104-010-0543-7

    Article  CAS  Google Scholar 

  157. Vial L, Cuny C, Gluchoff-Fiasson K, Comte G, Oger PM, Faure D, Dessaux Y, Bally R, Wisniewski-Dyé F (2006) N-acyl-homoserine lactone-mediated quorum-sensing in Azospirillum: an exception rather than a rule. FEMS Microbiol Ecol 58:155–168. https://doi.org/10.1111/j.1574-6941.2006.00153.x

    Article  PubMed  CAS  Google Scholar 

  158. Von Bülow JF, Döbereiner J (1975) Potential for nitrogen fixation in maize genotypes in Brazil. P Natl Acad Sci 72:2389–2393. https://doi.org/10.1073/pnas.72.6.2389

    Article  Google Scholar 

  159. Wisniewski-Dyé F, Borziak K, Khalsa-Moyers G, Alexandre G, Sukharnikov L, Wuichet K, Hurst G, McDonald W, Robertson J, Barbe V, Calteau A, Rouy Z, Mangenot S, Prigent-Combaret C, Norm P, Boyer M, Siguier P, Dessaux Y, Elmerich C, Condemine G, Krishnen G, Kennedy I, Paterson A, González V, Mavingui P, Zhulin I (2011) Azospirillum genomes reveal transition of bacteria from aquatic to terrestrial environments. PLoS Genet 7(12):e1002430. https://doi.org/10.1371/journal.pgen.1002430

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  160. Wisniewski-Dyé F, Lozano L, Acosta-Cruz E, Borland S, Drogue B, Prigent-Combaret C, Rouy Z, Barbe V, Mendoza Herrera A, González V, Mavingui P (2012) Genome sequence of Azospirillum brasilense CBG497 and comparative analyses of Azospirillum core and accessory genomes provide insight into niche adaptation. Genes 3:576–602. https://doi.org/10.3390/genes3040576

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  161. Xie CH, Yokota A (2005) Azospirillum oryzae sp. nov. a nitrogen-fixing bacterium isolated from the roots of the rice plant Oryza sativa. Int J Syst Evol Microbiol 55:1435–1438. https://doi.org/10.1099/ijs.0.63503-0

    Article  PubMed  CAS  Google Scholar 

  162. Young CC, Hupfer H, Siering C, Ho MJ, Arun AB, Lai WA, Rekha P, Shen F, Hung M, Chen W, Yassin AF (2008) Azospirillum rugosum sp. nov. isolated from oil-contaminated soil. Int J Syst Evol Microbiol 58:959–963. https://doi.org/10.1099/ijs.0.65065-0

    Article  PubMed  CAS  Google Scholar 

  163. Yu D, Kennedy IR, Tchan YT (1993) Verification of nitrogenase activity (C2H2 reduction) in Azospirillum populated, 2, 4-dichlorophenoxyacetic acid induced, root structures of wheat. Aust J Plant Physiol 20:187–195. https://doi.org/10.1071/PP9930187

    Article  CAS  Google Scholar 

  164. Zeman AMM, Tchan YT, Elmerich C, Kennedy IR (1992) Nitrogenase activity in wheat seedlings bearing paranodules induced by 2, 4-dichlorophenoxyacetic acid (2, 4-D) and inoculated with Azospirillum. Res Microbiol 143:847–855. https://doi.org/10.1016/0923-2508(92)90072-V

    Article  PubMed  CAS  Google Scholar 

  165. Zhang R, Feng J, Wang C, Chen J (2019) Azospirillum griseum sp. nov. isolated from lakewater. Int J Syst Evol Microbiol. https://doi.org/10.1099/ijsem.0.003460

  166. 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 55:1–7. https://doi.org/10.2323/jgam.55.1

    Article  PubMed  CAS  Google Scholar 

  167. Zhou S, Han L, Wang Y, Yang G, Zhuang L, Hu P (2013) Azospirillum humicireducens sp. nov. a nitrogen-fixing bacterium isolated from a microbial fuel cell. Int J Syst Evol Microbiol 63:2618–2624. https://doi.org/10.1099/ijs.0.046813-0

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Universidad Nacional de Río Cuarto (UNRC), Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET, Argentina), Fondo Nacional para la Investigación Científico tecnológica (FONCyT, Argentina), and Consejo Nacional de Ciencia y Tecnologia (CONACYT, Mexico). The authors acknowledge the collaboration of the following researchers for providing valuable information about registered products (brands, production companies, estimated use, etc.) used in this chapter: Carla Louge (SENASA) and Solon Cordeiro de Araujo, (ANPII) from Brazil.

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Cassán, F., Coniglio, A., López, G. et al. Everything you must know about Azospirillum and its impact on agriculture and beyond. Biol Fertil Soils 56, 461–479 (2020). https://doi.org/10.1007/s00374-020-01463-y

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Keywords

  • Azospirillum
  • Phytohormones
  • Nitrogen fixation
  • Plant growth promotion bacteria