SpringerLink
Log in

Assessment of affinity and specificity of Azospirillum for plants

  • Review Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background

Azospirillum spp. are the most studied plant growth-promoting bacteria (PGPB). The genus represents a common model for plant-bacteria interactions. This genus was initially isolated and tested on cereals and was subsequently commercialized.

Aims

Despite claims of plant specificity, particularly towards cereals, data over the past 40 years does not appear to substantiate claims of such specificity/affinity of Azospirillum species. Consequently an evaluation of the specificity/affinity of the genus Azospirillum across all plants, in general, and cereals, in particular, was undertaken.

Results

Although the majority of studies focused on cereals, Azospirillum spp. increase growth of 113 plant species across 35 botanical families, including 14 species of cereals. Amongst Azospirillum spp., several well studied strains have been effective in several plant species, making these organisms potentially valuable for further study.

Conclusions

This review demonstrates that azospirilla are not cereal-specific at the genus and species levels. Azospirillum serves as a general PGPB to every plant species tested so far. Given the paucity of widespread screening, affinity of strains to a plant genotype, cultivar, or plant species cannot be overruled. Definitive conclusions concerning such specificity require molecular and cross-inoculation studies, using various strains of bacteria, and re-isolation after growth of the plants in different plant species. (203 words).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Alexandre G, Greer SE, Zhulin IB (2000) Energy taxis is the dominant behavior in Azospirillum brasilense. J Bacteriol 182:6042–6048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amir HG, Shamsuddin ZH, Halimi MS, Ramlan MF, Marziah M (2001) Effects of Azospirillum inoculation on N2 fixation and growth of oil palm plantlets at nursery stage. J Oil Palm Res 13:42–49

    CAS  Google Scholar 

  • Amir HG, Shamsuddin ZH, Halimi MS, Marziah M, Ramlan MF (2005) Enhancement in nutrient accumulation and growth of oil palm seedlings caused by PGPR under field nursery conditions. Commun Soil Sci Plan 36:2059–2066

    Article  CAS  Google Scholar 

  • Antonyuk LP, Fomina OR, Galkin MA, Ignatov VV (1993) The effect of wheat germ agglutinin on dinitrogen fixation, glutamine synthetase activity and ammonia excretion in Azospirillum brasilense Sp 245. FEMS Microbiol Lett 110:285–289

    Article  CAS  Google Scholar 

  • Arias HOR, Wood MK, Nieto CM, López GR, de la Vega L (2004) Above- and below-ground responses of Eragrostis and Bouteloua grass seedlings to the plant-growth-promoting bacterium Azospirillium brasilense. J Arid Environ 59:19–26

    Article  Google Scholar 

  • Assmus B, Hutzler P, Kirchhof G, Amann R, Lawrence JR, Hartmann A (1995) In Situ localization of Azospirillum brasilense in the rhizosphere of wheat with fluorescently labeled, rRNA-targeted oligonucleotide probes and scanning confocal laser microscopy. Appl Environ Microbiol 61:1013–1019

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bacilio-Jimenez M, Aguilar-Flores S, del Valle MV, Perez A, Zepeda A, Zenteno E (2001) Endophytic bacteria in rice seeds inhibit early colonization of roots by Azospirillum brasilense. Soil Biol Biochem 33:167–172

    Article  CAS  Google Scholar 

  • Baldani VLD, Döbereiner J (1980) Host-plant specificity in the infection of cereals with Azospirillum spp. Soil Biol Biochem 12:433–439

    Article  Google Scholar 

  • Baldani VLD, Baldani JI, Döbereiner J (1983) Effects of Azospirillum inoculation on root infection and nitrogen incorporation in wheat. Can J Microbiol 29:924–929

    Article  Google Scholar 

  • Baldani VLD, de B. Alvarez MA, Baldani JI, Döbereiner J (1986) Establishment of inoculated Azospirillum spp. in the rhizosphere and in roots of field grown wheat and sorghum. Plant Soil 90:35–46

    Article  Google Scholar 

  • Baldani VLD, Baldani JI, Döbereiner J (1987) Inoculation of field-grown wheat (Triticum aestivum) with Azospirillum spp. in Brazil. Biol Fertil Soils 4:37–40

    Google Scholar 

  • Barassi CA, Ayrault G, Creus CM, Sueldo RJ, Sobrero MT (2006) Seed inoculation with Azospirillum mitigates NaCl effects on lettuce. Sci Hortic 109:8–14

    Article  CAS  Google Scholar 

  • Barbieri P, Galli E (1993) Effect on wheat root development of inoculation with an Azospirillum brasilense mutant with altered indole-3-acetic acid production. Res Microbiol 144:69–75

    Article  CAS  PubMed  Google Scholar 

  • Barbieri P, Zanelli T, Galli E, Zanetti G (1986) Wheat inoculation with Azospirillum brasilense Sp6 and some mutants altered in nitrogen fixation and indole-3-acetic acid production. FEMS Microbiol Lett 36:87–90

    Article  CAS  Google Scholar 

  • Basaglia M, Casella S, Peruch U, Poggiolini S, Vamerali T, Mosca G, Vanderleyden J, De Troch P, Nuti MP (2003) Field release of genetically marked Azospirillum brasilense in association with Sorghum bicolor L. Plant Soil 256:281–290

    Article  CAS  Google Scholar 

  • Bashan Y (1986a) Enhancement of wheat roots colonization and plant development by Azospirillum brasilense Cd. following temporary depression of the rhizosphere microflora. Appl Environ Microbiol 51:1067–1071

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bashan Y (1986b) Migration of the rhizosphere bacteria Azospirillum brasilense and Pseudomonas fluorescens towards wheat roots in the soil. J Gen Microbiol 132:3407–3414

    Google Scholar 

  • Bashan Y (1990) Short exposure to Azospirillum brasilense Cd inoculation enhanced proton efflux in intact wheat roots. Can J Microbiol 36:419–425

    Article  CAS  Google Scholar 

  • Bashan Y (1991) Changes in membrane potential of intact soybean root elongation zone cells induced by Azospirillum brasilense. Can J Microbiol 37:958–963

    Article  Google Scholar 

  • Bashan Y (1998) Azospirillum plant growth-promoting strains are nonpathogenic on tomato, pepper, cotton, and wheat. Can J Microbiol 44:168–174

    Article  CAS  Google Scholar 

  • Bashan Y, Levanony H (1987) Horizontal and vertical movement of Azospirillum brasilense Cd in the soil and along the rhizosphere of wheat and weeds in controlled and field environments. J Gen Microbiol 133:3473–3480

    Google Scholar 

  • Bashan Y, Levanony H (1988a) Adsorption of the rhizosphere bacterium Azospirillum brasilense Cd to soil, sand and peat particles. J Gen Microbiol 134:1811–1820

    Google Scholar 

  • Bashan Y, Levanony H (1988b) Active attachment of Azospirillum brasilense Cd to quartz sand and to a light-textured soil by protein bridging. J Gen Microbiol 134:2269–2279

    CAS  Google Scholar 

  • Bashan Y, Levanony H (1989a) Wheat root tips as a vector for passive vertical transfer of Azospirillum brasilense Cd. J Gen Microbiol 135:2899–2908

    Google Scholar 

  • Bashan Y, Levanony H (1989b) Factors affecting adsorption of Azospirillum brasilense Cd to root hairs as compared with root surface of wheat. Can J Microbiol 35:936–944

    Article  CAS  Google Scholar 

  • Bashan Y, Levanony H (1990) Current status of Azospirillum inoculation technology: Azospirillum as a challenge for agriculture. Can J Microbiol 36:591–608

    Article  CAS  Google Scholar 

  • Bashan Y, Levanony H (1991) Alterations in membrane potential and in proton efflux in plant roots induced by Azospirillum brasilense. Plant Soil 137:99–103

    Article  Google Scholar 

  • Bashan Y, Holguin G (1993) Anchoring of Azospirillum brasilense to hydrophobic polystyrene and wheat roots. J Gen Microbiol 139:379–385

    Article  CAS  Google Scholar 

  • Bashan Y, Holguin G (1994) Root-to-root travel of the beneficial bacterium Azospirillum brasilense. Appl Environ Microbiol 60:2120–2131

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bashan Y, Holguin G (1995) Inter-root movement of Azospirillum brasilense and subsequent root colonization of crop and weed seedlings growing in soil. Microb Ecol 29:269–281

    Article  CAS  PubMed  Google Scholar 

  • Bashan Y, Dubrovsky JG (1996) Azospirillum spp. participation in dry matter partitioning in grasses at the whole plant level. Biol Fertil Soils 23:435–440

    Article  Google Scholar 

  • Bashan Y, Vazquez P (2000) Effect of calcium carbonate, sand, and organic matter levels on mortality of five species of Azospirillum in natural and artificial bulk soils. Biol Fertil Soils 30:450–459

    Article  CAS  Google Scholar 

  • Bashan Y, de-Bashan LE (2002a) Protection of tomato seedlings against infection by Pseudomonas syringae pv tomato by using the plant growth-promoting bacterium Azospirillum brasilense. Appl Environ Microbiol 68:2637–2643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bashan Y, de-Bashan LE (2002b) Reduction of bacterial speck (Pseudomonas syringae pv tomato) of tomato by combined treatments of plant growth-promoting bacterium, Azospirillum brasilense, streptomycin sulfate, and chemo-thermal seed treatment. Eur J Plant Pathol 108:821–829

    Article  CAS  Google Scholar 

  • Bashan Y, de-Bashan LE (2005) Fresh-weight measurements of roots provide inaccurate estimates of the effects of plant growth-promoting bacteria on root growth: a critical examination. Soil Biol Biochem 37:1795–1804

    Article  CAS  Google Scholar 

  • Bashan Y, de-Bashan LE (2010) How the plant growth-promoting bacterium Azospirillum promotes plant growth – a critical assessment. Adv Agron 108:77–136

    Article  CAS  Google Scholar 

  • Bashan Y, Levanony H, Klein E (1986) Evidence for a weak active external adsorption of Azospirillum brasilense Cd to wheat roots. J Gen Microbiol 132:3069–3073

    Google Scholar 

  • Bashan Y, Levanony H, Mitiku G (1989a) Changes in proton efflux of intact wheat roots induced by Azospirillum brasilense Cd. Can J Microbiol 35:691–697

    Article  CAS  Google Scholar 

  • Bashan Y, Ream Y, Levanony H, Sade A (1989b) Nonspecific responses in plant growth, yield, and root colonization of noncereal crop plants to inoculation with Azospirillum brasilense Cd. Can J Bot 67:1317–1324

    Article  Google Scholar 

  • Bashan Y, Singh M, Levanony H (1989c) Contribution of Azospirillum brasilense Cd to growth of tomato seedlings is not through nitrogen fixation. Can J Bot 67:2429–2434

    Article  CAS  Google Scholar 

  • Bashan Y, Harrison SK, Whitmoyer RE (1990) Enhanced growth of wheat and soybean plants inoculated with Azospirillum brasilense is not necessarily due to general enhancement of mineral uptake. Appl Environ Microbiol 56:769–775

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bashan Y, Levanony H, Whitmoyer RE (1991) Root surface colonization of non-cereal crop plants by pleomorphic Azospirillum brasilense Cd. J Gen Microbiol 137:187–196

    Article  Google Scholar 

  • Bashan Y, Alcaraz-Melendez L, Toledo G (1992) Responses of soybean and cowpea root membranes to inoculation with Azospirillum brasilense. Symbiosis 13:217–228

    Google Scholar 

  • Bashan Y, Puente ME, Rodriguez-Mendoza MN, Toledo G, Holguin G, Ferrera-Cerrato R, Pedrin S (1995) Survival of Azospirillum brasilense in the bulk soil and rhizosphere of 23 soil types. Appl Environ Microbiol 61:1938–1945

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bashan Y, Rojas A, Puente ME (1999) Improved establishment and development of three cacti species inoculated with Azospirillum brasilense transplanted into disturbed urban desert soil. Can J Microbiol 45:441–451

    Article  CAS  Google Scholar 

  • Bashan Y, Moreno M, Troyo E (2000) Growth promotion of the seawater-irrigated oilseed halophyte Salicornia bigelovii inoculated with mangrove rhizosphere bacteria and halotolerant Azospirillum spp. Biol Fertil Soils 32:265–272

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bashan Y, Bustillos JJ, Leyva LA, Hernandez J-P, Bacilio M (2006) Increase in auxiliary photoprotective photosynthetic pigments in wheat seedlings induced by Azospirillum brasilense. Biol Fertil Soils 42:279–285

    Article  CAS  Google Scholar 

  • Bashan Y, Salazar B, Puente ME (2009a) Responses of native legume desert trees used for reforestation in the Sonoran Desert to plant growth-promoting microorganisms in screen house. Biol Fertil Soils 45:655–662

    Article  Google Scholar 

  • Bashan Y, Salazar B, Puente ME, Bacilio M, Linderman RG (2009b) Enhanced establishment and growth of giant cardon cactus in an eroded field in the Sonoran Desert using native legume trees as nurse plants aided by plant growth-promoting microorganisms and compost. Biol Fertil Soils 45:585–594

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Bashan Y, de-Bashan LE, Prabhu SR, Hernandez J-P (2014) Advances in plant growth-promoting bacterial inoculant technology: formulations and practical perspectives (1998–2013). Plant Soil 378:1–33

    Article  CAS  Google Scholar 

  • Becker D, Stanke R, Fendrik I, Frommer WB, Vanderleyden J, Kaiser WM, Hedrich R (2002) Expression of the NH4 +-transporter gene LEAMT1;2 is induced in tomato roots upon association with N2-fixing bacteria. Planta 215:424–429

    Article  CAS  PubMed  Google Scholar 

  • Beijerinck MW (1925) Über ein Spirillum welches freien Stickstof binden kann? Zentralblatt für Bakteriologie.Parasitenkunde, Infektionskrankheiten and Hygiene. Naturewissenschaftliche Abteilung 2 63:353–359

    CAS  Google Scholar 

  • 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 73:99–106

    Article  CAS  Google Scholar 

  • Berg RH, Vasil V, Vasil IK (1979) The biology of Azospirillum-sugarcane association. II Ultrastructure. Protoplasma 101:143–163

    Article  Google Scholar 

  • Bianciotto V, Andreotti S, Balestrini R, Bonfante P, Perotto S (2001) Extracellular polysaccharides are involved in the attachment of Azospirillum brasilense and Rhizobium leguminosarum to arbuscular mycorrhizal structures. Eur J Histochem 45:39–49

    Article  CAS  PubMed  Google Scholar 

  • Bible A, Russell M, Alexandre G (2012) The Azospirillum brasilense Che1 chemotaxis pathway controls swimming velocity, which affects transient cell-to-cell clum**. J Bacteriol 194:3343–3355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bilal R, Rasul G, Arshad M, Malik KA (1993) Attachment, colonization and proliferation of Azospirillum brasilense and Enterobacter spp. on root surface of grasses. World J Microbiol Biotechnol 9:63–69

    Article  CAS  PubMed  Google Scholar 

  • Boddey RM, Baldani VLD, Baldani JI, Döbereiner J (1986) Effect of inoculation of Azospirillum spp. on nitrogen accumulation by field-grown wheat. Plant Soil 95:109–121

    Article  Google Scholar 

  • Botta AL, Santacecilia A, Ercole C, Cacchio P, Del Gallo M (2013) In vitro and in vivo inoculation of four endophytic bacteria on Lycopersicon esculentum. New Biotechnol 30:666–674

    Article  CAS  Google Scholar 

  • Bouton JH, Smith RL, Schank SC, Burton GW, Tyler ME, Littell RC, Gallaher NR, Quesenberry KH (1979) Response of pearl millet inbrids and hybrids to inoculation with Azospirillum brasilense. Crop Sci 19:12–16

    Article  Google Scholar 

  • Boyer M, Bally R, Perrotto S, Chaintreuil C, Wisniewski-Dyé F (2008) A quorum quenching approach to identify quorum-sensing-regulated functions in Azospirillum lipoferum. Res Microbiol 159:699–708

    Article  CAS  PubMed  Google Scholar 

  • 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 62:3030–3033

    CAS  PubMed  PubMed Central  Google Scholar 

  • Calvo P, Nelson L, Kloepper JW (2014) Agricultural uses of plant biostimulants. Plant Soil 383:3–41

    Article  CAS  Google Scholar 

  • Camilios-Neto D et al (2014) Dual RNA-seq transcriptional analysis of wheat roots colonized by Azospirillum brasilense reveals up-regulation of nutrient acquisition and cell cycle genes. BMC Genomics 15:378

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cappellari LR, Santoro MV, Nievas F, Giordano W, Banchio E (2013) Increase of secondary metabolite content in marigold by inoculation with plant growth-promoting rhizobacteria. Appl Soil Ecol 70:16–22

    Article  Google Scholar 

  • Carrozzi LE, Creus CM, Barassi C, Monterubbianesi G, Di Benedetto A (2012) Reparation of aged lettuce (Lactuca sativa) seeds by osmotic priming and Azospirillum brasilense inoculation. Botany 90:1093–1102

    Article  CAS  Google Scholar 

  • 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 45:12–19

    Article  CAS  Google Scholar 

  • 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 45:28–35

    Article  CAS  Google Scholar 

  • Castellanos T, Ascencio F, Bashan Y (1997) Cell-surface hydrophobicity and cell-surface charge of Azospirillum spp. FEMS Microbiol Ecol 24:159–172

    Article  CAS  Google Scholar 

  • Castellanos T, Ascencio F, Bashan Y (1998) Cell-surface lectins of Azospirillum spp. Curr Microbiol 36:241–244

    Article  CAS  PubMed  Google Scholar 

  • Castellanos T, Ascencio F, Bashan Y (2000) Starvation induced changes in the cell surface of Azospirillum lipoferum. FEMS Microbiol Ecol 33:1–9

    Article  CAS  PubMed  Google Scholar 

  • Cervantes E, Rodriguez-Barrueco C (1991) The Infectivity and symbiotic performance of a Frankia strain as affected by its growth medium towards Hippophae rhamnoides L. In: Polsinelli M, Materassi R, Vincenzini M (eds) Nitrogen fixation. Springer, The Netherlands

    Google Scholar 

  • Chamam A, Sanguin H, Bellvert F, Meiffren G, Comte G, Wisniewski-Dyé F, Bertrand C, Prigent-Combaret C (2013) Plant secondary metabolite profiling evidences strain-dependent effect in the Azospirillum–Oryza sativa association. Phytochemistry 87:65–77

    Article  CAS  PubMed  Google Scholar 

  • Chebotar VK, Asis CA Jr, Akao S (2001) Production of growth-promoting substances and high colonization ability of rhizobacteria enhance the nitrogen fixation of soybean when coinoculated with Bradyrhizobium japonicum. Biol Fertil Soils 34:427–432

    CAS  Google Scholar 

  • 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. Enzym Microb Technol 51:294–299

    Article  CAS  Google Scholar 

  • 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. Enzym Microb Technol 51:300–309

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Christiansen-Weniger C (1992) N2-fixation by ammonium-excreting Azospirillum brasilense in auxin-induced tumours of wheat (Triticum aestivum L.). Biol Fertil Soils 12:100–106

    Article  Google Scholar 

  • Christiansen-Weniger C, Vanderleyden J (1994) Ammonium excreting Azospirillum sp. become intracellularly established in maize (Zea mays) para-nodules. Biol Fertil Soils 17:1–8

    Article  Google Scholar 

  • 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 54:97–103

    Article  CAS  Google Scholar 

  • Correa OS, Romero AM, Montecchia MS, Soria MA (2007) Tomato genotype and Azospirillum inoculation modulate the changes in bacterial communities associated with roots and leaves. J Appl Microbiol 102:781–786

    Article  CAS  PubMed  Google Scholar 

  • 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 221:297–303

    Article  CAS  PubMed  Google Scholar 

  • Croes C, van Bastelaere E, De Clercq E, Eyers M, Vanderleyden J, Michiels K (1991) Identification and map** of loci involved in motility, adsorption to wheat roots, colony morphology, and growth in minimal medium on the Azospirillum brasilense Sp7 90-MDa-plasmid. Plasmid 26:83–93

    Article  CAS  PubMed  Google Scholar 

  • Croes C, Moens S, van Bastelaere E, Vanderleyden J, Michiels K (1993) The polar flagellum mediates Azospirillum brasilense adsorption to wheat roots. J Gen Microbiol 139:2261–2269

    Article  CAS  Google Scholar 

  • Dardanelli MS, Fernandez de Cordoba FJ, Espuny MR, Rodriguez Carvajal MA, Soria Díaz ME, Gil Serrano AM, Okon Y, Megías M (2008) Effect of Azospirillum brasilense coinoculated with Rhizobium on Phaseolus vulgaris flavonoids and Nod factor production under salt stress. Soil Biol Biochem 40:2713–2721

    Article  CAS  Google Scholar 

  • de Oliveira Pinheiro R, Boddey LH, James EK, Sprent JI, Boddey RM (2002) Adsorption and anchoring of Azospirillum strains to roots of wheat seedlings. Plant Soil 246:151–166

    Article  Google Scholar 

  • De Troch P, Keijers V, Vanderleyden J (1994) Sequence analysis of the Azospirillum brasilense exoB gene, encoding UDP-glucose 4′-epimerase. Gene 144:143–144

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • de-Bashan LE, Antoun 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 54:197–203

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • de-Bashan LE, Hernandez J-P, Bashan Y, Maier RM (2010a) Bacillus pumilus ES4: candidate plant growth-promoting bacterium to enhance establishment of plants in mine tailings. Environ Exp Bot 69:343–352

    Article  PubMed  PubMed Central  Google Scholar 

  • de-Bashan LE, Hernandez J-P, Nelson KN, Bashan Y, Maier RM (2010b) 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de-Bashan LE, Schmid M, Rothballer M, Hartmann A, Bashan Y (2011) Cell-cell interaction in the eukaryote-prokaryote model using the microalgae Chlorella vulgaris and the bacterium Azospirillum brasilense immobilized in polymer beads. J Phycol 47:1350–1359

    Article  PubMed  Google Scholar 

  • del Amor FM, Porras I (2009) Effects of PGPB on growth and yield of pepper under limited nitrogen supply. Can J Plant Sci 89:349–358

    Article  Google Scholar 

  • del Amor FM, Cuadra-Crespo P (2011) Plant growth-promoting bacteria as a tool to improve salinity tolerance in sweet pepper. Funct Plant Biol 39:82–90

    Article  CAS  Google Scholar 

  • del Amor FM, Serrano-Martınez A, Fortea MI, Legua P, Nunez-Delicado E (2008) The effect of plant-associative bacteria (Azospirillum and Pantoea) on the fruit quality of sweet pepper under limited nitrogen supply. Sci Hortic 117:191–196

    Article  CAS  Google Scholar 

  • Del Gallo M, Haegi A (1990) Characterization and quantification of exocellular polysaccharides in Azospirillum brasilense and Azospirillum lipoferum. Symbiosis 9:155–161

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Dobbelaere S, Croonenborghs A, Thys A, Ptacek D, Vanderleyden J, Dutto P, Labandera-Gonzalez C, Caballero-Mellado J, Aguirre JF, Kapulnik Y, Brener S, Burdman S, Kadouri D, Sarig S, Okon Y (2001) Responses of agronomically important crops to inoculation with Azospirillum. Aust J Plant Physiol 28:871–879

    Google Scholar 

  • Döbereiner J (1988) Isolation and identification of root associated diazotrophs. Plant Soil 110:207–212

    Article  Google Scholar 

  • Döbereiner J, Day JM (1976) Associative symbioses in tropical grasses: characterization of microorganisms and dinitrogen-fixing sites. In: Newton WE, Nyman CJ (eds.), Proceedings of the 1st International Symposium on Nitrogen Fixation. Vol. 2. Edited by Washington State University Press, Pullman, Washington, pp. 518–538

  • Döbereiner J, Marriel IE, Nery M (1976) Ecological distribution of Spirillum lipoferum Beijerinck. Can J Microbiol 22:1464–1473

    Article  PubMed  Google Scholar 

  • Dominguez-Nuñez JA, Muñoz D, Planelles R, Grau JM, Artero F, Anriquez A, Albanesi A (2012) Inoculation with Azospirillum brasilense enhances the quality of mesquite Prosopis juliflora seedlings. For Syst 21:364–372

    Google Scholar 

  • Drogue B, Doré H, Borland S, Wisniewski-Dyé F, Prigent-Combaret C (2012) Which specificity in cooperation between phytostimulating rhizobacteria and plants? Res Microbiol 163:500–510

    Article  PubMed  Google Scholar 

  • Drogue B, Sanguin H, Chamam A, Mozar M, Llauro C, Panaud O, Prigent-Combaret C, Picault N, Wisniewski-Dyé F (2014) Plant root transcriptome profiling reveals a strain-dependent response during Azospirillum-rice cooperation. Front Plant Sci 5:607. doi:10.3389/fpls.2014.00607

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 hairs growth. Soil Biol Biochem 26:1657–1664

    Article  CAS  Google Scholar 

  • Elmerich C, Bozouklian H, Vieille C, Fogher C, Perroud B, Perrin A, Vanderleyden J (1987) Azospirillum: genetics of nitrogen fixation and interaction with plants. Phil Trans R Soc Lond B 317:183–192

    Article  CAS  Google Scholar 

  • Elmerich C, Zimmer W, Vieille C (1991) Associative nitrogen-fixing bacteria. In: Evans H, Borris R, Stacey G (eds) Biological nitrogen fixation. Chapman and Hall, New York, pp 211–257

    Google Scholar 

  • El-Mokadem MT, Helemish FA, Abou-Bakr ZYM, Sheteawi SA (1989) Associative effect of Azospirillum lipoferum and Azotobacter chroococcum with Rhizobium spp. on mineral composition and growth of chickpea (Cicer arietinum) on sandy soils. Zbl Mikrobiol 144:255–265

    Google Scholar 

  • Eskew DL, Focht DD, Ting IP (1977) Nitrogen fixation, denitrification, and pleomorphic growth in a highly pigmented Spirillum lipoferum. Appl Environ Microbiol 34:582–585

    CAS  PubMed  PubMed Central  Google Scholar 

  • Esquivel-Cote R, Ramírez-Gama RM, 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 337:65–75

    Article  CAS  Google Scholar 

  • Eyers M, Vanderleyden J, Van Gool A (1988a) Attachment of Azospirillum to isolated plant cells. FEMS Microbiol Lett 49:435–439

    Article  CAS  Google Scholar 

  • Eyers M, Waelkens F, Vanderleyden J, Van Gool AP (1988b) Quantitative measurement of Azospirillum plant cell attachment. In: Klingmüller W (ed) Azospirillum. IV. Genetics, Physiology, Ecology. Springer-Verlag, Berlin, pp 174–180

    Google Scholar 

  • Fages J, Arsac JF (1991) Sunflower inoculation with Azospirillum and other plant growth promoting rhizobacteria. Plant Soil 137:87–90

    Article  Google Scholar 

  • Fayez M, Daw ZY (1987) Effect of inoculation with different strains of Azospirium brasilense on cotton (Gossipium barbadense). Biol Fertil Soils 4:91–95

    Google Scholar 

  • Felici C, Vettori L, Giraldi E, Forino LMC, Toffanin A, Tagliasacchi AM, Nuti M (2008) Single and co-inoculation of Bacillus subtilis and Azospirillum brasilense on Lycopersicon esculentum: effects on plant growth and rhizosphere microbial community. Appl Soil Ecol 40:260–270

    Article  Google Scholar 

  • Feng L, Kennedy IR (1997) Biodegradation and plant protection from the herbicide 2,4-D by plant–microbial associations in cotton production systems. Biotechnol Bioeng 54:513–519

    Article  CAS  PubMed  Google Scholar 

  • Ferreira MCB, Fernandes MS, Döbereiner J (1987) Role of Azospirillum brasilense nitrate reductase in nitrate assimilation by wheat plants. Biol Fertil Soils 4:47–53

    CAS  Google Scholar 

  • Flores P, Fenoll J, Hellin P, Aparicio-Tejo P (2010) Isotopic evidence of significant assimilation of atmospheric-derived nitrogen fixed by Azospirillum brasilense co-inoculated with phosphate-solubilising Pantoea dispersa in pepper seedling. Appl Soil Ecol 46:335–340

    Article  Google Scholar 

  • Fulchieri M, Frioni L (1994) Azospirillum inoculation on maize (Zea mays): effect on yield in a field experiment in central Argentina. Soil Biol Biochem 26:921–923

    Article  Google Scholar 

  • Gadagi RS, Krishnaraj PU, Kulkarni JH, Sa T (2004) The effect of combined Azospirillum inoculation and nitrogen fertilizer on plant growth promotion and yield response of the blanket flower Gaillardia pulchella. Sci Hortic 100:323–332

    Article  Google Scholar 

  • Gafni R, Okon Y, Kapulnik Y, Fischer M (1986) Adsorption of Azospirillum brasilense to corn roots. Soil Biol Biochem 18:69–75

    Article  Google Scholar 

  • Galal YGM (1997) Dual inoculation with strains of Bradyrhizobium japonicum and Azospirillum brasilense to improve growth and biological nitrogen fixation of soybean (Glycine max L.). Biol Fertil Soils 24:317–322

    Article  CAS  Google Scholar 

  • Gamo T, Ahn SB (1991) Growth-promoting Azospirillum spp. isolated from the roots of several non-gramineous crops in Japan. Soil Sci Plant Nutr 37:455–461

    Article  CAS  Google Scholar 

  • Garcia de Salamone IE, Dobereiner J (1996) Maize genotype effects on the response to Azospirillum inoculation. Biol Fertil Soils 21:193–196

    Article  Google Scholar 

  • Garcia de Salamone IE, Dobereiner J, Urquiaga S, Boddey RM (1996) Biological nitrogen fixation in Azospirillum strain-maize genotype associations as evaluated by the 15N isotope dilution technique. Biol Fertil Soils 23:249–256

    Article  CAS  Google Scholar 

  • Garcia de Salamone IE, Funes JM, Di Salvo LP, Escobar Ortega JS, D’Auria F, Ferrando L, Fernandez Scavino A (2012) Inoculation of paddy rice with Azospirillum brasilense and Pseudomonas fluorescens: Impact of plant genotypes on the rhizosphere microbial communities and field crop production. Appl Soil Ecol 61:196–204

    Article  Google Scholar 

  • Garg SK, Bhatnagar A (1999) Effect of Azospirillum and Azotobacter inoculation on pond productivity and fish growth under fresh water conditions. Indian J Microbiol 39:227–233

    Google Scholar 

  • German MA, Burdman S, Okon Y, Kigel J (2000) Effects of Azospirillum brasilense on root morphology of common bean (Phaseolus vulgaris L.) under different water regimes. Biol Fertil Soils 32:259–264

    Article  Google Scholar 

  • Gonzalez LE, Bashan Y (2000) Increased growth of the microalga Chlorella vulgaris when coimmobilized and cocultured in alginate beads with the plant growth-promoting bacterium Azospirillum brasilense. Appl Environ Microbiol 66:1527–1531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Govindan M, Chandy KC (1985) Utilization of the diazotroph Azospirillum for inducing rooting in pepper (Piper nigrum L.). Curr Sci 54:1186–1188

    Google Scholar 

  • Greer-Phillips SE, Stephens BB, Alexandre G (2004) An energy taxis transducer promotes root colonization by Azospirillum brasilense. J Bacteriol 186:6595–6604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grilli-Caiola M, Canini A, Botta AL, Del Gallo M (2004) Localization of Azospirillum brasilense Cd in tomato (Lycopersicon esculentum Mill.) inoculated roots. Ann Microbiol 54:365–380

    Google Scholar 

  • Groppa MD, Zawoznik MS, Tomaro ML (1998) Effect of co-inoculation with Bradyrhizobium japonicum and Azospirillum brasilense on soybean plants. Eur J Soil Biol 34:75–80

    Article  Google Scholar 

  • Guerrero-Molina MF, Winik BC, Pedraza RO (2012) More than rhizosphere colonization of strawberry plants by Azospirillum brasilense. Appl Soil Ecol 61:205–212

    Article  Google Scholar 

  • Gupta S, Arora DK, Srivastava AK (1995) Growth promotion of tomato plants by rhizobacteria and imposition of energy stress on Rhizoctonia solani. Soil Biol Biochem 27:1051–1058

    Article  CAS  Google Scholar 

  • Haahtela K, Wartionaara T, Sundman V, Sku**s J (1981) Root-associated N2 fixation (acetylene reduction) by Enterobacteriaceae and Azospirillum strains in cold-climate spodosols. Appl Environ Microbiol 41:203–206

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hadas R, Okon Y (1987) Effect of Azospirillum brasilense inoculation on root morphology and respiration in tomato seedlings. Biol Fertil Soils 5:241–247

    Article  Google Scholar 

  • 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. Agron J (Paris) 21:553–560

    Google Scholar 

  • Holguin G, Glick BR (2001) Expression of the ACC Deaminase gene from Enterobacter cloacae UW4 in Azospirillum brasilense. Microb Ecol 41:281–288

    Article  CAS  PubMed  Google Scholar 

  • Holguin G, Glick BR (2003) Transformation of Azospirillum brasilense Cd with an ACC Deaminase gene from Enterobacter cloacae UW4 fused to the Tetr gene promoter improves its fitness and plant growth promoting ability. Microb Ecol 46:122–133

    Article  CAS  PubMed  Google Scholar 

  • Horemans S, De Koninck K, Vlassak K (1988) Aspects of the ecology of Azospirillum sp. in Belgian soils. In: Klingmüller W (ed) Azospirillum IV. Genetics, Physiology, Ecology. Springer-Verlag, Berlin, pp 207–214

    Google Scholar 

  • Hou X, McMillan M, Coumans JVF, Poljak A, Raftery MJ, Pereg L (2014) Cellular responses during morphological transformation in Azospirillum brasilense and its flcA knockout mutant. PLoS ONE 9(12), e114435. doi:10.1371/journal.pone.0114435

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Itzigsohn R, Kapulnik Y, Okon Y, Dovrat A (1993) Physiological and morphological aspects of interactions between Rhizobium meliloti and alfalfa (Medicago sativa) in association with Azospirillum brasilense. Can J Microbiol 39:610–615

    Article  Google Scholar 

  • Itzigsohn R, Yarden O, Okon Y (1995) Polyhydroxyalkanoate analysis in Azospirillum brasilense. Can J Microbiol 41:73–76

    Article  CAS  Google Scholar 

  • Jain DK, Patriquin DG (1984) Root hair deformation, bacterial attachment, and plant growth in wheat –Azospirillum associations. Appl Environ Microbiol 48:1208–1213

  • Joe M, Karthikeyan MB, Sekar C, Deiveekasundaram M (2010) Optimization of biofl oc production in Azospirillum brasilense (MTCC-125) and evaluation of its adherence with the roots of certain crops. Indian J Microbiol 50(Suppl 1):S21–S25

    Article  Google Scholar 

  • Jofre E, Lagares A, Mori G (2004) Disruption of dTDP-rhamnose biosynthesis modifies lipopolysaccharide core, exopolysaccharide production, and root colonization in Azospirillum brasilense. FEMS Microbiol Lett 231:267–275

    Article  CAS  PubMed  Google Scholar 

  • Kaneko T et al (2010) Complete genomic structure of the cultivated rice endophyte Azospirillum sp. B510. DNA Res 17:37–50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kapulnik Y, Sarig S, Nur I, Okon Y, Kigel J, Henis Y (1981) Yield increases in summer cereal crops of Israeli fields inoculated with Azospirillum. Exp Agric 17:179–187

    Article  CAS  Google Scholar 

  • Kapulnik Y, Sarig S, Nur I, Okon Y (1983) Effect of Azospirillum inoculation on yield of field-grown wheat. Can J Microbiol 29:895–899

    Article  Google Scholar 

  • Karpati E, Kiss P, Afsharian M, Marini F, Buglioni S, Fendrik L, Del Gallo M (1995) Molecular studies of the interaction of Azospirillum lipoferum with wheat germ agglutinin. NATO ASI Ser Ser G 37:213–221

    CAS  Google Scholar 

  • Katsy EI, Iosipenko AD, Egorenkov DA, Zhuravleva EA, Panasenko VI, Ignatov VV (1990) Involvement of Azospirillum brasilense plasmid DNA in the production of indole acetic acid. FEMS Microbiol Lett 60:1–4

    Article  Google Scholar 

  • Katupitiya S, Millet J, Vesk M, Viccars L, Zeman A, Lidong Z, Elmerich C, Kennedy IR (1995a) A mutant of Azospirillum brasilense Sp7 impaired in flocculation with a modified colonization pattern and superior nitrogen fixation in association with wheat. Appl Environ Microbiol 61:1987–1995

    CAS  PubMed  PubMed Central  Google Scholar 

  • Katupitiya S, New PB, Elmerich C, Kennedy IR (1995b) 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

    Article  CAS  Google Scholar 

  • Kennedy IR, Tchan YT (1992) Biological nitrogen-fixation in non-leguminous field crops: recent advances. Plant Soil 141:93–118

    Article  CAS  Google Scholar 

  • Kennedy IR, Pereg-Gerk LL, Wood C, Deaker R, Gilchrist K, Katupitiya S (1997) Biological nitrogen fixation in non-leguminous field crops: facilitating the evolution of an effective association between Azospirillum and wheat. Plant Soil 194:65–79

    Article  CAS  Google Scholar 

  • Kesava Rao PS, Arunachalam V, Tilak KVBR (1990) Genotype dependent response to Azospirillum treatment in yield and nitrogenase activity in Brassica juncea L. Curr Sci 59:607–609

    Google Scholar 

  • Khammas KM, Ageron E, Grimont PAD, Kaiser P (1989) Azospirillum irakense sp. nov., a new nitrogen-fixing bacterium associated with rice roots and rhizosphere soil. Res Microbiol 140:679–693

    CAS  PubMed  Google Scholar 

  • Kochar M, Srivastava S (2012) Surface colonization by Azospirillum brasilense SM in the indole‐3‐acetic acid dependent growth improvement of sorghum. J Basic Microb 52:123–131

    Article  CAS  Google Scholar 

  • Lamm RB, Neyra CA (1981) Characterization and cyst production of azospirilla isolated from selected grasses growing in New Jersey and New York. Can J Microbiol 27:1320–1325

    Article  Google Scholar 

  • Larraburu EE, Apóstolo NM, Llorente BE (2010) Anatomy and morphology of photinia (Photinia x fraseri Dress) in vitro plants inoculated with rhizobacteria. Trees 24:635–642

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lebsky VK, Gonzalez-Bashan LE, Bashan Y (2001) Ultrastructure of interaction in alginate beads between the microalga Chlorella vulgaris with its natural associative bacterium Phyllobacterium myrsinacearum and with the plant growth-promoting bacterium Azospirillum brasilense. Can J Microbiol 47:1–8

    Article  CAS  PubMed  Google Scholar 

  • Lerner A, Castro-Sowinski S, Valverde A, Lerner H, Dror R, Okon Y, Burdman S (2009) The Azospirillum brasilense Sp7 noeJ and noeL genes are involved in extracellular polysaccharide biosynthesis. Microbiology 155:4058–4068

    Article  CAS  PubMed  Google Scholar 

  • Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Promé JC, Dénarié J (1990) Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344:781–784

    Article  CAS  PubMed  Google Scholar 

  • Levanony H, Bashan Y (1991) Active attachment of Azospirillum brasilense to root surface of non-cereal plants and to sand particles. Plant Soil 137:91–97

    Article  Google Scholar 

  • Levanony H, Bashan Y, Romano B, Klein E (1989) Ultrastructural localization and identification of Azospirillum brasilense Cd on and within wheat root by immuno-gold labeling. Plant Soil 117:207–218

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Lin W, Okon Y, Hardy RWF (1983) Enhanced mineral uptake by Zea mays and Sorghum bicolor roots inoculated with Azospirillum brasilense. Appl Environ Microbiol 45:1775–1779

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lin S-Y, Hameed A, Shen F-T, Liu Y-C, Hsu Y-H, Shahina M, Lai W-A, Young C-C (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. Antonie Van Leeuwenhoek 105:1149–1162

    Article  CAS  PubMed  Google Scholar 

  • Madhaiyan M, Poonguzhali S, Kang B-G, Lee Y-J, Chung J-B, Sa T-M (2010) Effect of co-inoculation of methylotrophic Methylobacterium oryzae with Azospirillum brasilense and Burkholderia pyrrocinia on the growth and nutrient uptake of tomato, red pepper and rice. Plant Soil 328:71–82

    Article  CAS  Google Scholar 

  • Magalhães FM, Baldani JI, Souto SM, Kuykendall JR, Döbereiner J (1983) A new acid-tolerant Azospirillum species. An Acad Bras Cienc 55:417–430

    Google Scholar 

  • Mahfouz SA, Sharaf-Eldin MA (2007) Effect of mineral vs. biofertilizer on growth, yield, and essential oil content of fennel (Foeniculum vulgare Mill.). Int Agrophys 21:361–366

    CAS  Google Scholar 

  • Masciarelli O, Urbani L, Reinoso H, Luna V (2013) Alternative mechanism for the evaluation of indole-3-acetic acid (IAA) production by Azospirillum brasilense strains and its effects on the germination and growth of maize seedlings. J Microbiol 51:590–597

    Article  CAS  PubMed  Google Scholar 

  • Massena-Reis V, dos Santos Teixeira KR, 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, pp 123–138

    Chapter  Google Scholar 

  • Matthews SW, Schank SC, Aldrich HC, Smith RL (1983) Peroxidase-antiperoxidase labeling of Azospirillum brasilense in field-grown pearl millet. Soil Biol Biochem 6:699–703

    Article  Google Scholar 

  • McMillan M, Pereg L (2014) Evaluation of reference genes for gene expression analysis using quantitative RT-PCR in Azospirillum brasilense. PLoS ONE 9(5), e98162. doi:10.1371/journal.pone.0098162

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Meza B, de-Bashan LE, Bashan Y (2015a) Involvement of indole-3-acetic acid produced by Azospirillum brasilense in accumulating intra-cellular ammonium in Chlorella vulgaris. Res Microbiol 166:72–83

    Article  CAS  PubMed  Google Scholar 

  • Meza B, de-Bashan LE, Hernandez J-P, Bashan Y (2015b) Accumulation of intra-cellular polyphosphate in Chlorella vulgaris cells is related to indole-3-acetic acid produced by Azospirillum brasilense. Res Microbiol 166:399–407

    Article  CAS  PubMed  Google Scholar 

  • Michiels K, Vanderleyden J, Van Gool A, Signer ER (1988) Isolation and characterization of Azospirillum brasilense loci that correct Rhizobium meliloti exoB and exoC mutations. J Bacteriol 170:5401–5404

    CAS  PubMed  PubMed Central  Google Scholar 

  • Michiels K, De Troch P, Onyeocha I, Van Gool A, Elmerich C, Vanderleyden J (1989) Plasmid localization and map** of two Azospirillum brasilense loci that affect exopolysaccharides synthesis. Plasmid 21:142–146

    Article  CAS  PubMed  Google Scholar 

  • Michiels K, Verreth C, Vanderleyden J (1990) Azospirillum lipoferum and Azospirillum brasilense surface polysaccharide mutants that are affected in flocculation. J Appl Bacteriol 69:705–711

    Article  CAS  Google Scholar 

  • Michiels K, Croes CL, Vanderleyden J (1991) Two different modes of attachment of Azospirillum brasilense Sp7 to wheat roots. J Gen Microbiol 137:2241–2246

    Article  CAS  Google Scholar 

  • Mikhailouskaya N (2006) The effect of flax seed inoculation by Azospirillum brasilense on flax yield and its quality. Plant Soil Environ 52:402–406

    Google Scholar 

  • Millet E, Avivi Y, Feldman M (1986) Yield response of various wheat genotypes to inoculation with Azospirillum brasilense. Plant Soil 80:261–266

    Article  Google Scholar 

  • 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 21:1001–1009

    Article  CAS  PubMed  Google Scholar 

  • Molla AH, Shamsuddin ZH, Halimi MS (2001a) Mechanism of root growth and promotion of nodulation in vegetable soybean by Azospirillum brasilense. Commun Soil Sci Plan 32:2177–2187

    Article  CAS  Google Scholar 

  • Molla AH, Shamsuddin ZH, Halimi MS, Morziah M, Puteh AB (2001b) Potential for enhancement of root growth and nodulation of soybean co-inoculated with Azospirillum and Bradyrhizobium in laboratory systems. Soil Biol Biochem 33:457–463

    Article  CAS  Google Scholar 

  • Mortley DG, Hill WA (1990) Sweet potato growth and nitrogen content following nitrogen application and inoculation Azospirillum. Hortscience 25:758–759

    Google Scholar 

  • Murty MG, Ladha JK (1987) Differential colonization of Azospirillum lipoferum on roots of two varieties of rice (Oryza sativaL.). Biol Fertil Soils 4:3–7

    Google Scholar 

  • Nosheen A, Bano A, Ullah F (2011) Nutritive value of canola (Brassica napus L.) as affected by plant growth promoting rhizobacteria. Eur J Lipid Sci Technol 113:1342–1346

    Article  CAS  Google Scholar 

  • Okon Y, Kapulnik Y (1986) Development and function of Azospirillum-inoculated roots. Plant Soil 90:3–16

    Article  CAS  Google Scholar 

  • Okon Y, Itzigsohn R (1992) Poly-β-hydroxybutyrate metabolism in Azospirillum brasilense and the ecological role of PHB in the rhizosphere. FEMS Microbiol Rev 103:131–140

    CAS  Google Scholar 

  • Okon Y, Labandera-Gonzalez CA (1994) Agronomic applications of Azospirillum: An evaluation of 20 years worldwide field inoculation. Soil Biol Biochem 26:1591–1601

    Article  CAS  Google Scholar 

  • Okon Y, Cakmakci L, Nur I, Chet I (1980) Aerotaxis and chemotaxis of Azospirillum brasilense: a note. Microb Ecol 6:277–28

    Article  CAS  PubMed  Google Scholar 

  • Onyeocha I, Vieille C, Zimmer W, Baca BE, Flores M, Palacios R, Elmerich C (1990) Physical map and properties of a 90-MDa plasmid of Azospirillum brasilense Sp7. Plasmid 23:169–182

    Article  CAS  PubMed  Google Scholar 

  • Patriquin DG, Döbereiner J, Jain DK (1983) Sites and processes of association between diazotrophs and grasses. Can J Microbiol 29:900–915

    Article  Google Scholar 

  • Pereg Gerk L (2004) Expression of flcA, a gene regulating differentiation and plant interaction in Azospirillum. Soil Biol Biochem 36:1245–1252

    Article  CAS  Google Scholar 

  • Pereg Gerk L, Paquelin A, Gounon P, Kennedy IR, Elmerich C (1998) A transcriptional regulator of the LuxR-UhpA family, FlcA, controls flocculation and wheat root surface colonisation by Azospirillum brasilense Sp7. Mol Plant Microbe Interact 11:177–187

    Article  CAS  PubMed  Google Scholar 

  • Pereg Gerk L, Gilchrist K, Kennedy IR (2000) Mutants with enhanced nitrogenase activity in hydroponic Azospirillum brasilense-wheat associations. Appl Environ Microbiol 66:2175–2184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pereira JAR, Cavalcante VA, Baldani JI, Döbereiner J (1988) Field inoculation of sorghum and rice with Azospirillum spp. and Herbaspirillum seropedicae. Plant Soil 110:269–274

    Article  Google Scholar 

  • Pereyra CM, Ramella NA, Pereyra MA, Barassi CA, Creus CM (2010) Changes in cucumber hypocotyl cell wall dynamics caused by Azospirillum brasilense inoculation. Plant Physiol Biochem 48:62–69

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Petersen DJ, Eyers M, De Troch P, Michiels K, Vandeleyden J (1992) Differential complementation of Rhizobium meliloti 7027: isolation of a second ExoC locus from Azospirillum brasilense Sp7. Symbiosis 13:139–145

    CAS  Google Scholar 

  • Petrova LP, Shelud’ko AV, Katsy EI (2010) Plasmid rearrangements and alterations in Azospirillum brasilense biofilm formation. Microbiology 79:121–124

    Article  CAS  Google Scholar 

  • Plazinski J, Rolfe BG (1985) Influence of Azospirillum strains on the nodulation of clovers by Rhizobium Strains. Appl Environ Microbiol 49:984–989

    CAS  PubMed  PubMed Central  Google Scholar 

  • Poongguzhali S, Madhaiyan M, Thangaraju M, Ryu J, Chung K, Sa T (2005) Effects of co-cultures, containing N-fixer and P-solubilizer, on the growth and yield of pearl millet (Pennisetum glaucum (L.) R. Br.) and blackgram (Vigna mungo L.). J Microbiol Biotechnol 15:903–908

    Google Scholar 

  • Puente M-E, 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 

  • Puente ME, Holguin G, Glick BR, Bashan Y (1999) Root-surface colonization of black mangrove seedlings by Azospirillum halofraeferens and Azospirillum brasilense in seawater. FEMS Microbiol Ecol 29:283–292

    Article  CAS  Google Scholar 

  • Rajendran K, Devaraj P (2004) Biomass and nutrient distribution and their return of Casuarina equisetifolia inoculated with biofertilizers in farm land. Biomass Bioenerg 26:235–249

    Article  CAS  Google Scholar 

  • Ramos HJO, Roncato-Maccari LDB, Souza EM, Soares-Ramos JRL, Hungria M, Pedrosa FO (2002) Monitoring Azospirillum-wheat interactions using the gfp and gusA genes constitutively expressed from a new broad-host range vector. J Biotechnol 97:243–252

    Article  CAS  PubMed  Google Scholar 

  • Ratti N, Janardhanan KK (1996) Response of dual inoculation with V AM and Azospirillum on the yield and oil content of Palmarosa (Cymhopogon martinii var. motia). Microb Res 151:325–328

    Article  CAS  Google Scholar 

  • Raverkar KP, Konde BK (1988) Effect of Rhizobium and Azospirillum lipoferum inoculation on the nodulation, yield and nitrogen uptake of peanut cultivars. Plant Soil 106:249–252

    Article  CAS  Google Scholar 

  • Reiner O, Okon Y (1986) Oxygen recognition in aerotactic behaviour of Azospirillum brasilense Cd. Can J Microbiol 32:829–834

    Article  CAS  Google Scholar 

  • Reinhold B, Hurek T, Fendrik I (1985) Strain specific chemotaxis of Azospirillum spp. J Bacteriol 162:190–195

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reinhold B, Hurek T, Niemann E-G, Fendrik I (1986) Close association of Azospirillum and diazotrophic rods with different root zones of Kallar grass. Appl Environ Microbiol 52:520–526

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 Bacteriol 37:43–51

    Article  Google Scholar 

  • Reynders L, Vlassak K (1982) Use of Azospirillum brasilense as biofertilizer in intensive wheat crop**. Plant Soil 66:217–223

    Article  Google Scholar 

  • Ribaudo C, Krumpholz E, Cassan F, Bottini R, Cantore M, Cura A (2006) Azospirillum sp. promotes root hair development in tomato plants through a mechanism that involves ethylene. J Plant Growth Regul 25:175–185

    Article  CAS  Google Scholar 

  • Rodríguez-Barrueco C, Cervantes E, Subbarao NS, Rodríguez-Caceres E (1991) Growth promoting effect of Azospirillum brasilense on Casuarina cunninghamiana Miq. seedlings. Plant Soil 135:121–124

    Article  Google Scholar 

  • Romero AM, Correa OS, Moccia S, Rivas JG (2003) Effect of Azospirillum-mediated plant growth promotion on the development of bacterial diseases on fresh-market and cherry tomato. J Appl Microbiol 95:832–838

    Article  CAS  PubMed  Google Scholar 

  • Romero AM, Vega D, Correa OS (2014) Azospirillum brasilense mitigates water stress imposed by a vascular disease by increasing xylem vessel area and stem hydraulic conductivity in tomato. Appl Soil Ecol 82:38–43

    Article  Google Scholar 

  • Rothballer M, Schmid M, Hartmann A (2003) In situ localization and PGPR-effect of Azospirillum brasilense strains colonizing roots of different wheat varieties. Symbiosis 34:261–279

    Google Scholar 

  • Rueda-Puente E, Castellanos T, Troyo-Dieguez E, Leon-Alvarez JLD, Murillo-Amador B (2003) Effects of a nitrogen-fixing indigenous bacterium Klebsiella pneumoniae on the growth and development of the halophyte Salicornia bigelovii as a new crop for saline environments. J Agron Crop Sci 189:323–332

    Article  Google Scholar 

  • Saha KC, Sannigrahi S, Mandal LN (1985) Effect of inoculation of Azospirillum lipoferum on nitrogen fixation in rhizosphere soil, their association with root, yield and nitrogen uptake by mustard (Brassica juncea). Plant Soil 87:273–280

    Article  Google Scholar 

  • Sant’Anna FH, Almeida LG, Cecagno R, Reolon LA, Siqueira FM, Machado MR, Vasconcelos AT, Schrank IS (2011) Genomic insights into the versatility of the plant growth-promotingbacterium Azospirillum amazonense. BMC Genomics 12:409

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Santos F, Peñaflor MFG, Paré PW, Sanches PA, Kamiya AC, Tonelli M, Nardi C, Bento JMS (2014) A novel interaction between plant-beneficial rhizobacteria and roots: colonization induces corn resistance against the root herbivore Diabrotica speciosa. PLoS ONE 9(11), e113280. doi:10.1371/journal.pone.0113280

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schank SC, Smith RL, Weiser GC, Zuberer DA, Bouton JH, Quesenberry KH, Tyler ME, Milam JR, Littell RC (1979) Fluorescent antibody technique to identify Azospirillum brasilense associated with roots of grasses. Soil Biol Biochem 11:287–295

    Article  Google Scholar 

  • Schloter M, Hartmann A (1998) Endophytic and surface colonization of wheat roots (Triticum aestivum) by different Azospirillum brasilense strains studied with strain-specific monoclonal antibodies. Symbiosis 25:159–17

  • Schloter M, Borlinghaus R, Bode W, Hartmann A (1993) Direct identification, and localization of Azospirillum in the rhizosphere of wheat using fluorescence-labeled monoclonal antibodies and confocal scanning laser microscopy. J Microsc 171:173–177

    Article  Google Scholar 

  • Schloter M, Kirchhof G, Heinzmann U, Döbereiner J, Hartmann A (1994) Immunological studies of the wheat-root-colonization by the Azospirillum brasilense strains Sp7 and Sp245 using strain-specific monoclonal antibodies. The 6th International Symposium on Nitrogen Fixation with Non-Legumes, Ismailia/Egypt, The American University in Cairo Press

  • Schoebitz M, Mengual C, Roldán A (2014) Combined effects of clay immobilized Azospirillum brasilense and Pantoea dispersa and organic olive residue on plant performance and soil properties in the revegetation of a semiarid area. Sci Total Environ 466–467:67–73

    Article  PubMed  CAS  Google Scholar 

  • Siddiqui ZA (2004) Effects of plant growth promoting bacteria and composed organic fertilizers on the reproduction of Meloidogyne incognita and tomato growth. Bioresour Technol 95:223–227

    Article  CAS  PubMed  Google Scholar 

  • Singh CS, Subba NS (1979) Associative effect of Azospirillum brasilense with Rhizobium japonicum on nodulation and yield of soybean (Glycine max). Plant Soil 53:387–392

    Article  Google Scholar 

  • Siuti P, Green C, Edwards AN, Doktycz MJ, Alexandre G (2011) The chemotaxis-like Che1 pathway has an indirect role in adhesive cell properties of Azospirillum brasilense. FEMS Microbiol Lett 323:105–112

    Article  CAS  PubMed  Google Scholar 

  • Skvortsov IM, Ignatov VV (1998) Extracellular polysaccharides and polysaccharide-containing biopolymers from Azospirillum species: Properties and the possible role in interaction with plant roots. FEMS Microbiol Lett 165:223–229

    Article  CAS  PubMed  Google Scholar 

  • Skvortsov I, Konnova S, Makarov O, Prokhorova R, Ignatov V (1995) Azospirillum brasilense exopolysaccharide complexes, their possible involvement in bacteria-wheat roots interactions and the suggested nature of these interactions. NATO ASI Ser Ser G 37:279–290

    CAS  Google Scholar 

  • Smith RL, Schank SC, Milam JR, Baltensperger AA (1984) Responses of Sorghum and Pennisetum species to the N2-fixing bacterium Azospirillum brasilense. Appl Environ Microbiol 47:1331–1336

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sriskandarajah S, Kennedy IR, Yu D, Tchan YT (1993) Effects of plant growth regulators on acetylene-reducing associations between Azospirillum brasilense and wheat. Plant Soil 153:165–178

    Article  CAS  Google Scholar 

  • Steenhoudt O, Vanderleyden J (2000) Azospirillum, a freeliving nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol Rev 24:487–506

    Article  CAS  PubMed  Google Scholar 

  • Stephens BB, Loar SN, Alexandre G (2006) Role of CheB and CheR in the complex chemotactic and aerotactic pathways of Azospirillum brasilense. J Bacteriol 188:4759–4768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sukiman HI, New PB (1990) Relationship between root colonization and initial adsorption of Azospirillum to plant roots. Microb Ecol 20:65–74

    Article  CAS  PubMed  Google Scholar 

  • Tabary F, Balandreau J, Bourrillon R (1984) Purification of the rice embryo lectin and its binding to nitrogen-fixing bacteria from the rhizosphere of rice. Biochem Biophys Res Commun 119:549–555

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Tortora ML, Díaz-Ricci JC, Pedraza RO (2011a) Protection of strawberry plants (Fragaria ananassa Duch.) against anthracnose disease induced by Azospirillum brasilense. Plant Soil 356:279–290

    Article  CAS  Google Scholar 

  • Tortora ML, Dıaz-Ricci JC, Pedraza RO (2011b) Azospirillum brasilense siderophores with antifungal activity against Colletotrichum acutatum. Arch Microbiol 193:275–286

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Umali-Garcia M, Hubbell DH, Gaskins MH, Dazzo FB (1980) Association of Azospirillum with grass roots. Appl Environ Microbiol 39:219–226

    CAS  PubMed  PubMed Central  Google Scholar 

  • Umali-Garcia M, Hubbell DH, Gaskins MH, Dazzo FB (1981) Adsorption and mode of entry of Azospirillum brasilenseto grass roots. In: Vose B, Ruschel AP (eds) Associative N2-fxation, vol 1, PVol. CRC Press, Boca Raton, pp 49–62

    Google Scholar 

  • Valverde A, Okon Y, Burdman S (2006) cDNA-AFLP reveals differentially expressed genes related to cell aggregation of Azospirillum brasilense. FEMS Microbiol Lett 265:186–194

    Article  CAS  PubMed  Google Scholar 

  • Van Rhijn P, Vanstockem M, Vanderleyden J, De Mot R (1990) Isolation of behavioral mutants of Azospirillum brasilense by using Tn5 lacZ. Appl Environ Microbiol 56:990–996

    PubMed  PubMed Central  Google Scholar 

  • Vande Broek A, Vanderleyden J (1995) Review: genetics of the Azospirillum-plant root association. Crit Rev Plant Sci 14:445–466

    Article  CAS  Google Scholar 

  • Vande Broek A, Michiels J, Van Gool A, Vanderleyden J (1993) Spatial-temporal colonization patterns of Azospirillum brasilense on the wheat root surface and expression of the bacterial nifH gene during association. Mol Plant Microbe Interact 6:592–600

    Article  Google Scholar 

  • Vande Broek A, Lambrecht M, Vanderleyden J (1998) Bacterial chemotactic motility is important for the initiation of wheat root colonization by Azospirillum brasilense. Microbiology 144:2599–2606

  • Vasil V, Vasil IK, Zuberer DA, Hubbell DH (1979) The biology of Azospirillum-sugarcane association. I. Establishment of the association. Z Pflanzenphysiol 95:141–147

    Article  Google Scholar 

  • Vial L, Cuny C, Gluchoff-Fiasson K, Comte G, Oger PM, Faure D, Dessaux Y, Bally R, Wisniewski-Dyé F (2006a) N-acyl-homoserine lactone-mediated quorum sensingin Azospirillum: an exception rather than a rule. FEMS Microbiol Ecol 58:155–168

    Article  CAS  PubMed  Google Scholar 

  • Vial L, LavireC MP, Blaha D, Haurat J, Moenne-Loccoz Y, Bally R, Wisniewski-Dyé F (2006b) Phase variation and genomic architecture changes in Azospirillum. J Bacteriol 188:5364–5373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vieille C, Elmerich C (1990) Characterization of two Azospirillum brasilense Sp7 plasmid genes homologous to R. meliloti nodPQ. Mol Plant Microbe Interact 3:389–400

    Article  CAS  PubMed  Google Scholar 

  • Vieille C, Elmerich C (1992) Characterization of an Azospirillum brasilense Sp7 gene homologous to Alcaligenes eutrophus phbB and to Rhizobium meliloti nod. G. Mol Gen Genet 231:375–384

    Article  CAS  PubMed  Google Scholar 

  • Walker V, Bertrand C, Bellvert F, Moënne-Loccoz Y, Bally R, Comte G (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 189:494–506

    Article  CAS  PubMed  Google Scholar 

  • Wani SP, Chandrapalaiah S, Dart PJ (1985) Response of pearl millet cultivars to inoculation with nitrogen-fixing bacteria. Exp Agric 21:175–182

    Article  Google Scholar 

  • Whallon JH, Acker GF, El-Khawas H (1985) Electron microscopy of young wheat roots inoculated with Azospirillum. In: Klingmüller W (ed) Azospirillum. III. Genetics, Phsyiology, Ecology. Springer-Verlag, Berlin, pp 223–229

    Google Scholar 

  • Wisniewski-Dyé F et al (2011) Azospirillum genomes reveal transition of bacteria from aquatic to terrestrial environments. PLOS Genet 7, e1002430. doi:10.1371/journal.pgen.1002430

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wisniewski-Dyé F, Lozano L, Acosta-Cruz E, Borland S, Drogue B, Prigent-Combaret C, Rouy Z, Barde V, Mendoza A, Gonzalez 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • **e C-H, 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

    Article  CAS  PubMed  Google Scholar 

  • Yahalom E, Kapulnik Y, Okon Y (1984) Response of Setaria italica to inoculation with Azospirillum brasilense as compared to Azotobacter chroococcum. Plant Soil 82:77–85

    Article  Google Scholar 

  • 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 36:10–14

    Article  Google Scholar 

  • 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 73:2595–2599

    Article  CAS  PubMed  Google Scholar 

  • Yegorenkova I, Konnova S, Sachuk V, Ignatov V (2001) Azospirillum brasilense colonisation of wheat roots and the role of lectin–carbohydrate interactions in bacterial adsorption and root-hair deformation. Plant Soil 231:275–282

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Zaady E, Okon Y (1990) Cultural conditions affecting Azospirillum brasilense cell aggregation and adsorption to maize roots. Soil Biol Biochem 22:1103–1107

    Article  Google Scholar 

  • Zaady E, Perevolotsky A (1995) Enhancement of growth and establishment of oak seedlings (Quercus ithaburensis Decaisne) by inoculation with Azospirillum brasilense. For Ecol Manag 72:81–83

    Article  Google Scholar 

  • Zamudio M, Bastarrachea F (1994) Adhesiveness and root hair deformation capacity of Azospirillum strains for wheat seedlings. Soil Biol Biochem 26:791–797

    Article  Google Scholar 

  • Zawoznik MS, Ameneiros M, Benavides MP, Vázquez S, Groppa MD (2011) Response to saline stress and aquaporin expression in Azospirillum-inoculated barley seedlings. Appl Microbiol Biotechnol 90:1389–1397

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Zhu G-Y, Dobbelaere S, Vanderleyden J (2002) Use of green fluorescent protein to visualize rice root colonization by Azospirillum irakense and A. brasilense. Funct Plant Biol 29:1279–1285

    Article  Google Scholar 

  • Zhulin IB, Bespalov AV, Johnson MS, Taylor BL (1996) Oxygen taxis and proton motive force in Azospirillum brasilense. J Bacteriol 178:5199–5204

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank Manuel Moreno of CIBNOR, Mexico for drawing the figure, AM Babey at the University of New England, Australia and Ira Fogel of CIBNOR Mexico for providing English and editorial suggestions. This study was supported by Consejo Nacional de Ciencia y Tecnologia of Mexico (CONACYT-Basic Science-2009, contract 164548) and time for writing by The Bashan Foundation, USA. This is contribution 2015–006 from the Bashan Institute of Science, USA.

Author information

Authors and Affiliations

  1. Research Group of Molecular Biology, School of Science and Technology, University of New England, Armidale, NSW, 2351, Australia

    Lily Pereg

  2. Environmental Microbiology Group, The Northwestern Center for Biological Research (CIBNOR), Calle IPN 195, La Paz, B.C.S., 23096, Mexico

    Luz E. de-Bashan & Yoav Bashan

  3. The Bashan Institute of Science, 1730 Post Oak Court, Auburn, AL, 36830, USA

    Luz E. de-Bashan & Yoav Bashan

  4. Department of Entomology and Plant Pathology, Auburn University, 301 Funchess Hall, Auburn, AL, 36849, USA

    Luz E. de-Bashan & Yoav Bashan

Authors
  1. Lily Pereg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Luz E. de-Bashan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yoav Bashan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yoav Bashan.

Additional information

Responsible Editor: Philippe Hinsinger.

Dedication

This study is dedicated to the memory of the Israeli soil microbiologist Prof. Yigal Henis (1926–2010) of the Faculty of Agriculture, The Hebrew University of Jerusalem in Rehovot, Israel, one of the pioneers of research of Azospirillum.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 31 kb)

ESM 2

(DOCX 27 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pereg, L., de-Bashan, L.E. & Bashan, Y. Assessment of affinity and specificity of Azospirillum for plants. Plant Soil 399, 389–414 (2016). https://doi.org/10.1007/s11104-015-2778-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-015-2778-9

Keywords

Search

Navigation