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Azospirillum sp. as a Challenge for Agriculture

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Bacterial Metabolites in Sustainable Agroecosystem

Part of the book series: Sustainable Development and Biodiversity ((SDEB,volume 12))

Abstract

Several processes mediated by soil microorganisms play an important role in nutrient cycling. One such process is biological nitrogen fixation (BNF) by representatives of various bacterial phylogenetic groups, which are called diazotrophs. Most studies of the Azospirillum-plant association have been conducted on cereals and grasses. Currently, 17 species of Azospirillum have been described. However, a great diversity of these bacteria continues to be revealed, and little is known of the potential applications of the many species that have been described. The Azospirillum-plant association begins with the adsorption and adherence process of these bacteria in roots. Involved in these processes is the recognition of bacterial polysaccharides by the host plant, a step that is necessary in successfully forming a positive relationship between roots and Azospirillum. The presence of Azospirillum in the rhizosphere can minimize the susceptibility to diseases caused by plant pathogens. Furthermore, the ability to produce phytohormones, mainly auxins (indole-3-acetic acid) and other molecules from secondary metabolism has been suggested to underlie the growth response to inoculation by Azospirillum species. These positive aspects of Azospirillum colonization in the roots are also responsible for the alleviation of plant stress. For all of the above-mentioned reasons, Azospirillum are also widely used as commercial inoculants, resulting in a significant economic impact in crop yields in many countries. In fact, solid and liquid formulations containing Azospirillum are marketed in various countries, such as Brazil, Argentina, Mexico, Italy, France, Belgium, Africa, Germany, Pakistan, Uruguay, India and the USA. In addition, new formulations containing Azospirillum, such as polymeric inoculants (alginate, agar, chitosan and gum), are already used for the improvement of many crops. This chapter summarizes the positive effects of Azospirillum-plant interactions and their biological importance for the improvement of agriculture worldwide.

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References

  • Abdulkareem M, Aboud HM, Saood HM, Shibly MK (2014) Antagonistic activity of some plant growth rhizobacteria to Fusarium graminearum. Int J Phytopathol 3(1):49–54

    Google Scholar 

  • Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci 26(1):1–20

    Article  Google Scholar 

  • Albareda M, Rodríguez-Navarro DN, Camacho M, Temprano FJ (2008) Alternatives to peat as a carrier for rhizobia inoculants: solid and liquid formulations. Soil Biol Biochem 40(11):2771–2779

    Article  CAS  Google Scholar 

  • Aleńkina SA, Bogatyrev VA, Matora LY, Sokolova MK, Chernyshova MP, Trutneva KA, Nikitina VE (2014a) Signal effects of the lectin from the associative nitrogen-fixing bacterium Azospirillum brasilense Sp7 in bacterial-plant root interactions. Plant Soil 381(1–2):337–349

    Article  CAS  Google Scholar 

  • Aleńkina SA, Petrova LP, Sokolova MK, Chernyshova MP, Trutneva KA, Bogatyrev VA, Nikitina VE (2014b) Comparative assessment of inductive effects of Azospirillum lectins with different antigenic properties on the signal systems of wheat seedling roots. Microbiology 83(3):262–269

    Google Scholar 

  • Alexandre G (2010) Coupling metabolism and chemotaxis-dependent behaviours by energy taxis receptors. Microbiology 156(8):2283–2293

    Article  CAS  PubMed  Google Scholar 

  • Almaghrabi OA, Massoud SI, Abdelmoneim TS (2013) Influence of inoculation with plant growth promoting rhizobacteria (PGPR) on tomato plant growth and nematode reproduction under greenhouse conditions. Saudi J Biol Sci 20(1):57–61

    Article  PubMed  Google Scholar 

  • Alves BJR, Boddey RM, Urquiaga S (2003) The success of BNF in soybean in Brazil. Plant Soil 252(1):1–9

    Article  CAS  Google Scholar 

  • Araújo ASF, Leite LFC, Iwata BF, Lira Junior MA, Xavier G, Figueiredo MBV (2012) Microbiological process in agroforestry systems: a review. Agron Sustain Dev 32(1):215–216

    Article  CAS  Google Scholar 

  • Araujo FF, Araújo ASF, Figueiredo MVB (2011) Role of plant growth-promoting bacteria in sustainable agriculture. In: Salazar A, Rios I (eds) Sustainable agriculture: technology, planning and management. Nova Science Publishers, New York

    Google Scholar 

  • Austin AT, Piñeiro G, Gonzalez-Polo M (2006) More is less: agricultural impacts on the N cycle in Argentina. Biogeochemistry 79(1):45–60

    Article  Google Scholar 

  • Babalola OO (2010) Beneficial bacteria of agricultural importance. Biotechnol Lett 32:1559–1570

    Article  CAS  PubMed  Google Scholar 

  • Babalola OO, Glick BR (2012) The use of microbial inoculants in African agriculture: current practice and future prospects. J Food Agri Environ 10(3–4):540–549

    Google Scholar 

  • Bacilio M, Vazquez P, Bashan Y (2003) Alleviation of noxious effects of cattle ranch composts on wheat seed germination by inoculation with Azospirillum spp. Biol Fertil Soils 38:261–266

    Article  Google Scholar 

  • Bahat-Samet E, Castro-Sowinski S, Okon Y (2004) Arabinose content of extracellular polysaccharide plays a role in cell aggregation of Azospirillum brasilense. FEMS Microbiol Lett 237:195–203

    Article  CAS  PubMed  Google Scholar 

  • Baldani VLD, Döbereiner J (1986) Effect of inoculation of Azospirillum spp. on the nitrogen assimilation of field grown wheat. Plant Soil 95:109–121

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  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, Holguin G (1998) Proposal for the division of plant growth-promoting rhizobacteria into two classifications: biocontrol-PGPB (plant growth-promoting bacteria) and PGPB. Soil Biol Biochem 30:1225–1228

    Article  CAS  Google Scholar 

  • Bashan Y, Levanony H (1985) An improved selection technique and medium for the isolation and enumeration of Azospirillum brasilense. Can J Microbiol 31:947–952

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Bauer H, Ache P, Lautner S, Fromm J, Hartung W, Al-Rasheid KA, Sonnewald S, Sonnewald U, Kneitz S, Lachmann N, Mendel RR, Bittner F, Hetherington AM, Hedrich R (2013) The stomatal response to reduced relative humidity requires guard cell-autonomous ABA synthesis. Curr Biol 23(1):53–57

    Article  CAS  PubMed  Google Scholar 

  • Belyakov AY, Burygin GL, Arbatsky NP, Shashkov AS, Selivanov NY, Matora LY, Knirel YA, Shchyogolev SY (2012) Identification of an O-linked repetitive glycan chain of the polar flagellum flagellin of Azospirillum brasilense Sp7. Carbohyd Res 361:127–132

    Article  CAS  Google Scholar 

  • Berg G (2009) Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84(1):11–18

    Article  CAS  PubMed  Google Scholar 

  • Bhardwaj D, Ansari MW, Sahoo RK, Tuteja N (2014) Biofertilizers function as key player in sustainable agriculture by improving soil fertility, plant tolerance and crop productivity. Microb Cell Fact 13:66

    Article  PubMed  PubMed Central  Google Scholar 

  • Bhattacharjee RB, Singh A, Mukhopadhyay SN (2008) Use of nitrogen-fixing bacteria as biofertiliser for non-legumes: prospects and challenges. Appl Microbiol Biotechnol 80(2):199–209

    Article  CAS  PubMed  Google Scholar 

  • Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microb Biotechnol 28(4):1327–1350

    Article  CAS  Google Scholar 

  • Bogino PC, Oliva MDLM, Sorroche FG, Giordano W (2013) The role of bacterial biofilms and surface components in plant-bacterial associations. Int J Mol Sci 14(8):15838–15859

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bottini R, Fulchieri M, Pearce DW, Pharis RP (1989) Identification of Gibberellins A1, A3, and iso-A3 in cultures of Azospirillum lipoferum. Plant Physiol 90:45–47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bottini R, Cassán F, Piccoli P (2004) Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl Microbiol Biotechnol 65(5):497–503

    Article  CAS  PubMed  Google Scholar 

  • Boyko AS, Dmitrenok AS, Fedonenko YP, Zdorovenko EL, Konnova SA, Knirel YA, Ignatov VV (2012) Structural analysis of the O-polysaccharide of the lipopolysaccharide from Azospirillum brasilense Jm6B2 containing 3-O-methyl-d-rhamnose (d-acofriose). Carbohyd Res 355:92–95

    Article  CAS  Google Scholar 

  • Brasil, SDDA-MDAPE (2011) Normative Ruling no.13 of 2011 March 24. Federal Official Gazette—Section 1. National Press, Brasília

    Google Scholar 

  • Bunemann EK, Schwenke GD, Van Zwieten L (2006) Impact of agricultural inputs on soil organisms—a review. Aust J Soil Res 44(4):379–406

    Article  Google Scholar 

  • Calvo P, Nelson L, Kloepper JW (2014) Agricultural uses of plant biostimulants. Plant Soil 383(1–2):3–41

    Article  CAS  Google Scholar 

  • Carreño-López R, Sánchez A, Camargo N, Elmerich C, Baca BE (2009) Characterization of chsA, a new gene controlling the chemotactic response in Azospirillum brasilense Sp7. Arch Microbiol 191(6):501–507

    Article  PubMed  CAS  Google Scholar 

  • Cassán FD, Lucangeli CD, Bottini R, Piccoli PN (2001) Azospirillum spp. metabolize [17, 17-2H2] gibberellin A20 to [17, 17-2H2] gibberellin A1 in vivo in dry rice mutant seedlings. Plant Cell Physiol 42(7):763–767

    Article  PubMed  Google Scholar 

  • Cassán F, Maiale S, Masciarelli O, Vidal A, Luna V, Ruiz O (2009a) Cadaverine production by Azospirillum brasilense and its possible role in plant growth promotion and osmotic stress mitigation. Eur J Soil Biol 45:12–19

    Article  CAS  Google Scholar 

  • Cassán 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 

  • 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(2):440–459

    Article  CAS  Google Scholar 

  • Castañeda-Saucedo MC, Gómez-González G, Tapia-Campos E, Maciel ON, Pérez JSB, Silva MLR (2013) Efecto de Azospirillum brasilense y fertilización química sobre el crecimiento, desarrollo, rendimiento y calidad de fruto de fresa (Fragaria x ananassa Duch). Interciencia 38(10):737–744

    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. Phytochem 87:65–77

    Article  CAS  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(2):97–103

    Article  CAS  Google Scholar 

  • Cohen AC, Travaglia CN, Bottini R, Piccoli PN (2009) Participation of abscisic acid and gibberellins produced by endophytic Azospirillum in the alleviation of drought effects in maize. Botany 87:455–462

    Article  CAS  Google Scholar 

  • Cohen AC, Bottini R, Pontin M, Berli FJ, Moreno D, Boccanlandro H, Travaglia CN, Piccoli PN (2015) Azospirillum brasilense ameliorates the response of Arabidopsis thaliana to drought mainly via enhancement of ABA levels. Physiol Plant 153:79–90

    Article  CAS  PubMed  Google Scholar 

  • Couillerot O, Ramírez-Trujillo A, Walker V, von Felten A, Jansa J, Maurhofer M, Défago G, Prigent-Combaret C, Comte G, Caballero-Mellado J, Moënne-Loccoz Y (2013) Comparison of prominent Azospirillum strains in Azospirillum-Pseudomonas-Glomus consortia for promotion of maize growth. Appl Microbiol Biotechnol 97:4639–4649

    Article  CAS  PubMed  Google Scholar 

  • Dart PJ (1986) Nitrogen fixation associated with non-legumes in agriculture. Plant Soil 90(1–3):303–334

    Article  CAS  Google Scholar 

  • Di Salvo LP, Silva E, Teixeira KRS, Cote RE, Pereyra MA, García de Salamone IE (2014) Physiological and biochemical characterization of Azospirillum brasilense strains commonly used as plant growth-promoting rhizobacteria. J Basic Microbiol 54(12):1310–1321

    Article  PubMed  Google Scholar 

  • Dobbelaere S, Croonenborghs A, Thys A, van de Broek A, Vanderleyden J (1999) Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil 212:155–164

    Article  CAS  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 

  • Dodd IC, Zinovkina NY, Safronova VI, Belimov AA (2010) Rhizobacterial mediation of plant hormone status. Ann Appl Biol 157(3):361–379

    Article  CAS  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(8):500–510

    Article  PubMed  Google Scholar 

  • Duca D, Lorv J, Patten CL, Rose D, Glick BR (2014) Indole-3-acetic acid in plant-microbe interactions. Antonie Van Leeuwenhoek 106:85–125

    Article  CAS  PubMed  Google Scholar 

  • Dutta S, Podile AR (2010) Plant growth promoting rhizobacteria (PGPR): the bugs to debug the root zone. Crit Rev Microbiol 36(3):232–244

    Article  PubMed  Google Scholar 

  • Esquivel-Cote R, Ramírez-Gama RM, Tsuzuki-Reyes G, Orozco-Segovia A, Huante P (2010) Azospirillumlipoferum strain AZm5 containing 1-aminocyclopropane-1-carboxylic acid deaminase improves early growth of tomato seedlings under nitrogen deficiency. Plant Soil 337(1–2):65–75

    Article  CAS  Google Scholar 

  • Fedonenko YP, Boiko AS, Zdorovenko EL, Konnova SA, Shashkov AS, Ignatov VV, Knirel YA (2011) Structural peculiarities of the O-specific polysaccharides of Azospirillum bacteria of serogroup III. Biochemistry (Moscow) 76(7):797–802

    Article  CAS  Google Scholar 

  • Fedonenko YP, Burygin GL, Popova IA, Sigida EN, Surkina AK, Zdorovenko EL, Konnova SA (2013) Immunochemical characterization of the capsular polysaccharide of Azospirillum irakense KBC1. Curr Microbiol 67(2):234–239

    Article  CAS  PubMed  Google Scholar 

  • Ferreira AS, Pires RR, Rabelo PG, Oliveira RC, Luz JMQ, Brito CH (2013) Implications of Azospirillum brasilense inoculation and nutrient addition on maize in soils of the Brazilian Cerrado under greenhouse and field conditions. Appl Soil Ecol 72:103–108

    Article  Google Scholar 

  • Fibach-Paldi S, Burdman S, Okon Y (2012) Key physiological properties contributing to rhizosphere adaptation and plant growth promotion abilities of Azospirillum brasilense. FEMS Microbiol Lett 326:99–108

    Article  CAS  PubMed  Google Scholar 

  • Figueiredo MVB, Seldin L, Araujo FF, Mariano RLR (2010) Plant growth promoting rhizobacteria: fundamentals and applications. In: Maheshwari DK (ed) Plant growth and health promoting bacteria. Springer, Berlin

    Google Scholar 

  • França CRRS, Lira Junior MA, Figueiredo MVB, Stamford NP, Silva GA (2013) Feasibility of rhizobia conservation by liquid conditioners. Rev Cienc Agron 44(4):661–668

    Article  Google Scholar 

  • Fulchieri M, Lucangeli C, Bottini R (1993) Inoculation with Azospirillumlipoferum affects growth and gibberellin status of corn seedling roots. Plant Cell Physiol 34:1305–1309

    CAS  Google Scholar 

  • Gaind S, Rathi MS, Kaushik BD, Nain L, Verma OP (2007) Survival of bio-inoculants on fungicides-treated seeds of wheat, pea and chickpea and subsequent effect on chickpea yield. J Environ Sci Health, Part B 42(6):663–668

    Article  CAS  Google Scholar 

  • Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169(1):30–39

    Article  CAS  PubMed  Google Scholar 

  • Groppa MD, Benavides MP, Zawoznik MS (2012) Root hydraulic conductance, aquaporins and plant growth promoting microorganisms: a revision. Appl Soil Ecol 61:247–254

    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 K, Dey A, Gupta B (2013) Plant polyamines in abiotic stress responses. Acta Physiol Plant 35(7):2015–2036

    Article  CAS  Google Scholar 

  • Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60(4):579–598

    Article  Google Scholar 

  • Hoffland E, Hakulinen J, van Pelt JA (1995) Comparison of systemic resistance induced by avirulent and nonpathogenic Pseudomonas species. Phytopathology 86:757–762

    Article  Google Scholar 

  • Hou X, McMillan M, Coumans JV, 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hungria M, Campo RJ, Souza EM, Pedrosa FO (2010) Inoculation with selected strains of Azospirillum brasilense and A. lipoferum improves yields of maize and wheat in Brazil. Plant Soil 331(1):413–425

    Article  CAS  Google Scholar 

  • Ilyas N, Bano A (2010) Azospirillum strains isolated from roots and rhizosphere soil of wheat (Triticum aestivum L.) grown under different soil moisture conditions. Biol Fert Soils 46(4):393–406

    Google Scholar 

  • Iwashkiw JA, Vozza NF, Kinsella RL, Feldman MF (2013) Pour some sugar on it: the expanding world of bacterial protein O-linked glycosylation. Mol Microbiol 89:14–28

    Article  CAS  PubMed  Google Scholar 

  • Jacques RJS, Procópio SO, Santos JB, Kasuya MCM, Silva AA (2010) Sensitivity of Bradyrhizobium strains to glyphosate. Rev Ceres 57(1):28–33

    Article  CAS  Google Scholar 

  • Jansen R, Rood S, Dormar J, McGill W (1992) Azospirillum brasilense produces gibberellins in pure culture and chemically-medium and in co-culture on straw. Soil Biol Biochem 24:1061–1064

    Article  Google Scholar 

  • Jha M, Chourasia S, Sinha S (2013) Microbial consortium for sustainable rice production. Agroecol Sust Food 37(3):340–362

    Article  Google Scholar 

  • Jofré E, Fischer S, Príncipe A, Castro M, Ferrari W, Lagares A, Mori G (2009) Mutation in ad-alanine-d-alanine ligase of Azospirillum brasilense Cd results in an overproduction of exopolysaccharides and a decreased tolerance to saline stress. FEMS Microbiol Lett 290(2):236–246

    Article  PubMed  CAS  Google Scholar 

  • Kadouri D, Jurkevitch E, Okon Y (2003) Involvement of the reserve material poly-β-hydroxybutyrate in Azospirillum brasilense stress endurance and root colonization. Appl Environ Microbiol 69:3244–3250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kennedy IR, PeregGerk 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(1–2):65–79

    Article  CAS  Google Scholar 

  • Kloepper JW, Ryu CM, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1226

    Google Scholar 

  • Konnova ON, Boiko AS, Burygin GL, Fedonenko YP, Matora LY, Konnova SA, Ignatov VV (2008) Chemical and serological studies of liposaccharides of bacteria of the genus Azospirillum. Microbiology 77(3):305–312

    Article  CAS  Google Scholar 

  • Kuc J (1983) Induced systemic resistance in plants to diseases caused by fungi and bacteria. In: Bailey JA, Deveral BJ (eds) The dynamics of host defense. Academic Press, Sydney

    Google Scholar 

  • Lana MDC, Dartora J, Marini D, Hann JE (2012) Inoculation with Azospirillum, associated with nitrogen fertilization in maize. Rev Ceres 59(3):399–405

    Article  CAS  Google Scholar 

  • Laslo É, György É, Mara G, Tamás É, Ábrahám B, Lányi S (2012) Screening of plant growth promoting rhizobacteria as potential microbial inoculants. Crop Prot 40:43–48

    Article  CAS  Google Scholar 

  • Lerner A, Valverde A, Castro-Sowinski S, Lerner H, Okon Y, Burdman S (2010) Phenotypic variation in Azospirillum brasilense exposed to starvation. Environ Microbiol Rep 2(4):577–586

    Article  CAS  PubMed  Google Scholar 

  • Lucangeli C, Bottini R (1997) Effects of Azospirillum spp. on endogenous gibberellin content and growth of maize (Zea mays L.) treated with uniconazole. Symbiosis 23:63–72

    CAS  Google Scholar 

  • Maheshwari DK (2010) Plant growth and health promoting rhizobacteria. Microbiology Monograph. Springer Heidelberg Dordrecht: London New York, vol 18, p 453

    Google Scholar 

  • Malhotra M, Srivastava S (2009) Stress-responsive indole-3-acetic acid biosynthesis by Azospirillum brasilense SM and its ability to modulate plant growth. Eur J Soil Biol 45(1):73–80

    Article  CAS  Google Scholar 

  • Manivannan M, Tholkappian P (2013) Prevalence of Azospirillum isolates in tomato rhizosphere soils of coastal areas of Cuddalore District, Tamil Nadu. Int J Recent Sci Res 4:1610–1613

    Google Scholar 

  • Mariano RLR, Kloepper JW (2000) Método alternativo de biocontrole: resistência sistêmica induzida por rizobactérias. Rev An Patol Plantas 8:121–137

    Google Scholar 

  • Mehnaz S (2015) Azospirillum: a biofertilizer for every crop. In: Arora NK (ed) Plant microbes symbiosis: applied facets. Springer

    Google Scholar 

  • Merino S, Tomás JM (2014) Gram-negative flagella glycosylation. Int J Mol Sci 15:2840–2857

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mitter B, Brader G, Afzall M, Compant S, Naveed M, Trognitz F, Sessitsch A (2013) Advances in elucidating beneficial interactions between plants, soil, and bacteria. In: Sparks DL (ed) Advances in Agronomy. Academic Press, Burlington

    Google Scholar 

  • Moghadam HRT, Salimi H, Kasraie P, Jamshidpour F (2012) Effect of Azospirillum and Azotobacter in combination with nitrogen chemical fertilizer on wheat [Triticum aestivum L]. Res Crop 13(1):29–36

    Google Scholar 

  • Molina-Favero C, Creus CM, Lanteri ML, Correa-Aragunde N, Lombardo MC, Barassi CA, Lamattina L (2007) Nitric oxide and plant growth promoting rhizobacteria: common features influencing root growth and development. Adv Bot Res 46:1–33

    Article  CAS  Google Scholar 

  • Molinaro A, Newman MA, Lanzetta R, Parrilli M (2009) The structures of lipopolysaccharides from plant-associated Gram-negative bacteria. Eur J Org Chem 34:5887–5896

    Article  CAS  Google Scholar 

  • Monds RD, O’Toole GA (2009) The developmental model of microbial biofilms: ten years of a paradigm up for review. Trends Microbiol 17(2):73–87

    Article  CAS  PubMed  Google Scholar 

  • Mora P, Rosconi F, Fraguas LF, Castro-Sowinski S (2008) Azospirillum brasilense Sp7 produces an outer-membrane lectin that specifically binds to surface-exposed extracellular polysaccharide produced by the bacterium. Arch Microbiol 189:519–524

    Article  CAS  PubMed  Google Scholar 

  • Mostafa GG, Abo-Baker ABAM (2010) Effect of bio-and chemical fertilization on growth of sunflower (Helianthus annuus L.) at South Valley Area. Asian. J Crop Sci 2(3):137–146

    Google Scholar 

  • Moutia JFY, Saumtally S, Spaepen S, Vanderleyden J (2010) Plant growth promotion by Azospirillum sp. in sugarcane is influenced by genotype and drought stress. Plant Soil 337:233–242

    Article  CAS  Google Scholar 

  • Nadeem SM, Ahmad M, Zahir ZA, Javaid A, Ashraf M (2014) The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol Adv 32(2):429–448

    Article  PubMed  Google Scholar 

  • Naiman AD, Latrónico A, García de Salamone IE (2009) Inoculation of wheat with Azospirillum brasilense and Pseudomonas fluorescens: Impact on the production and culturable rhizosphere microflora. Eur J Soil Biol 45(1):44–51

    Article  Google Scholar 

  • Okon Y (1985) Azospirillum as a potential inoculant for agriculture. Trends Biotech 3:223–228

    Article  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(3):277–280

    Article  CAS  PubMed  Google Scholar 

  • Okon Y, Kapulnik Y, Sarig S (1988) Field inoculation studies with Azospirillum in Israel. In: Subba Rao NS (ed) Biological nitrogen fixation recent developments. Oxford and IBH Publishing Co, New Delhi

    Google Scholar 

  • Okon Y, Bar T, Tal S, Zaady E (1991) Physiological properties of Azospirillum brasilense involved in root growth promotion. In: Polsinelli M, Materassi R, Vincenzini M (eds) Nitrogen fixation: developments in plant and soil. Springer, Netherlands

    Google Scholar 

  • Pedraza RO, Bellone CH, Carrizo de Bellone S, Boa Sorte PMF, Teixeira KRS (2009) Azospirillum inoculation and nitrogen fertilization effect on grain yield and on the diversity of endophytic bacteria in the phyllosphere of rice rainfed crop. Eur J Soil Biol 45(1):36–43

    Article  CAS  Google Scholar 

  • Perez-Montano F, Alias-Villegas C, Bellogin RA, del Cerro P, Espuny MR, Jimenez-Guerrero I, Lopez-Baena FJ, Ollero FJ, Cubo T (2014) Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol Res 169(5–6):325–336

    Article  CAS  PubMed  Google Scholar 

  • Phillips PWB (2004) An economic assessment of the global inoculant industry. Crop Management 34:1

    Google Scholar 

  • Piccoli P, Bottini R (1996) Gibberellin production in Azospirillumlipoferum cultures is enhanced by light. Biocell 20(3):185–190

    CAS  Google Scholar 

  • Piccoli P, Masciarelli O, Bottini R (1999) Gibberellin production by Azospirillumlipoferum cultured in chemically-defined medium as affected by oxygen availability and water status. Symbiosis 27(2):135–145

    CAS  Google Scholar 

  • Pieterse CMJ, van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, van Loon LCA (1998) Novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–1580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raja P, Una S, Gopal H, Govindarajan K (2006) Impact of bioinoculants consortium on rice root exudates, biological nitrogen fixation and plant growth. J Biol Sci 6:815–823

    Article  Google Scholar 

  • Reddy CA, Saravanan RS (2013) Polymicrobial multi-functional approach for enhancement of crop productivity. Adv App Microbiol 82:53–113

    Article  CAS  Google Scholar 

  • Reis VM, Vanderleyden J, Spaepen S (2011) N2-Fixing endophytes of grasses and cereals. In: Polacco JC, Todd CD (eds) Ecological aspects of nitrogen metabolism in plants. John Wiley & Sons Inc, Hoboken, NJ/USA

    Google Scholar 

  • Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321(1–2):305–339

    Article  CAS  Google Scholar 

  • Rodrigues AC, Antunes JEL, Costa AF, Oliveira JP, Figueiredo MVB (2013a) Interrelationship of Bradyrhizobium sp. and plant growth-promoting bacteria in cowpea: survival and symbiotic performance. J Microbiol 51:49–55

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues AC, Silveira JAG, Bonifacio A, Figueiredo MVB (2013b) Metabolism of nitrogen and carbon: optimization of biological nitrogen fixation and cowpea development. Soil Biol Biochem 67:226–234

    Article  CAS  Google Scholar 

  • Rodriguez-Navarro DN, Dardanelli MS, Ruíz-Sainz JE (2007) Attachment of bacteria to the roots of higher plants. FEMS Microbiol Lett 272(2):127–136

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Salazar J, Suárez R, Caballero-Mellado J, Iturriaga G (2009) Trehalose accumulation in Azospirillum brasilense improves drought tolerance and biomass in maize plants. FEMS Microbiol Lett 296(1):52–59

    Article  PubMed  CAS  Google Scholar 

  • Romeiro RS (2000) PGPR e indução de resistência sistêmica em plantas a patógenos. Summa Phytopathologica 26:177–184

    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 

  • Russo A, Vettori L, Felici C, Fiaschi G, Morini S, Toffanin A (2008) Enhanced micropropagation response and biocontrol effect of Azospirillum brasilense Sp 245 on Prunus cerasifera L. clone Mr.S 2/5 plants. J Biotechnol 134(3–4):312–319

    Article  CAS  PubMed  Google Scholar 

  • Schelud’ko AV, Makrushin KV, Tugarova AV, Krestinenko VA, Panasenko VI, Antonyuk LP, Katsy EI (2009) Changes in motility of the rhizobacterium Azospirillum brasilense in the presence of plant lectins. Microbiol Res 164:149–156

    Article  PubMed  CAS  Google Scholar 

  • Shan X, Yan J, Xie D (2012) Comparison of phytohormone signaling mechanisms. Curr Opin Plant Biol 15(1):84–91

    Article  CAS  PubMed  Google Scholar 

  • Shelud’ko AV, Burygin GL, Filip’echeva YA, Belyakov AE, Shirokov AA, Burov AM, Katsy EI, Shchegolev SY, Matora LY (2014) Serological relationships of azospirilla revealed by their motility patterns in the presence of antibodies to lipopolysaccharides. Microbiology 83(1–2):102–109

    Article  CAS  Google Scholar 

  • Sigida EN, Fedonenko YP, Shashkov AS, Zdorovenko EL, Konnova SA, Ignatov VV, Knirel YA (2013) Structural studies of the O-specific polysaccharide(s) from the lipopolysaccharide of Azospirillum brasilense type strain Sp7. Carbohyd Res 380:76–80

    Article  CAS  Google Scholar 

  • Sigida EN, Fedonenko YP, Zdorovenko EL, Burygin GL, Konnova SA, Ignatov VV (2014) Characterization of the lipopolysaccharides of serogroup II Azospirillum strains. Microbiology 83(4):326–334

    Article  CAS  Google Scholar 

  • Sivasakthivelan P, Saranraj P (2013) Azospirillum and its formulations: a review. Int J Microbiol Res 4(3):275–287

    Google Scholar 

  • Smol’kina ON, Kachala VV, Fedonenko YP, Burygin GL, Zdorovenko EL, Matora LY, Konnova SA, Ignatov VV (2010) Capsular polysaccharide of the bacterium Azospirillum lipoferum Sp59b: structure and antigenic specificity. Biochemistry (Moscow) 75(5):606–613

    Article  CAS  Google Scholar 

  • Somers E, Ptacek D, Gysegom P, Srinivasan M, Vanderleyden J (2005) Azospirillum brasilense produces the auxin-like phenylacetic acid by using the key enzyme for indole-3-acetic acid biosynthesis. Appl Environ Microb 71(4):1803–1810

    Article  CAS  Google Scholar 

  • Spaepen S, Dobbelaere S, Croonenborghs A, Vanderleyden J (2008) Effects of Azospirillum brasilense indole-3-acetic acid production on inoculated wheat plants. Plant Soil 312:1–23

    Article  CAS  Google Scholar 

  • Spaepen S, Vanderleyden J, Okon Y (2009) Plant growth-promoting actions of rhizobacteria. Adv Bot Res 51:283–320

    Article  CAS  Google Scholar 

  • Tenuta M (2003) Plant growth promoting rhizobacteria: prospects for increasing nutrient acquisition and disease control. (en línea). http://www.umanitoba.ca/afs/agronomists_conf/2003/pdf/tenuta_rhizobacteria.pdf

  • Tien TM, Gaskins MH, Hubbell DH (1979) Plant growth substances produced by Azospirillum brasilense and their effect on the growth of pearl millet (Pennisetumamericanum L.). Appl Environ Microb 37:1016–1024

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Trivedi R, Bhatt SA (2011) Impact of biovolume inocula of Azospirillum spp. on winter wheat, oat and maize in semi-arid region of North Gujarat. Biotechnol 5(3):186–190

    CAS  Google Scholar 

  • Trujillo-Roldán MA, Valdez-Cruz NA, Gonzalez-Monterrubio CF, Acevedo-Sánchez EV, Martínez-Salinas C, García-Cabrera RI, Gamboa-Suasnavart RA, Marín-Palacio LD, Villegas J, Blancas-Cabrera A (2013) Scale-up from shake flasks to pilot-scale production of the plant growth-promoting bacterium Azospirillum brasilense for preparing a liquid inoculant formulation. App Microbiol Biotech 97(22):9665–9674

    Article  CAS  Google Scholar 

  • Turan M, Gulluce M, von Wirén N, Sahin F (2012) Yield promotion and phosphorus solubilization by plant growth-promoting rhizobacteria in extensive wheat production in Turkey. J Plant Nutr Soil Sc 175(6):818–826

    Article  CAS  Google Scholar 

  • Vacheron J, Desbrosses G, Bouffaud ML, Touraine B, Moënne-Loccoz Y, Muller D, Legendre L, Wisniewski-Dyé F, Prigent-Combaret C (2013) Plant growth-promoting rhizobacteria and root system functioning. Front Plant Sci 4:356

    Article  PubMed  PubMed Central  Google Scholar 

  • Verstraeten N, Braeken K, Debkumari B, Fauvart M, Fransaer J, Vermant J, Michiels J (2008) Living on a surface: swarming and biofilm formation. Trends Microbiol 16(10):496–506

    Article  CAS  PubMed  Google Scholar 

  • Vettori L, Felici C, Russo A, Morini S, Toffanin A, Cummings S (2010) Biocontrol activity of Azospirillum brasilense Sp 245 against Rhizoctonia solani by in vitro/in vivo tests, DGGE analysis. J Biotechnol 150:503–503

    Google Scholar 

  • Vieira Neto SA, Pires FR, Menezes CCE, Menezes JFS, Silva AG, Silva GP, Assis RL (2008) Forms of inoculant application and effects on soybean nodulation. Rev Bras Cienc Solo 32(2):861–870

    Article  Google Scholar 

  • Viera RM, Fernandez F (2006) Practical applications of bacterial biofertilizers and biostimulators. In: Uphoff N, Ball AS, Fernandes E (eds) Biological approaches to sustainable soil systems. CRC Press, Boca Raton

    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(2):494–506

    Article  CAS  PubMed  Google Scholar 

  • Walker V, Couillerot O, von Felten A, Bellvert F, Jansa J, Maurhofer M, Bally R, Moënne-Loccoz Y, Comte G (2012) Variation of secondary metabolite levels in maize seedling roots induced by inoculation with Azospirillum, Pseudomonas and Glomus consortium under field conditions. Plant Soil 356:151–163

    Article  CAS  Google Scholar 

  • Winik BC, Molina MFG, Pedraza RO (2009) Colonization of strawberry (Fragaria ananassa) plant tissues by Azospirillum brasilense. Acta Microsc 18:675–676

    Google Scholar 

  • Wisniewski-Dyé F, Drogue B, Borland S, Prigent-Combaret C (2013) Azospirillum-plant interaction: from root colonization to plant growth promotion. In: Rodelas González MB, González-López J (eds) Beneficial plant-microbial interactions: ecology and applications. CRC Press, London

    Google Scholar 

  • Yadegari M, Asadi Rahmani H, Noormohammadi G, Ayneband A (2010) Plant growth promoting rhizobacteria increase growth, yield and nitrogen fixation in Phaseolusvulgaris. J Plant Nutr 33(12):1733–1743

    Article  CAS  Google Scholar 

  • Yamaguchi S (2008) Gibberellin metabolism and its regulation. Ann Rev Plant Biol 59:225–251

    Article  CAS  Google Scholar 

  • Zilli JE, Gianluppi V, Campo RJ, Rouws JRC, Hungria M (2010) In-Furrow inoculation with Bradyrhizobium alternatively to seed inoculation of soybean. Rev Bras Ciênc Solo 34(6):1875–1881

    Article  Google Scholar 

  • Zilli JE, Silva Neto ML, França Júnior I, Perin L, Melo AR (2011) Cowpea response to inoculation with Bradyrhizobium strains recommended for soybean. Rev Bras Ciênc Solo 35:739–742

    Article  Google Scholar 

  • Zobiole LHS, Kremer RJ, Oliveira Junior RS, Constantin J (2011) Glyphosate affects chlorophyll, nodulation and nutrient accumulation of second generation glyphosate-resistant soybean (Glycinemax L.). Pestic Biochem Phys 99(1):53–60

    Google Scholar 

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Authors and Affiliations

  1. Department of Agricultural Engineering and Soil Science, Federal University of Piaui (UFPI), Center of Agrarian Science, Campus of Socopo, Teresina-PI, Brazil

    Artenisa Cerqueira Rodrigues

  2. Department of Biological Science, Federal University of Piaui, Center of Natural Science, Teresina-PI, Brazil

    Aurenivia Bonifacio

  3. Faculty of Agrarian Sciences, University of Oeste Paulista (UNOESTE), Presidente Prudente-SP, Brazil

    Fabio Fernando de Araujo

  4. Department of Agronomy, Agricultural University of Pernambuco (UFRPE), Recife-PE, Brazil

    Mario Andrade Lira Junior

  5. Agronomical Institute of Pernambuco IPA/SEAGRI, 1371, Gen. San Martin Avenue, Recife-PE, 50761-000, Brazil

    Marcia do Vale Barreto Figueiredo

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  1. Artenisa Cerqueira Rodrigues
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  2. Aurenivia Bonifacio
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  3. Fabio Fernando de Araujo
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  5. Marcia do Vale Barreto Figueiredo
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Correspondence to Marcia do Vale Barreto Figueiredo .

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  1. Dept Botany & Microbiology, Gurukul Kangri University, Haridwar (Uttarakhand), India

    Dinesh K. Maheshwari

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Rodrigues, A.C., Bonifacio, A., de Araujo, F.F., Junior, M.A.L., do Vale Barreto Figueiredo, M. (2015). Azospirillum sp. as a Challenge for Agriculture. In: Maheshwari, D. (eds) Bacterial Metabolites in Sustainable Agroecosystem. Sustainable Development and Biodiversity, vol 12. Springer, Cham. https://doi.org/10.1007/978-3-319-24654-3_2

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