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What Is Expected from the Genus Azospirillum as a Plant Growth-Promoting Bacteria?

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Bacteria in Agrobiology: Plant Growth Responses

Abstract

Bacteria capable of stimulating plant growth are generally known as plant growth-promoting bacteria (PGPB). Among them are Azospirillum species that influence plant growth through different mechanisms. Azospirillum is a Gram-negative bacterium that belongs to the alphaproteobacteria phylum. On the basis of the newly discovered species (at present 15), it is present not only in a wide diversity of plants, including those of agronomic importance such as cereals, sugarcane; and forage grasses, but also in other non-Poaceae plant species. Due to the capacity for improving plant yield in agronomically important crops, Azospirillum possesses biotechnological application as inoculant or biofertilizer. Among the mechanisms involved in promoting plant growth are N2 fixation, P solubilization, phytohormone production (auxins, cytokinins, and gibberellins), increased nutrient uptake, enhanced stress resistance, vitamin production, siderophores, and biocontrol activity. Some of them, as well as their agricultural application, are discussed in this chapter.

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References

  • Araújo LM, Monteiro RA, Souza EM, Steffens MBR, Rigo LU, Pedrosa FO, Chubatsu LS (2004) GlnB is specifically required for Azospirillum brasilense NifA acctivity in Escherichia coli. Res Microbiol 155:491–495

    Article  PubMed  Google Scholar 

  • Araújo LM, Huergo LF, Invitti AL, Gimenes CI, Bonatto AC, Monteiro RA, Souza EM, Pedrosa FO, Chubatsu LS (2008) Different responses of the GlnB and GlnZ proteins upon in vitro uridylylation by the Azospirillum brasilense GlnD protein. Braz J Med Biol Res 41:289–294

    Article  PubMed  Google Scholar 

  • Atkinson S, Chang CY, Sockett RE, Camara M, Williams P (2006) Quorum sensing in Yersinia enterocolitica controls swimming and swarming motility. J Bacteriol 188:1451–1461

    Article  PubMed  CAS  Google Scholar 

  • Bacilio-Jimenéz M, Aguilar-Flores S, Ventura-Zapata E, Pérez-Campo E, Bouquelet S, Zenteno E (2003) Chemical characterization of root exudates from rice (Oryza sativa) and their effects on the chemotactic response of endophytic bacteria. Plant Soil 249:271–277

    Article  Google Scholar 

  • Bashan Y, Bashan LE (2005) Plant growth-promoting. In: Hillel D (ed) Encyclopedia of soils in the environment, vol 1. Elsevier, Oxford, UK, pp 103–115, 2200 p

    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  PubMed  CAS  Google Scholar 

  • Ben Dekhil S, Cahill M, Stackebrandt E, Sly LI (1997) Transfer of Conglomeromonas largomobilis subsp. largomobilis to the genus Azospirillum as Azospirillum largomobile comb. nov., and elevation of Conglomeromonas largomobilis subsp. parooensis to the new type species of Conglomeromonas, Conglomeromonas parooensis sp. nov. System Appl Microbiol 20:72–77

    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  PubMed  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 191:501–507

    Article  PubMed  Google Scholar 

  • Chaiharn M, Chunhaleuchanon S, Lumyong S (2009) Screening siderophore producing bacteria as potential biological control agent for fungal rice pathogens in Thailand. W J Microbiol Biotechnol 25:1919–1928

    Article  Google Scholar 

  • Clough SJ, Lee KE, Schell MA, Denny TP (1997) A two component system in Ralstonia (Pseudomonas) solanacearum modulates production of PhcA-regulated virulence factors in response to 3-hydroxypalmitic acid methyl ester. J Bacteriol 179:3639–3648

    PubMed  CAS  Google Scholar 

  • Cohen AC, Bottini R, Piccoli P (2008) Azospirillum brasilense Sp 245 produces ABA in chemically-defined culture medium and increases ABA content in arabidopsis plants. Plant Growth Regul 54:97–103

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149

    Article  CAS  Google Scholar 

  • Eberl L, Winson MK, Sternberg C, Stewart GS, Christiansen G, Chhabra SR, Bycroft B, Williams P, Molin S, Givskov M (1996) Involvement of N-acyl-L-hormoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens. Mol Microbiol 20:127–136

    Article  PubMed  CAS  Google Scholar 

  • Eckert B, Weber OB, Kirchhof G, Halbritter A, Stoffels M, Hartmann A (2001) Azospirillum doebereinerae sp. Nov., a new nitrogen-fixing bacterium associated with the C4-grass Miscanthus. Int J Syst Evol Microbiol 51:17–26

    PubMed  CAS  Google Scholar 

  • Eckford R, Cook FD, Saul D, Aislabie J, Foght J (2002) Free-living heterotrophic nitrogen-fixing bacteria isolated from fuel-contaminated Antarctic soils. Appl Environ Microbiol 68:5181–5185

    Article  PubMed  CAS  Google Scholar 

  • Fages J (1994) Azospirillum inoculants and field experiments. In: Okon Y (ed) Azospirillum-plant associations. CRC Press, Boca Raton, FL, pp 87–109

    Google Scholar 

  • Fages J, Mulard D (1988) Isolement de bactéries rhizosphériques et effect de leur inoculation and pots chez Zea mays. Agronomie 8:309–315

    Article  Google Scholar 

  • Hartman A, Baldani JI (2006) The genus Azospirillum. In: Dworkin M, Flaknow S, Rosemberg E, Schleifer K-H, Stackerbrandt E (eds) The prokaryotes, vol 5, 3rd edn. Springer, New York, pp 115–140

    Chapter  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  PubMed  CAS  Google Scholar 

  • Huergo LF, Merrick M, Monteiro RA, Chubatsu LS, Steffens MBR, Pedrosa FO, Souza EM (2008) In vitro interactions between the PII proteins and the nitrogenase regulatory enzymes dinitrogenase reductase ADP-ribosyltransferase (DraT) and dinitrogenase reductase-activating glycohydrolase (DraG) in Azospirillum brasilense. J Biol Chem 284:6674–6682

    Article  Google Scholar 

  • Kaneko T, Minamisawa K, Isawa T, Nakatsukasa H, Mitsui H, Kawaharada Y, Nakamura Y, Watanabe A, Kawashima K, Ono A, Shimizu Y, Takahashi C, Minami C, Fujishiro T, Kohara M, Katoh M, Nakazaki N, Nakayama S, Yamada M, Tabata S, Sato S (2010) Complete genomic structure of the cultivated rice endophyte Azospirillum sp. B510. DNA Res. Advance Access doi: 10.1093/dnares/dsp026

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

    PubMed  CAS  Google Scholar 

  • Kloepper JW, Schroth MN (1981) Plant growth-promoting rhizobacteria and plant growth under gnotobiotic conditions. Phytopathology 71:642–644

    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 novel diazotrophic bacterium isolated from a sulfide spring. Int J Syst Evol Microbiol. doi:10.1099/ijs.0.018853-0

    PubMed  Google Scholar 

  • Lin S-Y, Young CC, Hupfer H, Siering C, Arun AB, Chen W-M, Lai WA, Shen FT, Rekha PD, Yassin AF (2009) Azospirillum picis sp. nov., isolated from discarded tar. Int J Syst Evol Microbiol 59:761–765

    Article  PubMed  CAS  Google Scholar 

  • Lindum PW, Anthoni U, Christophersen C, Eberl L, Molin S, Givskov M (1998) N-Acyl-L-homoserine lactone autoinducers control production of an extracellular lipopeptide biosurfactant required for swarming motility of Serratia liquefaciens MG1. J Bacteriol 180:6384–6388

    PubMed  CAS  Google Scholar 

  • List No. 39 (1991) Validation of the publication of new names and new combinations previously effectively published outside the IJSB. Int J Syst Bacteriol 41(4):580–581

    Google Scholar 

  • Lucangeli C, Bottini R (1996) Reversion of dwarfism in dwarf-1 maize (Zea mays L.) and dwarf-x rice (Oryza sativa L.) mutants by endophytic Azospirillum spp. Biocell 20:223–228

    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 23:63–71

    CAS  Google Scholar 

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

    Google Scholar 

  • Mehnaz S, Weselowski B, Lazarovits G (2007a) Azospirillum canadense sp. nov., a nitrogen-fixing bacterium isolated from corn rhizosphere. Int J Syst Evol Microbiol 57:620–624

    Article  PubMed  CAS  Google Scholar 

  • Mehnaz S, Weselowski B, Lazarovits G (2007b) Azospirillum zeae sp. nov., diazotrophic bacterium isolated from rhizosphere soil of Zea mays. Int J Syst Evol Microbiol 57:2805–2809

    Article  PubMed  CAS  Google Scholar 

  • Moens S, Michiels K, Keijers V, Vanleuven F, Vanderleyden J (1995) Cloning, sequencing, and phenotypic analysis of laf1, encoding the flagellin of the lateral flagella of Azospirillum brasilense Sp7. J Bacteriol 177:5419–5426

    PubMed  CAS  Google Scholar 

  • Nosko P, Bliss LC, Cook FD (1994) The association of free-living nitrogen-fixing bacteria with the roots of high Arctic graminoids. Arctic Alpine Res 26:180–186

    Article  Google Scholar 

  • Okon Y, Labanderas-González C (1994) Agronomic applications of Azospirillum: an evaluation of 20 years of worldwide field inoculation. Soil Biol Biochem 26: 1591–1601

    Google Scholar 

  • Oliveira ALM, Urquiaga S, Döbereiner J, Baldani JI (2002) The effect of inoculating endophytic N2-fixing bacteria on micropropagated sugarcane plants. Plant Soil 242:205–215

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Ona O, Van Impe J, Prinsen E, Vanderleyden J (2005) Growth and indole-3-acetic acid biosynthesis of Azospirillum brasilense Sp245 is environmentally controlled. FEMS Microbiol Lett 246:125–132

    Article  CAS  Google Scholar 

  • Pedraza RO, Motok J, Tortora ML, Salazar SM, Díaz Ricci JC (2007) Natural occurrence of Azospirillum brasilense in strawberry plants. Plant Soil 295:169–178

    Article  CAS  Google Scholar 

  • Pedraza RO, Bellone CH, Bellone SC, 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 45:36–43

    Article  CAS  Google Scholar 

  • Pedraza RO, Motok J, Salazar SM, Ragout AL, Mentel MI, Tortora ML, Guerrero-Molina MF, Winik BC, Díaz-Ricci JC (2010) Growth-promotion of strawberry plants inoculated with Azospirillum brasilense. W J Microbiol Biotechnol 26:265–272

    Article  Google Scholar 

  • Peng G, Wang H, Zhang G, Hou W, Liu Y, Wang ET, Tan Z (2006) Azospirillum melinis sp. nov., a group of diazotrophs isolated from tropical molasses grass. Int J Syst Evol Microbiol 56:1263–1271

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  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 

  • Reinhold R, Hurek T, Baldani I, Döbereiner J (1988) Temperature and salt tolerance of Azospirillum spp. from salt affected soil in Brazil. In Azospirillum IV: Genetics, Physiology, Ecology, ed. by Klingmüller, W., Springer Verlag, Berlin, pp. 234–241

    Google Scholar 

  • Reis jr FB, Silva MF, Teixeira KRS, Urquiaga S, Reis VM (2006) Identificação de isolados de Azospirillum amazonense associados a Brachiaria spp., em diferentes épocas e condições de cultivo e produção de fitormônio pela bactéria. Rev Bras Ciõn Solo 28:103–113

    Google Scholar 

  • Rodriguez H, Gonzalez T, Goire I, Bashan Y (2004) Gluconic acid production and phosphate solubilization by the plant growth-promoting bacterium Azospirillum spp. Naturwissenschaften 91:552–555

    Article  PubMed  CAS  Google Scholar 

  • Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signalling. Nature 459:1071–1078

    Article  PubMed  CAS  Google Scholar 

  • Santner A, Calderon-Villalobos LIA, Estelle M (2009) Plant hormone are versatile chemical regulators of plant growth. Nat Chem Biol 5:301–307

    Google Scholar 

  • Seshadri S, Muthukumarasamy R, Lakshminarasimhan C, Ignacimuthu S (2000) Solubilization of inorganic phosphates by Azospirillum halopraeferans. Curr Sci 79:565–567

    CAS  Google Scholar 

  • Sly LI, Stackebrandt E (1999) Description of Skermanella parooensis gen. nov., sp. nov. to accommodate Conglomeromonas largomobilis subsp. parooensis following the transfer of Conglomeromonas largomobilis subsp. largomobilis to the genus Azospirillum. Int J Syst Bacteriol 49:541–544

    Article  Google Scholar 

  • Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signalling. FEMS Microbiol Rev 31:425–448

    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 

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

    Article  PubMed  CAS  Google Scholar 

  • Sumner ME (1990) Crop responses to Azospirillum inoculation. Adv Soil Sci 12:54–123

    Google Scholar 

  • Tarrand JJ, Krieg NR, Döbereiner J (1978) A taxonomic study of the Spirillum lipoferum group, with descriptipn of a new genus, Azospirillum gen. nov., and two species, Azospirillum lipoferum (Beijerinck) com nov. and Azospirillum brasilense sp. nov. Can J Microbiol 24:967–980

    Article  PubMed  CAS  Google Scholar 

  • Teplitski M, Robinson JB, Bauer WD (2000) Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol Plant-Microbe Interact 13:637–648

    Article  PubMed  CAS  Google Scholar 

  • Uroz S, D’Angelo-Picard C, Carlier A, Elasri M, Sicot C, Petit A, Oger P, Faure D, Dessaux Y (2003) Novel bacteria degrading N-acylhomoserine lactones and their use as quenchers of quorum sensing-regulated functions of plant-pathogenic bacteria. Microbiology 149:1981–1989

    Article  PubMed  CAS  Google Scholar 

  • Urquiaga S, Cruz KHS, Boddey RM (1992) Contribution of nitrogen fixation to sugarcane: Nitrogen-15 and nitrogen balance estimates. Soil Sci Soc Am J 56:105–114

    Article  Google Scholar 

  • Vande Broek A, Gysegom P, Ona O, Hendrickx N, Prinsen E, Van Impe J, Vanderleyden J (2005) Transcriptional analysis of the Azospirillum brasilense indole-3-pyruvate decarboxylase gene and identification of a cis-acting sequence involved in auxin responsive expression. Mol Plant Microbe Inter 18:311–323

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Wang LH, He Y, Gao Y et al (2004) A bacterial cell–cell communication signal with cross-kingdom structural analogues. Mol Microbiol 51:903–912

    Article  PubMed  CAS  Google Scholar 

  • Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:225–251

    Article  Google Scholar 

  • Xie C, 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 Microb 55:1435–1438

    Article  CAS  Google Scholar 

  • Yoneyama T, Muraoka T, Kim TH, Dacanay EV, Nakanishi Y (1997) The natural 15N abundance of sugarcane and neighbouring plants in Brazil, the Philippines and Miyako (Japan). Plant Soil 189:239–244

    Article  CAS  Google Scholar 

  • Young CC, Hupfer H, Siering C, Ho M-J, Arun AB, Lai W-A, Rekha PD, Shen F-T, Hunn M-H, Chen W-M, Yassin AF (2008) Azospirillum rugosum sp. nov., isolated from oil-contaminated soil. Int J Syst Evol Microb 58:959–963

    Article  CAS  Google Scholar 

  • Zambrano ER, Jiménez Salgado T, Tapia Hernández A (2007) Estudio de bacterias asociadas a orquídeas (Orchidaceae). Lankesteriana 7(1–2):322–325

    Google Scholar 

  • Zhou Y, Wei W, Wang X, Xu L, Lai R (2009) Azospirillum palatum sp. nov., isolated from Forest soil in Zhejiang province, China. J Gen Appl Microbiol 55:1–7

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors acknowledge the support of CYTED (409AC0379) and CNPq (49.0013/2009-0) through the DIMIAGRI project. The first and second authors acknowledge the INCT – Instituto Nacional de C & T de Fixação Biológica de Nitrogênio. The third author acknowledges to CIUNT and ANPCyT (PICT 2007 N°472) grants and to Guerrero-Molina MF for providing Fig. 6.1.

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Reis, V.M., Teixeira, K.R.d.S., Pedraza, R.O. (2011). What Is Expected from the Genus Azospirillum as a Plant Growth-Promoting Bacteria?. In: Maheshwari, D. (eds) Bacteria in Agrobiology: Plant Growth Responses. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-20332-9_6

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