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AIMS Microbiology

2017, Volume 3, Issue 3: 413-434. doi: 10.3934/microbiol.2017.3.413
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The role of Plant Growth Promoting Bacteria in improving nitrogen use efficiency for sustainable crop production: a focus on wheat

  • 1.
    Laboratory of Nutritional and Healthy Quality of Herbaceous Crop, Department of the Science of Agriculture, Food and Environment (SAFE) University of Foggia, Foggia, Italy
  • 2.
    Laboratory of Predictive Microbiology, Department of the Science of Agriculture, Food and Environment (SAFE), University of Foggia, Foggia, Italy
  • Received: 24 March 2017 Accepted: 25 May 2017 Published: 07 June 2017

  • Due to the increase in both human population growth and environmental pressure, it is necessary to raise agricultural productivity without enhancing environmental footprint. Within this context, soil inoculation with PGPB (Plant Growth Promoting Bacteria) may be considered a promising tool of integrated management systems. In particular, PGPB may improve plant growth either directly, by facilitating resource use or modulating plant hormone levels, or indirectly by decreasing the inhibitory effects of various pathogenic agents. PGPB comprise different functional and taxonomic groups of bacteria like Pseudomonas, Bacillus, Rhizobium and others. Their ability to either mobilize mineral or organic bound nutrients from the pedosphere or to fix atmospheric N2 and make it available to the plants, is a crucial feature in their application. In literature some data are available on the use of commercial PGPB, while less efforts have been made on the study of the effect of autochthonous PGPB isolated from soils on sustainability of cropping systems; thus a literature survey on these aspects was carried out with special focus on wheat, a staple food for a large part of world population. In particular, the main topic of this review is the potential of PGPB to enhance use efficiency of agro-environmental resources focusing on the interaction PGPB-wheat for improving nitrogen use efficiency.

    Citation: Nilde Antonella Di Benedetto, Maria Rosaria Corbo, Daniela Campaniello, Mariagrazia Pia Cataldi, Antonio Bevilacqua, Milena Sinigaglia, Zina Flagella. The role of Plant Growth Promoting Bacteria in improving nitrogen use efficiency for sustainable crop production: a focus on wheat[J]. AIMS Microbiology, 2017, 3(3): 413-434. doi: 10.3934/microbiol.2017.3.413

    Related Papers:

  • Due to the increase in both human population growth and environmental pressure, it is necessary to raise agricultural productivity without enhancing environmental footprint. Within this context, soil inoculation with PGPB (Plant Growth Promoting Bacteria) may be considered a promising tool of integrated management systems. In particular, PGPB may improve plant growth either directly, by facilitating resource use or modulating plant hormone levels, or indirectly by decreasing the inhibitory effects of various pathogenic agents. PGPB comprise different functional and taxonomic groups of bacteria like Pseudomonas, Bacillus, Rhizobium and others. Their ability to either mobilize mineral or organic bound nutrients from the pedosphere or to fix atmospheric N2 and make it available to the plants, is a crucial feature in their application. In literature some data are available on the use of commercial PGPB, while less efforts have been made on the study of the effect of autochthonous PGPB isolated from soils on sustainability of cropping systems; thus a literature survey on these aspects was carried out with special focus on wheat, a staple food for a large part of world population. In particular, the main topic of this review is the potential of PGPB to enhance use efficiency of agro-environmental resources focusing on the interaction PGPB-wheat for improving nitrogen use efficiency.


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    [1] Godfray HCJ, Beddington JR, Crute IR, et al. (2010) Food security: the challenge of feeding 9 billion people. Science 327: 812–818.
    [2] de Souza R, Ambrosini A, Passaglia LMP (2015) Plant growth-promoting bacteria as inoculants in agricultural soils. Genet Mol Biol 38: 401–419. doi: 10.1590/S1415-475738420150053
    [3] Adesemoye AO, Torbert HA, Kloepper JW (2009) Plant Growth-Promoting Rhizobacteria allow reduced application rates of chemical fertilizers. Microb Ecol 58: 921–929. doi: 10.1007/s00248-009-9531-y
    [4] FAO (2009) How to Feed the World in 2050. Rome, Italy, Food and Agriculture Organization.
    [5] FAO (2014) 19 December Rome. Available from: http://www.fao.org/ news/story/ en/item/273303/icode.
    [6] Troccoli A, Borrelli GM, De Vita P, et al. (2000) Durum wheat quality: a multidisciplinary concept. J Cereal Sci 32: 99–113.
    [7] Hatfield JL, Sauer TJ, Prueger JH (2001) Managing soils to achieve greater water use efficiency: a review. Agron J 93: 271–280. doi: 10.2134/agronj2001.932271x
    [8] Cormier F, Foulkes J, Randhirel B, et al. (2016) Breeding for increased nitrogen-use efficiency: a review for wheat (T. Aestivum L.). Plant Breeding 135: 255–278. doi: 10.1111/pbr.12371
    [9] Hirel B, Tétu T, Lea PJ, et al. (2011) Improving nitrogen use efficiency in crops for sustainable agriculture. Sustainability 3: 1452–1485. doi: 10.3390/su3091452
    [10] Singh B, Ryan J (2015) Managing fertilizers to enhance soil health, In: International Fertilizer Industry Association, Paris, France, 1–24.
    [11] Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting Rhizobacteria: current perspective. J King Saud Univ Sci 26: 1–20.
    [12] Powell N, Ji X, Ravash R, et al. (2012) Yield stability for cereals in a changing climate. Funct Plant Biol 39: 539–552.
    [13] Semenov MA, Shewry PR (2011) Modelling predicts that heat stress, not drought, will increase vulnerability of wheat in Europe. Sci Rep 1: 66.
    [14] FAOSTAT Database Collections (Rome: Food and Agriculture Organization of the United Nations). Available from: http://faostat.fao.org/.
    [15] Canfield DE, Glazer AN, Falkowski PG (2010) The evolution and future of earth's nitrogen cycle. Science 330: 192–196. doi: 10.1126/science.1186120
    [16] Snyder CS, Bruulsema TW, Jensen TL, et al. (2009) Review of greenhouse gas emissions from crop production systems and fertilizer management effects. Agric Ecosyst Environ 133: 247–266.
    [17] Chen JH (2006) The combined use of chemical and organic fertilizers and/or biofertilizer for crop growth and soil fertility. International Workshop on Sustained Management of the Soil-Rhizosphere System for Efficient Crop Production and Fertilizer Use 16: 20.
    [18] Gill HK, Garg H (2014) Pesticides: Environmental impacts and management strategies, In: Marcelo L, Editor, Pesticides-Toxic aspects, CC BY, 187–230.
    [19] Aktar W, Sengupta D, Chowdhury A (2009) Impact of pesticides use in agriculture: their benefits and hazards. Interdisc Toxicol 2: 1–12. doi: 10.2478/v10102-009-0001-7
    [20] Saharan BS, Nehra V (2011) Plant Growth Promoting Rhizobacteria: a critical review. Life Sci Med Res 21: 1–30.
    [21] Walker TS, Bais HP, Grotewold E, et al. (2003) Root exudation and rhizosphere biology. Plant Physiol 132: 44–51. doi: 10.1104/pp.102.019661
    [22] Ortiz-Castro R, Contreras-Cornejo HA, Macías-Rodríguez L, et al. (2009) The role of microbial signals in plant growth and development. Plant Signal Behav 4: 701–712. doi: 10.4161/psb.4.8.9047
    [23] Dimkpa C, Wein T, Folkard A (2009) Plant-Rhizobacteria interactions alleviate abiotic stress conditions..Plant Cell Environ 32: 1682–1694. doi: 10.1111/j.1365-3040.2009.02028.x
    [24] Glick BR (2012) Plant Growth-Promoting Bacteria: mechanisms and applications. Scientifica 1–15.
    [25] Leigh GJ (2002) Nitrogen fixation at the millennium, London: Elsevier Science.
    [26] Lucas-Garcia JA, Probanza A, Ramos B, et al. (2004) Effects of Plant Growth Promoting Rhizobateria (PGPRs) on the biological nitrose fixation, nodulation and growth of Lupinus albus I. cv. Multolupa. Eng Life Sci 4: 71–77. doi: 10.1002/elsc.200400013
    [27] Bhattacharyya PN, Jha DK (2012) Plant Growth-Promoting Rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28: 1327–1350. doi: 10.1007/s11274-011-0979-9
    [28] Tabatabaei S, Ehsanzadeh P, Etesami H, et al. (2016) Indole-3-acetic acid (IAA) producing Pseudomonas isolates inhibit seed germination and α amylase activity in durum wheat (Triticum turgidum L.). Spain J Agric Res 14: e0802. doi: 10.5424/sjar/2016141-8859
    [29] Beneduzi A, Ambrosini A, Passaglia LMP (2012) Plant Growth-Promoting Rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet Mol Biol 35: 1044–1051. doi: 10.1590/S1415-47572012000600020
    [30] Kundan R, Pant G, Jadon N, et al. (2015) Plant Growth Promoting Rhizobacteria: mechanism and current prospective. J Fertil Pestic 6: 2.
    [31] Oteino N, Lalli RD, Kiwanuka S, et al. (2015) Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates. Front Microbiol 6: 745.
    [32] Haas D, Keel C (2003) Regulation of antibiotic production in root colonizing Pseudomonas spp. and relevance for biological control of plant disease. Annu Rev Phytopathol 41: 117–153.
    [33] Peñalver R, López MM (1999) Cocolonization of the rhizosphere by pathogenic Agrobacterium strains and non pathogenic strains K84 and K1026, used for crown gall biocontrol. Appl Environ Microb 65: 1936–1940.
    [34] Okon Y, Labandera-Gonzales CA (1994) Agronomic applications of Azospirillum: an evaluation of 20 years worldwide field inoculation. Soil Biol Biochem 26: 1591–1601. doi: 10.1016/0038-0717(94)90311-5
    [35] 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: 44–51. doi: 10.1016/j.ejsobi.2008.11.001
    [36] Piccinin GG, Dan LGM, Braccini ALE, et al. (2011) Agronomic efficiency of Azospirillum brasilense in physiological parameters and yield components in wheat crop. J Agron 10: 132–135. doi: 10.3923/ja.2011.132.135
    [37] Namvar A, Khandan T (2013) Response of wheat to mineral nitrogen fertilizer and biofertilizer (Azotobacter sp. and Azospirillum sp.) inoculation under different levels of weed interference. Ekologija 59: 85–94.
    [38] Amiri A, Rafiee M (2013) Effect of soil inoculation with Azospirillum and Azotobacter bacteria on nitrogen use efficiency and agronomic characteristics of corn. Ann Biol Res 4: 77–79.
    [39] Amanullah A, Kurd A, Khan S, et al. (2012) Biofertilizer-a possible substitute of fertilizers in production of wheat variety zardana in balochistan. Pakistan J Agric Res 25: 44–49.
    [40] Saia S, Rappa V, Ruisi P, et al. (2015) Soil inoculation with symbiotic microorganisms promotes plant growth and nutrient transporter genes expression in durum wheat. Front Plant Sci 6: 815.
    [41] Vessey JK (2003) Plant Growth Promoting Rhizobacteria as biofertilizers. Plant Soil 255: 571–586. doi: 10.1023/A:1026037216893
    [42] Dobbelaere S, Croonenborghs A, Thys A, et al. (1999) Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil 212: 155–164.
    [43] Pereyra MA, Ballesteros FM, Creus CM, et al. (2009) Seedlings growth promotion by Azospirillum brasilense under normal and drought conditions remains unaltered in Tebuconazole-treated wheat seeds. Eur J Soil Biol 45: 20–27. doi: 10.1016/j.ejsobi.2008.09.015
    [44] Meena KK, Kumar M, Kalyuzhnaya MG, et al. (2012) Epiphytic pink-pigmented methylotrophic bacteria enhance germination and seedling growth of wheat (Triticum aestivum) by producing phyto-hormone. Antonie van Leeuwenhoek 101: 777–786. doi: 10.1007/s10482-011-9692-9
    [45] García de Salamone IE, Funes JM, Di Salvo LP, et al. (2012) Inoculation of paddy rice with Azospirillum brasilense and Pseudomonas fluorescens: impact of plant genotypes on rhizosphere microbial communities and field crop production. Appl Soil Ecol 61: 196–204. doi: 10.1016/j.apsoil.2011.12.012
    [46] Ferreira AS, Pires RR, Rabelo PG, et al. (2013) Applied soil ecology 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. doi: 10.1016/j.apsoil.2013.05.020
    [47] Majeed A, Abbasi MK, Hameed S, et al. (2015) Isolation and characterization of Plant Growth-Promoting Rhizobacteria from wheat rhizosphere and their effect on plant growth promotion. Front Microbiol 6: 198.
    [48] Hassan TU, Bano A (2016) Biofertilizer: a novel formulation for improving wheat growth, physiology and yield. Pak J Bot 48: 2233–2241.
    [49] Charousová I, Medo J, Halenárová E, et al. (2016) Effect of fertilization on biological activity of community of soil Streptomycetes. J Cent Eur Agr 17: 1134–1149. doi: 10.5513/JCEA01/17.4.1822
    [50] Hao T, Chen S (2017) Colonization of wheat, maize and cucumber by Paenibacillus Polymyxa Wly78. PloS One 12: e0169980. doi: 10.1371/journal.pone.0169980
    [51] Veresoglou SD, Menexes G (2010) Impact of inoculation with Azospirillum spp. on growth properties and seed yield of wheat: a meta-analysis of studies in the ISI Web of Science from 1981 to 2008. Plant Soil 337: 469–480.
    [52] Pérez-Montano F, Alías-Villegas C, Bellogín RA, et al. (2014) Plant growth promotion in cereal and leguminous agricultural important plants: From microorganism capacities to crop production. Microbiol Res 169: 325–336. doi: 10.1016/j.micres.2013.09.011
    [53] Piccinin GG, Braccini ALE, Dan LGM, et al. (2013) Efficiency of seed inoculation with Azospirillum brasilense on agronomic characteristics and yield of wheat. Ind Crops Prod 43: 393–397. doi: 10.1016/j.indcrop.2012.07.052
    [54] Hungria M, Campo RJ, Souza EM, et al. (2010) Inoculation with selected strains of Azospirillum brasilense and A. lipoferum improves yields of maize and wheat in Brazil. Plant Soil 331: 413–425.
    [55] 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. doi: 10.1016/j.ejsobi.2008.07.001
    [56] Spaepen S, Dobbelaere S, Croonenborghs A, et al. (2008) Effects of Azospirillum brasilense indole-3-acetic acid production on inoculated wheat plants. Plant Soil 312: 15–23. doi: 10.1007/s11104-008-9560-1
    [57] Available from: https://www.ag.ndsu.edu/plantsciences/research/durum.
    [58] Colla G, Rouphael Y, Bonini P, et al. (2015) Coating seeds with endophytic fungi enhances growth, nutrient uptake, yield and grain quality of winter wheat. Int J Plant Prod 9: 171–190.
    [59] Di Benedetto NA, Campaniello D, Bevilacqua A, et al. (2016) Characterization of autochthonous plant growth promoting bacteria in relation to durum wheat nitrogen use efficiency, In: Proceedings of Plant Biology Europe Congress EPSO/FESPB, Prague Czech Republic, 26–30.
    [60] Baffoni L, Gaggia F, Dalanaj N, et al. (2015) Microbial inoculants for the biocontrol of Fusarium spp. in durum wheat. BMC Microbiol 15: 242. doi: 10.1186/s12866-015-0573-7
    [61] Mnasri N, Chennaoui C, Gargouri S, et al. (2017) Efficacy of some rhizospheric and endophytic bacteria in vitro and as seed coating for the control of Fusarium culmorum infecting durum wheat in Tunisia. Eur J Plant Pathol 147: 501–515. doi: 10.1007/s10658-016-1018-3
    [62] Indiragandhi P, Anandham R, Madhaiyan M, et al. (2008) Characterization of plant growth-promoting traits of bacteria isolated from larval guts of diamondback moth Plutella xylostella (Lepidoptera: Plutellidae). Curr Microbiol 56: 327–333. doi: 10.1007/s00284-007-9086-4
    [63] Xu G, Fan X, Miller T (2012) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 63: 153–182.
    [64] Han J, Shi J, Zeng L, et al. (2017) Impacts of continuous excessive fertilization on soil potential nitrification activity and nitrifying microbial community dynamics in greenhouse system. J Soils Sediments 17: 471–480. doi: 10.1007/s11368-016-1525-z
    [65] Shaw LJ, Nicol GW, Smith Z, et al. (2006) Nitrosospira spp. can produce nitrous oxide via a nitrifier denitrification pathway. Environ Microbiol 8: 214–222.
    [66] Xia W, Zhang C, Zeng X, et al. (2011) Autotrophic growth of nitrifying community in an agricultural soil. ISME J 5: 1226–1236. doi: 10.1038/ismej.2011.5
    [67] Wang YF, Gu JD (2014) Effects of allylthiourea, salinity, and pH on ammonia/ammonium-oxidizing prokaryotes in mangrove sediment incubated in laboratory microcosms. Appl Microbiol Biotechnol 98: 3257–3274. doi: 10.1007/s00253-013-5399-3
    [68] Shen JP, Zhang LM, Zhu YG, et al. (2008) Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environ Microbiol 10: 1601–1611. doi: 10.1111/j.1462-2920.2008.01578.x
    [69] Xiao R, Chen B, Liu Y, et al. (2014) Higher abundance of ammonia oxidizing archaea than ammonia oxidizing bacteria and their communities in Tibetan alpine meadow soils under long-term nitrogen fertilization. Geomicrobiol J 31: 597–604. doi: 10.1080/01490451.2013.875298
    [70] Nicol GW, Leininger S, Schleper C, et al. (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol 10: 2966–2978.
    [71] Ai C, Liang GQ, Sun JW, et al. (2013) Different roles of rhizosphere effect and long-term fertilization in the activity and community structure of ammonia oxidizers in a calcareous fluvoaquic soil. Soil Biol Biochem 57: 30–42. doi: 10.1016/j.soilbio.2012.08.003
    [72] Erguder TH, Boon N, Wittebolle L, et al. (2009) Environmental factors shaping the ecological niches of ammonia oxidizing archaea. FEMS Microbiol Rev 33: 855–869. doi: 10.1111/j.1574-6976.2009.00179.x
    [73] O'Sullivan CA, Wakelin SA, Fillery IR, et al. (2013) Factors affecting ammonia-oxidising microorganisms and potential nitrification rates in southern Australian agricultural soils. Soil Res 51: 240–252. doi: 10.1071/SR13039
    [74] Mokhele B, Zhan X, Yang G, et al. (2012) Review: Nitrogen assimilation in crop plants and its affecting factors. Can J Plant Sci 92: 399–405. doi: 10.4141/cjps2011-135
    [75] Kant S, Bi YM, Rothstein SJ (2011) Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency. J Exp Bot 62: 1499–1509. doi: 10.1093/jxb/erq297
    [76] Wickert S, Marcondes J, Lemos MV, et al. (2007) Nitrogen assimilation in citrus based on CitEST data mining. Genet Mol Biol 30: 810–818. doi: 10.1590/S1415-47572007000500009
    [77] Kaiser WM, Planchet E, Rümer S (2011) Nitrate reductase and nitric oxide, In: Foyer CH, Zhang H, Editors, Annual Plant Reviews, Nitrogen Metabolism in Plants in the Post-genomic Era, Chichester: Wiley-Blackwell, 127–146.
    [78] Boisson M, Mondon K, Torney V, et al. (2005) Partial sequences of nitrogen metabolism genes in hexaploid wheat. Theor Appl Genet 110: 932–940. doi: 10.1007/s00122-004-1913-4
    [79] Sakakibara Y, Kimura H, Iwamura A, et al. (2012) A new structural insight into differential interaction of cyanobacterial and plant ferredoxins with nitrite reductase as revealed by NMR and X-ray crystallographic studies. J Biochem 151: 483–492. doi: 10.1093/jb/mvs028
    [80] Lea PJ, Miflin BJ (2011) Nitrogen assimilation and its relevance to crop improvement, In: Zhang H, Editor, Annual Plant Reviews, Nitrogen Metabolism in Plants in the Post-genomic Era, Chichester: Wiley-Blackwell, 1–40.
    [81] Hawkins HJ, George H (2001) Reduces 15N-nitrogen transport through arbuscular hyphae to Triticum aestivum L supplied with ammonium vs. nitrate nutrition. Ann Bot 87: 303–311. doi: 10.1006/anbo.2000.1305
    [82] Mantelin S, Touraine B (2004) Plant growth promoting bacteria and nitrate availability: impacts on root development and nitrate uptake. J Exp Bot 394: 27–34.
    [83] Cacco G, Attina E, Gelsomino A, et al. (2000) Effect of nitrate and humic substances of different molecular size on kinetic parameters of nitrate uptake in wheat seedlings. J Plant Nutr Soil Sci 163: 313–320. doi: 10.1002/1522-2624(200006)163:3<313::AID-JPLN313>3.0.CO;2-U
    [84] Abenavoli MR, De Santis CD, Sidari M, et al. (2001) Influence of coumarin on the net nitrate uptake in durum wheat. New Phytol 150: 619–627. doi: 10.1046/j.1469-8137.2001.00119.x
    [85] Bloom AJ, Burger M, Kimball BA, et al. (2014) Nitrate assimilation is inhibited by elevated CO2 in field grown wheat. Nat Clim Chang 4: 477–480.
    [86] Good AG, Shrawat AK, Muench, DG (2004) Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends Plant Sci 9: 597–605.
    [87] Fageria NK, Baligar VC, Li YC (2008) The role of nutrient efficient plants in improving crop yields in the twenty first century. J Plant Nutr 31: 1121–1157. doi: 10.1080/01904160802116068
    [88] Giuliani MM, Giuzio L, De Caro A, et al. (2011a) Relationships between nitrogen utilization and grain technological quality in durum wheat. I. Nitrogen translocation and nitrogen use efficiency for protein. Agron J 103: 1487–1494.
    [89] Giuliani MM, Giuzio L, De Caro A, et al. (2011b) Relationships between nitrogen utilization and grain technological quality in durum wheat. II. Grain yield and quality. Agron J 103: 1668–1675.
    [90] Wu H, Haig T, Pratley J, et al. (2001) Allelochemicals in wheat (Triticum aestivum L.): cultivar difference in the exudation of phenolic acids. J Agric Food Chem 49: 3742–3745.
    [91] Germida J, Siciliano S (2001) Taxonomic diversity of bacteria associated with the roots of modern, recent and ancient wheat cultivars. Biol Fertil Soils 33: 410–415. doi: 10.1007/s003740100343
    [92] Cheng W, Johnson DW, Fu S (2003) Rhizosphere effects on decomposition. Soil Sci Soc Am J 67: 1418–1427. doi: 10.2136/sssaj2003.1418
    [93] Hsu SF, Buckley DH (2009) Evidence for the functional significance of diazotroph community structure in soil. ISME J 3: 124–136. doi: 10.1038/ismej.2008.82
    [94] Nelson DR, Mele PM (2006) The impact of crop residue amendments and lime on microbial community structure and nitrogenfixing bacteria in the wheat rhizosphere. Soil Res 44: 319–329. doi: 10.1071/SR06022
    [95] Venieraki A, Dimou M, Pergalis P, et al. (2011) The genetic diversity of culturable nitrogen-fixing bacteria in the rhizosphere of wheat. Microb Ecol 61: 277–285. doi: 10.1007/s00248-010-9747-x
    [96] Behl RK, Ruppel S, Kothe E, et al. (2012) Wheat × Azotobacter × VA Mycorrhiza interactions towards plant nutrition and growth-a review. J Appl Bot Food Qual 81: 95–109.
    [97] Neiverth A, Delai S, Garcia DM, et al. (2014) Performance of different wheat genotypes inoculated with the plant growth promoting bacterium Herbaspirillum seropedicae. Eur J Soil Biol 64: 1–5. doi: 10.1016/j.ejsobi.2014.07.001
    [98] Perin L, Martínez-Aguilar L, Castro-González R, et al. (2006) Diazotrophic Burkholderia species associated with field-grown maize and sugarcane. Appl Environ Microbiol 72: 3103–3110. doi: 10.1128/AEM.72.5.3103-3110.2006
    [99] Reardon CL, Gollany HT, Wuest SB (2014) Diazotroph community structure and abundance in wheat-fallow and wheat-pea crop rotations. Soil Biol Biochem 69: 406–412. doi: 10.1016/j.soilbio.2013.10.038
    [100] Coelho MRR, Marriel IE, Jenkins SN, et al. (2009) Molecular detection and quantification of nifH gene sequences in the rhizosphere of sorghum (Sorghum bicolor) sown with two levels of nitrogen fertilizer. Appl Soil Ecol 42: 48–53. doi: 10.1016/j.apsoil.2009.01.010
    [101] Christiansen-Weniger C, Groneman AF, van Veen JA (1992) Associative N2 fixation and root exudation of organic acids from wheat cultivars of different aluminium tolerance. Plant Soil 139: 167–174. doi: 10.1007/BF00009307
    [102] Manske GGB, Behl RK, Luttger AB, et al. (2000) Enhancement of mycorrhizal infection, nutrient efficiency and plant growth by Azotobacter in wheat: evidence of varietal effects, In: Narula N, Editors, Azotobacter in Sustainable Agriculture, New Delhi: CBS Publishers, 136-147.
    [103] Combes-Meynet E, Pothier JF, Moënne-Loccoz Y, et al. (2011) The Pseudomonas secondary metabolite 2,4-diacetylphloroglucinol is a signal inducing rhizoplane expression of Azospirillum genes involved in plant-growth promotion. Mol Plant Microbe In 24: 271–284.
    [104] Baldani JI, Baldani VLD (2005) History on the biological nitrogen fixation research in graminaceous plants: special emphasis on the Brazilian experience. An Acad Bras Ciênc 77: 549–579. doi: 10.1590/S0001-37652005000300014
    [105] Cassán F, Perrig D, Sgroy V, et al. (2009) Azospirillum brasilense Az39 and Bradyrhizobium japonicum E109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L.) and soybean (Glycine max L.). Eur J Soil Biol 45: 28–35.
    [106] Moubayidin L, Di Mambro R, Sabatini S (2009) Cytokinin-auxin crosstalk. Trends Plant Sci 14: 557–562. doi: 10.1016/j.tplants.2009.06.010
    [107] 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.
    [108] Upadhyay SK, Singh DP, Saikia R (2009) Genetic diversity of plant growth promoting rhizobacteria isolated from rhizospheric soil of wheat under saline condition. Curr Microbiol 59: 489–496. doi: 10.1007/s00284-009-9464-1
    [109] Graham JH, Linderman RG (1980) Ethylene production by ectomycorrhizal fungi, Fusarium oxysporum f. sp. pini, and by aseptically synthesized ectomycorrhizae and Fusarium-infected Douglas-fir roots. Can J Microbiol 26: 1340–1347.
    [110] Prigent-Combaret C, Blaha D, Pothier JF, et al. (2008) Physical organization and phylogenetic analysis of acdR as leucine-responsive regulator of the 1-aminocyclopropane-1-carboxylate deaminase gene acdS in phytobeneficial Azospirillum lipoferum 4B and other Proteobacteria. FEMS Microbiol Ecol 65: 202–219. doi: 10.1111/j.1574-6941.2008.00474.x
    [111] Bertrand H, Plassard C, Pinochet X, et al. (2000) Stimulation of the ionic transport system in Brassica napus by a plant growth-promoting rhizobacterium (Achromobacter sp.). Can J Microbiol 46: 229–236. doi: 10.1139/cjm-46-3-229
    [112] Mantelin S, Desbrosses G, Larcher M, et al. (2006) Nitrate-dependent control of root architecture and N nutrition are altered by a plant growth-promoting Phyllobacterium sp. Planta 223: 591–603. doi: 10.1007/s00425-005-0106-y
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AIMS Microbiology
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