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Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review

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Abstract

Plant growth-promoting rhizobacteria (PGPR) are soil bacteria that are able to colonize rhizosphere and to enhance plant growth by means of a wide variety of mechanisms like organic matter mineralization, biological control against soil-borne pathogens, biological nitrogen fixation, and root growth promotion. A very interesting feature of PGPR is their ability of enhancing nutrient bioavailability. Several bacterial species have been characterized as P-solubilizing microorganisms while other species have been shown to increase the solubility of micronutrients, like those that produce siderophores for Fe chelation. The enhanced amount of soluble macro- and micronutrients in the close proximity of the soil-root interface has indeed a positive effect on plant nutrition. Furthermore, several pieces of evidence highlight that the inoculation of plants with PGPR can have considerable effects on plant at both physiological and molecular levels (e.g., induction of rhizosphere acidification, up- and downregulation of genes involved in ion uptake, and translocation), suggesting the possibility that soil biota could stimulate plants being more efficient in retrieving nutrients from soil and coping with abiotic stresses. However, the molecular mechanisms underlying these phenomena, the signals involved as well as the potential applications in a sustainable agriculture approach, and the biotechnological aspects for possible rhizosphere engineering are still matters of discussion.

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References

  • Achtnich C, Bak F, Conrad R (1995) Competition for electron donors among nitrate reducers, ferric iron reducers, sulfate reducers, and methanogens in anoxic paddy soil. Biol Fertil Soils 19:65–72. doi:10.1007/BF00336349

    CAS  Google Scholar 

  • Adesemoye A, Kloepper J (2009) Plant–microbes interactions in enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol 85:1–12. doi:10.1007/s00253-009-2196-0

    CAS  PubMed  Google Scholar 

  • Adesemoye AO, Torbert HA, Kloepper JW (2009) Plant growth-promoting rhizobacteria allow reduced application rates of chemical fertilizer. Microb Ecol 58:921–929. doi:10.1007/s00248-009-9531-y

    CAS  PubMed  Google Scholar 

  • Artursson V, Finlay RD, Jansson JK (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8:1–10. doi:10.1111/j.1462-2920.2005.00942.x

    CAS  PubMed  Google Scholar 

  • Bashan Y (1990) Short exposure to Azospirillum brasilense Cd inoculation enhanced proton efflux of intact wheat roots. Can J Microbiol 36:419–425. doi:10.1139/m90-073

    CAS  Google Scholar 

  • Bashan Y, Levanony H, Mitiku G (1989) Changes in proton efflux of intact wheat roots induced by Azospirillum brasilense Cd. Can J Microbiol 35:691–697. doi:10.1139/m89-113

    CAS  Google Scholar 

  • Bashan Y, Kamnev A, de-Bashan L (2013a) A proposal for isolating and testing phosphate-solubilizing bacteria that enhance plant growth. Biol Fertil Soils 49:1–2. doi:10.1007/s00374-012-0756-4

    Google Scholar 

  • Bashan Y, Kamnev A, de-Bashan L (2013b) Tricalcium phosphate is inappropriate as a universal selection factor for isolating and testing phosphate-solubilizing bacteria that enhance plant growth: a proposal for an alternative procedure. Biol Fertil Soils 49:465–479. doi:10.1007/s00374-012-0737-7

    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 84:11–18. doi:10.1007/s00253-009-2092-7

    CAS  PubMed  Google Scholar 

  • Bertrand H, Plassard C, Pinochet X, Touraine B, Normand P, Cleyet-Marel JC (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/w99-137

    CAS  PubMed  Google Scholar 

  • Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–50. doi:10.1007/s11274-011-0979-9

    CAS  PubMed  Google Scholar 

  • Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol 24:225–252. doi:10.1146/annurev.pp. 24.060173.001301

    CAS  Google Scholar 

  • Brelles-Mariño G, Bedmar EJ (2001) Detection, purification and characterisation of quorum-sensing signal molecules in plant-associated bacteria. J Biotechnol 91:197–209. doi:10.1016/S0168-1656(01)00330-3

    PubMed  Google Scholar 

  • Bulgarelli D, Schlaeppi K, Spaepen S, Loren V, van Themaat E, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–38. doi:10.1146/annurev-arplant-050312-120106

    CAS  PubMed  Google Scholar 

  • Canellas LP, Olivares FL, Okorokova-fac AL (2002) Humic acids isolated from earthworm compost enhance root elongation, lateral root emergence, and plasma membrane H+-ATPase activity in maize roots. Plant Physiol 130:1951–1957. doi:10.1104/pp. 007088.loosens

    PubMed Central  CAS  PubMed  Google Scholar 

  • Canellas L, Balmori D, Médici L, Aguiar N, Campostrini E, Rosa R, Façanha A, Olivares F (2013) A combination of humic substances and Herbaspirillum seropedicae inoculation enhances the growth of maize (Zea mays L.). Plant Soil 366:119–132. doi:10.1007/s11104-012-1382-5

    CAS  Google Scholar 

  • Cartieaux F, Thibaud M, Zimmerli L, Lessard P, Sarrobert C, David P, Gerbaud A, Robaglia C, Somerville S, Nussaume L (2003) Transcriptome analysis of Arabidopsis colonized by a plant-growth promoting rhizobacterium reveals a general effect on disease resistance. Plant J 36:177–188. doi:10.1046/j.1365-313X.2003.01867.x

    CAS  PubMed  Google Scholar 

  • Cassman KG (1999) Ecological intensification of cereal production systems: yield potential, soil quality, and precision agriculture. Proc Natl Acad Sci U S A 96:5952–9

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cesco S, Neumann G, Tomasi N, Pinton R, Weisskopf L (2010) Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition. Plant Soil 329:1–25. doi:10.1007/s11104-009-0266-9

    CAS  Google Scholar 

  • Cesco S, Mimmo T, Tonon G, Tomasi N, Pinton R, Terzano R, Neumann G, Weisskopf L, Renella G, Landi L, Nannipieri P (2012) Plant-borne flavonoids released into the rhizosphere: impact on soil bio-activities related to plant nutrition. A review. Biol Fertil Soils 48:123–149. doi:10.1007/s00374-011-0653-2

    CAS  Google Scholar 

  • Chen A, Hu J, Sun S, Xu G (2007) Conservation and divergence of both phosphate- and mycorrhiza-regulated physiological responses and expression patterns of phosphate transporters in solanaceous species. New Phytol 173:817–831. doi:10.1111/j.1469-8137.2006.01962.x

    CAS  PubMed  Google Scholar 

  • Cheng Z, Duan J, Hao Y, McConkey B, Glick B (2009) Identification of bacterial proteins mediating the interactions between Pseudomonas putida UW4 and Brassica napus (Canola). Mol Plant-Microbe Interact 22:686–694. doi:10.1094/MPMI-22-6-0686

    CAS  PubMed  Google Scholar 

  • Chiou T-J, Liu H, Harrison MJ (2001) The spatial expression patterns of a phosphate transporter (MtPT1) from Medicago truncatula indicate a role in phosphate transport at the root/soil interface. Plant J 25:281–293. doi:10.1046/j.1365-313x.2001.00963.x

    CAS  PubMed  Google Scholar 

  • Colombo C, Palumbo G, He J, Pinton R, Cesco S (2013) Review on iron availability in soil: interaction of Fe minerals, plants, and microbes. J Soils Sediments 14:1–11. doi:10.1007/s11368-013-0814-z

    Google Scholar 

  • Connolly E, Campbell N, Grotz N, Prichard C, Guerinot M (2003) Overexpression of the FRO2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control. Plant Physiol 133:1102–1110. doi:10.1104/pp. 103.025122

    PubMed Central  CAS  PubMed  Google Scholar 

  • Correa-Aragunde N, Graziano M, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905. doi:10.1007/s00425-003-1172-7

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Curie C, Panaviene Z, Loulergue C, Dellaporta S, Briat J, Walker E (2001) Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409:346–349

    CAS  PubMed  Google Scholar 

  • Daram P, Brunner S, Persson B, Amrhein N, Bucher M (1998) Functional analysis and cell-specific expression of a phosphate transporter from tomato. Planta 206:225–233. doi:10.1007/s004250050394

    CAS  PubMed  Google Scholar 

  • De Santiago A, Quintero JM, Avilés M, Delgado A (2009) Effect of Trichoderma asperellum strain T34 on iron nutrition in white lupin. Soil Biol Biochem 41:2453–2459. doi:10.1016/j.soilbio.2009.07.033

    Google Scholar 

  • Diallo MD, Willems A, Vloemans N, Cousin S, Vandekerckhove TT, de Lajudie P, Neyra M, Vyverman W, Gillis M, Van der Gucht K (2004) Polymerase chain reaction denaturing gradient gel electrophoresis of the N2-fixing bacterial diversity in soil under Acacia tortilis ssp. raddiana and Balanites aegyptiaca in the dryland part of Senegal. Environ Microbiol 6:400–415

    CAS  Google Scholar 

  • Duc L, Noll M, Meier E, Burgmann H, Zeyer J (2009) High diversity of diazotrophs in the forefield of a receding alpine glacier. Microb Ecol 57:179–190

    PubMed  Google Scholar 

  • Fan B, Carvalhais L, Becker A, Fedoseyenko D, von Wiren N, Borriss R (2012) Transcriptomic profiling of Bacillus amyloliquefaciens FZB42 in response to maize root exudates. BMC Microbiol 12:116

    PubMed Central  CAS  PubMed  Google Scholar 

  • Furihata T, Suzuki M, Sakurai H (1992) Kinetic characterization of two phosphate uptake systems with different affinities in suspension-cultured Catharanthus roseus protoplasts. Plant Cell Physiol 33:1151–1157

    CAS  Google Scholar 

  • Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai ZC, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892

    CAS  PubMed  Google Scholar 

  • Gao M, Teplitski M, Robinson JB, Bauer WD (2003) Production of substances by Medicago truncatula that affect bacterial quorum sensing. Mol Plant-Microbe Interact 16:827–834. doi:10.1094/MPMI.2003.16.9.827

    CAS  PubMed  Google Scholar 

  • García M, Lucena C, Romera F, Alcántara E, Pérez-Vicente R (2010) Ethylene and nitric oxide involvement in the up-regulation of key genes related to iron acquisition and homeostasis in Arabidopsis. J Exp Bot 61:3885–99. doi:10.1093/jxb/erq203

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Glass ADM, Shaff JE, Kochian LV (1992) Studies of the uptake of nitrate in barley: IV. Electrophysiology. Plant Physiol 99:456–463. doi:10.1104/pp. 99.2.456

    PubMed Central  CAS  PubMed  Google Scholar 

  • Glassop D, Smith S, Smith F (2005) Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222:688–698. doi:10.1007/s00425-005-0015-0

    CAS  PubMed  Google Scholar 

  • Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica (Cairo) 2012:1–15. doi:10.6064/2012/963401

    Google Scholar 

  • Guerinot ML (1994) Microbial iron transport. Annu Rev Microbiol 48:743–772. doi:10.1146/annurev.mi.48.100194.003523

    CAS  PubMed  Google Scholar 

  • Gyaneshwar P, Naresh Kumar G, Parekh LJ, Poole PS (2002) Role of soil microorganisms in improving P nutrition of plants. Plant Soil 245:83–93. doi:10.1023/A:1020663916259

    CAS  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. doi:10.1007/BF00256908

    Google Scholar 

  • Hannula SE, de Boer W, van Veen JA (2014) Do genetic modifications in crops affect soil fungi? A review. Biol Fertil Soils 50:433–446. doi:10.1007/s00374-014-0895-x

    CAS  Google Scholar 

  • Harrison MJ, Dewbre GR, Liu J (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell Online 14:2413–2429. doi:10.1105/tpc.004861

    CAS  Google Scholar 

  • Hinsinger P, Plassard C, Tang C, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248:43–59. doi:10.1023/A:1022371130939

    CAS  Google Scholar 

  • Hinsinger P, Bengough AG, Vetterlein D, Young I (2009) Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321:117–152. doi:10.1007/s11104-008-9885-9

    CAS  Google Scholar 

  • Hobara S, McCalley C, Koba K, Giblin AE, Weiss MS, Gettel GM, Shaver GR (2006) Nitrogen fixation in surface soils and vegetation in an Arctic tundra watershed: a key source of atmospheric nitrogen. Arct Antarc Alp Res 38:363–372

    Google Scholar 

  • Hori T, Muller A, Igarashi Y, Conrad R, Friedrich M (2009) Identification of iron-reducing microorganisms in anoxic rice paddy soil by 13C-acetate probing. ISME J 4:267–278

    PubMed  Google Scholar 

  • Hurek T, Handley LL, Reinhold-Hurek B, Piché Y (2002) Azoarcus grass endophytes contribute fixed nitrogen to the plant in an unculturable state. Mol Plant-Microbe Interact 15:233–242. doi:10.1094/MPMI.2002.15.3.233

    CAS  PubMed  Google Scholar 

  • Igual JM, Valverde A, Cervantes E, Velázquez E (2001) Phosphate-solubilizing bacteria as inoculants for agriculture: use of updated molecular techniques in their study. Agronomie 21:561–568

    Google Scholar 

  • Iniguez AL, Dong Y, Triplett EW (2004) Nitrogen fixation in wheat provided by Klebsiella pneumoniae 342. Mol Plant-Microbe Interact 17:1078–1085. doi:10.1094/MPMI.2004.17.10.1078

    CAS  PubMed  Google Scholar 

  • Inoue H, Kobayashi T, Nozoye T, Takahashi M, Kakei Y, Suzuki K, Nakazono M, Nakanishi H, Mori S, Nishizawa N (2009) Rice OsYSL15 is an iron-regulated iron(III)-deoxymugineic acid transporter expressed in the roots and is essential for iron uptake in early growth of the seedlings. J Biol Chem 284:3470–9. doi:10.1074/jbc.M806042200

    CAS  PubMed  Google Scholar 

  • Ishimaru Y, Suzuki M, Tsukamoto T, Suzuki K, Nakazono M, Kobayashi T, Wada Y, Watanabe S, Matsuhashi S, Takahashi M, Nakanishi H, Mori S, Nishizawa N (2006) Rice plants take up iron as an Fe3+-phytosiderophore and as Fe2+. Plant J 45:335–346. doi:10.1111/j.1365-313X.2005.02624.x

    CAS  PubMed  Google Scholar 

  • Jetten MSM (2008) The microbial nitrogen cycle. Environ Microbiol 10:2903–2909. doi:10.1111/j.1462-2920.2008.01786.x

    CAS  PubMed  Google Scholar 

  • Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium‐Medicago model. Nature Rev Microbiol 5:619–633

    CAS  Google Scholar 

  • Kahindi JHP, Woomer P, George T, de Souza Moreira FM, Karanja NK, Giller KE (1997) Agricultural intensification, soil biodiversity and ecosystem function in the tropics: the role of nitrogen-fixing bacteria. Appl Soil Ecol 6:55–76

    Google Scholar 

  • Karthikeyan AS, Varadarajan DK, Mukatira UT, D’Urzo MP, Damsz B, Raghothama KG (2002) Regulated expression of Arabidopsis phosphate transporters. Plant Physiol 130:221–233. doi:10.1104/pp. 020007

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kechid M, Desbrosses G, Rokhsi W, Varoquaux F, Djekoun A, Touraine B (2013) The NRT2.5 and NRT2.6 genes are involved in growth promotion of Arabidopsis by the plant growth-promoting rhizobacterium (PGPR) strain Phyllobacterium brassicacearum STM196. New Phytol 198:514–24. doi:10.1111/nph.12158

    CAS  PubMed  Google Scholar 

  • Kobayashi T, Nishizawa NK (2012) Iron uptake, translocation, and regulation in higher plants. Annu Rev Plant Biol 63:131–52. doi:10.1146/annurev-arplant-042811-105522

    CAS  PubMed  Google Scholar 

  • Kojima S, Bohner A, Gassert B, Yuan L, von Wirén N (2007) AtDUR3 represents the major transporter for high-affinity urea transport across the plasma membrane of nitrogen-deficient Arabidopsis roots. Plant J 52:30–40. doi:10.1111/j.1365-313X.2007.03223.x

    CAS  PubMed  Google Scholar 

  • Lemanceau P, Expert D, Gaymand F, Bakker PAHM, Briat JF (2009) Role of iron in plant–microbe interactions. Adv Bot Res 51:491–549. doi:10.1016/S0065-2296(09)51012-9

    CAS  Google Scholar 

  • Lery LMS, Hemerly AS, Nogueira EM, Krüger WMA, Von Bisch PM (2011) Quantitative proteomic analysis of the interaction between the endophytic plant-growth-promoting bacterium Gluconacetobacter diazotrophicus and sugarcane. Mol Plant-Microbe Interact 24:562–576. doi:10.1094/MPMI-08-10-0178

    CAS  PubMed  Google Scholar 

  • Liang C, Wang J, Zhao J, Tian J, Liao H (2014) Control of phosphate homeostasis through gene regulation in crops. Curr Opin Plant Biol 21:59–66. doi:10.1016/j.pbi.2014.06.009

    CAS  PubMed  Google Scholar 

  • Liu C, Muchhal US, Uthappa M, Kononowicz AK, Raghothama KG (1998) Tomato phosphate transporter genes are differentially regulated in plant tissues by phosphorus. Plant Physiol 116:91–99. doi:10.1104/pp. 116.1.91

    PubMed Central  CAS  PubMed  Google Scholar 

  • Liu L-H, Ludewig U, Frommer WB, von Wirén N (2003) AtDUR3 encodes a new type of high-affinity urea/H+ symporter in Arabidopsis. Plant Cell Online 15:790–800. doi:10.1105/tpc.007120

    CAS  Google Scholar 

  • Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Rio TG, del Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lynch JM (1970) The rhizosphere. John Wiley and Sons, Chichester, UK

    Google Scholar 

  • Mantelin S, Desbrosses G, Larcher M, Tranbarger TJ, Cleyet-Marel JC, Touraine B (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

    CAS  PubMed  Google Scholar 

  • Mark GL, Dow JM, Kiely PD, Higgins H, Haynes J, Baysse C, Abbas A, Foley T, Franks A, Morrissey J, O’Gara F (2005) Transcriptome profiling of bacterial responses to root exudates identifies genes involved in microbe-plant interactions. Proc Natl Acad Sci U S A 102:17454–9. doi:10.1073/pnas.0506407102

    PubMed Central  CAS  PubMed  Google Scholar 

  • Marschner P (2011) Marschner’s mineral nutrition of higher plants, 3rd ed. London

  • Marschner H, Römheld V (1994) Strategies of plants for acquisition of iron. Plant Soil 165:261–274. doi:10.1007/BF00008069

    CAS  Google Scholar 

  • Marschner P, Crowley D, Rengel Z (2011) Rhizosphere interactions between microorganisms and plants govern iron and phosphorus acquisition along the root axis—model and research methods. Soil Biol Biochem 43:883–894. doi:10.1016/j.soilbio.2011.01.005

    CAS  Google Scholar 

  • Marulanda A, Azcón R, Chaumont F, Ruiz-Lozano JM, Aroca R (2010) Regulation of plasma membrane aquaporins by inoculation with a Bacillus megaterium strain in maize (Zea mays L.) plants under unstressed and salt-stressed conditions. Planta 232:533–43. doi:10.1007/s00425-010-1196-8

    CAS  PubMed  Google Scholar 

  • Mathesius U, Mulders S, Gao M, Teplitski M, Caetano-Anollés G, Rolfe BG, Bauer WD (2003) Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc Natl Acad Sci U S A 100:1444–1449. doi:10.1073/pnas.262672599

    PubMed Central  CAS  PubMed  Google Scholar 

  • Matson PA, Parton WJ, Power AG, Swift MJ (1997) Agricultural intensification and ecosystem properties. Science 277:504–509. doi:10.1126/science.277.5325.504

    CAS  PubMed  Google Scholar 

  • McClure PR, Kochian LV, Spanswick RM, Shaff JE (1990a) Evidence for cotransport of nitrate and protons in maize roots: I. Effects of nitrate on the membrane potential. Plant Physiol 93:281–289. doi:10.1104/pp. 93.1.281

    PubMed Central  CAS  PubMed  Google Scholar 

  • McClure PR, Kochian LV, Spanswick RM, Shaff JE (1990b) Evidence for cotransport of nitrate and protons in maize roots: II. Measurement of NO3 − and H+ fluxes with ion-selective microelectrodes. Plant Physiol 93:290–294. doi:10.1104/pp. 93.1.290

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mehnaz S, Lazarovits G (2006) Inoculation effects of Pseudomonas putida, Gluconacetobacter azotocaptans, and Azospirillum lipoferum on corn plant growth under greenhouse conditions. Microb Ecol 51:326–335. doi:10.1007/s00248-006-9039-7

    PubMed  Google Scholar 

  • Miller LD, Yost CK, Hynes MF, Alexandre G (2007) The major chemotaxis gene cluster of Rhizobium leguminosarum bv. viciae is essential for competitive nodulation. Mol Microbiol 63:348–362. doi:10.1111/j.1365-2958.2006.05515.x

    CAS  PubMed  Google Scholar 

  • Mimmo T, Hann S, Jaitz L, Cesco S, Gessa CE, Puschenreiter M (2011) Time and substrate dependent exudation of carboxylates by Lupinus albus L. and Brassica napus L. Plant Physiol Biochem 49:1272–1278. doi:10.1016/j.plaphy.2011.08.012

    CAS  PubMed  Google Scholar 

  • Mimmo T, Del Buono D, Terzano R, Tomasi N, Vigani G, Crecchio C, Pinton R, Zocchi G, Cesco S (2014) Rhizospheric organic compounds in the soil-microorganism-plant system: their role in iron availability. Eur J Soil Sci 65:629–642. doi:10.1111/ejss.12158

    CAS  Google Scholar 

  • Miransari M (2011) Arbuscular mycorrhizal fungi and nitrogen uptake. Arch Microbiol 193:77–81. doi:10.1007/s00203-010-0657-6

    CAS  PubMed  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. doi:10.1094/MPMI-21-7-1001

    CAS  PubMed  Google Scholar 

  • Mudge SR, Rae AL, Diatloff E, Smith FW (2002) Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis. Plant J 31:341–353. doi:10.1046/j.1365-313X.2002.01356.x

    CAS  PubMed  Google Scholar 

  • Nacry P, Bouguyon E, Gojon A (2013) Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource. Plant Soil. doi:10.1007/s11104-013-1645-9

    Google Scholar 

  • Nagata T, Oobo T, Aozasa O (2013) Efficacy of a bacterial siderophore, pyoverdine, to supply iron to Solanum lycopersicum plants. J Biosci Bioeng 115:686–90. doi:10.1016/j.jbiosc.2012.12.018

    CAS  PubMed  Google Scholar 

  • Nagy R, Karandashov V, Chague V, Kalinkevich K, Tamasloukht M, Xu G, Jakobsen I, Levy AA, Amrhein N, Bucher M (2005) The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant J 42:236–250. doi:10.1111/j.1365-313X.2005.02364.x

    CAS  PubMed  Google Scholar 

  • Neilands JB (1981) Iron absorption and transport in microorganisms. Annu Rev Nutr 1:27–46. doi:10.1146/annurev.nu.01.070181.000331

    CAS  PubMed  Google Scholar 

  • Nozoye T, Nagasaka S, Kobayashi T, Takahashi M, Sato YY, Uozumi N, Nakanishi H, Nishizawa N (2011) Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J Biol Chem 286:5446–54. doi:10.1074/jbc.M110.180026

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ollivier J, Töwe S, Bannert A, Hai B, Kastl EM, Meyer A, Su MX, Kleineidam K, Schloter M (2011) Nitrogen turnover in soil and global change. FEMS Microbiol Ecol 78:3–16. doi:10.1111/j.1574-6941.2011.01165.x

    CAS  PubMed  Google Scholar 

  • Pagnussat GC, Lanteri ML, Lamattina L (2003) Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol 132:1241–1248. doi:10.1104/pp. 103.022228

    PubMed Central  CAS  PubMed  Google Scholar 

  • Palacios O, Bashan Y, de-Bashan L (2014) Proven and potential involvement of vitamins in interactions of plants with plant growth-promoting bacteria—an overview. Biol Fertil Soils 50:415–432. doi:10.1007/s00374-013-0894-3

    CAS  Google Scholar 

  • Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 10:763–775

    Google Scholar 

  • Paszkowski U, Kroken S, Roux C, Briggs SP (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci 99:13324–13329. doi:10.1073/pnas.202474599

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pérez-Montaño F, Jiménez-Guerrero I, Contreras Sánchez-Matamoros R, López-Baena FJ, Ollero FJ, Rodríguez-Carvajal MA, Bellogín RA, Espuny MR (2013) Rice and bean AHL-mimic quorum-sensing signals specifically interfere with the capacity to form biofilms by plant-associated bacteria. Res Microbiol 164:749–760. doi:10.1016/j.resmic.2013.04.001

    PubMed  Google Scholar 

  • Pii Y, Crimi M, Cremonese G, Spena A, Pandolfini T (2007) Auxin and nitric oxide control indeterminate nodule formation. BMC Plant Biol 7:21. doi:10.1186/1471-2229-7-21

    PubMed Central  PubMed  Google Scholar 

  • Pinton R, Cesco S, Santi S, Varanini Z (1997) Soil humic substances stimulate proton release by intact oat seedling roots. J Plant Nutr 20:857–869. doi:10.1080/01904169709365301

    CAS  Google Scholar 

  • Pinton R, Varanini Z, Nannipieri P (2001) The rhizosphere as a site of biochemical interactions among soil components, plants and microorganisms. In: Pinton R, Vranini Z, Nannipieri P (eds) The rhizosphere biochemistry and organic substances at the soil-plant interface. Marcel Dekker, New York, pp 1–17

    Google Scholar 

  • Pivato B, Offre P, Marchelli S, Barbonaglia B, Mougel C, Lemanceau P, Berta G (2009) Bacterial effects on arbuscular mycorrhizal fungi and mycorrhiza development as influenced by the bacteria, fungi, and host plant. Mycorrhiza 19:81–90. doi:10.1007/s00572-008-0205-2

    PubMed  Google Scholar 

  • Plett D, Toubia J, Garnett T, Tester M, Kaiser BN, Baumann U (2010) Dichotomy in the NRT gene families of dicots and grass species. PLoS One 5:e15289. doi:10.1371/journal.pone.0015289

    PubMed Central  CAS  PubMed  Google Scholar 

  • Raaijmakers JM, van der Sluis L, Bakker PAHM, Schippers B, Koster M, Weisbeek PJ (1995) Utilization of heterologous siderophores and rhizosphere competence of fluorescent Pseudomonas spp. Can J Microbiol 41:126–135. doi:10.1139/m95-017

    CAS  Google Scholar 

  • Radwan TEE, Mohamed ZK, Reis VM (2002) Production of indole-3-acetic acid by different strains of Azospirillum and Herbaspirillum spp. Symbiosis 32:39–54

    CAS  Google Scholar 

  • Rajkumar M, Sandhya S, Prasad MN V, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv 30:1562–1574. doi:10.1016/j.biotechadv.2012.04.011

    CAS  PubMed  Google Scholar 

  • Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein N, Bucher M (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414:462–470

    CAS  PubMed  Google Scholar 

  • Reed SC, Cleveland CC, Townsend AR (2011) Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annu Rev Ecol Evol Syst 42:489–512

    Google Scholar 

  • Richardson AE (1994) Soil microorganisms and phosphorus availability. In: Pankhurst CE, Doube BM, Gupta VVSR, Grace PR (eds) Soil biota management in sustainable farming systems. CSIRO, Melbourne, pp 50–62

    Google Scholar 

  • Rodríguez H, Fraga R, Gonzalez T, Bashan Y (2006) Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria. Plant Soil 287:15–21. doi:10.1007/s11104-006-9056-9

    Google Scholar 

  • Römheld V (1991) The role of phytosiderophores in acquisition of iron and other micronutrients in graminaceous species: an ecological approach. Plant Soil 130:127–134. doi:10.1007/BF00011867

    Google Scholar 

  • Rubio F, Gassmann W, Schroeder JI (1995) Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270:1660–1663. doi:10.1126/science.270.5242.1660

    CAS  PubMed  Google Scholar 

  • Ryu CM, Farag MA, Hu CH, Reddy MS, Kloepper JW, Paré PW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci U S A 100:4927–4932. doi:10.1073/pnas.0730845100

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ryu C-M, Farag MA, Hu C-H, Reddy MS, Kloepper JW, Paré PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026. doi:10.1104/pp. 103.026583

    PubMed Central  CAS  PubMed  Google Scholar 

  • Santi S, Locci G, Pinton R, Cesco S, Varanini Z (1995) Plasma membrane H+-ATPase in maize roots induced for NO3 - uptake. Plant Physiol 109:1277–1283. doi:10.1104/pp. 109.4.1277

    PubMed Central  CAS  PubMed  Google Scholar 

  • Santi S, Cesco S, Varanini Z, Pinton R (2005) Two plasma membrane H(+)-ATPase genes are differentially expressed in iron-deficient cucumber plants. Plant Physiol Biochem 43:287–92. doi:10.1016/j.plaphy.2005.02.007

    CAS  PubMed  Google Scholar 

  • Santi C, Bogusz D, Franche C (2013) Nitrogen fixation in non legumes. Ann Bot 111:743–767

    PubMed Central  CAS  PubMed  Google Scholar 

  • Schaaf G, Ludewig U, Erenoglu BE, Mori S, Kitahara T, von Wirén N (2004) ZmYS1 functions as a proton-coupled symporter for phytosiderophore- and nicotianamine-chelated metals. J Biol Chem 279:9091–6. doi:10.1074/jbc.M311799200

    CAS  PubMed  Google Scholar 

  • Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453. doi:10.1104/pp. 116.2.447

    PubMed Central  CAS  PubMed  Google Scholar 

  • Schünmann PHD, Richardson AE, Smith FW, Delhaize E (2004) Characterization of promoter expression patterns derived from the Pht1 phosphate transporter genes of barley (Hordeum vulgare L.). J Exp Bot 55:855–865. doi:10.1093/jxb/erh103

    PubMed  Google Scholar 

  • Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751. doi:10.1128/AEM. 67.10.4742-4751.2001

    PubMed Central  CAS  PubMed  Google Scholar 

  • Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–7. doi:10.1104/pp. 111.174581

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sturz AV, Nowak J (2000) Endophytic communities of rhizobacteria and the strategies required to create yield enhancing associations with crops. Appl Soil Ecol 15:183–190. doi:10.1016/S0929-1393(00)00094-9

    Google Scholar 

  • Sudhakar P, Chattopadhyay GN, Gangwar SK, Ghosh JK (2000) Effect of foliar application of Azotobacter, Azospirillum and Beijerinckia on leaf yield and quality of mulberry (Morus alba). J Agric Sci 134:227–234

    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. doi:10.1094/MPMI.2000.13.6.637

    CAS  PubMed  Google Scholar 

  • Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–7. doi:10.1038/nature01014

    CAS  PubMed  Google Scholar 

  • Tomasi N, Weisskopf L, Renella G, Landi L, Pinton R, Varanini Z, Nannipieri P, Torrent J, Martinoia E, Cesco S (2008) Flavonoids of white lupin roots participate in phosphorus mobilization from soil. Soil Biol Biochem 40:1971–1974. doi:10.1016/j.soilbio.2008.02.017

    CAS  Google Scholar 

  • Tomasi N, Kretzschmar T, Espen L, Weisskopf L, Fuglsang AT, Palmgren MG, Neumann G, Varanini Z, Pinton R, Martinoia E, Cesco S (2009) Plasma membrane H+-ATPase-dependent citrate exudation from cluster roots of phosphate-deficient white lupin. Plant Cell Environ 32:465–475. doi:10.1111/j.1365-3040.2009.01938.x

    CAS  PubMed  Google Scholar 

  • Touraine B, Glass ADM (1997) NO3 - and CIO3 - fluxes in the chl1-5 mutant of Arabidopsis thaliana. 114:137–144

  • Ullrich-Eberius CI, Novacky A, Bel AJE (1984) Phosphate uptake in Lemna gibba G1: energetics and kinetics. Planta 161:46–52. doi:10.1007/BF00951459

    CAS  PubMed  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. doi:10.3389/fpls.2013.00356

    PubMed Central  PubMed  Google Scholar 

  • Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586. doi:10.1023/A:1026037216893

    CAS  Google Scholar 

  • Von Wirén N, Merrick M (2004) Regulation and function of ammonium carriers in bacteria, fungi, and plants. Mol. Mech. Control. Transmembrane Transp. SE - 3. Springer Berlin Heidelberg, pp 95–120

  • Von Wirén N, Gazzarrini S, Gojont A, Frommer WB (2000) The molecular physiology of ammonium uptake and retrieval. Curr Opin Plant Biol 3:254–261. doi:10.1016/S1369-5266(00)80074-6

    Google Scholar 

  • Weller DM, Raaijmakers JM, Gardener BBM, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40:309–348. doi:10.1146/annurev.phyto.40.030402.110010

    CAS  PubMed  Google Scholar 

  • White PJ (2003) Ion transport. In: Thomas B, Murphy DJ, Murray BG (eds) Encyclopedia of Applied Plant Sciences. Academic Press, London, pp 625–634

    Google Scholar 

  • Widmer F, Shaffer BT, Porteous LA, Seidleret RJ (1999) Analysis of nifH gene pool complexity in soil and litter at a Douglas Fir Forest Site in Oregon Cascade Mountain Range. Appl Environ Microbiol 65:374–380

    PubMed Central  CAS  PubMed  Google Scholar 

  • Witte C-P (2011) Urea metabolism in plants. Plant Sci 180:431–438. doi:10.1016/j.plantsci.2010.11.010

    CAS  PubMed  Google Scholar 

  • Xiong H, Kakei Y, Kobayashi T, Guo X, Nakazono M, Takahashi H, Nakanishi H, Shen H, Zhang F, Nishizawa N, Zuo Y (2013) Molecular evidence for phytosiderophore-induced improvement of iron nutrition of peanut intercropped with maize in calcareous soil. Plant Cell Environ 36:1888–902. doi:10.1111/pce.12097

    CAS  PubMed  Google Scholar 

  • Yao J, Allen C (2006) Chemotaxis is required for virulence and competitive fitness of the bacterial wilt pathogen Ralstonia solanacearum. J Bacteriol 188:3697–3708. doi:10.1128/JB.188.10.3697

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zanin L, Tomasi N, Wirdnam C, Meier S, Komarova NY, Mimmo T, Cesco S, Rentsch D, Pinton R (2014) Isolation and functional characterization of a high affinity urea transporter from roots of Zea mays. BMC Plant Biol 14:222. doi:10.1186/s12870-014-0222-6

    PubMed Central  PubMed  Google Scholar 

  • Zhang H, Kim M-S, Sun Y, Dowd SE, Shi H, Paré PW (2008) Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Mol Plant Microbe Interact 21:737–44. doi:10.1094/MPMI-21-6-0737

    PubMed  Google Scholar 

  • Zhang H, Sun Y, Xie X, Kim MS, Dowd SE, Paré PW (2009) A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms. Plant J 58:568–577. doi:10.1111/j.1365-313X.2009.03803.x

    CAS  PubMed  Google Scholar 

  • Zhang F, Shen J, Zhang J, Zuo Y, Li L, Chen X (2010) Rhizosphere processes and management for improving nutrient use efficiency and crop productivity: implications for China, 1st ed. Adv Agron 107:1–32. doi:10.1016/S0065-2113(10)07001-X

    CAS  Google Scholar 

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Acknowledgments

This research was supported by grants from the Italian MIUR (FIRB-Programma “Futuro in Ricerca”), Free University of Bolzano (TN5056). All authors contributed equally to this work.

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Authors and Affiliations

  1. Faculty of Science and Technology, Free University of Bolzano, 39100, Bolzano, Italy

    Youry Pii, Tanja Mimmo & Stefano Cesco

  2. Dipartimento di Scienze Agrarie e Ambientali, University of Udine, 33100, Udine, Italy

    Nicola Tomasi

  3. Dipartimento di Scienze del Suolo, della Pianta e degli Alimenti, University of Bari “Aldo Moro”, 70126, Bari, Italy

    Roberto Terzano & Carmine Crecchio

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  1. Youry Pii
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Pii, Y., Mimmo, T., Tomasi, N. et al. Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review. Biol Fertil Soils 51, 403–415 (2015). https://doi.org/10.1007/s00374-015-0996-1

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