Biology and Fertility of Soils

, Volume 51, Issue 4, pp 403–415 | Cite as

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

  • Youry Pii
  • Tanja Mimmo
  • Nicola Tomasi
  • Roberto Terzano
  • Stefano Cesco
  • Carmine Crecchio


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.


Nutrient availability Soil bacteria Nitrogen Phosphorus Iron PGPR 



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.


  1. 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 Google Scholar
  2. 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 PubMedGoogle Scholar
  3. 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 PubMedGoogle Scholar
  4. 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 PubMedGoogle Scholar
  5. 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 Google Scholar
  6. 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 Google Scholar
  7. 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
  8. 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 Google Scholar
  9. 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 PubMedGoogle Scholar
  10. 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 PubMedGoogle Scholar
  11. 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 PubMedGoogle Scholar
  12. 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 Google Scholar
  13. 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 PubMedGoogle Scholar
  14. 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 PubMedGoogle Scholar
  15. 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 PubMedCentralPubMedGoogle Scholar
  16. 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 Google Scholar
  17. 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 PubMedGoogle Scholar
  18. Cassman KG (1999) Ecological intensification of cereal production systems: yield potential, soil quality, and precision agriculture. Proc Natl Acad Sci U S A 96:5952–9PubMedCentralPubMedGoogle Scholar
  19. 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 Google Scholar
  20. 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 Google Scholar
  21. 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 PubMedGoogle Scholar
  22. 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 PubMedGoogle Scholar
  23. 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 PubMedGoogle Scholar
  24. 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
  25. 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 PubMedCentralPubMedGoogle Scholar
  26. 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 PubMedGoogle Scholar
  27. 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 PubMedGoogle Scholar
  28. 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 409:346–349PubMedGoogle Scholar
  29. 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 PubMedGoogle Scholar
  30. 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
  31. 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 6:400–415Google Scholar
  32. 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 57:179–190PubMedGoogle Scholar
  33. 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 12:116PubMedCentralPubMedGoogle Scholar
  34. 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 33:1151–1157Google Scholar
  35. 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 320:889–892PubMedGoogle Scholar
  36. 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 PubMedGoogle Scholar
  37. 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 PubMedGoogle Scholar
  38. 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
  39. 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 PubMedCentralPubMedGoogle Scholar
  40. 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 PubMedGoogle Scholar
  41. Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica (Cairo) 2012:1–15. doi: 10.6064/2012/963401 Google Scholar
  42. Guerinot ML (1994) Microbial iron transport. Annu Rev Microbiol 48:743–772. doi: 10.1146/annurev.mi.48.100194.003523 PubMedGoogle Scholar
  43. 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 Google Scholar
  44. 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
  45. 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 Google Scholar
  46. 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 Google Scholar
  47. 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 Google Scholar
  48. 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 Google Scholar
  49. 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 38:363–372Google Scholar
  50. 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 4:267–278PubMedGoogle Scholar
  51. 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 PubMedGoogle Scholar
  52. 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 21:561–568Google Scholar
  53. 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 PubMedGoogle Scholar
  54. 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 PubMedGoogle Scholar
  55. 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 PubMedGoogle Scholar
  56. Jetten MSM (2008) The microbial nitrogen cycle. Environ Microbiol 10:2903–2909. doi: 10.1111/j.1462-2920.2008.01786.x PubMedGoogle Scholar
  57. Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the SinorhizobiumMedicago model. Nature Rev Microbiol 5:619–633Google Scholar
  58. 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 6:55–76Google Scholar
  59. 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 PubMedCentralPubMedGoogle Scholar
  60. 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 PubMedGoogle Scholar
  61. 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 PubMedGoogle Scholar
  62. 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 PubMedGoogle Scholar
  63. 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 Google Scholar
  64. 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 PubMedGoogle Scholar
  65. 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 PubMedGoogle Scholar
  66. 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 PubMedCentralPubMedGoogle Scholar
  67. 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 Google Scholar
  68. 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 488:86–90PubMedCentralPubMedGoogle Scholar
  69. Lynch JM (1970) The rhizosphere. John Wiley and Sons, Chichester, UKGoogle Scholar
  70. 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 PubMedGoogle Scholar
  71. 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 PubMedCentralPubMedGoogle Scholar
  72. Marschner P (2011) Marschner’s mineral nutrition of higher plants, 3rd ed. LondonGoogle Scholar
  73. Marschner H, Römheld V (1994) Strategies of plants for acquisition of iron. Plant Soil 165:261–274. doi: 10.1007/BF00008069 Google Scholar
  74. 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 Google Scholar
  75. 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 PubMedGoogle Scholar
  76. 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 PubMedCentralPubMedGoogle Scholar
  77. 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 PubMedGoogle Scholar
  78. 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 PubMedCentralPubMedGoogle Scholar
  79. 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 PubMedCentralPubMedGoogle Scholar
  80. 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 PubMedGoogle Scholar
  81. 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 PubMedGoogle Scholar
  82. 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 PubMedGoogle Scholar
  83. 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 Google Scholar
  84. Miransari M (2011) Arbuscular mycorrhizal fungi and nitrogen uptake. Arch Microbiol 193:77–81. doi: 10.1007/s00203-010-0657-6 PubMedGoogle Scholar
  85. 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 PubMedGoogle Scholar
  86. 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 PubMedGoogle Scholar
  87. 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
  88. 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 PubMedGoogle Scholar
  89. 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 PubMedGoogle Scholar
  90. Neilands JB (1981) Iron absorption and transport in microorganisms. Annu Rev Nutr 1:27–46. doi: 10.1146/ PubMedGoogle Scholar
  91. 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 PubMedCentralPubMedGoogle Scholar
  92. 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 PubMedGoogle Scholar
  93. 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 PubMedCentralPubMedGoogle Scholar
  94. 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 Google Scholar
  95. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 10:763–775Google Scholar
  96. 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 PubMedCentralPubMedGoogle Scholar
  97. 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 PubMedGoogle Scholar
  98. 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 PubMedCentralPubMedGoogle Scholar
  99. 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 Google Scholar
  100. 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 1–17Google Scholar
  101. 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 PubMedGoogle Scholar
  102. 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 PubMedCentralPubMedGoogle Scholar
  103. 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 Google Scholar
  104. Radwan TEE, Mohamed ZK, Reis VM (2002) Production of indole-3-acetic acid by different strains of Azospirillum and Herbaspirillum spp. Symbiosis 32:39–54Google Scholar
  105. 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 PubMedGoogle Scholar
  106. 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 414:462–470PubMedGoogle Scholar
  107. Reed SC, Cleveland CC, Townsend AR (2011) Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annu Rev Ecol Evol Syst 42:489–512Google Scholar
  108. 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 50–62Google Scholar
  109. 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
  110. 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
  111. 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 PubMedGoogle Scholar
  112. 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 PubMedCentralPubMedGoogle Scholar
  113. 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 PubMedCentralPubMedGoogle Scholar
  114. 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 PubMedCentralPubMedGoogle Scholar
  115. 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 PubMedGoogle Scholar
  116. Santi C, Bogusz D, Franche C (2013) Nitrogen fixation in non legumes. Ann Bot 111:743–767PubMedCentralPubMedGoogle Scholar
  117. 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 PubMedGoogle Scholar
  118. 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 PubMedCentralPubMedGoogle Scholar
  119. 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 PubMedGoogle Scholar
  120. 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 PubMedCentralPubMedGoogle Scholar
  121. 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 PubMedCentralPubMedGoogle Scholar
  122. 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
  123. 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 134:227–234Google Scholar
  124. 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 PubMedGoogle Scholar
  125. 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 PubMedGoogle Scholar
  126. 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 Google Scholar
  127. 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 PubMedGoogle Scholar
  128. Touraine B, Glass ADM (1997) NO3 - and CIO3 - fluxes in the chl1-5 mutant of Arabidopsis thaliana. 114:137–144Google Scholar
  129. 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 PubMedGoogle Scholar
  130. 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 PubMedCentralPubMedGoogle Scholar
  131. Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586. doi: 10.1023/A:1026037216893 Google Scholar
  132. 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 95–120Google Scholar
  133. 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
  134. 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 PubMedGoogle Scholar
  135. White PJ (2003) Ion transport. In: Thomas B, Murphy DJ, Murray BG (eds) Encyclopedia of Applied Plant Sciences. Academic Press, London, pp 625–634Google Scholar
  136. 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 65:374–380PubMedCentralPubMedGoogle Scholar
  137. Witte C-P (2011) Urea metabolism in plants. Plant Sci 180:431–438. doi: 10.1016/j.plantsci.2010.11.010 PubMedGoogle Scholar
  138. 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 PubMedGoogle Scholar
  139. 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 PubMedCentralPubMedGoogle Scholar
  140. 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 PubMedCentralPubMedGoogle Scholar
  141. 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 PubMedGoogle Scholar
  142. 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 PubMedGoogle Scholar
  143. 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 Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Youry Pii
    • 1
  • Tanja Mimmo
    • 1
  • Nicola Tomasi
    • 2
  • Roberto Terzano
    • 3
  • Stefano Cesco
    • 1
  • Carmine Crecchio
    • 3
  1. 1.Faculty of Science and TechnologyFree University of BolzanoBolzanoItaly
  2. 2.Dipartimento di Scienze Agrarie e AmbientaliUniversity of UdineUdineItaly
  3. 3.Dipartimento di Scienze del Suolo, della Pianta e degli AlimentiUniversity of Bari “Aldo Moro”BariItaly

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