Challenges Faced in Field Application of Phosphate-Solubilizing Bacteria

  • Abdul Aziz Eida
  • Heribert HirtEmail author
  • Maged M. Saad
Part of the Microorganisms for Sustainability book series (MICRO, volume 2)


The general inaccessibility of soil phosphorous (P) to plants in combination with the depletion of global P reserves provides an incentive for researchers to find sustainable solutions to sustain food security for the ever-increasing world population. Bio-fertilizers based on bacteria and fungi able to solubilize endogenous P in soils have a high potential for increasing nutrient availability in agriculture. However, the inconsistency of bio-fertilizer performance in the field poses a major challenge for farmers. This discrepancy is thought to stem from the complexity of the interactions between crop plants, microbes, and their soil environments, as well as our lack of understanding of the processes involved. For farmers, a clear beneficial effect across different soil types, crop species, environmental conditions, and microbial communities will be required to make it worth to adopt bio-fertilizer technology based on phosphate-solubilizing microbes (PSMs). Here, we attempt to review the current knowledge of the complexity of the P-solubilization mechanisms used by PSMs and how they may be affected by interactions in the field. We also identify possible explanations for the inconsistent performance of P-solubilizing bacteria in the field and ways to solve these obstacles.



The authors would like to thank KAUST for their financial support, Florian Mette for his highly useful comments, the members of the Center for Desert Agriculture, and the Hirt’s lab group members for their support and fruitful discussion.


  1. Adesemoye AO, Kloepper JW (2009) Plant–microbes interactions in enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol 85(1):1–12. doi: 10.1007/s00253-009-2196-0 CrossRefPubMedGoogle Scholar
  2. 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):1–10CrossRefPubMedGoogle Scholar
  3. Azcón R (1989) Selective interaction between free-living rhizosphere bacteria and vesicular arbuscular mycorrhizal fungi. Soil Biol Biochem 21(5):639–644CrossRefGoogle Scholar
  4. Azcon R, Barea J, Hayman D (1976) Utilization of rock phosphate in alkaline soils by plants inoculated with mycorrhizal fungi and phosphate-solubilizing bacteria. Soil Biol Biochem 8(2):135–138CrossRefGoogle Scholar
  5. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32(6):666–681CrossRefPubMedGoogle Scholar
  6. Bago B, Pfeffer PE, Abubaker J et al (2003) Carbon export from arbuscular mycorrhizal roots involves the translocation of carbohydrate as well as lipid. Plant Physiol 131(3):1496–1507CrossRefPubMedPubMedCentralGoogle Scholar
  7. Barea JM, Azcón R, Azcón-Aguilar C (2005) Interactions between mycorrhizal fungi and bacteria to improve plant nutrient cycling and soil structure. In: Buscot F, Varma A (eds) Microorganisms in soils: roles in genesis and functions, vol 3. Springer, Berlin, pp 195–212CrossRefGoogle Scholar
  8. Barea J, Toro M, Azcón R (2007) The use of 32P isotopic dilution techniques to evaluate the interactive effects of phosphate-solubilizing bacteria and mycorrhizal fungi at increasing plant P availability. In: Velazquez E, Rodriguez-Barrueco C (eds) First international meeting on microbial phosphate solubilization, vol 102. Springer, Dordrecht, pp 223–227CrossRefGoogle Scholar
  9. Bashan Y, Kamnev AA, de-Bashan LE (2013) 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(4):465–479. doi: 10.1007/s00374-012-0737-7 CrossRefGoogle Scholar
  10. Bieleski R (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol 24(1):225–252CrossRefGoogle Scholar
  11. de Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29(4):795–811CrossRefPubMedGoogle Scholar
  12. de Zelicourt A, Al-Yousif M, Hirt H (2013) Rhizosphere microbes as essential partners for plant stress tolerance. Mol Plant 6(2):242–245CrossRefPubMedGoogle Scholar
  13. Bonfante P, Anca I-A (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol 63:363–383CrossRefPubMedGoogle Scholar
  14. Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat Commun 1:48CrossRefPubMedGoogle Scholar
  15. Brunner I, Goren A, Schlumpf A (2014) Patterns of organic acids exuded by pioneering fungi from a glacier forefield are affected by carbohydrate sources. Environ Res Lett 9(2):025002CrossRefGoogle Scholar
  16. Carvalhais LC, Dennis PG, Fedoseyenko D et al (2011) Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency. J Plant Nut Soil Sci/Z Pflanzenernähr Bodenkd 174(1):3CrossRefGoogle Scholar
  17. Chen XW, Wu FY, Li H et al (2013) Phosphate transporters expression in rice (Oryza sativa L.) associated with arbuscular mycorrhizal fungi (AMF) colonization under different levels of arsenate stress. Environ Exp Bot 87:92–99. doi:
  18. 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(3):281–293. doi: 10.1046/j.1365-313x.2001.00963.x CrossRefPubMedGoogle Scholar
  19. Cordell D, White S (2015) Tracking phosphorus security: indicators of phosphorus vulnerability in the global food system. Food Sec 7(2):337–350CrossRefGoogle Scholar
  20. Crowley DE, Kraemer SM (2007) Function of siderophores in the plant rhizosphere. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil–plant interface, 2nd edn. CRC, Boca Raton, pp 173–200CrossRefGoogle Scholar
  21. Deveau A, Palin B, Delaruelle C et al (2007) The mycorrhiza helper Pseudomonas fluorescens BBc6R8 has a specific priming effect on the growth, morphology and gene expression of the ectomycorrhizal fungus Laccaria bicolor S238N. New Phytol 175(4):743–755CrossRefPubMedGoogle Scholar
  22. Downie JA (2014) Legume nodulation. Curr Biol 24(5):R184–R190CrossRefPubMedGoogle Scholar
  23. Duca M (2015) Mineral nutrition of plants. In: Mohr H, Schopfer P (eds) Plant physiology. Springer, Berlin, pp 149–185CrossRefGoogle Scholar
  24. Duponnois R, Garbaye J (1991) Mycorrhization helper bacteria associated with the Douglas fir-Laccaria laccata symbiosis: effects in aseptic and in glasshouse conditions. Ann Sci For 3:239–251CrossRefGoogle Scholar
  25. Eivazi F, Tabatabai M (1977) Phosphatases in soils. Soil Biol Biochem 9(3):167–172CrossRefGoogle Scholar
  26. Filius JD, Hiemstra T, Van Riemsdijk WH (1997) Adsorption of small weak organic acids on goethite: modeling of mechanisms. J Colloid Interface Sci 195(2):368–380CrossRefPubMedGoogle Scholar
  27. Gao LL, Delp G, Smith SE (2001) Colonization patterns in a mycorrhiza-defective mutant tomato vary with different arbuscular-mycorrhizal fungi. New Phytol 151(2):477–491. doi: 10.1046/j.0028-646x.2001.00193.x CrossRefGoogle Scholar
  28. Geurts R, Lillo A, Bisseling T (2012) Exploiting an ancient signalling machinery to enjoy a nitrogen fixing symbiosis. Curr Opin Plant Biol 15(4):438–443CrossRefPubMedGoogle Scholar
  29. Glassop D, Godwin RM, Smith SE, Smith FW (2007) Rice phosphate transporters associated with phosphate uptake in rice roots colonised with arbuscular mycorrhizal fungi. Can J Bot 85(7):644–651. doi: 10.1139/B07-070 CrossRefGoogle Scholar
  30. Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169(1):30–39CrossRefPubMedGoogle Scholar
  31. Glick BR (2015) Beneficial plant-bacterial interactions. Springer, ChamCrossRefGoogle Scholar
  32. Goldstein AH (1994) Involvement of the quinoprotein glucose dehydrogenase in the solubilization of exogenous phosphates by gram-negative bacteria. In: Torriani-Gorini A, Yagil E, Silver S (eds) Phosphate in microorganisms: cellular and molecular biology. ASM Press, Washington, DC, pp 197–203Google Scholar
  33. Grierson P, Comerford N, Jokela E (1998) Phosphorus mineralization kinetics and response of microbial phosphorus to drying and rewetting in a Florida Spodosol. Soil Biol Biochem 30(10):1323–1331CrossRefGoogle Scholar
  34. Gutiérrez-Luna FM, López-Bucio J, Altamirano-Hernández J et al (2010) Plant growth-promoting rhizobacteria modulate root-system architecture in Arabidopsis thaliana through volatile organic compound emission. Symbiosis 51(1):75–83CrossRefGoogle Scholar
  35. Hodge A, Helgason T, Fitter A (2010) Nutritional ecology of arbuscular mycorrhizal fungi. Fungal Ecol 3(4):267–273CrossRefGoogle Scholar
  36. Johnson JF, Allan DL, Vance CP (1994) Phosphorus stress-induced proteoid roots show altered metabolism in Lupinus albus. Plant Physiol 104(2):657–665CrossRefPubMedPubMedCentralGoogle Scholar
  37. Jones DL, Oburger E (2011) Solubilization of phosphorus by soil microorganisms. In: Bunemann E, Oberson A, Frossard E (eds) Phosphorus in action, vol 26. Springer, Berlin, pp 169–198CrossRefGoogle Scholar
  38. Kamilova F, Kravchenko LV, Shaposhnikov AI, Makarova N, Lugtenberg B (2006) Effects of the tomato pathogen Fusarium oxysporum f. sp. radicis-lycopersici and of the biocontrol bacterium Pseudomonas fluorescens WCS365 on the composition of organic acids and sugars in tomato root exudate. Mol Plant Microbe Interact 19(10):1121–1126. doi: 10.1094/MPMI-19-1121 CrossRefPubMedGoogle Scholar
  39. Khan MS, Zaidi A, Ahemad M, Oves M, Wani PA (2010) Plant growth promotion by phosphate solubilizing fungi–current perspective. Arch Agron Soil Sci 56(1):73–98CrossRefGoogle Scholar
  40. Khan M, Ahmad E, Zaidi A, Oves M (2013) Functional aspect of phosphate-solubilizing bacteria: importance in crop production. In: Maheshwari DK, Saraf M, Aeron A (eds) Bacteria in agrobiology: crop productivity. Springer, Berlin/Heidelberg. doi: 10.1007/978-3-642-37241-4_10 Google Scholar
  41. Khan MS, Zaidi A, Ahmad E (2014) Mechanism of phosphate solubilization and physiological functions of phosphate-solubilizing microorganisms. In: Khan MS, Zaidi A, Musarrat J (eds) Phosphate solubilizing microorganisms. Springer, Cham, pp 31–62. doi: 10.1007/978-3-319-08216-5_2 Google Scholar
  42. Kim K, Jordan D, McDonald G (1997) Effect of phosphate-solubilizing bacteria and vesicular-arbuscular mycorrhizae on tomato growth and soil microbial activity. Biol Fertil Soils 26(2):79–87CrossRefGoogle Scholar
  43. Kim KY, Jordan D, McDonald G (1998) Enterobacter agglomerans, phosphate solubilizing bacteria, and microbial activity in soil: effect of carbon sources. Soil Biol Biochem 30(8):995–1003CrossRefGoogle Scholar
  44. Kohler J, Caravaca F, Carrasco L, Roldan A (2007) Interactions between a plant growth-promoting rhizobacterium, an AM fungus and a phosphate-solubilising fungus in the rhizosphere of Lactuca sativa. Appl Soil Ecol 35(3):480–487CrossRefGoogle Scholar
  45. Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann Bot 98(4):693–713CrossRefPubMedPubMedCentralGoogle Scholar
  46. Leprince F, Quiquampoix H (1996) Extracellular enzyme activity in soil: effect of pH and ionic strength on the interaction with montmorillonite of two acid phosphatases secreted by the ectomycorrhizal fungus Hebeloma cylindrosporum. Eur J Soil Sci 47(4):511–522. doi: 10.1111/j.1365-2389.1996.tb01851.x CrossRefGoogle Scholar
  47. Liang C, Wang J, Zhao J, Tian J, Liao H (2014) Control of phosphate homeostasis through gene regulation in crops. Curr Opin Plant Biol 21:59–66CrossRefPubMedGoogle Scholar
  48. Lim BL, Yeung P, Cheng C, Hill JE (2007) Distribution and diversity of phytate-mineralizing bacteria. ISME J 1(4):321–330PubMedGoogle Scholar
  49. Lipton DS, Blanchar RW, Blevins DG (1987) Citrate, malate, and succinate concentration in exudates from P-sufficient and P-stressed Medicago sativa L. seedlings. Plant Physiol 85(2):315–317CrossRefPubMedPubMedCentralGoogle Scholar
  50. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556CrossRefPubMedGoogle Scholar
  51. Maougal R, Brauman A, Plassard C, Abadie J, Djekoun A, Drevon J-J (2014) Bacterial capacities to mineralize phytate increase in the rhizosphere of nodulated common bean (Phaseolus vulgaris) under P deficiency. Eur J Soil Biol 62:8–14CrossRefGoogle Scholar
  52. Mardad I, Serrano A, Soukri A (2013) Solubilization of inorganic phosphate and production of organic acids by bacteria isolated from a Moroccan mineral phosphate deposit. Afr J Microbiol Res 7:626–635Google Scholar
  53. Marques JM, da Silva TF, Vollu RE et al (2014) Plant age and genotype affect the bacterial community composition in the tuber rhizosphere of field-grown sweet potato plants. FEMS Microbiol Ecol 88(2):424–435. doi: 10.1111/1574-6941.12313 CrossRefPubMedGoogle Scholar
  54. Medveczky N, Rosenberg H (1971) Phosphate transport in Escherichia coli. Biochim Biophys Acta Biomembr 241(2):494–506CrossRefGoogle Scholar
  55. Meena KK, Mesapogu S, Kumar M et al (2010) Co-inoculation of the endophytic fungus Piriformospora indica with the phosphate-solubilising bacterium Pseudomonas striata affects population dynamics and plant growth in chickpea. Biol Fertil Soils 46(2):169–174CrossRefGoogle Scholar
  56. Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bunemann E, Oberson A, Frossard E (eds) Phosphorus in action, vol 26. Springer, Heidelberg, pp 215–243CrossRefGoogle Scholar
  57. Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170(1):265–270CrossRefPubMedGoogle Scholar
  58. Naves LP, Corrêa A, Bertechini A, Gomide E, Cd S (2012) Effect of pH and temperature on the activity of phytase products used in broiler nutrition. Rev Bras Ciências Avícola 14:181–185CrossRefGoogle Scholar
  59. Nesme T, Colomb B, Hinsinger P, Watson CA (2014) Soil phosphorus management in organic cropping systems: from current practices to avenues for a more efficient use of P resources. In: Bellon S, Penvern S (eds) Organic farming, prototype for sustainable agriculture. Springer, Dordrecht, pp 23–45CrossRefGoogle Scholar
  60. Neumann G, Römheld V (2007) The release of root exudates as affected by the plant physiological status. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface, 2nd edn. CRC, Boca Ratoon, pp 23–72CrossRefGoogle Scholar
  61. Nguyen C (2003) Rhizodeposition of organic C by plants: mechanisms and controls. Agron Sci Prod Veg Environ 23(5–6):375–396Google Scholar
  62. Oberson A, Joner EJ, Turner B, Frossard E, Baldwin D (2005) Microbial turnover of phosphorus in soil. In: Turner BL, Frossard E, Baldwin DS (eds) Organic phosphorus in the environment. CABI publishers, Wallingford, pp 133–164CrossRefGoogle Scholar
  63. Osman KT (2012) Soils: principles, properties and management. Springer Science & Business Media, ChittagongGoogle Scholar
  64. Park KH, Lee CY, Son HJ (2009) Mechanism of insoluble phosphate solubilization by Pseudomonas fluorescens RAF15 isolated from ginseng rhizosphere and its plant growth-promoting activities. Lett Appl Microbiol 49(2):222–228CrossRefPubMedGoogle Scholar
  65. Péret B, Desnos T, Jost R, Kanno S, Berkowitz O, Nussaume L (2014) Root architecture responses: in search of phosphate. Plant Physiol 166(4):1713–1723CrossRefPubMedPubMedCentralGoogle Scholar
  66. Peters NK, Frost JW, Long SR (1986) A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233(4767):977–980CrossRefPubMedGoogle Scholar
  67. Pikovskaya R (1948) Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Mikrobiologiya 17(362):e370Google Scholar
  68. Rashid M, Khalil S, Ayub N, Alam S, Latif F (2004) Organic acids production and phosphate solubilization by phosphate solubilizing microorganisms (PSM) under in vitro conditions. Pak J Biol Sci 7(2):187–196CrossRefGoogle Scholar
  69. Requena N, Jimenez I, Toro M, Barea J (1997) Interactions between plant-growth-promoting rhizobacteria (PGPR), arbuscular mycorrhizal fungi and Rhizobium spp. in the rhizosphere of Anthyllis cytisoides, a model legume for revegetation in mediterranean semi-arid ecosystems. New Phytol 136(4):667–677CrossRefGoogle Scholar
  70. Rudrappa T, Czymmek KJ, Paré PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148(3):1547–1556CrossRefPubMedPubMedCentralGoogle Scholar
  71. Saxena J, Jha A (2014) Impact of a phosphate solubilizing bacterium and an arbuscular mycorrhizal fungus (Glomus etunicatum) on growth, yield and P concentration in wheat plants. Clean Soil Air Water 42(9):1248–1252CrossRefGoogle Scholar
  72. Scervino JM, Papinutti VL, Godoy MS et al (2011) Medium pH, carbon and nitrogen concentrations modulate the phosphate solubilization efficiency of Penicillium purpurogenum through organic acid production. J Appl Microbiol 110(5):1215–1223. doi: 10.1111/j.1365-2672.2011.04972.x CrossRefPubMedGoogle Scholar
  73. Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116(2):447–453CrossRefPubMedPubMedCentralGoogle Scholar
  74. Shahab S, Ahmed N, Khan NS (2009) Indole acetic acid production and enhanced plant growth promotion by indigenous PSBs. Afr J Agric Res 4(11):1312–1316Google Scholar
  75. Sharma SB, Sayyed RZ, Trivedi MH, Gobi TA (2013) Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. Springer Plus 2:587CrossRefPubMedPubMedCentralGoogle Scholar
  76. Smith SE, Facelli E, Pope S, Andrew Smith F (2010) Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant Soil 326(1):3–20. doi: 10.1007/s11104-009-9981-5 CrossRefGoogle Scholar
  77. 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(3):1050–1057CrossRefPubMedPubMedCentralGoogle Scholar
  78. Steinkellner S, Lendzemo V, Langer I et al (2007) Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 12(7):1290–1306CrossRefPubMedGoogle Scholar
  79. Sukumar P, Legue V, Vayssieres A, Martin F, Tuskan GA, Kalluri UC (2013) Involvement of auxin pathways in modulating root architecture during beneficial plant–microorganism interactions. Plant Cell Environ 36(5):909–919CrossRefPubMedGoogle Scholar
  80. Suri V, Choudhary AK, Chander G, Verma T, Gupta M, Dutt N (2011) Improving phosphorus use through co-inoculation of vesicular arbuscular mycorrhizal fungi and phosphate-solubilizing bacteria in maize in an acidic Alfisol. Commun Soil Sci Plant Anal 42(18):2265–2273CrossRefGoogle Scholar
  81. Tian J, Wang X, Tong Y, Chen X, Liao H (2012) Bioengineering and management for efficient phosphorus utilization in crops and pastures. Curr Opin Biotechnol 23 (6):866–871. doi:
  82. Turner BL, McKelvie ID, Haygarth PM (2002) Characterisation of water-extractable soil organic phosphorus by phosphatase hydrolysis. Soil Biol Biochem 34(1):27–35CrossRefGoogle Scholar
  83. Uren NC (2007) Types, amounts, and possible functions of compounds released into the rhizosphere by soil-grown plants. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere biochemistry and organic substances at the soil-plant interface, 2nd edn. CRC Press, Boca Raton, pp 1–21Google Scholar
  84. Vacheron J, Desbrosses G, Bouffaud M-L et al (2013) Plant growth-promoting rhizobacteria and root system functioning. Front Plant Sci 4:356. doi: 10.3389/fpls.2013.00356 CrossRefPubMedPubMedCentralGoogle Scholar
  85. Van Vuuren DP, Bouwman A, Beusen A (2010) Phosphorus demand for the 1970–2100 period: a scenario analysis of resource depletion. Glob Environ Chang 20(3):428–439CrossRefGoogle Scholar
  86. Van Wees SC, Van der Ent S, Pieterse CM (2008) Plant immune responses triggered by beneficial microbes. Curr Opin Plant Biol 11(4):443–448CrossRefPubMedGoogle Scholar
  87. Verbon EH, Liberman LM (2016) Beneficial microbes affect endogenous mechanisms controlling root development. Trends Plant Sci 21(3):218–229CrossRefPubMedPubMedCentralGoogle Scholar
  88. Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13(2):87–115CrossRefGoogle Scholar
  89. Vyas P, Gulati A (2009) Organic acid production in vitro and plant growth promotion in maize under controlled environment by phosphate-solubilizing fluorescent Pseudomonas. BMC Microbiol 9:174. doi: 10.1186/1471-2180-9-174 CrossRefPubMedPubMedCentralGoogle Scholar
  90. Weller DM, Thomashow LS (1994) Current challenges in introducing beneficial microorganisms into the rhizosphere. In: O’Gara F, Dowling DN, Boesten B (eds) Molecular ecology of rhizosphere microorganisms: biotechnology and the release of GMOs. VCH, Weinheim, pp p1–18Google Scholar
  91. Wu S, Cao Z, Li Z, Cheung K, Wong M (2005) Effects of biofertilizer containing N-fixer, P and K solubilizers and AM fungi on maize growth: a greenhouse trial. Geoderma 125(1):155–166CrossRefGoogle Scholar
  92. Yang J, Kloepper JW, Ryu C-M (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14(1):1–4CrossRefPubMedGoogle Scholar
  93. Yarzábal L (2010) Agricultural development in tropical acidic soils: potential and limits of phosphate-solubilizing bacteria. In: Dion P (ed) Soil biology and agriculture in the tropics, Soil biology, vol 21. Springer, Berlin/Heidelberg, pp 209–233. doi: 10.1007/978-3-642-05076-3_10 CrossRefGoogle Scholar
  94. Yi Y, Huang W, Ge Y (2008) Exopolysaccharide: a novel important factor in the microbial dissolution of tricalcium phosphate. World J Microbiol Biotechnol 24(7):1059–1065. doi: 10.1007/s11274-007-9575-4 CrossRefGoogle Scholar
  95. Yoneyama K, Yoneyama K, Takeuchi Y, Sekimoto H (2007) Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta 225(4):1031–1038CrossRefPubMedGoogle Scholar
  96. Zaidi A, Khan MS (2006) Co-inoculation effects of phosphate solubilizing microorganisms and Glomus fasciculatum on green gram-Bradyrhizobium symbiosis. Turk J Agri Forest 30(3):223–230Google Scholar
  97. Zarei M, Saleh-Rastin N, Alikhani HA, Aliasgharzadeh N (2006) Responses of lentil to co-inoculation with phosphate-solubilizing rhizobial strains and arbuscular mycorrhizal fungi. J Plant Nutr 29(8):1509–1522CrossRefGoogle Scholar
  98. Zhang L, Fan J, Ding X, He X, Zhang F, Feng G (2014a) Hyphosphere interactions between an arbuscular mycorrhizal fungus and a phosphate solubilizing bacterium promote phytate mineralization in soil. Soil Biol Biochem 74:177–183CrossRefGoogle Scholar
  99. Zhang Z, Liao H, Lucas WJ (2014b) Molecular mechanisms underlying phosphate sensing, signaling, and adaptation in plants. J Integr Plant Biol 56(3):192–220CrossRefPubMedGoogle Scholar
  100. Zhang L, Xu M, Liu Y, Zhang F, Hodge A, Feng G (2016) Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate-solubilizing bacterium. New Phytol 210(3):1022–1032. doi: 10.1111/nph.13838 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  • Abdul Aziz Eida
    • 1
  • Heribert Hirt
    • 1
    Email author
  • Maged M. Saad
    • 1
  1. 1.Center for Desert Agriculture4700 King Abdullah University of Science and Technology (KAUST)ThuwalKingdom of Saudi Arabia

Personalised recommendations