Phosphorus Nutrition: Plant Growth in Response to Deficiency and Excess

  • Hina Malhotra
  • Vandana
  • Sandeep Sharma
  • Renu Pandey


Phosphorus (P) is an essential element determining plants’ growth and productivity. Due to soil fixation of P, its availability in soil is rarely sufficient for optimum growth and development of plants. The uptake of P from soil followed by its long-distance transport and compartmentation in plants is outlined in this chapter. In addition, we briefly discuss the importance of P as a structural component of nucleic acids, sugars and lipids. Furthermore, the role of P in plant’s developmental processes at both cellular and whole plant level, viz. seed germination, seedling establishment, root, shoot, flower and seed development, photosynthesis, respiration and nitrogen fixation, has been discussed. Under P-deficient condition, plants undergo various morphological, physiological and biochemical adaptations, while P toxicity is rarely reported. We also summarize the antagonistic and synergistic interaction of P with other macro- and micronutrients.


Abiotic stress Macronutrients Nutrient deficiencies Plant metabolism Soil fertility 


  1. Assuero SG, Mollier A, Pellerin S (2004) The decrease in growth of phosphorus-deficient maize leaves is related to a lower cell production. Plant Cell Environ 27:887–895CrossRefGoogle Scholar
  2. Aulakh MS, Pasricha NS (1977) Interaction effect of sulphur and phosphorus on growth and nutrient content of moong (Phaseolus aureus L.) Plant Soil 47:341–350CrossRefGoogle Scholar
  3. Aung K, Lin SI, Wu CC, Huang YT, Su CL, Chiou TJ (2006) Pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol 141:1000–1011CrossRefPubMedPubMedCentralGoogle Scholar
  4. Baldwin JC, Athikkattuvalasu SK, Raghothama KG (2001) LEPS2, a phosphorus starvation-induced novel acid phosphatase from tomato. Plant Physiol 125:728–737CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bayle V, Arrighi JF, Creff A, Nespoulous C, Vialaret J, Rossignol M, Gonzalez E, Paz-Ares J, Nussaume L (2011) Arabidopsis thaliana high affinity phosphate transporters exhibit multiple levels of posttranslational regulation. Plant Cell 23:1523–1535CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bhagwat AS (1981) Activation of spinach ribulose 1,5-bisphosphate carboxylase by inorganic phosphate. Plant Sci Lett 23:197–206CrossRefGoogle Scholar
  7. Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol 24:225–252CrossRefGoogle Scholar
  8. Bonetti R, Montanheiro M, Saito S (1984) The effects of phosphate and soil moisture on the nodulation and growth of Phaseolus vulgaris. J Agric Sci 103:95–102CrossRefGoogle Scholar
  9. Byrne SL, Foito A, Hedley PE, Morris JA, Stewart D, Barth S (2011) Early response mechanisms of perennial ryegrass (Lolium perenne) to phosphorus deficiency. Ann Bot 107:243–254CrossRefPubMedPubMedCentralGoogle Scholar
  10. Charlton WA (1996) Lateral root initiation. In: Waisel Y, Eshel A, Kfkafa U (eds) Plant roots: the hidden half, 2nd edn. Marcel Dekker, New York, pp 149–173Google Scholar
  11. Chatterjee C, Sinha P, Agarwala SC (1990) Interactive effect of boron and phosphorus on growth and metabolism of maize grown in refined sand. Can J Plant Sci 70:455–460CrossRefGoogle Scholar
  12. Chen YP, Rekha PD, Arun AB, Shen FT, Lai WA, Young CC (2006) Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl Soil Ecol 34:33–41CrossRefGoogle Scholar
  13. Chen R, Song S, Li X, Liu H, Huang D (2013) Phosphorus deficiency restricts plant growth but induces pigment formation in the flower stalk of Chinese kale. Hortic Environ Biotechnol 54:243–248CrossRefGoogle Scholar
  14. Chowdhury SZ, Sobahan MA, Shamim AHM, Akter N, Hossain MM (2015) Interaction effect of phosphorus and boron on yield and quality of lettuce. Azarian J Agric 2:147–154Google Scholar
  15. Comerford NB (1998) Soil phosphorus bioavailability. In: Lynch JP, Deikman J (eds) Phosphorus in plant biology: regulatory roles in molecular, cellular, organismic, and ecosystem processes. American Society of Plant Physiologists, Rockville, pp 136–147Google Scholar
  16. Correll DL (1998) The role of phosphorus in the eutrophication of receiving waters: a review. J Environ Qual 27:261–266CrossRefGoogle Scholar
  17. De Iorio AF, Gorgoschide L, Rendina A, Barros MJ (1996) Effect of phosphorus, copper, and zinc addition on the phosphorus/copper and phosphorus/zinc interaction in lettuce. J Plant Nutr 19:481–491CrossRefGoogle Scholar
  18. Devaiah B, Karthikeyan AS, Raghothama KG (2007) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143:1789–1801CrossRefPubMedPubMedCentralGoogle Scholar
  19. Dong B, Rengel Z, Delhaize E (1998) Uptake and translocation of phosphate by pho2 mutant and wild-type seedlings of Arabidopsis thaliana. Planta 205:251–256CrossRefPubMedGoogle Scholar
  20. Drissi S, Houssa AA, Bamouh A, Coquant JM, Benbella M (2015) Effect of zinc-phosphorus interaction on corn silage grown on sandy soil. Agriculture 5:1047–1059CrossRefGoogle Scholar
  21. Duff SMG, Lefebvre DD, Plaxton WC (1989) Purification and characterization of a phosphoenolpyruvate phosphatase from Brassica nigra suspension cells. Plant Physiol 90:734–741CrossRefPubMedPubMedCentralGoogle Scholar
  22. Duff SM, Plaxton WC, Lefebvre DD (1991) Phosphate-starvation response in plant cells: de novo synthesis and degradation of acid phosphatases. PNAS, USA 88:9538–9542CrossRefGoogle Scholar
  23. Duff SMG, Sarath G, Plaxton WC (1994) The role of acid phosphatases in plant phosphorus metabolism. Physiol Plant 90:791–800CrossRefGoogle Scholar
  24. Elser JJ, Fagan WF, Kerkhoff AJ, Swenson NG, Enquist BJ (2010) Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change. New Phytol 186:593–608CrossRefGoogle Scholar
  25. Flugge UI, Heldt HW (1984) The phosphate-triose phosphate-phosphoglycerate translocator of the chloroplast. Trends Biochem Sci 9:530–533CrossRefGoogle Scholar
  26. 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
  27. Gaude N, Nakamura Y, Scheible WR, Ohta H, Dormann P (2008) Phospholipase C5 (NPC5) is involved in galactolipid accumulation during phosphate limitation in leaves of Arabidopsis. Plant J 56:28–39CrossRefPubMedGoogle Scholar
  28. Ge Z, Rubio G, Lynch JP (2000) The importance of root gravitropism for inter-root competition and phosphorus acquisition efficiency: results from a geometric simulation model. Plant Soil 218:159–171CrossRefPubMedGoogle Scholar
  29. George TS, Richardson AE, Simpson RJ (2005) Behaviour of plant derived extracellular phytase upon addition to soil. Soil Biol Biochem 37:977–988CrossRefGoogle Scholar
  30. Gniazdowska A, Mikulska M, Rychter AM (1998) Growth, nitrate uptake and respiration rate in bean roots under phosphate deficiency. Biol Plant 41:217–226CrossRefGoogle Scholar
  31. Goldstein AH, Baertlein DA, McDaniel RG (1988) Phosphate starvation inducible metabolism in Lycopersicon esculentum. I. Excretion of acid phosphatase by tomato plants and suspension-cultured cells. Plant Physiol 87:711–715CrossRefPubMedPubMedCentralGoogle Scholar
  32. Guo FQ, Wand R, Crawford NM (2002) The Arabidopsis dual-affinity nitrate transporter gene AtNTR1.1 (CHL1) is regulated by auxin in both shoots and roots. J Exp Bot 53:835–844CrossRefPubMedPubMedCentralGoogle Scholar
  33. Halsted M, Lynch J (1996) Phosphorus responses of C-3 and C-4 species. J Exp Bot 47:497–505CrossRefGoogle Scholar
  34. Hasan MM, Hasan MM, da Silva JAT, Li X (2016) Regulation of phosphorus uptake and utilization: transitioning from current knowledge to practical strategies. Cell Mol Biol Lett 21:1–19CrossRefGoogle Scholar
  35. Heber U, Heldt HW (1981) The chloroplast envelope: structure, function, and role in leaf metabolism. Annu Rev Plant Physiol 32:139–168CrossRefGoogle Scholar
  36. Heldt HW, Chon CJ, Lorimer H (1978) Phosphate requirement for the light activation of ribulose-1,5-biphosphate carboxylase in intact spinach chloroplasts. FEBS Lett 92:234–240CrossRefGoogle Scholar
  37. Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195CrossRefGoogle Scholar
  38. Hinsinger P, Gobran GR, Gregory PJ, Wenzel WW (2005) Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes. New Phytol 168:293–303CrossRefPubMedGoogle Scholar
  39. Horton P (1989) Interactions between electron transport and carbon assimilation: regulation of light harvesting. In: Briggs WR (ed) Photosynthesis, vol 8. Alan R Liss, New York, pp 393–406Google Scholar
  40. Huang C, Barker SJ, Langridge P, Smith FW, Graham RD (2000) Zinc deficiency up-regulates expression of high-affinity phosphate transporter genes in both phosphate-sufficient and -deficient barley roots. Plant Physiol 124:415–422CrossRefPubMedPubMedCentralGoogle Scholar
  41. Huang CY, Shirley N, Genc Y, Shi B, Langridge P (2011) Phosphate utilization efficiency correlates with expression of low-affinity phosphate transporters and noncoding RNA, IPS1, in barley. Plant Physiol 156:1217–1229CrossRefPubMedPubMedCentralGoogle Scholar
  42. Huber SC, Huber JL (1992) Role of sucrose-phosphate synthase in sucrose metabolism in leaves. Plant Physiol 99:1275–1278CrossRefPubMedPubMedCentralGoogle Scholar
  43. Huber SC, Huber JL (1996) Role and regulation of sucrose phosphate synthase in higher plants. Annu Rev Plant Physiol Plant Mol Biol 47:431–444CrossRefPubMedPubMedCentralGoogle Scholar
  44. Jahn T, Baluska F, Michalke W, Harper JF, Volkmann D (1998) A membrane H+-ATPase in the root apex: evidence for strong expression in xylem parenchyma and asymmetric localization within cortical and epidermal cells. Physiol Plant 104:311–316CrossRefGoogle Scholar
  45. Jakobsen I (1985) The role of phosphorus in nitrogen fixation by young pea plants (Pisum sativum). Plant Physiol 64:190–196CrossRefGoogle Scholar
  46. Jones DL, Oburger E (2011) Solubilization of phosphorus by soil microorganism. In: Buenemann EK, Oberson A, Frossard E (eds) Phosphorus in action. Springer, New York, pp 169–198CrossRefGoogle Scholar
  47. Jungk A (2001) Root hairs and acquisition of plant nutrients from soil. J Plant Nutr Soil Sci 164:121–129CrossRefGoogle Scholar
  48. Lal MK (2015) Effect of high [CO2] on phosphorus efficiency in wheat grown under phosphorus stress with different sulphur levels. Dissertation, Indian Agricultural Research InstituteGoogle Scholar
  49. Liao H, Rubio G, Yan X, Cao A, Brown KM, Lynch JP (2001) Effect of phosphorus availability on basal root shallowness in common bean. Plant Soil 232:69–79CrossRefPubMedPubMedCentralGoogle Scholar
  50. Lin WY, Huang TK, Leong SJ, Chiou TJ (2014) Long-distance call from phosphate: systemic regulation of phosphate starvation responses. J Exp Bot 65:1817–1827CrossRefPubMedPubMedCentralGoogle Scholar
  51. Liu F, Wang Z, Ren H, Shen C, Li Y, Ling HQ, Wu C, Lian X, Wu P (2010a) OsSPX1 suppresses the function of OsPHR2 in the regulation of expression of OsPT2 and phosphate homeostasis in shoots of rice. Plant J 62:508–517CrossRefPubMedPubMedCentralGoogle Scholar
  52. Liu H, Hu C, Hu X, Nie Z, Sun X, Tan Q, Hu H (2010b) Interaction of molybdenum and phosphorus supply on uptake and translocation of phosphorus and molybdenum by Brassica napus. J Plant Nutr 33:1751–1760CrossRefGoogle Scholar
  53. Liu XM, Zhao XL, Zhang LJ, Xiao K (2013) TaPht1;4, a high-affinity phosphate transporter gene in wheat (Triticum aestivum L.), plays an important role in plant phosphate acquisition under phosphorus deprivation. Funct Plant Biol 40:329–341CrossRefGoogle Scholar
  54. Lynch JP, Brown KM (2001) Topsoil foraging–an architectural adaptation of plants to low phosphorus. Plant Soil 237:225–237CrossRefGoogle Scholar
  55. Ma Q, Longnecker N, Atkins C (2002) Varying phosphorus supply and development, growth and seed yield in narrow-leafed lupin. Plant Soil 239:79–85CrossRefGoogle Scholar
  56. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, London, p 889Google Scholar
  57. Miao J, Sun J, Liu D, Li B, Zhang A, Li Z, Tong Y (2009) Characterization of the promoter of phosphate transporter TaPHT1.2 differentially expressed in wheat varieties. J Genet Genomics 36:455–466CrossRefPubMedPubMedCentralGoogle Scholar
  58. Miller SS, Liu J, Allan DL, Menzhuber CJ, Fedorova M, Vance CP (2001) Molecular control of acid phosphatase secretion into the rhizosphere of proteoid roots from phosphorus-stressed white lupin. Plant Physiol 127:594–606CrossRefPubMedPubMedCentralGoogle Scholar
  59. Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, Baek D, Koo YD, Jin JB, Bressan RA, Yun DJ, Hasegawa PM (2005) The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. PNAS, USA 102:7760–7765CrossRefGoogle Scholar
  60. Nacry P, Canivenc G, Muller B (2005) A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiol 138:2061–2074CrossRefPubMedPubMedCentralGoogle Scholar
  61. Nadeem M, Mollier A, Morel C, Vives A, Prud'homme L, Pellerin S (2011) Relative contribution of seed phosphorus reserves and exogenous phosphorus uptake to maize (Zea mays L.) nutrition during early growth stages. Plant Soil 346:231–244CrossRefGoogle Scholar
  62. Nadeem M, Mollier A, Morel C, Vives A, Prud'homme L, Pellerin S (2012) Seed phosphorus remobilization is not a major limiting step for phosphorus nutrition during early growth of maize. J Plant Nutr Soil Sci 175:805–809CrossRefGoogle Scholar
  63. Nakamura Y (2013) Phosphate starvation and membrane lipid remodeling in seed plants. Prog Lipid Res 52:43–50CrossRefPubMedPubMedCentralGoogle Scholar
  64. Nakamura Y, Koizumi R, Shui G, Shimojima M, Wenk MR, Ito T, Ohta H (2009) Arabidopsis lipins mediate eukaryotic pathway of lipid metabolism and cope critically with phosphate starvation. PNAS, USA 106:20978–20983CrossRefGoogle Scholar
  65. Neumann G, Römheld V (2002) Root-induced changes in the availability of nutrients in the rhizosphere. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots, the hidden half, 3rd edn. Marcel Dekker, New York, pp 617–649CrossRefGoogle Scholar
  66. Neumann G, Massonneau A, Martinoia E, Romheld V (1999) Physiological adaptations to phosphorus deficiency during proteoid root development in white lupin. Planta 208:373–382CrossRefGoogle Scholar
  67. Nielsen TH, Krapp A, Roper-Schwarz U, Stitt M (1998) The sugar-mediated regulation of genes encoding the small subunit of Rubisco and the regulatory subunit of ADP glucose pyrophosphorylase is modified by phosphate and nitrogen. Plant Cell Environ 21:443–454CrossRefGoogle Scholar
  68. Parets-Soler A, Pardo JM, Serrano R (1990) Immunocytolocalization of plasma membrane H1-ATPase. Plant Physiol 93:1654–1658CrossRefPubMedPubMedCentralGoogle Scholar
  69. Pariasca-Tanaka J, Vandamme E, Mori A, Segda Z, Saito K, Rose TJ, Wissuwa M (2015) Does reducing seed-P concentrations affect seedling vigor and grain yield of rice? Plant Soil 392:253–266CrossRefGoogle Scholar
  70. Peaslee DE (1977) Effects of nitrogen, phosphorus, and potassium nutrition on yield, rates of kernel growth and grain filling periods of two corn hybrids. Commun Soil Sci Plant Anal 8:373–389CrossRefGoogle Scholar
  71. Péret B, Clement M, Nussaume L, Desnos T (2011) Root developmental adaptation to phosphate starvation: better safe than sorry. Trends Plant Sci 16:442–450CrossRefPubMedPubMedCentralGoogle Scholar
  72. Pettersson G, Ryde-Pettersson U (1989) Metabolites controlling the rate of starch synthesis in chloroplast of C3 plants. Eur J Biochem 179:169–172CrossRefPubMedPubMedCentralGoogle Scholar
  73. Preiss J (1994) Regulation of the C3 reductive cycle and carbohydrate synthesis. In: Tolbert NE (ed) Regulation of atmospheric CO2 and O2 by photosynthetic carbon metabolism. Oxford University Press, New York, pp 93–102Google Scholar
  74. Ratcliffe RG (1994) In vivo NMR studies of higher plants and algae. Adv Bot Res 20:43–123CrossRefGoogle Scholar
  75. Rausch C, Bucher M (2002) Molecular mechanisms of phosphate transport in plants. Planta 216:23–37CrossRefPubMedPubMedCentralGoogle Scholar
  76. Razaq M, Zhang P, Shen H-l, Salahuddin (2017) Influence of nitrogen and phosphorus on the growth and root morphology of Acer mono. PLoS One 12:1–13CrossRefGoogle Scholar
  77. Reid RJ, Mimura T, Ohsumi Y, Walker NA, Smith FA (2000) Phosphate transport in Chara: membrane transport via Na/Pi cotransport. Plant Cell Environ 23:223–228CrossRefGoogle Scholar
  78. Robinson SP, Giersch C (1987) Inorganic-phosphate concentration in the stroma of isolated-chloroplasts and its influence on photosynthesis. Aust J Plant Physiol 14:451–462CrossRefGoogle Scholar
  79. Rodriguez D, Zubillaga MM, Ploschuk EL, Keltjens WG, Goudriaan J, Lavado RS (1998) Leaf area expansion and assimilate production in sunflower (Helianthus annuus L.) growing under low phosphorus conditions. Plant Soil 202:133–147CrossRefGoogle Scholar
  80. Rose TJ, Pariasca-Tanaka J, Rose MT, Mori A, Wissuwa M (2012) Seeds of doubt: re-assessing the impact of grain P concentrations on seedling vigor. J Plant Nutr Soil Sci 175:799–804CrossRefGoogle Scholar
  81. Rychter AM, Mikulska M (1990) The relationship between phosphate status and cyanide-resistant respiration in bean roots. Physiol Plant 79:663–667CrossRefPubMedGoogle Scholar
  82. Rychter AM, Rao RM (2005) Role of phosphorus in photosynthetic carbon metabolism. In: Pessarakali M (ed) Handbook of photosynthesis, 2nd edn. CRC Press, Boca Raton, pp 1–27Google Scholar
  83. Rychter AM, Chauveau M, Bomsel JL, Lance C (1992) The effect of phosphate deficiency on mitochondrial activity and adenylate levels in bean roots. Physiol Plant 84:80–86CrossRefGoogle Scholar
  84. Sakano K (1990) Proton/phosphate stoichiometry in uptake of inorganic phosphate by cultured cells of Catharanthus roseus (L.) G. Don. Plant Physiol 93:479–483CrossRefPubMedPubMedCentralGoogle Scholar
  85. Sanyal SK, De Datta SK (1991) Chemistry of phosphorus transformations in soil. Adv Soil Sci 16:1–120CrossRefGoogle Scholar
  86. Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453CrossRefPubMedPubMedCentralGoogle Scholar
  87. Schlegel A, Bond HD (2017) Long-term nitrogen and phosphorus fertilization of irrigated grain sorghum. Kansas Agric Exp Station Res Rep 3:1–8Google Scholar
  88. Shen J, Li H, Neumann G, Zhang F (2005) Nutrient uptake, cluster root formation and exudation of protons and citrate in Lupinus albus as affected by localized supply of phosphorus in a split-root system. Plant Sci 168:837–845CrossRefGoogle Scholar
  89. Shen J, Yuan L, Zhang J, Li H, Bai Z, Chen X, Zhang W, Zhang F (2011) Phosphorus dynamics: from soil to plant. Plant Physiol 156:997–1005CrossRefPubMedPubMedCentralGoogle Scholar
  90. Singh B, Pandey R (2003) Differences in root exudation among phosphorus-starved genotypes of maize and green gram and its relationship with phosphorus uptake. J Plant Nutr 26:2391–2401CrossRefGoogle Scholar
  91. Smith VH (2003) Eutrophication of freshwater and coastal marine ecosystems: a global problem. Environ Sci Pollut Res Int 10:126–139CrossRefPubMedGoogle Scholar
  92. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Elsevier and Academic, New York, p 800Google Scholar
  93. Smith FW, Rae AL, Hawkesford MJ (2000) Molecular mechanisms of phosphate and sulfate transport in plants. Biochim Biophys Acta 1465:236–245CrossRefPubMedGoogle Scholar
  94. Soares MM, Sediyama T, Neves JCL, dos Santos Junior HC, da Silva LJ (2016) Nodulation, growth and soybean yield in response to seed coating and split application of phosphorus. J Seed Sci 38:030–040CrossRefGoogle Scholar
  95. Sondergaard TE, Schulz A, Palmgren MG (2004) Energization of transport processes in plants. Roles of the plasma membrane H1-ATPase. Plant Physiol 136:2475–2482CrossRefPubMedPubMedCentralGoogle Scholar
  96. Stitt M, Wirtz W, Heldt HW (1983) Regulation of sucrose synthesis by cytoplasmic fructose bisphosphatase and sucrose phosphate synthase during photosynthesis in varying light and carbon-dioxide. Plant Physiol 72:767–774CrossRefPubMedPubMedCentralGoogle Scholar
  97. Su T, Xu Q, Zhang FC, Chen Y, Li LQ, Wu WH, Chen YF (2015) WRKY42 modulates phosphate homeostasis through regulating phosphate translocation and acquisition in Arabidopsis. Plant Physiol 167:1579–1591CrossRefPubMedPubMedCentralGoogle Scholar
  98. Suzuki Y, Kihara-Doi T, Kawazu T, Miyake C, Makino A (2010) Differences in Rubisco content and its synthesis in leaves at different positions in Eucalyptus globulus seedlings. Plant Cell Environ 33:1314–1323PubMedPubMedCentralGoogle Scholar
  99. Uhde-Stone C, Gilbert G, Jonhson JMF, Litjens R, Zinn KE, Temple SJ, Vance CP, Allan DL (2003) Acclimation of white lupin to phosphorus deficiency involves enhanced expression of genes related to organic acid metabolism. Plant Soil 248:99–116CrossRefGoogle Scholar
  100. Ullrich C, Novacky A (1990) Extra- and intracellular pH and membrane potential changes induced by K+, Cl, H2PO- and NO- uptake and fusicoccin in root hairs of Limnobium stoloniferum. Plant Physiol 94:1561–1567CrossRefPubMedPubMedCentralGoogle Scholar
  101. Usherwood NR, Segars WI (2001) Nitrogen interactions with phosphorus and potassium for optimum crop yield, nitrogen use effectiveness and environmental stewardship. Sci World 1:57–60CrossRefGoogle Scholar
  102. Vance CP (2010) Quantitative trait loci, epigenetics, sugars, and microRNAs: quaternaries in phosphate acquisition and use. Plant Physiol 154:582–588CrossRefPubMedPubMedCentralGoogle Scholar
  103. Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447CrossRefGoogle Scholar
  104. Vengavasi K, Pandey R (2016a) Root acidification, a rapid method of screening soybean genotypes for low-phosphorus stress. Indian J Genet 76:213–216Google Scholar
  105. Vengavasi K, Pandey R (2016b) Root exudation index: screening organic acid exudation and phosphorus acquisition efficiency in soybean genotypes. Crop Pasture Sci 67:1–14CrossRefGoogle Scholar
  106. Vengavasi K, Kumar A, Pandey R (2016) Transcript abundance, enzyme activity and metabolite concentration regulates differential carboxylate efflux in soybean under low phosphorus stress. Indian J Plant Physiol 21:179–188CrossRefGoogle Scholar
  107. Wang BL, Shen JB, Zhang WH, Zhang FS, Neumann G (2007) Citrate exudation from white lupin induced by phosphorus deficiency differs from that induced by aluminum. New Phytol 176:581–589CrossRefPubMedGoogle Scholar
  108. Wang BL, Tang XY, Cheng LY, Zhang AZ, Zhang WH, Zhang FS, Liu JQ, Cao Y, Allan DL, Vance CP, Shen JB (2010) Nitric oxide is involved in phosphorus deficiency-induced cluster-root development and citrate exudation in white lupin. New Phytol 187:1112–1123CrossRefPubMedGoogle Scholar
  109. Wang Z, Ruan W, Shi J, Zhang L, Xiang D, Yang C, Li C, Wu Z, Liu Y, Yu Y, Shou H, Mo X, Mao C, Wu P (2014) Rice SPX1 and SPX2 inhibit phosphate starvation responses through interacting with PHR2 in a phosphate-dependent manner. PNAS, USA 111:14953–14958CrossRefGoogle Scholar
  110. White PJ, Veneklaas EJ (2012) Nature and nurture: the importance of seed phosphorus content. Plant Soil 357:1–8CrossRefGoogle Scholar
  111. Williamson LC, Ribrioux SP, Fitter AH (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–882CrossRefPubMedPubMedCentralGoogle Scholar
  112. Yan F, Zhu Y, Mueller C, Schubert S (2002) Adaptation of H+ pumping and plasma membrane H+ATPase activity in proteoid roots of white lupin under phosphate deficiency. Plant Physiol 129:50–63CrossRefPubMedPubMedCentralGoogle Scholar
  113. Zhang LY, Peng YB, Pelleschi-Travier S, Fan Y, Lu YF, Lu YM, Gao XP, Shen YY, Delrot S, Zhang DP (2004) Evidence for apoplasmic phloem unloading in developing apple fruit. Plant Physiol 135:574–586CrossRefPubMedPubMedCentralGoogle Scholar
  114. 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. Adv Agron 107:1–32CrossRefGoogle Scholar
  115. Zheng L, Huang F, Narsai R, Wu J, Giraud E, He F, Cheng L, Wang F, Wu P, Whelan J, Shou H (2009) Physiological and transcriptome analysis of iron and phosphorus interaction in rice seedlings. Plant Physiol 151:262–274CrossRefPubMedPubMedCentralGoogle Scholar
  116. Zhu YG, Smith SE (2001) Seed phosphorus (P) content affects growth, and P uptake of wheat plants and their association with arbuscular mycorrhizal (AM) fungi. Plant Soil 231:105–112CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Hina Malhotra
    • 1
  • Vandana
    • 1
  • Sandeep Sharma
    • 1
  • Renu Pandey
    • 1
  1. 1.Mineral Nutrition Laboratory, Division of Plant PhysiologyICAR- Indian Agricultural Research InstituteNew DelhiIndia

Personalised recommendations