Roles of Organic Acid Metabolism in Plant Tolerance to Phosphorus-Deficiency

  • Li-Song ChenEmail author
  • Lin-Tong Yang
  • Zheng-He Lin
  • Ning Tang
Part of the Progress in Botany book series (BOTANY, volume 74)


On 30–40% of the world’s arable land, crop yield is limited by phosphorus (P) availability. Phosphorus fertilizer use increased fourfold to fivefold between 1960 and 2000 and the demand for P was predicted to increase by 50–100% by 2050 with increased global demand for food and diets. Continually increasing demand for P will deplete existing phosphate (Pi) rock reserves by the end of the century. Improvement of soil P-acquisition and utilization by plants is one approach to alleviate the scarcity of P resources and to reduce environmental pollution. Many plants have evolved different strategies of enhancing P-acquisition from low-P soils, and one of these strategies involves the secretion of organic acid (OA) anions. Although the causes are not fully understood, the P-deficiency-induced secretion of OA anions may be related to several factors, including (a) internal concentrations of OAs in plant tissues; (b) proteoid or cluster root formation; (c) permeability of root membranes; (d) root plasma membrane H+-ATPase; and (e) anion channels. Besides increased acquisition of soil P, plants respond adaptively to P-deficiency through the induction of alternative glycolytic pathways and tonoplast pumping bypassing Pi- and/or adenylate-dependent reactions. Apart from pyrophosphate (PPi)-dependent tonoplast pyrophosphatase (V-PPiase), several Pi- and adenylate-independent glycolytic bypass enzymes [i.e., UDP-glucose pyrophosphorylase (UGPase), PPi-dependent phosphofructokinase (PPi-PFK), NADP-dependent glyceraldehyde-3-phosphate dehydrogenase (NAD-G3PDH), phosphoenolpyruvate carboxylase (PEPC), phosphoenolpyruvate phosphatase (PEPP), pyruvate phosphate dikinase (PPDK), NAD-malic enzyme (NAD-ME)] in plant tissues have been reported to be upregulated by P-deficiency. Genetically modified plants and cells with higher P-deficiency-tolerance by overexpressing genes for the transporter and biosynthesis of OAs, as well as V-PPiase have been obtained. In addition, some aspects needed to be further studied are also discussed.


White Lupin Cluster Root PEPC Activity Organic Acid Anion Proteoid Root 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work was financially supported by the earmarked fund for China Agriculture Research System and the National Natural Science Foundation of China (No. 30771487).


  1. Abdolzadeh A, Wang X, Veneklaas EJ, Lambers H (2010) Effects of phosphorus supply on growth, phosphate concentration and cluster-root formation in three Lupinus species. Ann Bot 105:365–374PubMedGoogle Scholar
  2. Abel S, Ticconi CA, Delatorre CA (2002) Phosphate sensing in higher plants. Physiol Plant 115:1–8PubMedGoogle Scholar
  3. Achituv M, Bar-Akiva A (1978) Metabolic pathway of α-ketoglutarate in citrus leaves as affected by phosphorus nutrition. Plant Physiol 61:703–705PubMedGoogle Scholar
  4. Ae N, Arihara J, Okada K, Yoshihara T, Johansen C (1990) Phosphorus uptake by pigeonpea and its role in cropping systems of Indian subcontinent. Science 248:477–480PubMedGoogle Scholar
  5. Alonsoa AP, Raymond P, Hernould M, Rondeau-Mouro C, de Graaf A, Chourey P, Lahaye M, Shachar-Hill Y, Rolin D, Dieuaide-Noubhani M (2007) A metabolic flux analysis to study the role of sucrose synthase in the regulation of the carbon partitioning in central metabolism in maize root tips. Metab Eng 9:419–432Google Scholar
  6. Begum HH, Osaki M, Shinano T, Miyatake H, Wasaki J, Yamamura T, Watanabe T (2005) The function of a maize-derived phosphoenolpyruvate carboxylase (PEPC) in phosphorus-deficient transgenic rice. Soil Sci Plant Nutr 51:497–506Google Scholar
  7. Begum HH, Osaki M, Nanamori M, Watanabe T, Shinano T, Rao IM (2006) Role of phosphoenolpyruvate carboxylase in the adaptation of a tropical forage grass to low-phosphorus acid soils. J Plant Nutr 29:35–57Google Scholar
  8. Braum SM (1995) Mobilization of phosphorus and other mineral nutrients by citrate in the rhizosphere of Lupinus albus L. PhD thesis, University of Wisconsin, MadisonGoogle 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 107:243–254PubMedGoogle Scholar
  10. Chen LS, Tang N, Jiang HX, Yang LT, Li Q, Smith BR (2009) Changes in organic acid metabolism differ between roots and leaves of Citrus grandis in response to phosphorus and aluminum interactions. J Plant Physiol 166:2023–2034PubMedGoogle Scholar
  11. Ciereszko I, Zambrzycka A, Rychter A (1998) Sucrose hydrolysis in bean roots (Phaseolus vulgaris L.) under phosphate deficiency. Plant Sci 133:139–144Google Scholar
  12. Ciereszko I, Johansson H, Hurry V, Kleczkowski LA (2001) Phosphate status affects the gene expression, protein content and enzymatic activity of UDP-glucose pyrophosphorylase in wild-type and pho mutants of Arabidopsis. Planta 212:598–605PubMedGoogle Scholar
  13. Ciereszko I, Johansson H, Kleczkowski LA (2005) Interactive effects of phosphate deficiency, sucrose and light/dark conditions on gene expression of UDP-glucose pyrophosphorylase in Arabidopsis. J Plant Physiol 162:343–353PubMedGoogle Scholar
  14. Cordell D, Drangert J-O, White S (2009) The story of phosphorus: global food security and food for thought. Global Environ Change 19:292–305Google Scholar
  15. Dancer J, Veith R, Feil R, Komor E, Stitt MK (1990) Independent changes of inorganic pyrophosphate and the ATP/ ADP or UTP/ UDP ratios in plant suspension cultures. Plant Sci 66:59–63Google Scholar
  16. Dechassa N, Schenk MK (2004) Exudation of organic anions by roots of cabbage, carrot, and potato as influenced by environmental factors and plant age. J Plant Nutr Soil Sci 167:623–629Google Scholar
  17. Dechassa N, Schenk MK, Steingrobe N (2003) Phosphorus efficiency of cabbage (Brassica oleracea L. var. capitata), carrot (Daucus carota L.), and potato (Solanum tuberosum L). Plant Soil 250:215–224Google Scholar
  18. Delhaize E, Ryan PR, Randall PJ (1993) Aluminum tolerance in wheat (Triticum aestivum L.) II. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiol 103:695–702PubMedGoogle Scholar
  19. Delhaize E, Hebb DM, Ryan PR (2001) Expression of a Pseudomonas aeruginosa citrate synthase gene in tobacco is not associated with either enhanced citrate accumulation or efflux. Plant Physiol 125:2059–2067PubMedGoogle Scholar
  20. Delhaize E, Taylor P, Hocking PJ, Simpson RJ, Ryan PR, Richardson AE (2009) Transgenic barley (Hordeum vulgare L.) expressing the wheat aluminium resistance gene (TaALMT1) shows enhanced phosphorus nutrition and grain production when grown on an acid soil. Plant Biotechnol J 7:391–400PubMedGoogle Scholar
  21. Diatloff E, Roberts M, Sanders D, Roberts SK (2004) Characterization of anion channels in the plasma membrane of Arabidopsis epidermal root cells and the identification of a citrate-permeable channel induced by phosphate starvation. Plant Physiol 136:4136–4149PubMedGoogle Scholar
  22. Dinkelaker B, Römheld V, Marschner H (1989) Citric acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L.). Plant Cell Environ 12:285–292Google Scholar
  23. Dinkelaker B, Hengeler C, Marschner H (1995) Distribution and function of proteoid roots and other root clusters. Bot Acta 108:183–200Google Scholar
  24. Dong D, Peng X, Yan X (2004) Organic acid exudation induced by phosphorus deficiency and/or aluminum toxicity in two contrasting soybean genotypes. Physiol Plant 122:190–199Google Scholar
  25. Duff SMG, Lefebvre DD, Plaxton WC (1989) Purification and characterization of a phosphoenolpyruvate phosphatase from Brassica nigra suspension cells. Plant Physiol 90:734–741PubMedGoogle Scholar
  26. Fang ZY, Shao C, Meng YJ, Wu P, Chen M (2009) Phosphate signaling in Arabidopsis and Oryza sativa. Plant Sci 176:170–180Google Scholar
  27. Fernie AR, Roscher A, Ratcliffe RG, Kruger NJ (2002) Activation of pyrophosphate:fructose-6-phosphate 1-phosphotransferase by fructose 2,6-bisphosphate stimulates conversion of hexose phosphates to triose phosphates but does not influence accumulation of carbohydrates in phosphate-deficient tobacco cells. Physiol Plant 114:172–181PubMedGoogle Scholar
  28. Fredeen AL, Rao IM, Terry N (1989) Influence of phosphorus nutrition on growth and carbon partitioning in Glycine max. Plant Physiol 89:225–230PubMedGoogle Scholar
  29. Fukuda T, Saito A, Wasaki J, Shinano T, Osaki M (2007) Metabolic alterations proposed by proteome in rice roots grown under low P and high Al concentration under low pH. Plant Sci 172:1157–1165Google Scholar
  30. Gahoonia TS, Asmar F, Giese H, Nielsen GG, Nielsen NE (2000) Root-released organic acids and phosphorus uptake of two barley cultivars in laboratory and field experiments. Eur J Agron 12:281–289Google Scholar
  31. Gardner WK, Barber DA, Parbery DG (1983) The acquisition of phosphorus by Lupinus albus L. III. The probable mechanism by which phosphorus movement in the soil root interface is enhanced. Plant Soil 70:107–124Google Scholar
  32. Gaume A, Mächler F, De León C, Narro L, Frossard E (2001) Low-P tolerance by maize (Zea mays L.) cultivars: significance of root growth, and organic acids and acid phosphatase root exudation. Plant Soil 228:253–264Google Scholar
  33. Gaxiola RA, Edwards M, Elser JJ (2011) A transgenic approach to enhance phosphorus use efficiency in crops as part of a comprehensive strategy for sustainable agriculture. Chemosphere 84:840–845PubMedGoogle Scholar
  34. Graham JH, Leonard RT, Menge JA (1981) Membrane-mediated decrease in root exudation responsible for phosphorus inhibition of vesicular-arbuscular mycorrhiza formation. Plant Physiol 68:548–552PubMedGoogle Scholar
  35. Gregory AL, Hurley BA, Tran HT, Valentine AJ, She YM, Knowles VL, Plaxton WC (2009) In vivo regulatory phosphorylation of the phosphoenolpyruvate carboxylase AtPPC1 in phosphate-starved Arabidopsis thaliana. Biochem J 420:57–65PubMedGoogle Scholar
  36. Guo W, Zhang L, Zhao J, Liao H, Yan X (2008) Identification of temporally and spatially phosphate-starvation responsive genes in Glycine max. Plant Sci 175:574–584Google Scholar
  37. Hammond JP, Broadley MR, White PJ (2004) Genetic responses to phosphorus deficiency. Ann Bot 94:323–332PubMedGoogle Scholar
  38. Hernández G, Ramírez M, Valdés-López O, Tesfaye M, Graham MA, Czechowski T, Schlereth A, Wandrey M, Erban A, Cheung F, Wu HC, Lara M, Town CD, Kopka J, Udvardi MK, Vance CP (2007) Phosphorus stress in common bean: root transcript and metabolic responses. Plant Physiol 144:752–767PubMedGoogle Scholar
  39. Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195Google Scholar
  40. Hocking PJ, Jeffery S (2004) Cluster-root production and organic acid exudation in a group of Old-World lupins and a New-World lupin. Plant Soil 258:135–150Google Scholar
  41. Hoffland E, Findenegg GR, Nelemans JA (1989) Solubilization of rock phosphate by rape. II. Local root exudation of organic acids as a response to P-starvation. Plant Soil 113:161–165Google Scholar
  42. Hoffland E, Van den Boogaard R, Nelemans J, Findenegg G (1992) Biosynthesis and root exudation of citric and malic acids in phosphate-starved rape plants. New Phytol 122:675–680Google Scholar
  43. Hoffland E, Wei C, Wissuwa M (2006) Organic anion exudation by lowland rice (Oryza sativa L.) at zinc and phosphorus deficiency. Plant Soil 283:155–162Google Scholar
  44. Holford ICR (1997) Soil phosphorus: its measurement and its uptake by plants. Aust J Soil Res 35:227–239Google Scholar
  45. Huang CY, Roessner U, Eickmeier I, Genc Y, Callahan DL, Shirley N, Langridge P, Bacic A (2008) Metabolite profiling reveals distinct changes in carbon and nitrogen metabolism in phosphate-deficient barley plants (Hordeum vulgare L.). Plant Cell Physiol 49:691–703PubMedGoogle Scholar
  46. Ishikawa S, Adu-Gyamfi JJ, Nakamura T, Yoshihara T, Watanabe T, Wagastsum T (2002) Genotypic variability in phosphorus solubilizing activity of root exudates by pigeonpea grown in low-nutrient environments. Plant Soil 245:71–81Google Scholar
  47. Jemo M, Abaidoo RC, Nolte C, Horst J (2007) Aluminum resistance of cowpea as affected by phosphorus-deficiency stress. J Plant Physiol 164:442–451PubMedGoogle Scholar
  48. Johnson JF, Allan DL, Vance CP (1994) Phosphorus stress-induced proteoid roots show altered metabolism in Lupinus albus. Plant Physiol 104:657–665PubMedGoogle Scholar
  49. Johnson JF, Allan DL, Vance CP, Weiblen G (1996a) Root carbon dioxide fixation by phosphorus-deficient Lupinus albus. Plant Physiol 112:19–30PubMedGoogle Scholar
  50. Johnson JF, Vance CP, Allan DL (1996b) Phosphorus deficiency in Lupinus albus. Altered lateral root development and enhanced expression of phosphoenolpyruvate carboxylase. Plant Physiol 112:31–41PubMedGoogle Scholar
  51. Jones DL (1998) Organic acids in the rhizosphere—a critical review. Plant Soil 205:25–44Google Scholar
  52. Juszczuk IM, Rychter AN (2002) Pyruvate accumulation during phosphate deficiency stress of bean roots. Plant Physiol Biochem 40:783–788Google Scholar
  53. Kania A, Langlade N, Martinoia E, Neumann G (2003) Phosphorus deficiency-induced modifications in citrate catabolism and in cytosolic pH as related to citrate exudation in cluster roots of white lupin. Plant Soil 248:117–127Google Scholar
  54. Keerthisinghe G, Hocking PJ, Ryan PR, Delhaize E (1998) Effect of phosphorus supply on the formation and function of proteoid roots of white lupin (Lupinus albus L.). Plant Cell Environ 21:467–478Google Scholar
  55. Khorassani R, Hettwer U, Ratzinger A, Steingrobe B, Karlovsky P, Claassen N (2011) Citramalic acid and salicylic acid in sugar beet root exudates solubilize soil phosphorus. BMC Plant Biol 11:121PubMedGoogle Scholar
  56. Kirk GJD, Santos EE, Findenegg GR (1999) Phosphate solubilization by organic anion excretion from rice (Oryza sativa L.) growing in aerobic soil. Plant Soil 211:11–18Google Scholar
  57. Kochian LV, Hoekenga OA, Piñeros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol 55:459–493PubMedGoogle Scholar
  58. Koyama H, Takita E, Kawamura A, Hara T, Shibata D (1999) Over expression of mitochondrial citrate synthase gene improves the growth of carrot cells in Al-phosphate medium. Plant Cell Physiol 40:482–488PubMedGoogle Scholar
  59. Koyama H, Kawamura A, Kihara T, Hara T, Takita E, Shibata D (2000) Overexpression of mitochondrial citrate synthase in Arabidopsis thaliana improved growth on a phosphorus-limited soil. Plant Cell Physiol 41:1030–1037PubMedGoogle Scholar
  60. Lan M, Comerford NB, Fox TR (1995) Organic anions effect on phosphorus release from spodic horizons. Soil Sci Soc Am J 59:1745–1749Google Scholar
  61. Langlade NB, Messerli G, Weisskopf L, Plaza S, Tomasi N, Smutny J, Neumann G, Martinoia E, Massonneau A (2002) ATP citrate lyase: cloning, heterologous expression and possible implication in root organic acid metabolism and excretion. Plant Cell Environ 25:1561–1569Google Scholar
  62. Li XN, Ashihara H (1990) Effects of inorganic phosphate on sugar catabolism by suspension-cultured Catharanthus roseus. Phytochemistry 29:497–500Google Scholar
  63. Li C, Liang R (2005) Root cluster formation and citrate exudation of white lupin (Lupinus albus L.) as related to phosphorus availability. J Integrative Plant Biol 47:172–177Google Scholar
  64. Li K, Xu C, Zhang K, Yang A, Zhang J (2007) Proteomic analysis of roots growth and metabolic changes under phosphorus deficit in maize (Zea mays L.) plants. Proteomics 7:1501–1512PubMedGoogle Scholar
  65. Li K, Xu C, Li Z, Zhang K, Yang A, Zhang J (2008) Comparative proteome analyses of phosphorus responses in maize (Zea mays L.) roots of wild-type and a low-P-tolerant mutant reveal root characteristics associated with phosphorus efficiency. Plant J 55:927–939PubMedGoogle Scholar
  66. Li XF, Zuo FH, Ling GZ, Li YY, Yu YX, Yang PQ, Tang XL (2009) Secretion of citrate from roots in response to aluminum and low phosphorus stresses in Stylosanthes. Plant Soil 325:219–229Google Scholar
  67. Liao H, Wan H, Shaff J, Wang X, Yan X, Kochian LV (2006) Phosphorus and aluminum interactions in soybean in relation to aluminum tolerance. Exudation of specific organic acids from different regions of the intact root system. Plant Physiol 141:674–684PubMedGoogle Scholar
  68. Ligaba A, Shen H, Shibata K, Yamamoto Y, Tanakamaru S, Matsumoto H (2004a) The role of phosphorus in aluminum-induced citrate and malate exudation from rape (Brassica napus). Physiol Plant 120:575–584PubMedGoogle Scholar
  69. Ligaba A, Yamaguchi M, Shen H, Sasaki T, Yamamoto Y, Matsumoto H (2004b) Phosphorus deficiency enhances plasma membrane H+-ATPase activity and citrate exudation in greater purple lupin (Lupinus pilosus). Funct Plant Biol 31:1075–1083Google Scholar
  70. Lin ZH, Chen LS, Chen RB, Zhang FZ, Jiang HX, Tang N, Smith BR (2011) Root release and metabolism of organic acids in tea plants in response to phosphorus supply. J Plant Physiol 168:644–652PubMedGoogle Scholar
  71. 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 85:315–317PubMedGoogle Scholar
  72. López-Bucio J, Nieto-Jacobo MF, Ramírez-Rodríguez V, Herrera-Estrella L (2000a) Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils. Plant Sci 160:1–13PubMedGoogle Scholar
  73. López-Bucio J, de la Vega OM, Guevara-García A, Herrera-Estrella L (2000b) Enhanced phosphorus uptake in transgenic tobacco plants that overproduce citrate. Nat Biotechnol 18:450–453PubMedGoogle Scholar
  74. Lü J, Gao X, Dong Z, Yi J, An L (2012) Improved phosphorus acquisition by tobacco through transgenic expression of mitochondrial malate dehydrogenase from Penicillium oxalicum. Plant Cell Rep 31:49–56PubMedGoogle Scholar
  75. Massonneau A, Langlade N, Léon S, Smutny J, Vogt E, Neumann G, Martinoia E (2001) Metabolic changes associated with cluster root development in white lupin (Lupinus albus L.): relationship between organic acid excretion, sucrose metabolism and energy status. Planta 213:534–542PubMedGoogle Scholar
  76. Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, Ortet P, Creff A, Somerville S, Rolland N (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci USA 102:11934–11939PubMedGoogle Scholar
  77. Murley VR, Theodorou ME, Plaxton WC (1998) Phosphate starvation-inducible pyrophosphate-dependent phosphofructokinase occurs in plants whose roots do not form symbiotic associations with mycorrhizal fungi. Physiol Plant 103:405–414Google Scholar
  78. Nagarajah S, Posner AM, Quirk JP (1970) Competitive adsorption of phosphate with polygalacturonate and other organic anions on kaolinite and oxide surfaces. Nature 228:83–85PubMedGoogle Scholar
  79. Nanamori M, Shinano T, Wasaki J, Yamamura T, Rao IM, Osaki M (2004) Low phosphorus tolerance mechanisms: phosphorus recycling and photosynthate partitioning in the tropical forage grass, Brachiaria hybrid cultivar Mulato compared with rice. Plant Cell Physiol 45:460–469PubMedGoogle Scholar
  80. Narang RA, Bruene A, Altmann T (2000) Analysis of phosphate acquisition efficiency in different Arabidopsis accessions. Plant Physiol 124:1786–1799PubMedGoogle Scholar
  81. Neumann G, Römheld V (1999) Root excretion of carboxylic acids and protons in phosphorus-deficient plants. Plant Soil 211:121–130Google Scholar
  82. Neumann C, Massonneau A, Martinoia E, Römheld V (1999) Physiological adaptations to phosphorus deficiency during proteoid root development in white lupin. Planta 208:373–382Google Scholar
  83. Neumann C, Massonneau A, Langlade N, Dinkelaker B, Hengeler C, Römheld V, Martinoia E (2000) Physiological aspects of cluster root function and development in phosphorus-deficient white lupin (Lupinus albus L.). Ann Bot 85:909–919Google Scholar
  84. Nian H, Ahn SJ, Yang ZM, Matsumoto H (2003) Effect of phosphorus deficiency on aluminum-induced citrate exudation in soybean (Glycine max). Physiol Plant 117:229–236Google Scholar
  85. Ohwaki Y, Hirata H (1992) Differences in carboxylic acid exudation among P-starved leguminous crops in relation to carboxylic acid contents in plant tissues and phospholipid level in roots. Soil Sci Plant Nutr 38:235–243Google Scholar
  86. Palma DA, Blumwald E, Plaxton WC (2000) Upregulation of vacuolar H+-translocating pyrophosphatase by phosphate starvation of Brassica napus (rapeseed) suspension cell cultures. FEBS Lett 486:155–158PubMedGoogle Scholar
  87. Peñaloza E, Corcuera LJ, Martinez J (2002) Spatial and temporal variation in citrate and malate exudation and tissue concentration as affected by P stress in roots of white lupin. Plant Soil 241:209–221Google Scholar
  88. Pilbeam DJ, Cakmak I, Marschner H, Kirkby EA (1993) Effect of withdrawal of phosphorus on nitrate assimilation and PEP carboxylase activity in tomato. Plant Soil 154:111–117Google Scholar
  89. Plaxton WC, Carswell MC (1999) Metabolic aspects of the phosphate starvation response in plants. In: Lerner HD (ed) Plant responses to environmental stress: from phytohormones to genome reorganization. Marcel Dekker, New York, pp 350–372Google Scholar
  90. Plaxton WC, Podestá FE (2006) The functional organization and control of plant respiration. Crit Rev Plant Sci 25:159–198Google Scholar
  91. Plaxton WC, Tran HT (2011) Metabolic adaptations of phosphate-starved plants. Plant Physiol 156:1006–1015PubMedGoogle Scholar
  92. Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Physiol Mol Biol 50:665–693Google Scholar
  93. Rea PA, Poole RJ (1993) Vacuolar H+-translocating pyrophosphatase. Annu Rev Plant Physiol Plant Mol Biol 44:157–180Google Scholar
  94. Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol 52:527–560PubMedGoogle Scholar
  95. Rychter AM, Randall DD (1994) The effect of phosphate deficiency on carbohydrate metabolism in bean roots. Physiol Plant 91:383–388Google Scholar
  96. Schwab SM, Menge JA, Leonard RT (1983) Quantitative and qualitative effects of phosphorus on extracts and exudates of sudangrass roots in relation to vesicular-arbuscular mycorrhiza formation. Plant Physiol 73:761–765PubMedGoogle Scholar
  97. Shane MW, Lambers H (2005) Cluster roots: a curiosity in context. Plant Soil 274:101–125Google Scholar
  98. Shane MW, de Vos M, De Roock S, Cawthray GR, Lambers H (2003) Effects of external phosphorus supply on internal phosphorus concentration and the initiation, growth and exudation of cluster roots in Hakea prostrata R.Br. Plant Soil 248:209–219Google Scholar
  99. Shen H, Wang X, Cao Z, Shi W, Yan X (2001) Isolation and identification of specific root exudates in elephantgrass in response to mobilization of iron- and aluminum-phosphates. J Plant Nutr 24:1131–1144Google Scholar
  100. Shen H, Yan X, Zhao M, Zheng S, Wang X (2002) Exudation of organic acids in common bean as related to mobilization of aluminum- and iron-bound phosphates. Environ Exp Bot 48:1–9Google Scholar
  101. 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 168:837–845Google Scholar
  102. Shen H, Chen J, Wang Z, Yang C, Sasaki T, Yamamoto Y, Matsumoto H, Yan X (2006) Root plasma membrane H+-ATPase is involved in the adaptation of soybean to phosphorus starvation. J Exp Bot 57:1353–1362PubMedGoogle Scholar
  103. Shinano T, Nanamori M, Dohi M, Wasaki J, Osaki M (2005) Evaluation of phosphorus starvation inducible genes relating to efficient phosphorus utilization in rice. Plant Soil 269:81–87Google Scholar
  104. Sung SS, Xu DP, Galloway CM, Black CC (1988) A reassessment of glycolysis and gluconeogenesis in higher plants. Physiol Plant 72:650–654Google Scholar
  105. Tang C, Han XZ, Qiao YF, Zheng SJ (2009) Phosphorus deficiency does not enhance proton release by roots of soybean [Glycine max (L.) Murr.]. Environ Exp Bot 67:228–234Google Scholar
  106. Tesfaye M, Temple SJ, Allan DL, Vance CP, Samac DA (2001) Overexpression of malate dehydrogenase in transgenic alfalfa enhances organic acid synthesis and confers tolerance to aluminum. Plant Physiol 127:1836–1844PubMedGoogle Scholar
  107. Theodorou ME, Plaxton WC (1993) Metabolic adaptations of plant respiration to nutritional phosphate deprivation. Plant Physiol 101:339–344PubMedGoogle Scholar
  108. 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 32:465–475PubMedGoogle Scholar
  109. Uhde-Stone C, Gibert G, Johnson JMF, Litjens R, Zinn KE, Temple SJ, Vance CP, Allan DL (2003a) Acclimation of white lupin to phosphorus deficiency involves enhanced expression of genes related to organic acid metabolism. Plant Soil 248:99–116Google Scholar
  110. Uhde-Stone C, Zinn KE, Ramirez-Yáñez M, Li A, Vance CP, Allan DL (2003b) Nylon filter arrays reveal differential gene expression in proteoid roots of white lupin in response to phosphorus deficiency. Plant Physiol 131:1064–1079PubMedGoogle Scholar
  111. Usuda H, Shimogawara Y (1992) Phosphate deficiency in maize. III. Changes in enzyme activities during the course of phosphate deprivation. Plant Physiol 99:1680–1685PubMedGoogle Scholar
  112. Vaccari DA (2009) Phosphorus: a looming crisis. Sci Am 300:42–47Google Scholar
  113. Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447Google Scholar
  114. 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 aluminium. New Phytol 176:581–589PubMedGoogle Scholar
  115. Wasaki J, Yonetani R, Kuroda S, Shinano T, Yazaki J, Fujii F, Shimbo K, Yamamoto K, Sakata K, Sasaki T, Kishimoto N, Kikuchi S, Yamagishi M, Osaki M (2003) Transcriptomic analysis of metabolic changes by phosphorus stress in rice plant roots. Plant Cell Environ 26:1515–1523Google Scholar
  116. Watt M, Evans JR (1999a) Linking development and determinacy with organic acid efflux from proteoid roots of white lupin grown with low phosphorus and ambient or elevated atmospheric CO2 concentration. Plant Physiol 120:705–716PubMedGoogle Scholar
  117. Watt M, Evans JR (1999b) Proteoid roots. Physiology and development. Plant Physiol 121:317–323PubMedGoogle Scholar
  118. Weiner H, Stitt M, Heldt HW (1987) Subcellular compartmentation of pyrophosphate and alkaline pyrophosphatase in leaves. Biochim Biophys Acta 893:13–21Google Scholar
  119. Wouterlood M, Cawthray GR, Turner S, Lambers H, Veneklaas EJ (2004a) Rhizosphere carboxylate concentrations of chickpea are affected by genotype and soil type. Plant Soil 261:1–10Google Scholar
  120. Wouterlood M, Cawthray GR, Scanlon T, Lambers H, Veneklaas EJ (2004b) Carboxylate concentrations in the rhizosphere of lateral roots of chickpea (Cicer arietinum) increase during plant development, but are not correlated with phosphorus status of soil or plants. New Phytol 162:745–753Google Scholar
  121. Wouterlood M, Lambers H, Veneklaas EJ (2005) Plant phosphorus status has a limited influence on the concentration of phosphorus-mobilising carboxylates in the rhizosphere of chickpea. Funct Plant Biol 32:153–159Google Scholar
  122. Wu P, Ma L, Hou X, Wang M, Wu Y, Liu F, Deng XW (2003) Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol 132:1260–1271PubMedGoogle Scholar
  123. Xia M, Wang X-B, Li H-B, Wu P (2002) Identification of the rice vacuolar ATPase B subunit gene and its expression pattern analysis under phosphorus deficiency. Acta Bot Sin 44:573–578Google Scholar
  124. Yan F, Zhu Y, Müller C, Zörb SS (2002) Adaptation of H+-pumping and plasma membrane H+-ATPase activity in proteoid roots of white lupin under phosphate deficiency. Plant Physiol 129:50–63PubMedGoogle Scholar
  125. Yan XL, Wu P, Lin HQ, Xu GH, Xu FS, Zhang QF (2006) Plant nutriomics in China: an overview. Ann Bot 98:473–482PubMedGoogle Scholar
  126. Yang H, Knapp J, Koirala P, Rajagopal D, PeerWA SLK, Murphy A, Gaxiola RA (2007) Enhanced phosphorus nutrition in monocots and dicots over-expressing a phosphorus-responsive type I H+-pyrophosphatase. Plant Biotechnol J 5:735–745PubMedGoogle Scholar
  127. Yang LT, Jiang HX, Tang N, Chen LS (2011) Mechanisms of aluminum-tolerance in two species of citrus: Secretion of organic acid anions and immobilization of aluminum by phosphorus in roots. Plant Sci 180:521–530PubMedGoogle Scholar
  128. Yang LT, Jiang HX, Qi YP, Chen LS (2012) Differential expression of genes involved in alternative glycolytic pathways, phosphorus scavenging and recycling in response to aluminum and phosphorus interactions in citrus roots. Mol Biol Rep 39:6353–6366PubMedGoogle Scholar
  129. Yao Y, Sun H, Xu F, Zhang X, Li S (2011) Comparative proteome analysis of metabolic changes by low phosphorus stress in two Brassica napus genotypes. Planta 233:523–537PubMedGoogle Scholar
  130. Zhang FS, Ma J, Cao YP (1997) Phosphorus deficiency enhances root exudation of low-molecular weight organic acids and utilization of sparingly soluble inorganic phosphates by radish (Raghanus satiuvs L.) and rape (Brassica napus L.) plants. Plant Soil 196:261–264Google Scholar
  131. Zhang WH, Ryan PR, Tyerman SD (2004) Citrate-permeable channels in the plasma membrane of cluster roots from white lupin. Plant Physiol 136:3771–3783PubMedGoogle Scholar
  132. Zhang HW, Huang Y, Ye XS, Xu FS (2011) Genotypic variation in phosphorus acquisition from sparingly soluble P sources is related to root morphology and root exudates in Brassica napus. Sci China (Life Sci) 54:1134–1142Google Scholar
  133. Zhou XB, Huang JG, Zhou YX, Shi WM (2012) Genotypic variation of rape in phosphorus uptake from sparingly soluble phosphate and its active mechanism. Afr J Biotechnol 11:3061–3069Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Li-Song Chen
    • 1
    • 2
    • 3
    Email author
  • Lin-Tong Yang
    • 1
    • 2
    • 3
  • Zheng-He Lin
    • 2
    • 3
    • 4
  • Ning Tang
    • 2
    • 3
    • 5
  1. 1.College of Resources and Environmental SciencesFujian Agriculture and Forestry UniversityFuzhouChina
  2. 2.Institute of Horticultural Plant Physiology, Biochemistry and Molecular BiologyFujian Agriculture and Forestry UniversityFuzhouChina
  3. 3.College of HorticultureFujian Agriculture and Forestry UniversityFuzhouChina
  4. 4.Tea Research InstituteFujian Academy of Agricultural SciencesFuanChina
  5. 5.Bioengineering CollegeChongqing UniversityChongqingChina

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