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Phosphorus nutrition of terrestrial plants

  • Philip J. White
  • John P. Hammond
Part of the Plant Ecophysiology book series (KLEC, volume 7)

Phosphorus (P) is essential for plant growth and fecundity. It is an integral component of genetic, metabolic, structural and regulatory molecules, in many of which it cannot be substituted by any other elements. Tissue P concentrations in well fertilized plants approximate 0.4–1.5% of the dry matter (Broadley et al. 2004), most of which is present as nucleic acids and nucleotides, phosphorylated intermediates of energy metabolism, membrane phospholipids and, in some tissues (principally seeds), as inositol phosphates. Some P also occurs in phosphoproteins and as inorganic phosphate (Pi) and pyrophosphate (PPi). It has been estimated that small metabolites, nucleic acids and phospholipids contribute approximately equally to leaf P content in P-replete plants (Figure 4.1; Marschner 1995; Dörmann and Benning 2002). Tissue P concentrations show no systematic differences between angiosperm species grown in P-replete conditions, but strong positive correlations occur between shoot P and shoot organic-N concentrations (Broadley et al. 2004). When plants are sampled from their natural environment, shoot N:P mass ratios vary between about 5:1 and 40:1 (e.g. Garten 1976; Thompson et al. 1997; Elser et al. 2000a; Tessier and Raynal 2003; Güsewell 2004; McGroddy et al. 2004; Güsewell et al. 2005; Han et al. 2005; Niklas et al. 2005; Wassen et al. 2005; Wright et al. 2005; Kerkhoff et al. 2006) and leaf N appears to scale as the 3/4 power of leaf P (Niklas et al. 2005; Niklas 2008). Ratios of 10:1 approximate the maximum critical organic-N:P ratios reported for a range of crop plants (Greenwood et al. 1980; Güsewell 2004). In general, leaf N:P ratios below 13.5 suggest N-limited plant growth, whilst leaf N:P ratios above 16 suggest P-limited plant growth (Aerts and Chapin 2000; Güsewell and Koerselman 2002; Tessier and Raynal 2003). Stoichiometric relationships between leaf N and leaf P appear to be a consequence of the requirements of N for proteins and of P for nucleic acids, membranes and metabolism (Elser et al. 2000b; Niklas 2008). Plant relative growth rate (RGR) is positively correlated with rRNA concentration and negatively correlated with protein concentration (Ågren 1988; Elser et al. 2000b; Niklas 2008).

Keywords

Root Hair Common Bean Plant Soil Plant Cell Environ White Lupin 
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.

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References

  1. Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84: 597–608Google Scholar
  2. Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30: 1–67Google Scholar
  3. Ågren GI (1988) Ideal nutrient productivities and nutrient proportions in plant growth. Plant Cell Environ 11: 613–620Google Scholar
  4. Al-Ghazi Y, Muller B, Pinloche S, Tranbarger TJ, Nacry P, Rossignol M, Tardieu F, Doumas P (2003) Temporal responses of Arabidopsis root architecture to phosphate starvation: evidence for the involvement of auxin signalling. Plant Cell Environ 26: 1053–1066Google Scholar
  5. Alt D (1987) Influence of P- and K-fertilization on yield of different vegetable species. J Plant Nutr 10: 1429–1435Google Scholar
  6. Amtmann A, Hammond JP, Armengaud P, White PJ (2006) Nutrient sensing and signalling in plants: potassium and phosphorus. Adv Bot Res 43: 209–257Google Scholar
  7. Andersson MX, Stridh MH, Larsson KE, Liljenberg C, Sandelius AS (2003) Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol. FEBS Lett 537: 128–132PubMedGoogle Scholar
  8. Andersson MX, Larsson KE, Tjellström H, Liljenberg C, Sandelius AS (2005) Phosphate-limited oat. The plasma membrane and the tonoplast as major targets for phospholipid-to-glycolipid replacement and stimulation of phospholipases in the plasma membrane. J Biol Chem 280: 27578–27586PubMedGoogle Scholar
  9. Asmar F, Gahoonia TS, Nielsen NE (1995) Barley genotypes differ in activity of soluble extracellular phosphatase and depletion of organic phosphorus in the rhizosphere soil. Plant Soil 172: 117–122Google Scholar
  10. 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: 1000–1011PubMedGoogle Scholar
  11. Baligar VC, Fageria NK, He ZL (2001) Nutrient use efficiency in plants. Commun Soil Sci Plant Anal 32: 921–950Google Scholar
  12. Barber SA (1995) Soil Nutrient Bioavailability: A Mechanistic Approach. Wiley, New YorkGoogle Scholar
  13. Barea JM, Pozo MJ, Azcón R, Azcón-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56: 1761–1778PubMedGoogle Scholar
  14. Bari R, Pant BD, Stitt M, Scheible WR (2006) PHO2, MicroRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141: 988–999PubMedGoogle Scholar
  15. Bariola PA, Howard CJ, Taylor CB, Verburg MT, Jaglan VD, Green PJ (1994) The Arabidopsis ribonuclease gene RNS1 is tightly controlled in response to phosphate limitation. Plant J 6: 673–685PubMedGoogle Scholar
  16. Basu P, Zhang YJ, Lynch JP, Brown KM (2007) Ethylene modulates genetic, positional, and nutritional regulation of root plagiogravitropism. Funct Plant Biol 34: 41–51Google Scholar
  17. Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 19: 529–538Google Scholar
  18. Beebe S, Lynch J, Galwey N, Tohme J, Ochoa I (1997) A geographical approach to identify phosphorus-efficient genotypes among landraces and wild ancestors of common bean. Euphytica 95: 325–336Google Scholar
  19. Benning C, Ohta H (2005) Three enzyme systems for galactoglycerolipid biosynthesis are coordinately regulated in plants. J Biol Chem 280: 2397–2400PubMedGoogle Scholar
  20. Bentsink L, Yuan K, Koorneef M, Vreugdenhil D (2003) The genetics of phytate and phosphate accumulation in seeds and leaves of Arabidopsis thaliana, using natural variation. Theor Appl Genet 106: 1234–1243PubMedGoogle Scholar
  21. Berger S, Bell E, Sadka A, Mullet JE (1995) Arabidopsis thaliana Atvsp is homologous to soybean VspA and VspB, genes encoding vegetative storage protein acid phosphatases, and is regulated similarly by methyl jasmonate, wounding, sugars, light and phosphate. Plant Mol Biol 27: 933–942PubMedGoogle Scholar
  22. Bergmann W (1992) Nutritional Disorders of Plants. Visual and Analytical Diagnosis. Gustav Fischer, Jena, GermanyGoogle Scholar
  23. Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Ann Rev Plant Physiol 24: 225–252Google Scholar
  24. Blackshaw RE, Brandt RN, Janzen HH, Entz T (2004) Weed species response to phosphorus fertilization. Weed Sci 42: 406–412Google Scholar
  25. Bolland MDA, Siddique KHM, Loss SP, Baker MJ (1999) Comparing responses of grain legumes, wheat and canola to applications of superphosphate. Nutr Cycl Agroecosyst 53: 157–175Google Scholar
  26. Bonser AM, Lynch J, Snapp S (1996) Effect of phosphorus deficiency on growth angle of basal roots in Phaseolus vulgaris. New Phytol 132: 281–288PubMedGoogle Scholar
  27. Bosse D, Köck M (1998) Influence of phosphate starvation on phosphohydrolases during development of tomato seedlings. Plant Cell Environ 21: 325–332Google Scholar
  28. Bould C, Hewitt EJ, Needham P (1983) Diagnosis of Mineral Disorders in Plants. Volume 1: Principles. HMSO, LondonGoogle Scholar
  29. Bradshaw AD, Chadwick MJ, Jowett D, Lodge RW, Snaydon RW (1960) Experimental investigations into the mineral nutrition of several grass species. Part III: phosphate level. J Ecol 48: 631–637Google Scholar
  30. Brinch-Pedersen H, Sorensen LD, Holm PB (2002) Engineering crop plants: getting a handle on phosphate. Trends Plant Sci 7: 118–125PubMedGoogle Scholar
  31. Broadley MR, Bowen HC, Cotterill HL, Hammond JP, Meacham MC, Mead A, White PJ (2004) Phylogenetic variation in the shoot mineral concentration of angiosperms. J Exp Bot 55: 321–336PubMedGoogle Scholar
  32. Bryson R (2005) Proceedings of the International Fertiliser Society 577. Improvements in Farm and Nutrient Management Through Precision Farming. IFS, YorkGoogle Scholar
  33. Bucher M (2007) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol 173: 11–26PubMedGoogle Scholar
  34. Burleigh SH, Harrison MJ (1999) The down-regulation of Mt4-like genes by phosphate fertilization occurs systemically and involves phosphate translocation to the shoots. Plant Physiol 119: 241–248PubMedGoogle Scholar
  35. Cakmak I, Hengeler C, Marschner H (1994) Partitioning of shoot and root dry matter and carbohydrates in bean plants suffering from phosphorus, potassium and magnesium deficiency. J Exp Bot 45: 1245–1250Google Scholar
  36. Casimiro I, Beekman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci 8: 165–171PubMedGoogle Scholar
  37. Casson SA, Lindsey K (2003) Genes and signalling in root development. New Phytol 158: 11–38Google Scholar
  38. Chapin FS, Vitousek PM, Vancleve K (1986) The nature of nutrient limitation in plant-communities. Am Nat 127: 48–58Google Scholar
  39. Chevalier F, Pata M, Nacry P, Doumas P, Rossignol M (2003) Effects of phosphate availability on the root system architecture: large scale analysis of the natural variation between Arabidopsis accessions. Plant Cell Environ 26: 1839–1850Google Scholar
  40. Chiou TJ (2007) The role of microRNAs in sensing nutrient stress. Plant Cell Environ 30: 323–332PubMedGoogle Scholar
  41. Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CI (2006) Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18: 412–421PubMedGoogle Scholar
  42. Ciereszko I, Barbachowska A (2000) Sucrose metabolism in leaves and roots of bean (Phaseolus vulgaris L.) during phosphate deficiency. J Plant Physiol 156: 640–644Google Scholar
  43. Clarkson DT, Scattergood CB (1982) Growth and phosphate transport in barley and tomato plants during the development of, and recovery from, phosphate stress. J Exp Bot 33: 865–875Google Scholar
  44. Clarkson DT, Sanderson J, Scattergood CB (1978) Influence of phosphate-stress on phosphate absorption and translocation by various parts of the root system of Hordeum vulgare L. (barley). Planta 139: 47–53Google Scholar
  45. Coello P (2002) Purification and characterization of secreted acid phosphatase in phosphorus-deficient Arabidopsis thaliana. Physiol Plant 116: 293–298Google Scholar
  46. Cogliatti DH, Clarkson DT (1983) Physiological changes in, and phosphate uptake by potato plants during development of, and recovery from phosphate deficiency. Physiol Plant 58: 287–294Google Scholar
  47. Cohen D (2007) Earth’s natural wealth: an audit. New Scientist 2605: 35–41Google Scholar
  48. Coltman RR, Gerloff GC, Gabelman WH (1986) Equivalent stress comparisons among tomato strains differentially tolerant to phosphorus deficiency. J Am Soc Hort Sci 111: 422–426Google Scholar
  49. Coruzzi G, Last R (2000) Amino acids. In: Buchanan BB, Gruissem W, Jones RL (eds), Biochemistry & Molecular Biology of Plants. ASPP, Rockville, MD, pp 358–419Google Scholar
  50. Cruz-Ramírez A, Oropeza-Aburto A, Razo-Hernández F, Ramírez-Chávez E, Herrera-Estrella L (2006) Phospholipase Dζ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Proc Natl Acad Sci USA 103: 6765–6770PubMedGoogle Scholar
  51. Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245: 35–47Google Scholar
  52. 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
  53. Dechassa N, Schenk MK, Claassen N, Steingrobe B (2003) Phosphorus efficiency of cabbage (Brassica oleraceae L. var. capitata), carrot (Daucus carota L.), and potato (Solanum tuberosum L.). Plant Soil 250: 215–224Google Scholar
  54. Defra (2000) Fertiliser Recommendations for Agricultural and Horticultural Crops (RB209) (7th edition). HMSO, NorwichGoogle Scholar
  55. Delhaize E, Randall PJ (1995) Characterization of a phosphate-accumulator mutant of Arabidopsis thaliana. Plant Physiol 107: 207–213PubMedGoogle Scholar
  56. Delhaize E, Hebb DM, Ryan PR (2001) Expression of a Pseudomonas aeruginosa citrate synthase gene is not associated with either enhanced citrate accumulation or efflux. Plant Physiol 125: 2059–2067PubMedGoogle Scholar
  57. Delhaize E, Gruber BD, Ryan PR (2007) The roles of organic anion permeases in aluminium resistance and mineral nutrition. FEBS Lett 581: 2255–2262PubMedGoogle Scholar
  58. Dennis DT, Blakeley SD (2000) Carbohydrate metabolism. In: Buchanan BB, Gruissem W, Jones RL (eds), Biochemistry & Molecular Biology of Plants. ASPP, Rockville, MD, pp 630–675Google Scholar
  59. Dinkelaker B, Hengeler C, Marschner H (1995) Distribution and function of proteoid roots and other root clusters. Bot Acta 108: 183–200Google Scholar
  60. Dörmann P, Benning C (2002) Galactolipids rule in seed plants. Trends Plant Sci 7: 112–118PubMedGoogle Scholar
  61. Drew MC (1975) Comparison of the effects of a localized supply of phosphate, nitrate, ammonium and potassium on the growth of the seminal root system, and the shoot, in barley. New Phytol 75: 479–490Google Scholar
  62. Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR, Folarin A, Huberty A, Interlandi S, Kilham SS, McCauley E, Schulz KL, Siemann EH, Sterner RW (2000a) Nutritional constraints in terrestrial and freshwater food webs. Nature 408: 578–580PubMedGoogle Scholar
  63. Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow TA, Cotner JB, Harrison JF, Hobbie SE, Odell GM, Weider LJ (2000b) Biological stoichiometry from genes to ecosystems. Ecol Lett 3: 540–550Google Scholar
  64. Epstein E (1972) Mineral Nutrition of Plants: Principles and Perspectives. Wiley, New YorkGoogle Scholar
  65. Essigmann B, Güler S, Narang RA, Linke D, Benning C (1998) Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 95: 1950–1955PubMedGoogle Scholar
  66. Fageria NK, Baligar VC (1997) Phosphorus use efficiency by corn genotypes. J Plant Nutr 20: 1267–1277Google Scholar
  67. Fageria NK, Baligar VC (1999) Phosphorus-use efficiency in wheat genotypes. J Plant Nutr 22: 331–340Google Scholar
  68. Fageria NK, Wright RJ, Baligar VC (1988) Rice cultivar evaluation for phosphorus use efficiency. Plant Soil 111: 105–109Google Scholar
  69. Fenner M (1986) The allocation of minerals to seeds in Senecio vulgaris plants subjected to nutrient shortage. J Ecol 74: 385–392Google Scholar
  70. Fixen PE (2005) Proceedings of the International Fertiliser Society 569. Decision Support Systems in Integrated Crop Nutrient Management. IFS, YorkGoogle Scholar
  71. Flügge U-I, Häusler RE, Ludewig F, Fischer K (2003) Functional genomics of phosphate antiport systems of plastids. Physiol Plant 118: 475–482Google Scholar
  72. Föhse D, Claassen N, Jungk A (1988) Phosphorus efficiency of plants. I. External and internal P requirement and P uptake efficiency of different plant species. Plant Soil 110: 101–109Google Scholar
  73. Föhse D, Claassen N, Jungk A (1991) Phosphorus efficiency of plants. II. Significance of root radius, root hairs and cation-anion balance for phosphorus influx in seven plant species. Plant Soil 132: 261–272Google Scholar
  74. Forde B, Lorenzo H (2001) The nutritional control of root development. Plant Soil 232: 51–68Google Scholar
  75. Franco-Zorrilla JM, Martín AC, Solano R, Rubio V, Leyva A, Paz-Ares J (2002) Mutations at CRE1 impair cytokinin-induced repression of phosphate starvation responses in Arabidopsis. Plant J 32: 353–360PubMedGoogle Scholar
  76. Franco-Zorrilla JM, González E, Bustos R, Linhares F, Leyva A, Paz-Ares J (2004) The transcriptional control of plant responses to phosphate limitation. J Exp Bot 55: 285–293PubMedGoogle Scholar
  77. Franco-Zorrilla JM, Martín AC, Leyva A, Paz-Ares J (2005) Interaction between phosphate-starvation, sugar, and cytokinin signaling in Arabidopsis and the roles of cytokinin receptors CRE1/AHK4 and AHK3. Plant Physiol 138: 847–857PubMedGoogle Scholar
  78. Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, García JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nature Genet 39: 1033–1037PubMedGoogle Scholar
  79. Frentzen M (2004) Phosphatidylglycerol and sulfoquinovosyldiacylglycerol: anionic membrane lipids and phosphate regulation. Curr Opin Plant Biol 7: 270–276PubMedGoogle Scholar
  80. Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Current Biol 15: 2038–2043Google Scholar
  81. Gahoonia TS, Nielsen NE (2004a) Root traits as tools for creating phosphorus efficient crop varieties. Plant Soil 260: 47–57Google Scholar
  82. Gahoonia TS, Nielsen NE (2004b) Barley genotypes with long root hairs sustain high grain yields in low-P field. Plant Soil 262: 55–62Google Scholar
  83. Garten CT (1976) Correlations between concentrations of elements in plants. Nature 261: 686–688Google Scholar
  84. Gaude N, Tippmann H, Flemetakis E, Katinakis P, Udvardi M, Dormann P (2004) The galactolipid digalactosyldiacylglycerol accumulates in the peribacteroid membrane of nitrogen-fixing nodules of soybean and Lotus. J Biol Chem 279: 34624–34630PubMedGoogle Scholar
  85. Gaume A, Mächler F, De León C, Narro L, Frossard E (2001) Low-P tolerance by maize (Zea mays L.) genotypes: significance of root growth, and organic acids and acid phosphatase root exudation. Plant Soil 228: 253–264Google Scholar
  86. George TS, Richardson AE (2008) Potential and limitations to improving crops for enhanced phosphorus utilization. In: White PJ, Hammond JP (eds), The Ecophysiology of Plant-Phosphorus Interactions. Springer, Dordrecht, The Netherlands, pp 247–270Google Scholar
  87. George TS, Richardson AE, Hadobas PA, Simpson RJ (2004) Characterisation of transgenic Trifolium subterraneum L. which expresses phyA and releases extracellular phytase: growth and P nutrition in laboratory media and soil. Plant Cell Environ 27: 1351–1361Google Scholar
  88. George TS, Richardson AE, Smith JB, Hadobas PA, Simpson RJ (2005a) Limitations to the potential of transgenic Trifolium subterraneum L. plants that exude phytase when grown in soils with a range of organic P content. Plant Soil 278: 263–274Google Scholar
  89. George TS, Simpson RJ, Hadobas PA, Richardson AE (2005b) Expression of a fungal phytase gene in Nicotiana tabacum improves phosphorus nutrition in plants grown in amended soil. Plant Biotech J 3: 129–140Google Scholar
  90. George TS, Gregory PJ, Hocking PJ, Richardson AE (2008) Variation in root-associated phosphatase activities in wheat contributes to the utilisation of organic P substrates in vitro, but does not explain differences in the P nutrition of plants when grown in soil. Environ Exp Bot (in press)Google Scholar
  91. Górny AG, Sodkiewicz T (2001) Genetic analysis of the nitrogen and phosphorus utilization efficiencies in mature spring barley plants. Plant Breeding 120: 129–132Google Scholar
  92. Gourley CJP, Allan DL, Russelle MP (1994) Plant nutrient efficiency: a comparison of definitions and suggested improvement. Plant Soil 158: 29–37Google Scholar
  93. Graham JH (2000) Assessing the costs of arbuscular mycorrhizal symbiosis in agroecosystems. In: Podilha GK, Douds DD (eds), Current Advances in Mycorrhizae Research. APS Press, St Paul, MN, pp 127–142Google Scholar
  94. Green DG, Ferguson WS, Warder FG (1973) Accumulation of toxic levels of phosphorus in the leaves of phosphorus-deficient barley. Can J Plant Sci 53: 241–246Google Scholar
  95. Greenwood DJ, Cleaver TJ, Turner MK, Hunt J, Niendorf KB, Loquens SMH (1980) Comparison of the effects of phosphate fertilizer on the yield, phosphate content and quality of 22 different vegetable and agricultural crops. J Agric Sci 95: 457–469Google Scholar
  96. Greenwood DJ, Stellacci AM, Meacham MC, Broadley MR, White PJ (2005) Phosphorus response components of different Brassica oleracea genotypes are reproducible in different environments. Crop Sci 45: 1728–1735Google Scholar
  97. Greenwood DJ, Stellacci AM, Meacham MC, Mead A, Broadley MR, White PJ (2006) Relative values of physiological parameters of P response of different genotypes can be measured in experiments with only two P treatments. Plant Soil 281: 159–172Google Scholar
  98. Gregory PJ, George TS (2005) Soil Management for Nutrient Use Efficiency - An Overview. Proceedings 564, International Fertiliser Society, YorkGoogle Scholar
  99. Grime JP (2001) Plant Strategies, Vegetation Processes, and Ecosystem Properties (2nd edition). Wiley, ChichesterGoogle Scholar
  100. Grime JP, Thompson K, Hunt R, Hodgson JG, Cornelissen JHC, Rorison IH, Hendry GAF, Ashenden TW, Askew AP, Band SR, Booth RE, Bossard CC, Campbell BD, Cooper JEL, Davison AW, Gupta PL, Hall W, Hand DW, Hannah MA, Hillier SH, Hodkinson DJ, Jalili A, Liu Z, Mackey JML, Matthews N, Mowforth MA, Neal AM, Reader RJ, Reiling K, Ross-Fraser W, Spencer RE, Sutton F, Tasker DE, Thorpe PC, Whitehouse J (1997) Integrated screening validates primary axes of specialisation in plants. Oikos 79: 259–281Google Scholar
  101. Gunawardena SFBN, Danso SKA, Zapata F (1993) Phosphorus requirement and sources of nitrogen in three soybean (Glycine max) genotypes, Bragg, nts 382 and Chippewa. Plant Soil 151: 1–9Google Scholar
  102. Güsewell S (2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytol 164: 243–266Google Scholar
  103. Güsewell S (2005) Nutrient resorption of wetland graminoids is related to the type of nutrient limitation. Funct Ecol 19: 344–354Google Scholar
  104. Güsewell S, Koerselman W (2002) Variation in nitrogen and phosphorus concentrations of wetland plants. Perspect Plant Ecol Evol Syst 5: 37–61Google Scholar
  105. Güsewell S, Bollens U, Ryser P, Klötzli F (2003) Contrasting effects of nitrogen, phosphorus and water regime on first- and second-year growth of 16 wetland plant species. Funct Ecol 11: 754–765Google Scholar
  106. Güsewell S, Bailey KM, Roem WJ, Bedford BL (2005) Nutrient limitation and botanical diversity in wetlands: can fertilisation raise species richness? Oikos 109: 71–80Google Scholar
  107. Hammond JP, White PJ (2008a) Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J Exp Bot 59: 93–109PubMedGoogle Scholar
  108. Hammond JP, White PJ (2008b) Diagnosing phosphorus deficiency in crops. In: White PJ, Hammond JP (eds), The Ecophysiology of Plant-Phosphorus Interactions. Springer, Dordrecht, The Netherlands, pp 225–246Google Scholar
  109. Hammond JP, Bennett MJ, Bowen HC, Broadley MR, Eastwood DC, May ST, Rahn C, Swarup R, Woolaway KE, White PJ (2003) Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiol 132: 578–596PubMedGoogle Scholar
  110. Hammond JP, Broadley MR, White PJ (2004) Genetic responses to phosphorus deficiency. Ann Bot 94: 323–332PubMedGoogle Scholar
  111. Hammond JP, Broadley MR, Craigon DJ, Higgins J, Emmerson Z, Townsend H, White PJ, May ST (2005) Using genomic DNA-based probe-selection to improve the sensitivity of high-density oligonucleotide arrays when applied to heterologous species. Plant Methods 1: 10PubMedGoogle Scholar
  112. Han W, Fang J, Guo D, Zhang Y (2005) Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China. New Phytol 168: 377–385PubMedGoogle Scholar
  113. Haran S, Logendra S, Seskar M, Bratanova M, Raskin I (2000) Characterization of Arabidopsis acid phosphatase promoter and regulation of acid phosphatase expression. Plant Physiol 124: 615–626PubMedGoogle Scholar
  114. Harrison MJ (1999) Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annu Rev Plant Physiol Plant Mol Biol 50: 361–389PubMedGoogle Scholar
  115. Härtel H, Dörmann P, Benning C (2000) DGD1-independent biosynthesis of extraplastidic galactolipids after phosphate deprivation in Arabidopsis. Proc Natl Acad Sci USA 97: 10649–10654PubMedGoogle Scholar
  116. He Z, Ma Z, Brown KM, Lynch JP (2005) Assessment of inequality of root hair density in Arabidopsis thaliana using the Gini coefficient: a close look at the effect of phosphorus and its interaction with ethylene. Ann Bot 95: 287–293PubMedGoogle Scholar
  117. Heathwaite L, Sharpley A, Bechmann M (2003) The conceptual basis for a decision support framework to assess the risk of phosphorus loss at the field scale across Europe. J Plant Nutr Soil Sci 166: 447–458Google Scholar
  118. Hedley MJ, Mortvedt JJ, Bolan NS, Syers JK (1995) Phosphorus fertility management in agroecosystems. In: Tiessen H (ed), Phosphorus in the Global Environment. Transfers Cycles and Management, Wiley, Chichester, pp 59–92Google Scholar
  119. Hermans C, Hammond JP, White PJ, Verbruggen N (2006) How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci 11: 610–617PubMedGoogle Scholar
  120. 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
  121. Hewitt MM, Carr JM, Williamson CL, Slocum RD (2005) Effects of phosphate limitation on expression of genes involved in pyrimidine synthesis and salvaging in Arabidopsis. Plant Physiol Biochem 43: 91–99PubMedGoogle Scholar
  122. 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
  123. Hipps NA, Davies MJ, Dodds P, Buckley GP (2005) The effects of phosphorus nutrition and soil pH on the growth of some ancient woodland indicator plants and their interaction with competitor species. Plant Soil 271: 131–141Google Scholar
  124. Ho MD, Rosas JC, Brown KM, Lynch JP (2005) Root architectural tradeoffs for water and phosphorus acquisition. Funct Plant Biol 32: 737–748Google Scholar
  125. Hoch WA, Zeldin EL, McCown BH (2001) Physiological significance of anthocyanins during autumnal leaf senescence. Tree Physiol 21: 1–8PubMedGoogle Scholar
  126. Hocking P (2001) Organic acids exuded from roots in phosphorus uptake and aluminium tolerance of plants in acid soils. Adv Agron 74: 63–97Google Scholar
  127. Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162: 9–24Google Scholar
  128. Hoffland E (1992) Quantitative evaluation of the role of organic acid exudation in the mobilization of rock phosphate by rape. Plant Soil 140: 279–289Google Scholar
  129. Horst WJ, Kamh M, Jibrin JM, Chude VO (2001) Agronomic measures for increasing P availability to crops. Plant Soil 237: 211–223Google Scholar
  130. Hou XL, Wu P, Jiao FC, Jia QJ, Chen HM, Yu J, Song XW, Yi KK (2005) Regulation of the expression of OsIPS1 and OsIPS2 in rice via systemic and local Pi signalling and hormones. Plant Cell Environ 28: 353–364Google Scholar
  131. Hutchings MJ, John EA (2004) The effects of environmental heterogeneity on root growth and root/shoot partitioning. Ann Bot 94: 1–8PubMedGoogle Scholar
  132. Ishikawa S, Adu-Gyamfi JJ, Nakamura T, Yoshihara T, Watanabe T, Wagatsuma T (2002) Genotypic variability in phosphorus solubilising activity of root exudates by pigeon pea grown in low-nutrient environments. Plant Soil 245: 71–81Google Scholar
  133. Jain A, Poling MD, Karthikeyan AS, Blakeslee JJ, Peer WA, Titapiwatanakun B, Murphy AS, Raghothama KG (2007a) Differential effects of sucrose and auxin on localized phosphate deficiency-induced modulation of different traits of root system architecture in Arabidopsis. Plant Physiol 144: 232–247PubMedGoogle Scholar
  134. Jain A, Vasconcelos MJ, Raghothama KG, Sahi SV (2007b) Molecular mechanisms of plant adaptation to phosphate deficiency. Plant Breeding Rev 29: 359–419Google Scholar
  135. Janssens F, Peeters A, Tallowin JRB, Bakker JP, Bekker RM, Fillat F, Oomes MJM (1998) Relationship between soil chemical factors and grassland diversity. Plant Soil 202: 69–78Google Scholar
  136. Jeschke WD, Kirkby EA, Peuke AD, Pate JS, Hartung W (1997) Effects of P deficiency on assimilation and transport of nitrate and phosphate in intact plants of castor bean (Ricinus communis L.). J Exp Bot 48: 75–91Google Scholar
  137. Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135: 575–586Google Scholar
  138. Johnston AE, Lane PW, Mattingly GEG, Poulton PR, Hewitt MV (1986) Effects of soil and fertilizer P on yields of potatoes, sugar beet, barley and winter wheat on a sandy clay loam soil at Saxmundham, Suffolk. J Agric Sci 106: 155–167Google Scholar
  139. Jones DL (1998) Organic acids in the rhizosphere - a critical review. Plant Soil 205: 25–44Google Scholar
  140. Jones DL, Dennis PG, Owen AG, van Hees PAW (2003) Organic acid behavior in soils - misconceptions and knowledge gaps. Plant Soil 248: 31–41Google Scholar
  141. Jouhet J, Maréchal E, Baldan B, Bligny R, Joyard J, Block MA (2004) Phosphate deprivation induces transfer of DGDG galactolipid from chloroplast to mitochondria. J Cell Biol 167: 863–874PubMedGoogle Scholar
  142. Jungk A (2001) Root hairs and the acquisition of plant nutrients from soil. J Plant Nutr Soil Sci 164: 121–129Google Scholar
  143. Karandashov V, Bucher M (2005) Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci 10: 22–29PubMedGoogle Scholar
  144. Karthikeyan AS, Varadarajan DK, Jain A, Held MA, Carpita NC, Raghothama KG (2007) Phosphate starvation responses are mediated by sugar signaling in Arabidopsis. Planta 225: 907–918PubMedGoogle Scholar
  145. Kerkhoff AJ, Fagan WF, Elser JJ, Enquist BJ (2006) Phylogenetic and growth form variation in the scaling of nitrogen and phosphorus in the seed plants. Am Nat 168: E103–E122PubMedGoogle Scholar
  146. Kirkby EA, Johnston AE (2008) Soil and fertilizer phosphorus in relation to crop nutrition. In: White PJ, Hammond JP (eds), The Ecophysiology of Plant-Phosphorus Interactions. Springer, Dordrecht, The Netherlands, pp 177–223Google Scholar
  147. Klepper B (1992) Development and growth of crop root systems. Adv Soil Sci 19: 1–25Google Scholar
  148. Kobayashi K, Masuda T, Takamiya K-I, Ohta H (2006) Membrane lipid alteration during phosphate starvation is regulated by phosphate signaling and auxin/cytokinin cross-talk. Plant J 47: 238–248PubMedGoogle Scholar
  149. 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
  150. Laegreid M, Bøckman OC, Kaarstad O (1999) Agriculture, Fertilizers and the Environment. CABI, WallingfordGoogle Scholar
  151. 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: 693–713PubMedGoogle Scholar
  152. Lamont BB (2003) Structure, ecology and physiology of root clusters – a review. Plant Soil 248: 1–19Google Scholar
  153. Lee RB, Ratcliffe RG, Southon TE (1990) 31P NMR measurements of the cytoplasmic and vacuolar Pi content of mature maize roots: relationships with phosphorus status and phosphate fluxes. J Exp Bot 41: 1063–1078Google Scholar
  154. Li M, Osaki M, Rao IM, Tadano T (1997) Secretion of phytase from the roots of several plant species under phosphorus-deficient conditions. Plant Soil 195: 161–169Google Scholar
  155. Li M, Welti R, Wang X (2006) Quantitive profiling of Arabidopsis polar glycerolipids in response to phosphorus starvation. Roles of phospholipases Dζ1 and Dζ2 in phosphatidylcholine hydrolysis and digalactosyldiacylglycerol accumulation in phosphorus-starved plants. Plant Physiol 142: 750–761PubMedGoogle Scholar
  156. Liao H, Yan X, Rubio G, Beebe SE, Blair MW, Lynch JP (2004) Genetic mapping of basal root gravitropism and phosphorus acquisition efficiency in common bean. Funct Plant Biol 31: 959–970Google Scholar
  157. 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
  158. Liu C, Muchhal US, Raghothama KG (1997) Differential expression of TPSI1, a phosphate starvation-induced gene in tomato. Plant Mol Biol 33: 867–874PubMedGoogle Scholar
  159. Liu J, Li Y, Tong Y, Gao J, Li B, Li J, Li Z (2001) Chromosomal location of genes conferring the tolerance to Pi starvation stress and acid phosphatase (APase) secretion in the genome of rye (Secale cereale L.) Plant Soil 237: 267–274Google Scholar
  160. Liu J, Samac DA, Bucciarelli B, Allan DL, Vance CP (2005) Signaling of phosphorus deficiency-induced gene expression in white lupin requires sugar and phloem transport. Plant J 41: 257–268PubMedGoogle Scholar
  161. Lloyd JC, Zakhleniuk OV (2004) Responses of primary and secondary metabolism to sugar accumulation revealed by microarray expression analysis of the Arabidopsis mutant, pho3. J Exp Bot 55: 1221–1230PubMedGoogle Scholar
  162. Loneragan JF, Asher CH (1967) Responses of plants to phosphate concentration in solution culture. II. Role of phosphate absorption and its relation to growth. Soil Sci 103: 311–318Google Scholar
  163. Loneragan JF, Grunes DL, Welch RM, Aduayi EA, Tengah A, Lazar VA, Cary EE (1982) Phosphorus accumulation and toxicity in leaves in relation to zinc supply. Soil Sci Soc Am J 46: 345–352Google Scholar
  164. López-Bucio J, de la Vega OM, Guevara-García A, Herrera-Estrella L (2000a) Enhanced phosphorus uptake in transgenic tobacco plants that overproduce citrate. Nature Biotech 18: 450–453Google Scholar
  165. López-Bucio J, Nieto-Jacobo MF, Ramírez-Rodríguez V, Herrera-Estrella L (2000b) Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils. Plant Sci 160: 1–13PubMedGoogle Scholar
  166. López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129: 244–256PubMedGoogle Scholar
  167. López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6: 280–287PubMedGoogle Scholar
  168. López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Pérez-Torres A, Rampey RA, Bartel B, Herrera-Estrella L (2005) An auxin transport independent pathway is involved in phosphate stress-induced root architectural alterations in Arabidopsis. Identification of BIG as a mediator of auxin pericycle cell activation. Plant Physiol 137: 681–691PubMedGoogle Scholar
  169. Lott JNA, Ockenden I, Raboy V, Batten GD (2000) Phytic acid and phosphorus in crop seeds and fruits: a global estimate. Seed Sci Res 10: 11–33Google Scholar
  170. Lynch JP, Brown KM (2001) Topsoil foraging - an architectural adaptation of plants to low phosphorus availability. Plant Soil 237: 225–237Google Scholar
  171. Ma Z, Baskin TI, Brown KM, Lynch JP (2003) Regulation of root elongation under phosphorus stress involves changes in ethylene responsiveness. Plant Physiol 131: 1381–1390PubMedGoogle Scholar
  172. Malamy JE (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ 28: 67–77PubMedGoogle Scholar
  173. Malkin R, Niyogi K (2000) Photosynthesis. In: Buchanan BB, Gruissem W, Jones RL (eds), Biochemistry & Molecular Biology of Plants. ASPP, Rockville, MD, pp 568–628Google Scholar
  174. Mamolos AP, Veresoglou DS, Barbayiannis N (1995) Plant species abundance and tissue concentrations of limiting nutrients in low-nutrient grasslands: a test of competition theory. J Ecol 83: 485–495Google Scholar
  175. Manske GGB, Ortiz-Monasterio JI, Van Grinkel M, González R, Rajaram S, Molina E, Vlek PLG (2000) Traits associated with improved P-uptake efficiency in CIMMYT’s semidwarf spring bread wheat grown on an acid Andisol in Mexico. Plant Soil 221: 189–204Google Scholar
  176. Marschner H (1995) Mineral Nutrition of Higher Plants (2nd edition). Academic, LondonGoogle Scholar
  177. Marschner P (2008) The effect of rhizosphere microorganisms on P uptake by plants. In: White PJ, Hammond JP (eds), The Ecophysiology of Plant-Phosphorus Interactions. Springer, Dordrecht, The Netherlands, pp 165–176Google Scholar
  178. Marschner P, Solaiman Z, Rengel Z (2007) Brassica genotypes differ in growth, phosphorus uptake and rhizosphere properties under P-limiting conditions. Soil Biol Biochem 39: 87–98Google Scholar
  179. Martín AC, del Pozo JC, Iglesias J, Rubio V, Solano R, de la Peña A, Leyva A, Paz-Ares J (2000) Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J 24: 559–567PubMedGoogle Scholar
  180. McCrea AR, Trueman IC, Fullen MA (2004) Factors relating to soil fertility and species diversity in both semi-natural and created meadows in the West Midlands of England. Eur J Soil Sci 55: 335–348Google Scholar
  181. McGroddy ME, Daufresne T, Hedin LO (2004) Scaling of C:N:P stoichiometry in forests worldwide: implications of terrestrial Redfield-type ratios. Ecology 85: 2390–2401Google Scholar
  182. Mengel K (1997) Agronomic measures for better utilization of soil and fertilizer phosphates. Eur J Agron 7: 221–233Google Scholar
  183. Mengel K, Kirkby EA (2001) Principles of Plant Nutrition (5th edition). Kluwer, Dordrecht, The NetherlandsGoogle Scholar
  184. 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: 594–606PubMedGoogle Scholar
  185. Mimura T (1999) Regulation of phosphate transport and homeostasis in plant cells. Int Rev Cytol 191: 149–200Google Scholar
  186. Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, Ortet P, Creff A, Somerville S, Rolland N, Doumas P, Nacry P, Herrerra-Estrella L, Nussaume L, Thibaud M-C (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
  187. Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, Baek D, Koo YD, Jin JB, Bressan RA, Yun D-J, Hasegawa PM (2005) The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci USA 102: 7760–7765PubMedGoogle Scholar
  188. Morcuende R, Bari R, Gibon Y, Zheng WM, Pant BD, Bläsing O, Usadel B, Czechowski T, Udvardi MK, Stitt M, Scheible WR (2007) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 30: 85–112PubMedGoogle Scholar
  189. Morgan JAW, Bending GD, White PJ (2005) Biological costs and benefits to plant-microbe interactions in the rhizosphere. J Exp Bot 56: 1729–1739PubMedGoogle Scholar
  190. Mudge SR, Smith FW, Richardson AE (2003) Root-specific and phosphate-regulated expression of phytase under the control of a phosphate transporter promoter enables Arabidopsis to grow on phytate as a sole phosphorus source. Plant Sci 165: 871–878Google Scholar
  191. Müller R, Nilsson L, Krintel C, Nielsen TH (2004) Gene expression during recovery from phosphate starvation in roots and shoots of Arabidopsis thaliana. Physiol Plant 122: 233–243Google Scholar
  192. Müller R, Nilsson L, Nielsen LK, Nielsen TH (2005) Interaction between phosphate starvation signalling and hexokinase-independent sugar sensing in Arabidopsis leaves. Physiol Plant 124: 81–90Google Scholar
  193. Müller R, Morant M, Jarmer H, Nilsson L, Nielsen TH (2007) Genome-wide analysis of the Arabidopsis leaf transcriptome reveals interaction of phosphate and sugar metabolism. Plant Physiol 143: 156–171PubMedGoogle Scholar
  194. Nacry P, Canivenc G, Muller B, Azmi A, Van Onckelen H, Rossignol M, Doumas P (2005) A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiol 138: 2061–2074PubMedGoogle Scholar
  195. Narang RA, Bruene A, Altmann T (2000) Analysis of phosphate acquisition efficiency in different Arabidopsis accessions. Plant Physiol 124: 1786–1799PubMedGoogle Scholar
  196. Neumann G, Römheld V (1999) Root excretion of carboxylic acids and protons in phosphorus-deficient plants. Plant Soil 211: 121–130Google Scholar
  197. Niklas KJ (2008) Carbon/nitrogen/phosphorus allometric relations across species. In: White PJ, Hammond JP (eds), The Ecophysiology of Plant-Phosphorus Interactions. Springer, Dordrecht, The Netherlands, pp 9–30Google Scholar
  198. Niklas KJ, Owens T, Reich PB, Cobb ED (2005) Nitrogen/phosphorus leaf stoichiometry and the scaling of plant growth. Ecol Lett 8: 636–642Google Scholar
  199. Oberson A, Joner EJ (2005) Microbial turnover of phosphorus in soil. In: Turner BL, Frossard E, Baldwin DS (eds), Organic Phosphorus in the Environment. CABI, Wallingford, pp 133–164Google Scholar
  200. 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
  201. Oracka T, Łapiñski B (2006) Nitrogen and phosphorus uptake and utilization efficiency in D(R) substitution lines of hexaploid triticale. Plant Breeding 125: 221–224Google Scholar
  202. Osborne LD, Rengel Z (2002) Screening cereals for genotypic variation in efficiency of phosphorus uptake and utilisation. Aust J Agric Res 53: 295–303Google Scholar
  203. O’Toole JC, Bland WL (1987) Genotypic variation in crop plant root systems. Adv Agron 41: 91–145Google Scholar
  204. Oyanagi A (1994) Gravitropic response growth angle and vertical distribution of roots of wheat (Triticum aestivum L.). Plant Soil 165: 323–326Google Scholar
  205. Ozanne PG, Keay J, Biddiscombe EF (1969) The comparative applied phosphate requirement of eight annual pasture species. Aust J Biol Sci 20: 809–818Google Scholar
  206. Ozturk L, Eker S, Torun B, Cakmak I (2005) Variation in phosphorus efficiency among 73 bread and durum wheat genotypes grown in a phosphorus-deficient calcareous soil. Plant Soil 269: 69–80Google Scholar
  207. Paterson E, Sim A, Standing D, Dorward M, McDonald AJS (2006) Root exudation from Hordeum vulgare in response to localized nitrate supply. J Exp Bot 57: 2413–2420PubMedGoogle Scholar
  208. Paul MJ, Pellny TK (2003) Carbon metabolite feedback regulation of leaf photosynthesis and development. J Exp Bot 54: 539–547PubMedGoogle Scholar
  209. Pearse SJ, Venaklaas EJ, Cawthray G, Bolland MDA, Lambers H (2007) Carboxylate composition of root exudates does not relate consistently to a crop species’ ability to use phosphorus from aluminium, iron or calcium phosphate sources. New Phytol 173: 181–190PubMedGoogle Scholar
  210. Pearse SJ, Veneklaas EJ, Cawthray G, Bolland MDA, Lambers H (2008) Rhizosphere processes do not explain variation in P acquisition from sparingly soluble forms of P among Lupinus albus accessions. Aust J Agric Res 59: (in press)Google Scholar
  211. Perrott KW, Kear MJ (2000) Laboratory comparison of nutrient release rates from fertilizers. Commun Soil Sci Plant Anal 31: 2007–2017Google Scholar
  212. Petters J, Göbel C, Scheel D, Rosahl S (2002) A pathogen-responsive cDNA from potato encodes a protein with homology to a phosphate starvation-induced phosphatase. Plant Cell Physiol 43: 1049–1053PubMedGoogle Scholar
  213. Plaxton WC, Carswell MC (1999) Metabolic aspects of the phosphate starvation response in plants. In: Lerner HR (ed), Plant Responses to Environmental Stresses: From Phytohormones to Genome Reorganisation. Dekker, New York, pp 349–372Google Scholar
  214. Raghothama KG, Karthikeyan AS (2005) Phosphate acquisition. Plant Soil 274: 37–49Google Scholar
  215. Rao IM, Fredeen AL, Terry N (1990) Leaf phosphate status, photosynthesis, and carbon partitioning in sugar beet. Plant Physiol 92: 29–36PubMedGoogle Scholar
  216. Raven JA (2008) Phosphorus and the future. In: White PJ, Hammond JP (eds), The Ecophysiology of Plant-Phosphorus Interactions. Springer, Dordrecht, The Netherlands, pp 271–283Google Scholar
  217. Rengel Z, Marschner P (2005) Nutrient availability and management in the rhizosphere: exploiting genotypic differences. New Phytol 168: 305–312PubMedGoogle Scholar
  218. Reymond M, Svistoonoff S, Loudet O, Nussaume L, Desnos T (2006) Identification of QTL controlling root growth response to phosphate starvation in Arabidopsis thaliana. Plant Cell Environ 29: 115–125PubMedGoogle Scholar
  219. Richardson AE, Hadobas PA, Hayes JE (2001) Extracellular secretion of Aspergillus phytase from Arabidopsis roots enables plants to obtain phosphorus from phytate. Plant J 25: 641–649PubMedGoogle Scholar
  220. Robinson D (1994) The responses of plants to non-uniform supplies of nutrients. New Phytol 127: 635–674Google Scholar
  221. Rook F, Hadingham SA, Li Y, Bevan MW (2006) Sugar and ABA response pathways and the control of gene expression. Plant Cell Environ 29: 426–434PubMedGoogle Scholar
  222. Rorison IM (1968) The response to phosphorus of some ecologically distinct plant species. I. Growth rates and phosphorus absorption. New Phytol 67: 913–923Google Scholar
  223. Rubio G, Liao H, Yan XL, Lynch JP (2003) Topsoil foraging and its role in plant competitiveness for phosphorus in common bean. Crop Sci 43: 598–607Google Scholar
  224. Rubio G, Sorgonà A, Lynch JP (2004) Spatial mapping of phosphorus influx in bean root systems using digital autoradiography. J Exp Bot 55: 2269–2280PubMedGoogle Scholar
  225. Rubio V, Linhares F, Solano R, Martín AC, Iglesias J, Leyva A, Paz-Ares J (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev 15: 2122–2133PubMedGoogle Scholar
  226. 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
  227. Sánchez-Calderón L, López-Bucio J, Chacón-López A, Cruz-Ramírez A, Nieto-Jacobo F, Dubrovsky JG, Herrera-Estrella L (2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol 46: 174–184PubMedGoogle Scholar
  228. Sánchez-Calderón L, López-Bucio J, Chacón-López A, Gutiérrez-Ortega A, Hernández-Abreu E, Herrera-Estrella L (2006) Characterization of low phosphorus insensitive mutants reveals a crosstalk between low P-induced determinate root development and the activation of genes involved in the adaptation of Arabidopsis to P deficiency. Plant Physiol 140: 879–889PubMedGoogle Scholar
  229. Sanginga N, Lyasse O, Singh BB (2000) Phosphorus use efficiency and nitrogen balance of cowpea breeding lines in a low P soil derived from savanna zone in West Africa. Plant Soil 220: 119–128Google Scholar
  230. Sattelmacher B, Kuene R, Malagamba P, Moreno U (1990) Evaluation of tuber bearing Solanum species belonging to different ploidy levels for its yielding potential at low soil fertility. Plant Soil 129: 227–233Google Scholar
  231. Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116: 447–453PubMedGoogle Scholar
  232. Schulze J, Temple G, Temple SJ, Beschow H, Vance CP (2006) Nitrogen fixation by white lupin under phosphorus deficiency. Ann Bot 98: 731–740PubMedGoogle Scholar
  233. Schünmann PHD, Richardson AE, Vickers CE, Delhaize E (2004) Promoter analysis of the barley Pht1;1 phosphate transporter gene identifiesregions controlling root expression and responsiveness to phosphate deprivation. Plant Physiol 136: 4205–4214PubMedGoogle Scholar
  234. Shane MW, de Vos M, De Roock S, Lambers H (2003) Shoot P status regulates cluster-root growth and citrate exudation in Lupinus albus grown with a divided root system. Plant Cell Environ 26: 265–273Google Scholar
  235. Shane MW, McCully ME, Lambers H (2004) Tissue and cellular phosphorus storage during development of phosphorus toxicity in Hakea prostrata (Proteaceae). J Exp Bot 55: 1033–1044PubMedGoogle Scholar
  236. 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
  237. Shin H, Shin HS, Chen R, Harrison MJ (2006) Loss of At4 function impacts phosphate distribution between the roots and the shoots during phosphate starvation. Plant J 45: 712–726PubMedGoogle Scholar
  238. Siedow JN, Day DA (2000) Respiration and photorespiration. In: Buchanan BB, Gruissem W, Jones RL (eds), Biochemistry & Molecular Biology of Plants. ASPP, Rockville, MD, pp 676–728Google Scholar
  239. Smith FW, Mudge SR, Rae AL, Glassop D (2003) Phosphate transport in plants. Plant Soil 248: 71–83Google Scholar
  240. Smith SE, Read DJ (2007) Mycorrhizal Symbiosis (3rd edition). Elsevier, LondonGoogle Scholar
  241. Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133: 16–20PubMedGoogle Scholar
  242. Smith VH (1992) Effects of nitrogen: phosphorus supply ratios on nitrogen fixation in agricultural and pastoral ecosystems. Biogeochemistry 18: 19–35Google Scholar
  243. Solfanelli C, Poggi A, Loreti E, Alpi A, Perata P (2006) Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol 140: 637–646PubMedGoogle Scholar
  244. Somerville C, Browse J, Jaworski JG, Ohlrogge JB (2000) Lipids. In: Buchanan BB, Gruissem W, Jones RL (eds), Biochemistry & Molecular Biology of Plants. ASPP, Rockville, MD, pp 456–527Google Scholar
  245. Stalham MA, Allen EJ (2001) Effect of variety, irrigation regime and planting date on depth, rate, duration and density of root growth in the potato (Solanum tuberosum) crop. J Agric Sci 137: 251–270Google Scholar
  246. Steen I (1998) Phosphorus availability in the 21st century: management of a non-renewable resource. Phosphorus Potassium 217: 25–31Google Scholar
  247. Stöcklin J, Schweizer K, Körner C (1998) Effects of elevated CO2 and phosphorus addition on productivity and community composition of intact monoliths from calcareous grassland. Oecologia 116: 50–56Google Scholar
  248. Ström L (1997) Root exudation of organic acids: importance to nutrient availability and the calcifuge and calcicole behaviour of plants. Oikos 80: 459–466Google Scholar
  249. Su J, Xiao Y, Li M, Liu Q, Li B, Tong Y, Jia J, Li Z (2006) Mapping QTLs for phosphorus-deficiency tolerance at wheat seedling stage. Plant Soil 281: 25–36Google Scholar
  250. Subbarao GV, Ae N, Otani T (1997) Genotypic variation in the iron- and aluminium-phosphate solubilising activity of pigeon pea root exudates under P deficient conditions. Soil Sci Plant Nutr 43: 295–305Google Scholar
  251. Sunkar R, Zhu J-K (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16: 2001–2019PubMedGoogle Scholar
  252. Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L, Blanchet A, Nussaume L, Desnos T (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet 39: 792–796PubMedGoogle Scholar
  253. Tadano T, Sasaki H (1991) Secretion of acid phosphatase by the roots of several crop species under phosphorus-deficient conditions. Soil Sci Plant Nutr 37: 129–140Google Scholar
  254. Teng S, Keurentjes J, Bentsink L, Koornneef M, Smeekens S (2005) Sucrose-specific induction of anthocyanin biosynthesis in Arabidopsis requires the MYB75/PAP1 gene. Plant Physiol 139: 1840–1852PubMedGoogle Scholar
  255. Tesfaye M, Liu J, Allan DL, Vance CP (2007) Genomic and genetic control of phosphate stress in legumes. Plant Physiol 144: 594–603PubMedGoogle Scholar
  256. Tessier JT, Raynal DJ (2003) Use of nitrogen to phosphorus ratios in plant tissue as an indicator of nutrient limitation and nitrogen saturation. J Appl Ecol 40: 523–534Google Scholar
  257. Thomas C, Sun Y, Naus K, Lloyd A, Roux S (1999) Apyrase functions in plant phosphate nutrition and mobilizes phosphate from extracellular ATP. Plant Physiol 119: 543–551PubMedGoogle Scholar
  258. Thompson K, Parkinson JA, Band SR, Spencer RE (1997) A comparative study of leaf nutrient concentrations in a regional herbaceous flora. New Phytol 136: 679–689Google Scholar
  259. Thornton B, Paterson E, Midwood AJ, Sim A, Pratt SM (2004) Contribution of current carbon assimilation in supplying root exudates of Lolium perenne measured using steady-state 13C labeling. Physiol Plant 120: 434–441PubMedGoogle Scholar
  260. Tian G, Carsky RJ, Kang BT (1998) Differential phosphorus responses of leguminous cover crops on soil with variable history. J Plant Nutr 21: 1641–1653Google Scholar
  261. Ticconi CA, Abel S (2004) Short on phosphate: plant surveillance and countermeasures. Trends Plant Sci 9: 548–555PubMedGoogle Scholar
  262. Ticconi CA, Delatorre CA, Lahner B, Salt DE, Abel S (2004) Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. Plant J 37: 801–814PubMedGoogle Scholar
  263. Tomscha JL, Trull MC, Deikman J, Lynch JP, Guiltinan MJ (2004) Phosphatase under-producer mutants have altered phosphorus relations. Plant Physiol 135: 334–345PubMedGoogle Scholar
  264. Trehan SP, Sharma RC (2003) External phosphorus requirement of different potato (Solanum tuberosum) cultivars resulting from different internal requirements and uptake efficiencies. Indian J Agric Sci 73: 54–56Google Scholar
  265. Turner BL (2007) Inositol phosphates in soil: amounts, forms and significance of the phosphorylated inositol stereoisomers. In: Turner BL, Richardson AE, Mullaney EJ (eds), Inositol Phosphates: Linking Agriculture and the Environment. CABI, Wallingford, pp 186–206Google Scholar
  266. Uhde-Stone C, Zinn KE, Ramirez-Yáñez M, Li A, Vance CP, Allan DL (2003) Nylon filter arrays reveal differential gene expression in proteoid roots of white lupin in response to phosphorous deficiency. Plant Physiol 131: 1064–1079PubMedGoogle Scholar
  267. Vádez V, Lasso JH, Beck DP, Drevon JJ (1999) Variability of N2-fixation in common bean (Phaseolus vulgaris L.) under P deficiency is related to P use efficiency. Euphytica 106: 231–242Google Scholar
  268. 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
  269. Vančura V, Hovadík A (1965) Root exudates of plants. II. Composition of root exudates of some vegetables. Plant Soil 22: 21–32Google Scholar
  270. 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
  271. Wasaki J, Shinano T, Onishi K, Yonetani R, Yazaki J, Fujii F, Shimbo K, Ishikawa M, Shimatani Z, Nagata Y, Hashimoto A, Ohta T, Sato Y, Miyamoto C, Honda S, Kojima K, Sasaki T, Kishimoto N, Kikuchi S, Osaki M (2006) Transcriptomic analysis indicates putative metabolic changes caused by manipulation of phosphorus availability in rice leaves. J Exp Bot 57: 2049–2059PubMedGoogle Scholar
  272. Wassen MJ, Olde Venterink H, Lapshina ED, Tanneberger F (2005) Endangered plants persist under phosphorus limitation. Nature 437: 547–550PubMedGoogle Scholar
  273. White PJ (2003) Ion transport. In: Thomas B, Murphy DJ, Murray BG (eds), Encyclopaedia of Applied Plant Sciences. Academic, London, pp 625–634Google Scholar
  274. White PJ, Broadley MR, Greenwood DJ, Hammond JP (2005a) Genetic Modifications to Improve Phosphorus Acquisition by Roots. Proceedings 568, International Fertiliser Society, YorkGoogle Scholar
  275. White PJ, Broadley MR, Hammond JP, Thompson AJ (2005b) Optimising the potato root system for phosphorus and water acquisition in low-input growing systems. Aspects Appl Biol 73: 111–118Google Scholar
  276. Wissuwa M (2003) How do plants achieve tolerance to phosphorus deficiency? Small causes with big effects. Plant Physiol 133: 1947–1958PubMedGoogle Scholar
  277. Wissuwa M (2005) Combining a modeling with a genetic approach in establishing associations between genetic and physiological effects in relation to phosphorus uptake. Plant Soil 269: 57–68Google Scholar
  278. Wissuwa M, Gamat G, Ismail AM (2005) Is root growth under phosphorus deficiency affected by source or sink limitations? J Exp Bot 56: 1943–1950PubMedGoogle Scholar
  279. Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Garnier E, Hikosaka K, Lamont BB, Lee W, Oleksyn J, Osada N, Poorter H, Villar R, Warton DI, Westoby M (2005) Assessing the generality of global leaf trait relationships. New Phytol 166: 485–496PubMedGoogle Scholar
  280. 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
  281. Xiao K, Harrison MJ, Wang Z-Y (2005) Transgenic expression of a novel M. truncatula phytase gene results in improved acquisition of organic phosphorus by Arabidopsis. Planta 222: 27–36PubMedGoogle Scholar
  282. Xiao K, Katagi H, Harrison M, Wang ZY (2006) Improved phosphorus acquisition and biomass production in Arabidopsis by transgenic expression of a purple acid phosphatase gene from M. truncatula. Plant Sci 170: 191–202Google Scholar
  283. Yan X, Beebe SE, Lynch JP (1995a) Genetic variation for phosphorus efficiency of common bean in contrasting soil types. II. Yield response. Crop Sci 35: 1094–1099Google Scholar
  284. Yan X, Lynch JP, Beebe SE (1995b) Genetic variation for phosphorus efficiency of common bean in contrasting soil types. I. Vegetative response. Crop Sci 35: 1086–1093Google Scholar
  285. Yan X, Liao H, Beebe SE, Blair MW, Lynch JP (2004) QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant Soil 265: 17–29Google Scholar
  286. Yan Y, Wu P, Ling H, Xu G, Xu F, Zhang Q (2006) Plant nutriomics in China: an overview. Ann Bot 98: 473–482PubMedGoogle Scholar
  287. Yu B, Xu C, Benning C (2002) Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth. Proc Natl Acad Sci USA 99: 5732–5737PubMedGoogle Scholar
  288. Zhang K, Greenwood DJ, White PJ, Burns IG (2007) A dynamic model for the combined effects of N, P and K fertilizers on yield and mineral composition; description and experimental test. Plant Soil 298: 81–98Google Scholar
  289. Zhang YJ, Lynch JP, Brown KM (2003) Ethylene and phosphorus availability have interacting yet distinct effects on root hair development. J Exp Bot 54: 2351–2361PubMedGoogle Scholar
  290. Zhao J, Fu J, Liao H, He Y, Nian H, Hu Y, Qiu L, Dong Y, Yan X (2004) Characterisation of root architecture in an applied core collection for phosphorus efficiency of soybean germplasm. Chinese Sci Bull 49: 1611–1620Google Scholar
  291. Zhu J, Lynch JP (2004) The contribution of lateral rooting to phosphorus acquisition efficiency in maize (Zea mays) seedlings. Funct Plant Biol 31: 949–958Google Scholar
  292. Zhu J, Kaeppler SM, Lynch JP (2005) Topsoil foraging and phosphorus acquisition efficiency in maize (Zea mays). Funct Plant Biol 32: 749–762Google Scholar
  293. Zhu J, Mickelson SM, Kaeppler SM, Lynch JP (2006) Detection of quantitative trait loci for seminal root traits in maize (Zea mays L.) seedlings grown under differential phosphorus levels. Theor Appl Genet 113: 1–10PubMedGoogle Scholar
  294. Zimmermann P, Zardi G, Lehmann M, Zeder C, Amrhein N, Frossard E, Bucher M (2003) Engineering the root-soil interface via targeted expression of a synthetic phytase gene in trichoblasts. Plant Biotech J 1: 353–360Google Scholar
  295. Zimmermann P, Regierer B, Kossmann J, Frossard E, Amrhein N, Bucher M (2004) Differential expression of three purple acid phosphatases from potato. Plant Biol 6: 519–528PubMedGoogle Scholar

Copyright information

© Springer Science + Business Media B.V 2008

Authors and Affiliations

  • Philip J. White
    • 1
  • John P. Hammond
    • 2
  1. 1.Scottish Crop Research InstituteUK
  2. 2.Warwick HRIUniversity of WarwickUK

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