Advertisement

Potential and limitations to improving crops for enhanced phosphorus utilization

  • Timothy S. George
  • Alan E. Richardson
Part of the Plant Ecophysiology book series (KLEC, volume 7)

Phosphorus (P) is an essential element required for cellular function and when deficient has a significant impact on plant growth and fecundity. Poor availability of P in soil and consequent P-deficiency represents a major constraint to crop production globally (Runge-Metzger 1995). Soil P status is also a key factor that controls the competitive dynamics and species composition in different natural ecosystems (McGill and Cole 1981; Attiwill and Adams 1993), and thus may have significant impact on biodiversity (Wassen et al. 2005). Many plant species have evolved in P-limited environments and, as a consequence, are known to possess a number of adaptive features that can enhance the acquisition of P from soil (Raghothama 1999; Vance et al. 2003; Richardson et al. 2005). However, ongoing selection of crop cultivars, in nutrient replete environments, for traits such as yield and vigor (and thus an adaptation to optimal production systems), may have resulted in cultivars that have ‘lost’ adaptive traits that are required to cope with P-deficiency (Manske et al. 2000; Buso and Bliss 1988). Identification of such traits and their introduction into elite material from traditional cultivars, wild relatives and other species through modern approaches in breeding (e.g. marker-assisted selection and/or genetic manipulation) may provide new opportunities to improve the efficiency of P-uptake by crop plants.

Keywords

Root Hair Plant Soil Organic Phosphorus Arbuscular Mycorrhizae 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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ae N, Arihara J, Okada K (1991) Phosphorus uptake mechanisms of pigeon pea grown in alfisols and vertisols. In: Johansen C, Lee KK, Sahrawat KL (eds), Phosphorus Nutrition in Grain Legumes in the Semi-arid Tropics. ICRISAT, Patancheru, pp 91–98Google Scholar
  2. 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
  3. Anderson G (1980) Assessing organic phosphorus in soils. In: Khasawneh, FE, Sample EC, Kamprath EJ (eds), The Role of Phosphorus in Agriculture. ASA/CSSA/SSSA, Madison, WI, pp 263–310Google Scholar
  4. Asmar F (1997) Variation in activity of root extracellular phytase between genotypes of barley. Plant Soil 195: 61–64Google Scholar
  5. 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
  6. Attiwill PM, Adams MA (1993) Nutrient cycling in forests. New Phytol 124: 561–582Google Scholar
  7. 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
  8. Barber SA (1984) Soil Nutrient Bioavailability: A Mechanistic Approach. Wiley, New YorkGoogle Scholar
  9. Barley KP, Rovira AD (1970) The influence of root hairs on the uptake of phosphate. Commun Soil Sci Plant Anal 1: 287–292Google Scholar
  10. 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
  11. Barrett-Lennard EG, Dracup M, Greenway H (1993) Role of extracellular phosphatases in the phosphorus-nutrition of clover. J Exp Bot 44: 1595–1600Google Scholar
  12. Bar-Yosef B (1991) Root excretions and their environmental effects. Influence on availability of phosphorus. In: Waisel Y, Eshel A, Kafkafi U (eds), Plant Roots: The Hidden Half. Marcel Dekker, New York, pp 529–557Google Scholar
  13. Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 19: 529–538Google Scholar
  14. Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Ann Rev Plant Physiol 24: 225–252Google Scholar
  15. Bolan NS (1991) A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants. Plant Soil 134: 189–207Google Scholar
  16. 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
  17. Buso GSC, Bliss FA (1988) Variability among lettuce cultivars grown at two levels of available phosphorus. Plant Soil 111: 67–73Google Scholar
  18. Caradus JR (1979) Selection for root hair length in white clover (Trifolium repens L.). Euphytica 28: 489–494Google Scholar
  19. Caradus JR (1995) Genetic control of phosphorus uptake and phosphorus status in plants. In: Johansen C, Lee KK, Sharma KK, Subbarao GV, Kueneman EA (eds), Genetic Manipulation of Crop Plants to Enhance Integrated Nutrient Management in Cropping Systems. 1. Phosphorus. ICRISAT, Patancheru, pp 55–74Google Scholar
  20. Chen CR, Condron LM, Davis MR, Sherlock RR (2002) Phosphorus dynamics in the rhizosphere of perennial ryegrass (Lolium perenne L.) and radiata pine (Pinus radiata D.Don). Soil Biol Biochem 34: 487–499Google Scholar
  21. Christie EK (1975) Physiological responses of semiarid grasses. II The pattern of root growth in relation to external phosphorus concentration. Aust J Agric Res 26: 437–446Google Scholar
  22. Ciarelli DM, Furlani AMC, Dechen AR, Lima M (1998) Genetic variation among maize genotypes for phosphorus uptake and phosphorus-use efficiency in nutrient solution. J Plant Nutr 21: 2219–2229Google Scholar
  23. Condron LM, Frossard E, Tiessen H, Newman RH, Stewart JWB (1990) Chemical nature of organic phosphorus in cultivated and uncultivated soils under different environmental conditions. J Soil Sci 41: 41–50Google Scholar
  24. Dalal RC (1977) Soil organic phosphorus. Adv Agron 29: 85–117Google Scholar
  25. de la Fuente-Martínez JM, Ramirez-Rodriguez V, Cabrera-Ponce JL, Herrera-Estrella L (1997) Aluminum tolerance in transgenic plants by alteration of citrate synthesis. Science 276: 1566–1588Google Scholar
  26. 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
  27. Delhaize E, Ryan PR, Hocking PJ, Richardson AE (2003) Effects of altered citrate synthase and isocitrate dehydrogenase expression on internal citrate concentrations in tobacco (Nicotiana tabacum L.). Plant Soil 248: 137–144Google Scholar
  28. Delhaize E, Ryan PR, Hebb DM, Yamamoto Y, Sasaki T, Matsumoto H (2004) Engineering high level aluminum tolerance in barley with the ALMT1 gene. Proc Natl Acad Sci USA 101: 15249–15254PubMedGoogle Scholar
  29. Dinkelaker B, Hengeler C, Marschner H (1995) Distribution and function of proteoid roots and other root clusters. Bot Acta 108: 183–200Google Scholar
  30. Dracup MNH, Barrett-Lennard EG, Greenway H, Robson AD (1984) Effect of phosphorus deficiency on phosphatase activity of cell walls from roots of subterranean clover. J Exp Bot 35: 466–480Google Scholar
  31. Duff SMG, Sarath G, Plaxton WC (1994) The role of acid phosphatases in plant phosphorus metabolism. Physiol Plant 90: 791–800Google Scholar
  32. Fageria NK, Baligar VC (1997a) Phosphorus use efficiency by corn genotypes. J Plant Nutr 20: 1267–1277Google Scholar
  33. Fageria NK, Baligar VC (1997b) Upland rice genotypes evaluation for phosphorus use efficiency. J Plant Nutr 20: 499–509Google Scholar
  34. Fageria NK, Wright RJ, Baligar VC (1988) Rice cultivar evaluation for phosphorus use efficiency. Plant Soil 111: 105–109Google Scholar
  35. Feng G, Song YC, Li XL, Christie P (2003) Contribution of arbuscular mycorrhizal fungi to utilization of organic sources of phosphorus by red clover in calcareous soil. Appl Soil Ecol 22: 139–148Google Scholar
  36. Findenegg GR, Nelemans JA (1993) The effect of phytase on the availability of phosphorus from myo-inositol hexaphosphate (phytate) for maize roots. Plant Soil 154: 189–196Google Scholar
  37. Fitter AH (1985) Functional significance of root morphology and root system architecture. In: Fitter AH, Atkinson D, Read DJ, Useher MB (eds), Ecological Interactions in Soil-Plant, Microbes and Animals. Blackwell, London, pp 87–106Google Scholar
  38. 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
  39. Fox TR, Comerford NB (1992) Rhizosphere phosphatase activity and phosphatase hydrolyzable organic phosphorus in two forested spodosols. Soil Biol Biochem 24: 579–583Google Scholar
  40. Furlani AMC, Furlani PR, Tanaka RT, Mascarenhas HAA, Delgado MDDP (2002) Variability in soybean germplasm in relation to phosphorus uptake and use efficiency. Sci Agric 59: 529–536.Google Scholar
  41. Gahoonia TS, Nielsen NE (1992) The effect of root induced pH changes on the depletion of inorganic and organic phosphorus in the rhizosphere. Plant Soil 143: 185–191Google Scholar
  42. Gahoonia TS, Nielsen NE (1996) Variation in acquisition of soil phosphorus among wheat and barley genotypes. Plant Soil 178: 223–230Google Scholar
  43. Gahoonia TS, Nielsen NE (1997) Variation in root hairs of barley cultivars doubled soil phosphorus uptake. Euphytica 98: 177–182Google Scholar
  44. Gahoonia TS, Nielsen NE, Lyshede OB (1999) Phosphorus (P) acquisition of cereal cultivars in the field at three levels of P fertilization. Plant Soil 211: 269–281Google Scholar
  45. Gardner WK, Parbury DG, Barber DA (1981) Proteoid root morphology and function in Lupinus albus. Plant Soil 60: 143–147Google Scholar
  46. Gaume A, Machler 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
  47. Gavito ME, Olsson PA (2003) Allocation of plant carbon to foraging and storage in arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 45: 181–187PubMedGoogle Scholar
  48. George TS, Gregory PJ, Robinson JS, Buresh RJ (2002) Changes in phosphorus concentrations and pH in the rhizosphere of some agroforestry and crop species. Plant Soil 246: 65–73Google Scholar
  49. 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
  50. George TS, Richardson AE, Simpson RJ (2005a) Behaviour of plant-derived extracellular phytase upon addition to soil. Soil Biol Biochem 37: 977–988Google Scholar
  51. 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
  52. George TS, Richardson AE, Smith JB, Hadobas PA, Simpson RJ (2005c) 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
  53. George TS, Turner BL, Gregory PJ, Cade-Menun BJ, Richardson AE (2006) Depletion of organic phosphorus from oxisols in relation to phosphatase activities in the rhizosphere. Eur J Soil Sci 57: 47–57Google Scholar
  54. George TS, Gregory PJ, Simpson RJ, Richardson AE (2007) Differential interactions of Aspergillus niger and Peniophora lycii phytases with soil particles affects the hydrolysis of inositol phosphates. Soil Biol Biochem 39: 793–803Google Scholar
  55. 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
  56. 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
  57. Gregory PJ, George TS (2005) Soil Management for Nutrient Use Efficiency - An Overview. Proceedings 564, International Fertiliser Society, YorkGoogle Scholar
  58. Hamburger D, Rezzonico E, MacDonald-Comber Petétot J, Somerville C, Poirier Y (2002) Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell 14: 889–902PubMedGoogle Scholar
  59. Hammond JP, Broadley MR, White PJ (2004) Genetic responses to phosphorus deficiency. Ann Bot 94: 323–332PubMedGoogle Scholar
  60. 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
  61. 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
  62. Harrison AF (1987) Soil Organic Phosphorus - A Review Of World Literature. CAB International, WallingfordGoogle Scholar
  63. Hawkes GE, Powlson DS, Randall EW, Tate KR (1984) A 31P nuclear magnetic resonance study of the phosphorus species in alkali extracts of soils from long-term field experiments. J Soil Sci 35: 35–45Google Scholar
  64. Hayes JE, Richardson AE, Simpson RJ (1999) Phytase and acid phosphatase activities in extracts from roots of temperate pasture grasses and legumes. Aust J Plant Physiol 26: 801–809Google Scholar
  65. Hayes JE, Richardson AE, Simpson RJ (2000a) Components of organic phosphorus in soil extracts that are hydrolyzed by phytase and acid phosphatase. Biol Fertil Soils 32: 279–286Google Scholar
  66. Hayes JE, Simpson RJ, Richardson AE (2000b) The growth and phosphorus utilisation of plants in sterile media when supplied with inositol hexaphosphate, glucose 1-phosphate or inorganic phosphate. Plant Soil 220: 165–174Google Scholar
  67. Hayes JE, Zhu Y-G, Mimura T, Reid RJ (2004) An assessment of the usefulness of solution culture in screening for phosphorus efficiency in wheat. Plant Soil 261: 91–97Google Scholar
  68. Hedley MJ, White RE, Nye PH (1982) Plant-induced changes in the rhizosphere of rape (Brassica napus var. Emerald) seedlings III. Changes in L value, soil phosphate fractions and phosphatase activity. New Phytol 91: 45–56Google Scholar
  69. Hens M, Turner BL, Hocking PJ (2003) Chemical nature and bioavailability of soil organic phosphorus mobilized by organic anions. In: Rengel Z (ed), Proceedings of the Second International Symposium on Phosphorus Dynamics in the Soil-Plant Continuum. University of Western Australia, Uniprint, Perth, pp 16–17Google Scholar
  70. 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
  71. Hill JO, Simpson RJ, Moore AD, Chapman DF (2006) Morphology and response of roots of pasture species to phosphorus and nitrogen nutrition. Plant Soil 286: 7–19Google Scholar
  72. 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
  73. 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
  74. Hocking PJ, Keerthisinghe G, Smith FW, Randall PJ (1997) Comparison of the ability of different crop species to access poorly-available soil phosphorus. In: Ando T, Fujita K, Mae T, Matsumoto H, Mori S, Sekiya J (eds), Plant nutrition for sustainable food production and agriculture. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 305–308Google Scholar
  75. Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162: 9–24Google Scholar
  76. 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
  77. Hunter DA, McManus MT (1999) Comparison of acid phosphatase in two genotypes of white clover with different responses to applied phosphate. J Plant Nutr 22: 679–692Google Scholar
  78. 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
  79. Itoh S, Barber SA (1983) Phosphorus uptake by six plant species as related to root hairs. Agron J 75: 457–461Google Scholar
  80. Jakobsen I, Leggett ME, Richardson AE (2005) Rhizosphere microorganisms and plant phosphorus uptake. In: Sims JT, Sharpley AN (eds), Phosphorus, Agriculture and the Environment. American Society for Agronomy, Madison, WI, pp 437–494Google Scholar
  81. Joner EJ, van Aarle IM, Vosatka M (2000) Phosphatase activity of extra-radical arbuscular mycorrhizal hyphae: a review. Plant Soil 226: 199–210Google Scholar
  82. Jones DL (1998) Organic acids in the rhizosphere - a critical review. Plant Soil 205: 25–44Google Scholar
  83. Jones DL, Darrah PR (1994) Role of root derived organic acids in the mobilization of nutrients in the rhizosphere. Plant Soil 166: 247–257Google Scholar
  84. Karandashov V, Nagy R, Wegmuller S, Amrhein N, Bucher M (2004) Evolutionary conservation of a phosphate transporter in the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 101: 6285–6290PubMedGoogle Scholar
  85. 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
  86. Kirk GJD, Santos EE, Findenegg GR (1999) Phosphate solubilization by organic anion secretion from rice (Oryza sativa L.) growing in aerobic soil. Plant Soil 211: 11–18Google Scholar
  87. 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
  88. 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
  89. Leggett M, Gleddie S, Holloway G (2001) Phosphate-solubilising microorganisms and their use. In: Ae N, Arihara J, Okada K, Srinivasan A (eds), Plant Nutrient Acquisition: New Perspectives. Springer, Tokyo, pp 299–318Google Scholar
  90. Li L, Tang C, Rengel Z, Zhang F (2003) Chickpea facilitates phosphorus uptake by intercropped wheat from an organic phosphorus source. Plant Soil 248: 297–303Google Scholar
  91. 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
  92. Liao M, Hocking PJ, Dong B, Delhaize E, Richardson AE, Ryan PR (2008) Variation in early phosphorus uptake efficiency among wheat genotypes grown on two contrasting Australian soils. Aust J Agric Res 59: 157–166Google Scholar
  93. 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
  94. Liu H, Trieu AT, Blaylock LA and Harrison MJ (1998) Cloning and characterization of two phosphate transporters from Medicago truncatula roots: Regulation in response to phosphate and to colonization by arbuscular mycorrhizal (AM) fungi. Mol Plant-Microbe Interact 11: 14–22PubMedGoogle Scholar
  95. López-Bucio J, de la Vega OM, Guevara-Garcia A, Herrera-Estrella L (2000) Enhanced phosphorus uptake in transgenic tobacco plants that overproduce citrate. Nature Biotechnol 18: 450–453Google Scholar
  96. Lopez-Hernandez D, Brossard M, Frossard E (1998) P-isotopic exchange values in relation to P mineralization in soils with very low P-sorbing capacities. Soil Biol Biochem 30: 1663–1670Google Scholar
  97. Lung S-C, Chan W-L, Yip W, Wang L, Yeung EC, Lim BL (2005) Secretion of beta-propeller phytase from tobacco and Arabidopsis roots enhances phosphorus utilisation. Plant Sci 169: 341–349Google Scholar
  98. Lynch J (1995) Root architecture and plant productivity. Plant Physiol 109: 7–13PubMedGoogle Scholar
  99. Lynch JP (2005) Root architecture and nutrient acquisition. In: BassiriRad H (ed), Nutrient Acquisition by Plants: An Ecological Perspective. Springer, Berlin, pp 147–183Google Scholar
  100. Lynch JP, Brown KM (2001) Topsoil foraging - an architectural adaptation of plants to low phosphorus availability. Plant Soil 237: 225–237Google Scholar
  101. Lynch JP, van Beem JJ (1993) Growth and architecture of seedling roots of common bean genotypes. Crop Sci 33: 1253–1257Google Scholar
  102. Ma Z, Walk TC, Marcus A, Lynch JP (2001) Morphological synergism in root hair length, density, initiation and geometry for phosphorus acquisition in Arabidopsis thaliana: a modeling approach. Plant Soil 236: 221–235Google Scholar
  103. Manske GGB, Ortiz-Monasterio JI, Van Grinkel M, 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
  104. Maroko JB, Buresh RJ, Smithson PC (1999) Soil phosphorus fractions in unfertilized fallow-maize systems on two tropical soils Soil Sci Soc Am J 63: 320–326CrossRefGoogle Scholar
  105. Marschner H, Römheld V, Horst WJ, Martin P (1986) Root induced changes in the rhizosphere: importance for the mineral nutrition of plants. Z Pflanz Bodenkunde 149: 441–456Google Scholar
  106. 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
  107. McGill WB, Cole CV (1981) Comparative aspects of cycling of organic C, N, S and P through soil organic matter. Geoderma 26: 267–286Google Scholar
  108. McLachlan KD (1980) Acid phosphatase activity of intact roots and phosphorus nutrition of plants. I Assay conditions and phosphatase activity. Aust J Agric Res 31: 429–440Google Scholar
  109. 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
  110. Mitsukawa N, Okumura S, Shirano Y, Sato S, Kato T, Harashima S, Shibata D (1997) Overexpression of an Arabidopsis thaliana high-affinity phosphate transporter gene in tobacco cultured cells enhances cell growth under phosphate-limited conditions. Proc Natl Acad Sci USA 94: 7098–7102PubMedGoogle Scholar
  111. Mudge SR, Rae AL, Diatloff E, Smith FW (2002) Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis. Plant J 31: 341–353PubMedGoogle Scholar
  112. 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
  113. Neumann G, Massonneau A, Martinoia E, Römheld V (1999) Physiological adaptations to phosphorus deficiency during proteiod root development in white lupin. Planta 208: 373–382Google Scholar
  114. Newman RH, Tate KR (1980) Soil phosphorus characterization by 31P-nuclear magnetic resonance. Commun Soil Sci Plant Anal 11: 835–842Google Scholar
  115. Nziguheba G, Palm CA, Buresh RJ, Smithson PC (1998) Soil phosphorus fractions and adsorption as affected by organic and inorganic sources. Plant Soil 198: 159–168Google Scholar
  116. Oberson A, Joner EJ (2005) Microbial turnover of phosphorus in soil. In: Turner BL, Frossard E, Baldwin DS (eds), Organic Phosphorus in the Environment. CAB International, Wallingford, pp 133–164Google Scholar
  117. Oberson A, Besson JM, Maire N, Sticher H (1996) Microbial processes in soil organic transformations in conventional and biological cropping systems. Biol Fertil Soils 21: 138–148Google Scholar
  118. Oberson A, Friesen DK, Rao IM, Bühler S, Frossard E (2001) Phosphorus transformations in an oxisol under contrasting land-use systems: the role of the microbial biomass. Plant Soil 237: 197–210Google Scholar
  119. Oehl F, Oberson A, Sinaj S, Frossard E (2001) Organic phosphorus mineralization studies using isotopic dilution techniques. Soil Sci Soc Am J 65: 780–787Google Scholar
  120. Oehl F, Frossard E, Fliessbach A, Dubois D, Oberson A (2004) Basal organic phosphorus mineralization in soils under different farming systems. Soil Biol Biochem 36: 667–675Google Scholar
  121. Osborne LD, Rengel Z (2002) Screening cereals for genotypic variation in the efficiency of phosphorus uptake and utilization. Aust J Agric Res 53: 295–303Google Scholar
  122. Otani T, Ae N (1999) Extraction of organic phosphorus in andosols by various methods. Soil Sci Plant Nutr 45: 151–161Google Scholar
  123. Otani T, Ae N, Tanaka H (1996) Uptake mechanisms of crops grown in soils with low P status. II. Significance of organic acids in root exudates of pigeon pea. Soil Sci Plant Nutr 42: 553–560Google Scholar
  124. 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
  125. Pearse SJ, Venaklaas EJ, Cawthray G, Bolland MDA, Lambers H (2008) Rizosphere processes do not explain variation in P acquisition from sparingly soluble forms of P among Lupinus albus accessions. Aust J Agri Res 59: (in press)Google Scholar
  126. Polglase PJ, Attiwill PM, Adams MA (1992) Nitrogen and phosphorus cycling in relation to stand age of Eucalyptus regnans F. Muell. III. Labile inorganic and organic P, phosphatase activity and P availability. Plant Soil 142: 177–185Google Scholar
  127. Rae AL, Jarmey JM, Mudge SR, Smith FW (2004) Over-expression of a high-affinity phosphate transporter in transgenic barley plants does not enhance phosphate uptake rates. Funct Plant Biol 31: 141–148Google Scholar
  128. Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Phys 50: 665–693Google Scholar
  129. Rausch C, Bucher M (2002) Molecular mechanisms of phosphate transport in plants. Planta 216: 23–37PubMedGoogle Scholar
  130. Richardson AE (1994) Soil microorganisms and phosphorus availability. In: Pankhurst CE, Doube BM, Gupta VVSR, Grace PR (eds), Management of the Soil Biota in Sustainable Farming Systems. CSIRO, Melbourne, pp 50–62Google Scholar
  131. Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Aust J Plant Physiol 28: 897–906Google Scholar
  132. Richardson AE, Hadobas PA, Hayes JE (2000) Phosphomonoesterase and phytase activities of wheat (Triticum aestivum L.) roots and utilisation of organic phosphorus substrates by seedlings grown in sterile culture. Plant Cell Environ 23: 397–405Google Scholar
  133. Richardson AE, Hadobas PA, Hayes JE (2001a) Extracellular secretion of Aspergillus phytase from Arabidopsis roots enables plants to obtain phosphorus from phytate. Plant J 25: 641–649PubMedGoogle Scholar
  134. Richardson AE, Hadobas PA, Hayes JE, O’Hara CP, Simpson RJ (2001b) Utilization of phosphorus by pasture plants supplied with myo-inositol hexaphosphate is enhanced by the presence of soil microorganisms. Plant Soil 229: 47–56Google Scholar
  135. Richardson AE, George TS, Hens M, Simpson RJ (2005) Utilisation of soil organic phosphorus by higher plants. In: Turner BL, Frossard E, Baldwin DS (eds), Organic Phosphorus in the Environment. CAB International, Wallingford, pp 165–184Google Scholar
  136. Richardson AE, George TS, Jakobsen I, Simpson RJ (2007) Plant utilization of inositol phosphates. In: Turner BL, Richardson AE, Mullaney EJ (eds), Inositol Phosphates: Linking Agriculture and the Environment. CAB International, Wallingford, pp 242–260Google Scholar
  137. Runge-Metzger A (1995) Closing the cycle: obstacles to efficient P management for improved global security. In: Tiessen H (ed), Phosphorus in the Global Environment: Transfers, Cycles And Management. Wiley, Chichester, pp 27–42Google Scholar
  138. 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
  139. Sanyal SK, De Datta SK (1991) Chemistry of phosphorus transformations in soil. Adv Soil Sci 16: 1–120Google Scholar
  140. Sasaki T, Yamomoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Delhaize E, Matsumoyo H (2004) A wheat gene encoding an aluminium-activated malate transporter. Plant J 37: 645–653PubMedGoogle Scholar
  141. Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116: 447–453PubMedGoogle Scholar
  142. Schünmann PHD, Richardson AE, Vickers CE, Delhaize E (2004) Promoter analysis of the barley Pht1;1 phosphate transporter gene identifies regions controlling root expression and responsiveness to phosphate deprivation. Plant Physiol 136: 4205–4214PubMedGoogle Scholar
  143. Smith SE, Read DJ (1997) Mycorrhizal Symbiosis. Academic, San Diego, CAGoogle Scholar
  144. 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
  145. Tadano T, Ozawa K, Sakai H, Osaki M, Matsui H (1993) Secretion of acid phosphatase by the roots of crop plants under phosphorus-deficient conditions and some properties of the enzyme secreted by lupin roots. Plant Soil 155/156: 95–98Google Scholar
  146. Tarafdar JC, Claassen N (1988) Organic phosphorus compounds as a phosphorus source for higher plants through the activity of phosphatases produced by plant roots and microorganisms. Biol Fertil Soils 5: 308–312Google Scholar
  147. Tarafdar JC, Marschner H (1994) Efficiency of VAM hyphae in utilisation of organic phosphorus by wheat plants. Soil Sci Plant Nutr 40: 593–600Google Scholar
  148. Tarafdar JC, Yadav RS, Meena SC (2001) Comparative efficiency of acid phosphatase originated from plant and fungal sources. J Plant Nutr Soil Sci 164: 279–282Google Scholar
  149. 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
  150. Ticconi CA, Abel S (2004) Short on phosphate: plant surveillance and countermeasures. Trends Plant Sci 9: 548–555PubMedGoogle Scholar
  151. Trasar-Cepeda MC, Carballas T (1991) Liming and the phosphatase activity and mineralization of phosphorus in an acidic soil. Soil Biol Biochem 23: 209–215Google Scholar
  152. 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
  153. Veneklaas EJ, Stevens J, Cawthray GR, Turner S, Grigg AM, Lambers H (2003) Chickpea and white lupin rhizosphere carboxylates vary with soil properties and enhance phosphorus uptake. Plant Soil 248: 187–197Google Scholar
  154. Vesterager JM, Nielsen NE, Hogh-Jensen, H (2006) Variation in phosphorus uptake and use efficiencies between pigeonpea genotypes and cowpea. J Plant Nutr 29: 1869–1888Google Scholar
  155. Wakelin SA, Warren RA, Ryder MH (2004) Effect of soil properties on growth promotion of wheat by Penicillium radicum. Aust J Soil Res 42: 897–904Google Scholar
  156. Wang L, Liao H, Yan X, Zhuang B, Dong Y (2004) Genetic variability for root hair traits as related to phosphorus status in soybean. Plant Soil 261: 77–84Google Scholar
  157. Wang QR, Li JY, Li ZS, Christie P (2005) Screening Chinese wheat germplasm for phosphorus efficiency in calcareous soils. J Plant Nutr 28: 489–505Google Scholar
  158. Wasaki J, Omura M, Ando M, Dateki H, Shinano T, Osaki M, Ito H, Matsui H, Tadano T (2000) Molecular cloning and root specific expression of secretory acid phosphatase from phosphate deficient lupin (Lupinus albus L.). Soil Sci Plant Nutr 46: 427–437Google Scholar
  159. 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
  160. Wassen MJ, Venterink HO, Lapshina ED, Tanneberger L (2005) Endangered plants persist under phosphorus limitation. Nature 437: 547–550PubMedGoogle Scholar
  161. Watt M, Evans JR (1999) 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
  162. White PJ, Hammond JP (2008) Phosphorus nutrition of terrestrial plants. In: White PJ, Hammond JP (eds), The Ecophysiology of Plant-Phosphorus Interactions. Springer, Dordrecht, The Netherlands, pp 51–81Google Scholar
  163. White PJ, Broadley MR, Greenwood DJ, Hammond JP (2005) Genetic Modifications to Improve Phosphorus Acquisition by Roots. Proceedings 568, International Fertiliser Society, YorkGoogle Scholar
  164. Williamson LC, Ribrioux SPCP, Fitter AH, Leyser HMO (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126: 875–890PubMedGoogle Scholar
  165. Wissuwa M (2003) How do plants achieve tolerance to phosphorus deficiency? Small causes with big effects. Plant Physiol 133: 1947–1958PubMedGoogle Scholar
  166. Wissuwa M (2005) Mapping nutritional traits in crop plants. In: Broadley MR, White PJ (eds), Plant Nutritional Genomics. Blackwell, Cambridge, pp 220–241Google Scholar
  167. Wissuwa M, Ae N (2001a) Further characterization of two QTLs that increase phosphorus uptake of rice (Oryza sativa L.) under phosphorus deficiency. Plant Soil 237: 275–286Google Scholar
  168. Wissuwa M, Ae N (2001b) Genotypic variation for tolerance to phosphorus deficiency in rice and the potential for its exploitation in rice improvement. Plant Breeding 120: 43–48Google Scholar
  169. Wouterlood M, Cawthray GR, Scanlon TT, Lambers H, Veneklaas EJ (2004) 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
  170. 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
  171. 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
  172. Yan X, Lynch JP, Beebe SE (1995) Genetic variation for phosphorus efficiency of common bean in contrasting soil types. I. Vegetative response. Crop Sci 35: 1086–1093CrossRefGoogle Scholar
  173. 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
  174. Yip W, Wang L, Cheng C, Wu W, Lung S, Lim BL (2003) The introduction of a phytase gene from Bacillus subtilis improved the growth performance of transgenic tobacco. Biochem Biophys Res Commun 310: 1148–1154PubMedGoogle Scholar
  175. Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279: 407–409PubMedGoogle Scholar
  176. 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
  177. 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
  178. Zhu J, Kaeppler SM, Lynch JP (2005) Mapping of QTL controlling root hair length in maize (Zea mays L.) under phosphorus deficiency. Plant Soil 270: 299–310Google Scholar
  179. 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

Copyright information

© Springer Science + Business Media B.V 2008

Authors and Affiliations

  • Timothy S. George
    • 1
  • Alan E. Richardson
    • 2
  1. 1.Scottish Crop Research InstituteUK
  2. 2.CSIRO Plant IndustryAustralia

Personalised recommendations