Abstract
Management of soil phosphorus (P) remains a crucial issue for the economic and environmental sustainability of agriculture and natural ecosystems globally. It is therefore essential that we have appropriate understanding of the mechanisms by which plants are able to acquire P from soil. In this chapter, various processes and physiological traits of plants that facilitate the availability and acquisition of P from soil are outlined, and some possibilities for deploying these traits into agricultural germplasm discussed. Better understanding of these processes and the development of improved germplasm may ultimately improve the P-use efficiency of agricultural systems and provide valuable information for wider-scale land and resource management. However, at present it is evident that the full extent of the complexity of the gene-by-gene and gene-by-environment interactions that are associated with plant P nutrition are not well appreciated. It is therefore important that a systems approach to P management continues to be developed for a more sustainable agriculture.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
AbuQamar S, Luo HL, Laluk K, Mickelbart MV, Mengiste T (2009) Crosstalk between biotic and abiotic stress responses in tomato is mediated by the AIM1 transcription factor. Plant J 58:347–360
Amtmann A, Hammond JP, Armengaud P, White PJ (2006) Nutrient sensing and signalling in plants: potassium and phosphorus. Adv Bot Res 43:209–257
Attiwill PM, Adams MA (1993) Nutrient cycling in forests. New Phytol 124:561–582
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 141:1000–1011
Barber SA (1984) Soil nutrient bioavailability: a mechanistic approach. Wiley, New York
Bari R, Pant BD, Stitt M, Scheible WR (2006) PHO2, microrna399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999
Barrett-Lennard EG, Dracup M, Greenway H (1993) Role of extracellular phosphatase in the phosphorus-nutrition of clover. J Exp Bot 44:1595–1600
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. Dekker, New York, pp 529–557
Basu P, Zhang YJ, Lynch JP, Brown KM (2007) Ethylene modulates genetic, positional, and nutritional regulation of root plagiogravitropism. Funct Plant Biol 34:41–51
Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 19:529–538
Benning C, Ohta H (2005) Three enzyme systems for galactoglycerolipid biosynthesis are coordinately regulated in plants. J Biol Chem 280:2397–2400
Bieleski RL (1973) Phosphate pools, phosphate transport and phosphate availability. Annu Rev Plant Physiol 24:225–252
Boot GA, Mensink M (1990) Size and morphology of root systems of perennial grasses from contrasting habitats as affected by nitrogen supply. Plant Soil 129:291–299
Bradshaw AD, Chadwick MJ, Jowett D, Lodge RW, Snaydon RW (1960) Experimental investigations into the mineral nutrition of several grass species. III. Phosphate level. J Ecol 48:631–637
Brown LK, George TS, Thompson JA, Wright G, Lyon J, Hubbard SF, White PJ (2010) What are the implications of variation in root hair length on P-limited yield in barley (Hordeum vulgare L.)? Plant Cell Environ (in press)
Bucher M (2007) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol 173:11–26
Buhtz A, Springer F, Chappell L, Baulcombe D, Kehr J (2008) Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J 53:739–749
Chapin FS (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260
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 34:487–499
Chiou TJ (2007) The role of microRNAs in sensing nutrient stress. Plant Cell Environ 30:323–332
Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CI (2006) Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18:412–421
Christie EK (1975) Physiological responses of semiarid grasses. II. The pattern of root growth in relation to external phosphorus concentration. Aust J Agric Res 26:437–446
Christie EK, Moorby J (1975) Physiological responses of semiarid grasses. I. The influence of phosphorus supply on growth and phosphorus absorption. Aust J Agric Res 26:423–436
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 41:41–50
Cordell D, Drangert J-O, White S (2009) The story of phosphorus: global food security and food for thought. Glob Environ Change 19:292–305
de la Fuente-MartÃnez JM, Ramirez-Rodriguez V, Cabrera-Ponce JL, Herrera-Estrella L (1997) Aluminum tolerance in transgenic plants by alteration of citrate synthesis. Science 276: 1566–1588
del Pozo JC, Allona I, Rubio V, Leyva A, De la Pena A, Aragoncillo C, Paz-Ares J (1999) Type 5 acid phosphatase gene from Arabidopsis thaliana is induced by phosphate starvation and by some other types of phosphate mobilising/oxidative stress conditions. Plant J 19:579–589
Delhaize E, Randall PJ (1995) Characterisation of a phosphate-accumulator mutant of Arabidopsis thaliana. Plant Physiol 107:207–213
Delhaize E, Hebb DM, Ryan PR (2001) Expression of a Pseudomonas aeruginosa citrate synthase gene in tobacco is not associated with either enhanced citrate accumulation or efflux. Plant Physiol 125:2059–2067
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 248:137–144
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 101:15249–15254
Delhaize E, Gruber BD, Ryan PR (2007) The roles of organic anion permeases in aluminium resistance and mineral nutrition. FEBS Lett 581:2255–2262
Delhaize E, Taylor P, Hocking PJ, Simpson RJ, Ryan PR, Richardson AE (2009) Transgenic barley (Hordeum vulgare L.) expressing the wheat aluminium resistance gene (TaALMT1) shows enhanced phosphorus nutrition and grain production when grown on an acid soil. Plant Biotechnol J 7:391–400
Dinkelaker B, Hengeler C, Marschner H (1995) Distribution and function of proteoid and other root clusters. Bot Acta 108:183–200
Dörmann P, Benning C (2002) Galactolipids rule in seed plants. Trends Plant Sci 7:112–118
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 35:466–480
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 75:479–490
Duan K, Yi K, Dang L, Huang H, Wu W, Wu P (2008) Characterization of a sub-family of Arabidopsis genes with the SPX domain reveals their diverse functions in plant tolerance to phosphorus starvation. Plant J 54:965–975
Duff SMG, Sarath G, Plaxton WC (1994) The role of acid phosphatases in plant phosphorus metabolism. Physiol Plant 90:791–800
Fan M, Zhu J, Richards C, Brown KM, Lynch JP (2003) Physiological roles for aerenchyma in phosphorus-stressed roots. Funct Plant Biol 30:493–506
Fang Z, Shao C, Meng Y, Wua P, Chen M (2009) Phosphate signaling in Arabidopsis and Oryza sativa. Plant Sci 176:170–180
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 87–106
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 132:261–272
Fox TR, Comerford NB (1992) Rhizosphere phosphatase activity and phosphatase hydrolyzable organic phosphorus in two forested spodosols. Soil Biol Biochem 24:579–583
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 55:285–293
Franco-Zorrilla JM, MartÃn 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 138:847–857
Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, GarcÃa JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39:1033–1037
Gahoonia TS, Nielsen NE (1997) Variation in root hairs of barley cultivars doubled soil phosphorus uptake. Euphytica 98:177–182
Gardner WK, Parbury DG, Barber DA (1981) Proteoid root morphology and function in Lupinus albus. Plant Soil 60:143–147
Gaude N, Nakamura Y, Scheible W, Ohta H, Dörmann P (2008) Phospholipase C5 (NPC5) is involved in galactolipid accumulation during phosphate limitation in leaves of Arabidopsis. Plant J 56:28–39
Gaume A, Machler F, Deleon 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 228:253–264
George TS, Richardson AE (2008) Potential and limitations to improving crops for enhanced phosphorus utilization. In: Hammond JP, White PJ (eds) The ecophysiology of plant–phosphorus interactions. Springer, Dordrecht, pp 247–270
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 246:65–73
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 27:1351–1361
George TS, Simpson RJ, Hadobas PA, Richardson AE (2005a) Expression of a fungal phytase gene in Nicotiana tabacum improves phosphorus nutrition in plants grown in amended soil. Plant Biotechnol J 3:129–140
George TS, Richardson AE, Smith JB, Hadobas PA, Simpson RJ (2005b) 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 278:263–274
George TS, Turner BL, Gregory PJ, Richardson AE (2006) Depletion of organic phosphorus from oxisols in relation to phosphatase activities in the rhizosphere. Eur J Soil Sci 57:47–57
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 effectively predict P-nutrition in different soils. Environ Exp Bot 64:239–249
Gilbert N (2009) The disappearing nutrient. Nature 461:716–718
González E, Solano R, Rubio V, Leyva A, Paz-Ares J (2005) PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1 is a plant-specific SEC12-related protein that enables the endoplasmic reticulum exit of a high-affinity phosphate transporter in Arabidopsis. Plant Cell 17: 3500–3512
Guo A, He K, Liu D, Bai S, Gu X, Wei L, Luo J (2005) DATF: a database of Arabidopsis transcription factors. Bioinformatics 21:2568–2569, http://datf.cbi.pku.edu.cn. Accessed 30 July 2010
Haling RE, Simpson RJ, Delhaize E, Hocking PJ, Richardson AE (2010) Effect of lime on root growth, morphology and the rhizosheath of cereals growing in an acid soil. Plant Soil 327:199–212
Hammond JP, White PJ (2008) Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J Exp Bot 59:93–109
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 132:578–596
Hammond JP, Broadley MR, White PJ (2004) Genetic responses to phosphorus deficiency. Ann Bot 94:323–332
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 1:10
Hammond JP, Broadley MR, White PJ, King GJ, Bowen HC, Hayden R, Meacham MC, Mead A, Overs T, Spracklen WP, Greenwood DJ (2009) Shoot yield drives phosphorus use efficiency in Brassica oleracea and correlates with root architectural traits. J Exp Bot 60:1953–1968
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 124:615–626
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 35:35–45
Hayes JE, Richardson AE, Simpson RJ (1999) Phytase and acid phosphatase activities in roots of temperate pasture grasses and legumes. Aust J Plant Physiol 26:801–809
Hayes JE, Richardson AE, Simpson RJ (2000a) Components of organic phosphorus in soil extracts that are hydrolysed by phytase and acid phosphatase. Biol Fertil Soils 32:279–286
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 220:165–174
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 91:45–56
Heffer P, Prud’homme MPR, Muirheid B, Isherwood KF (2006) Phosphorus fertilisation: issues and outlook. Proceedings 586. International Fertiliser Society, York
Helsel ZR (1992) Energy and alternatives for fertiliser and pesticide use. In: Fluck RC (ed) Energy in world agriculture, vol 6. Elsevier, Oxford, pp 177–210
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. Uniprint: University of Western Australia, Perth, pp 16–17
Hermans C, Hammond JP, White PJ, Verbruggen N (2006) How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci 11:610–617
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 43:91–99
Hill JO, Simpson RJ, Moore AD, Chapman DF (2006) Morphology and response of roots of pasture species to phosphorus and nitrogen nutrition. Plant Soil 286:7–19
Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root induced chemical changes: a review. Plant Soil 237:173–195
Hodge A (2009) Root decisions. Plant Cell Environ 32:628–640
Hoffland E, Findenegg GR, Nelemans JA (1989) Solubilization of rock phosphorus by rape. II. Local root exudation of organic acids in response to P-starvation. Plant Soil 113:161–165
Hunter DA, McManus MT (1999) Comparison of acid phosphatase in two genotypes of white clover with different responses to applied phosphate. J Plant Nutr 22:679–692
Itoh S, Barber SA (1983) Phosphorus uptake by six plant species as related to root hairs. Agron J 75:457–461
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 144:232–247
Jain A, Vasconcelos MJ, Raghothama KG, Sahi SV (2007b) Molecular mechanisms of plant adaptation to phosphate deficiency. Plant Breed Rev 29:359–419
Jansa J, Finlay R, Wallander H, Smith FA, Smith SE (2011) Role of mycorrhizal symbioses in phosphorus cycling. In: Bünemann EK, Oberson A, Frossard E (eds) Phosphorus in action: biological processes in soil phosphorus cycling. Soil biology, vol 26. Springer, Heidelberg. doi:10.1007/978-3-642-15271-9_6
Jenssen TK, Kongshaug G (2003) Energy consumption and greenhouse gas emissions in fertiliser production. Proceedings 509. International Fertiliser Society, York
Jones DL (1998) Organic acids in the rhizosphere – a critical review. Plant Soil 205:25–44
Jones DL, Darrah PR (1994) Role of root derived organic acids in the mobilization of nutrients in the rhizosphere. Plant Soil 166:247–257
Jones DL, Dennis PG, Owen AG, van Hees PAW (2003) Organic acid behavior in soils – misconceptions and knowledge gaps. Plant Soil 248:31–41
Karthikeyan AS, Varadarajan DK, Jain A, Held MA, Carpita NC, Raghothama KG (2007) Phosphate starvation responses are mediated by sugar signaling in Arabidopsis. Planta 225:907–918
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 21:467–478
Kelly AA, Froehlich JE, Dörmann P (2003) Disruption of the two digalactosyldiacylglycerol synthase genes DGD1 and DGD2 in Arabibopsis reveals the existence of an additional enzyme of galactolipid synthase. Plant Cell 15:2694–2706
Kirk GJD, Santos EE, Findenegg GR (1999) Phosphate solubilization by organic anion secretion from rice (Oryza sativa L.) growing in aerobic soil. Plant Soil 211:11–18
Kirkby EA, Johnston AE (2008) Soil and fertilizer phosphorus in relation to crop nutrition. In: Hammond JP, White PJ (eds) The ecophysiology of plant–phosphorus interactions. Springer, Dordrecht, pp 177–223
Koyama H, Kanamura 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 41:1030–1037
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 98:693–713
Lamont BB (2003) Structure, ecology and physiology of root clusters – a review. Plant Soil 248:1–19
Lan M, Comerford NB, Fox TR (1995) Organic anions effect on phosphorus release from spodic horizons. Soil Sci Soc Am J 59:1745–1749
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 195:161–169
Li D, Zhu H, Liu K, Liu X, Leggewie G, Urdvardi M, Wang D (2002) Purple acid phosphatase of Arabidopsis thaliana. Comparative analysis and differential regulation by phosphate deprivation. J Biol Chem 277:27772–27781
Li L, Tang C, Rengel Z, Zhang F (2003) Chickpea facilitates phosphorus uptake by intercropped wheat from an organic phosphorus source. Plant Soil 248:297–303
Lin SI, Chiang SF, Lin WY, Chen JW, Tseng CY, Wu PC, Chiou TJ (2008) Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147:732–746
Lin WY, Lin SI, Chiou TJ (2009) Molecular regulators of phosphate homeostasis in plants. J Exp Bot 60:1427–1438
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 85:315–317
Liu Y, Mi G, Chen F, Zhang J, Zhang F (2004) Rhizosphere effect and root growth of two maize (Zea mays L.) genotypes with contrasting P efficiency at low P availability. Plant Sci 167:217–223
Liu JQ, 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 41:257–268
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 55:1221–1230
López-Bucio J, de la Vega OM, Guevara-GarcÃa A, Herrera-Estrella L (2000) Enhanced phosphorus uptake in transgenic tobacco plants that overproduce citrate. Nat Biotechnol 18:450–453
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 30:1663–1670
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 169:341–349
Lynch JP (1995) Root architecture and plant productivity. Plant Physiol 109:7–13
Lynch JP (2005) Root architecture and nutrient acquisition. In: BassiriRad H (ed) Nutrient acquisition by plants: an ecological perspective. Springer, Berlin, pp 147–183
Lynch JP, Brown KM (2008) Root strategies for phosphorus acquisition. In: White PJ, Hammond JP (eds) The ecophysiology of plant–phosphorus interactions. Springer, Dordrecht, pp 83–116
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 236:221–235
Maroko JB, Buresh RJ, Smithson PC (1999) Soil phosphorus fractions in unfertilized fallow-maize systems on two tropical soils. Soil Sci Soc Am J 63:320–326
Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, London
McGill WB, Cole CV (1981) Comparative aspects of cycling of organic C, N, S and P through soil organic matter. Geoderma 26:267–286
McLachlan KD (1980) Acid phosphatase activity of intact roots and phosphorus nutrition of plants. I. Assay conditions and phosphatase activity. Aust J Agric Res 31:429–440
Miller SS, Liu JQ, 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 127:594–606
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 102:11934–11939
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 94:7098–7102
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 102:7760–7765
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 30:85–112
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 31:341–353
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 165:871–878
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 143:156–171
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 138:2061–2074
Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bünemann EK, Oberson A, Frossard E (eds) Phosphorus in action: biological processes in soil phosphorus cycling. Soil biology, vol 26. Springer, Heidelberg. doi:10.1007/978-3-642-15271-9_9
Neumann G, Massonneau A, Martinoia A, Römheld V (1999) Physiological adaptations to phosphorus deficiency during proteiod root development in white lupin. Planta 208:373–382
Newman RH, Tate KR (1980) Soil phosphorus characterization by 31P-nuclear magnetic resonance. Commun Soil Sci Plant Anal 11:835–842
Nilsson L, Müller R, Nielsen TH (2007) Increased expression of the MYB-related transcription factor, PHR1, leads to enhanced phosphate uptake in Arabidopsis thaliana. Plant Cell Environ 30:1499–1512
Nziguheba G, Palm CA, Buresh RJ, Smithson PC (1998) Soil phosphorus fractions and adsorption as affected by organic and inorganic sources. Plant Soil 198:159–168
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 133–164
Oberson A, Besson JM, Maire N, Sticher H (1996) Microbial processes in soil organic transformations in conventional and biological cropping systems. Biol Fertil Soils 21:138–148
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 237:197–210
Oehl F, Oberson A, Sinaj S, Frossard E (2001) Organic phosphorus mineralization studies using isotopic dilution techniques. Soil Sci Soc Am J 65:780–787
Oehl F, Frossard E, Fliessbach A, Dubois D, Oberson A (2004) Basal organic phosphorus mineralization in soils under different farming systems. Soil Biol Biochem 36:667–675
Otani T, Ae N (1999) Extraction of organic phosphorus in andosols by various methods. Soil Sci Plant Nutr 45:151–161
Pant BD, Buhtz A, Kehr J, Scheible W-R (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53:731–738
Parsons HL, Yip JYH, Vanlerberghe GC (1999) Increased respiratory restriction during phosphate-limited growth in transgenic tobacco cells lacking alternative oxidase. Plant Physiol 121:1309–1320
Pearse SJ, Venaklaas EJ, Cawthray G, Bolland MDA, Lambers H (2006) 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 173:181–190
Pérez-Torres C-A, López-Bucio J, Cruz-RamÃrez A, Ibarra-Laclette E, Dharmasiri S, Estelle M, Herrera-Estrella L (2008) Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20:3258–3272
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 349–372
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 142:177–185
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 31:141–148
Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol 50: 665–693
Raven JA (2008) Phosphorus and the future. In: White PJ, Hammond JP (eds) The ecophysiology of plant–phosphorus interactions. Springer, Dordrecht, pp 271–283
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 23:397–405
Richardson AE, Hadobas PA, Hayes JE (2001) Extracellular secretion of Aspergillus phytase from Arabidopsis roots enables plants to obtain phosphorus from phytate. Plant J 25:641–649
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. CABI, Wallingford, pp 165–184
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. CABI, Wallingford, pp 242–260
Rook F, Hadingham SA, Li Y, Bevan MW (2006) Sugar and ABA response pathways and the control of gene expression. Plant Cell Environ 29:426–434
Rubio V, Linhares F, Solano R, MartÃn 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 15:2122–2133
Rubio G, Liao H, Yan XL, Lynch JP (2003) Topsoil foraging and its role in plant competitiveness for phosphorus in common bean. Crop Sci 43:598–607
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 27–42
Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol 52:527–560
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 140:879–889
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 37:645–653
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 26:265–273
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 168:837–845
Skene KR (1998) Cluster roots: some ecological considerations. J Ecol 86:1060–1064
Smith SE, Read DJ (2007) Mycorrhizal symbiosis, 3rd edn. Elsevier, London
Smith FW, Mudge SR, Rae AL, Glassop D (2003) Phosphate transport in plants. Plant Soil 248:71–83
Solfanelli C, Poggi A, Loreti E, Alpi A, Perata P (2006) Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol 140:637–646
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 39:792–796
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):95–98
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 5:308–312
Tarafdar JC, Yadav RS, Meena SC (2001) Comparative efficiency of acid phosphatase originated from plant and fungal sources. J Plant Nutr Soil Sci 164:279–282
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 139:1840–1852
Tesfaye M, Liu J, Allan DL, Vance CP (2007) Genomic and genetic control of phosphate stress in legumes. Plant Physiol 144:594–603
Ticconi CA, Delatorre CA, Lahner B, Salt DE, Abel S (2004) Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. Plant J 37:801–814
Trasar-Cepeda MC, Carballas T (1991) Liming and the phosphatase activity and mineralization of phosphorus in an acidic soil. Soil Biol Biochem 23:209–215
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 186–206
Vance CP (2008) Plants without arbuscular mycorrhizae. In: Hammond JP, White PJ (eds) The ecophysiology of plant–phosphorus interactions. Springer, Dordrecht, pp 117–142
Vance CP, Ehde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447
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 248:187–197
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 46:427–437
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: 2049–2059
Wassen MJ, Venterink HO, Lapshina ED, Tanneberger L (2005) Endangered plants persist under phosphorus limitation. Nature 437:547–550
White PJ, Hammond JP (2008) Phosphorus nutrition of terrestrial plants. In: White PJ, Hammond JP (eds) The ecophysiology of plant–phosphorus interactions. Springer, Dordrecht, pp 51–81
White PJ, Broadley MR, Greenwood DJ, Hammond JP (2005) Genetic modifications to improve phosphorus acquisition by roots. Proceedings 568. International Fertiliser Society, York
Williamson LC, Ribrioux SPCP, Fitter AH, Leyser HMO (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–890
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 162:745–753
Wu P, Ma L, Hou X, Wang M, Wu Y, Liu F, Deng XW (2003) Phosphate starvation triggers distinct alterations if genome expression in Arabidopsis roots and leaves. Plant Physiol 132:1260–1271
Xiao K, Harrison MJ, Wang ZY (2005) Transgenic expression of a novel Medicago truncatula phytase gene results in improved acquisition of organic phosphorus by Arabidopsis. Planta 222:27–36
Yi K, Wu Z, Zhou J, Du L, Guo L, Wu Y, Wu P (2005) OsPTF1, a novel transcription factor involved in tolerance to phosphate starvation in rice. Plant Physiol 138:2087–2096
Zhang WH, Ryan PR, Tyerman SD (2004) Citrate-permeable channels in the plasma membrane of cluster roots from white lupin. Plant Physiol 136:3771–3783
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 Biotechnol J 1:353–360
Zrenner R, Stitt M, Schmidt R, Sonnewald U, Boldt R (2006) Pyramidine and purine biosynthesis and degradation in plants. Annu Rev Plant Biol 57:805–836
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer Berlin Heidelberg
About this chapter
Cite this chapter
George, T.S., Fransson, AM., Hammond, J.P., White, P.J. (2011). Phosphorus Nutrition: Rhizosphere Processes, Plant Response and Adaptations. In: Bünemann, E., Oberson, A., Frossard, E. (eds) Phosphorus in Action. Soil Biology, vol 26. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-15271-9_10
Download citation
DOI: https://doi.org/10.1007/978-3-642-15271-9_10
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-15270-2
Online ISBN: 978-3-642-15271-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)