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Plant and microbial strategies to improve the phosphorus efficiency of agriculture

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Abstract

Background

Agricultural production is often limited by low phosphorus (P) availability. In developing countries, which have limited access to P fertiliser, there is a need to develop plants that are more efficient at low soil P. In fertilised and intensive systems, P-efficient plants are required to minimise inefficient use of P-inputs and to reduce potential for loss of P to the environment.

Scope

Three strategies by which plants and microorganisms may improve P-use efficiency are outlined: (i) Root-foraging strategies that improve P acquisition by lowering the critical P requirement of plant growth and allowing agriculture to operate at lower levels of soil P; (ii) P-mining strategies to enhance the desorption, solubilisation or mineralisation of P from sparingly-available sources in soil using root exudates (organic anions, phosphatases), and (iii) improving internal P-utilisation efficiency through the use of plants that yield more per unit of P uptake.

Conclusions

We critically review evidence that more P-efficient plants can be developed by modifying root growth and architecture, through manipulation of root exudates or by managing plant-microbial associations such as arbuscular mycorrhizal fungi and microbial inoculants. Opportunities to develop P-efficient plants through breeding or genetic modification are described and issues that may limit success including potential trade-offs and trait interactions are discussed. Whilst demonstrable progress has been made by selecting plants for root morphological traits, the potential for manipulating root physiological traits or selecting plants for low internal P concentration has yet to be realised.

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References

  • Abdolzadeh A, Wang X, Veneklaas EJ, Lambers H (2010) Effects of phosphorus supply on growth, phosphate concentration and cluster-root formation in three Lupinus species. Ann Bot 105:365–374

    PubMed  CAS  Google Scholar 

  • Adams MA, Pate JS (1992) Availability of organic and inorganic forms of phosphorus to Lupins (Lupinus spp). Plant Soil 145:107–113

    Google Scholar 

  • Adams MA, Bell TL, Pate JS (2002) Phosphorus sources and availability modify growth and distribution of root clusters and nodules of native Australian legumes. Plant Cell Environ 25:837–850

    CAS  Google Scholar 

  • Adesemoye AO, Kloepper JW (2009) Plant-microbes interactions in enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol 85:1–12

    PubMed  CAS  Google Scholar 

  • 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 of grain legumes in the semi arid tropics. ICRISAT, Andra Pradesh, pp 91–98

    Google Scholar 

  • Akhtar MS, Yoko O, Tadashi A (2008) Intraspecific variations of phosphorus absorption and remobilization, P forms, and their internal buffering in Brassica cultivars exposed to a P-stressed environment. J Integr Plant Biol 50:703–716

    PubMed  CAS  Google Scholar 

  • Altomare C, Norvell WA, Björkman T, Harman GE (1999) Solubilization of phosphates and micronutrients by the plant-growth-promoting and biocontrol fungus Trichoderma harzianum Rifai 1295–22. Appl Environ Microbiol 65:2926–2933

    PubMed  CAS  Google Scholar 

  • Anderson G, Williams EG, Moir JO (1974) A comparison of the sorption of inorganic orthophosphate and inositol hexaphosphate by six acid soils. J Soil Sci 25:51–62

    CAS  Google Scholar 

  • Anoop VM, Basu U, McCammon MT, McAlister-Henn L, Taylor GJ (2003) Modulation of citrate metabolism alters aluminum tolerance in yeast and transgenic canola overexpressing a mitochondrial citrate synthase. Plant Physiol 132:2205–2217

    PubMed  CAS  Google Scholar 

  • Anstis ST (2004) Penicillium radicum: Studies on the mechanisms of plant growth promotion in wheat. PhD thesis, The University of Adelaide, Australia

  • Asea PEA, Kucey RMN, Stewart JWB (1988) Inorganic phosphate solubilisation by two Penicillium species in solution culture and soil. Soil Biol Biochem 20:459–464

    CAS  Google Scholar 

  • 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 172:117–122

    CAS  Google Scholar 

  • Babana AH, Antoun H (2006) Effect of Tilemsi phosphate rock-solubilizing microorganisms on phosphorus uptake and yield of field-grown wheat (Triticum aestivum L.) in Mali. Plant Soil 287:51–58

    CAS  Google Scholar 

  • Babu-Khan S, Yeo TC, Martin WL, Duron MR, Rogers RD, Goldstein AH (1995) Cloning of a mineral phosphate-solubiliizing gene from Pseudomonas cepacia. Appl Environ Microbiol 61:972–978

    PubMed  CAS  Google Scholar 

  • Baon JB, Smith SE, Alston AM (1993) Mycorrhizal responses of barley cultivars differing in P efficiency. Plant Soil 157:97–105

    Google Scholar 

  • Baon JB, Smith SE, Alston AM (1994) Growth-response and phosphorus uptake of rye with long and short root hairs—interactions with mycrorrhizal infection. Plant Soil 167:247–254

    CAS  Google Scholar 

  • Barrett-Lennard EG, Dracup M, Greenway H (1993) Role of extracellular phosphatase in the phosphorus-nutrition of clover. J Exp Bot 44:1595–1600

    CAS  Google Scholar 

  • Barrow NJ (1980) Evaluation and utilisation of residual phosphorus in soils. In: Khasawneh FE, Sample EC, Kamprath EJ (eds) The role of phosphorus in agriculture. American Society of Agronomy, Madison, pp 333–339

    Google Scholar 

  • Bates TR, Lynch JP (2000a) The efficiency of Arabidopsis thaliana (Brassicaceae) root hairs in phosphorus acquisition. Am J Bot 87:964–970

    PubMed  CAS  Google Scholar 

  • Bates TR, Lynch JP (2000b) Plant growth and phosphorus accumulation of wild type and two root hair mutants of Arabidopsis thaliana (Brassicaceae). Am J Bot 87:958–963

    PubMed  CAS  Google Scholar 

  • Bates TR, Lynch JP (2000c) The efficiency of Arabidopsis thaliana (Brassicaceae) root hairs in phosphorus acquisition. Am J Bot 87:964–970

    PubMed  CAS  Google Scholar 

  • Batten GD, Khan MA (1987) Uptake and utilisation of phosphorus and nitrogen by bread wheats grown under natural rainfall. Aust J Exp Agric 27:405–410

    Google Scholar 

  • Beckie HJ, Schlechte D, Moulin AP, Gleddie SC, Pulkinen DA (1998) Response of alfalfa to inoculation with Penicillium bilaii (Provide). Can J Plant Sci 78:91–102

    Google Scholar 

  • Beebe SE, Rojas-Pierce M, Yan X, Blair MW, Pedraza F, Muñoz F, Tohme J, Lynch JP (2006) Quantitative trait loci for root architecture traits correlated with phosphorus acquisition in common bean. Crop Sci 46:413–423

    CAS  Google Scholar 

  • Begum HH, Osaki M, Shinano T, Miyataki H, Wasaki J, Yamamura T, Watanabe T (2005) The function of a maize-derived phosphoenolpyruvate carboxylase in phosphorus-deficient transgenic rice. Soil Sci Plant Nutr 51:497–506

    CAS  Google Scholar 

  • Bhat KKS, Nye PH (1974) Diffusion of phosphate to plant roots in soil III. Depletion around onion roots without root hairs. Plant Soil 41:383–394

    Google Scholar 

  • Bolan NS (1991) A critical review on the role of mycrorrhizal fungi in the uptake of phosphorus by plants. Plant Soil 134:189–207

    CAS  Google Scholar 

  • Bolland MDA, Baker MJ (1988) High phosphorus concentrations in seed of wheat and annual medic are related to higher rates of dry matter production of seedlings and plants. Aust J Experim Agric 28:765–770

    Google Scholar 

  • Bonser AM, Lynch J, Snapp S (1996) Effect of phosphorus deficiency on growth angle of basal roots in Phaseolus vulgaris. New Phytol 132:281–288

    PubMed  CAS  Google Scholar 

  • Borch K, Bouma TJ, Lynch JP, Brown KM (1999) Ethylene: a regulator of root architectural responses to soil phosphorus availability. Plant Cell Environ 22:425–431

    CAS  Google Scholar 

  • Bouldin DR (1961) Mathematical description of diffusion process in the soil. Soil Sci Soc Am Proc 25:476–480

    CAS  Google Scholar 

  • Bouranis DL, Chorianopoulou SN, Siyiannis VF, Protonotarios VE, Hawkesford MJ (2003) Aerenchyma formation in roots of maize during sulphate starvation. Planta 217:382–391

    PubMed  CAS  Google Scholar 

  • Bouwman AF, Beusen AHW, Billen G (2009) Human alteration of the global nitrogen and phosphorus soil balances for the period 1970-2050. Global Biogeochem Cycles 23:GB0A04. doi:10.1029/2009GB003576

    Google Scholar 

  • Bowen GD, Rovira AD (1999) The rhizosphere and its management to improve plant growth. Adv Agron 66:1–102

    Google Scholar 

  • Brooks A (1986) Effects of phosphorus nutrition on ribulose-1,5-bisphosphate carboxylase activation, photosynthetic quantum yield and amounts of some Calvin-cycle metabolites in spinach leaves. Func Plant Biol 13:221–237

    CAS  Google Scholar 

  • Bünemann EK (2008) Enzyme additions as a tool to assess the potential bioavailability of organically bound nutrients. Soil Biol Biochem 40:2116–2129

    Google Scholar 

  • Burkitt LL, Small DR, McDonald JW, Wales WJ, Jenkin ML (2007) Comparing irrigated, biodynamic and conventionally managed dairy farms. 1. Soil and pasture properties. Aust J Experim Agric 47:479–488

    CAS  Google Scholar 

  • Caradus JR (1981) Effect of root hair length on white clover growth over a range of soil phosphorus levels. New Zeal J Agric Res 24:353–358

    Google Scholar 

  • Caradus JR (1994) Selection for improved adaptation of white clover to low phosphorus and acid soils. Euphytica 77:243–250

    Google Scholar 

  • Caradus JR, Dunn A (2000) Adaptation to low fertility hill country in New Zealand of white clover lines selected for differences in response to phosphorus. New Zeal J Agric Res 43:63–69

    Google Scholar 

  • Caradus JR, Mackay AD, Wewala S, Dunlop J, Hart A, van den Bosch J, Lambert MG, Hay MJM (1992) Inheritance of phosphorus response in white clover. Plant Soil 146:199–208

    CAS  Google Scholar 

  • Celi L, Barberis E (2005) Abiotic stabilization of organic phosphorus in the environment. In: Turner BL, Frossard E, Baldwin D (eds) organic phosphorus in the environment. CABI Publishing, Wallingford, pp 113–132

    Google Scholar 

  • Chapin FS, Bieleski RL (1982) Mild phosphorus stress in barley and a related low-phosphorus-adapted barley grass: Phosphorus fractions and phosphate absorption in relation to growth. Physiol Plantarum 54:309–317

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Chen CR, Condron LM, Turner BL, Mahieu N, Davis MR, Xu ZH, Sherlock RR (2004) Mineralisation of soil orthophosphate monoesters under pine seedlings and ryegrass. Aust J Soil Res 42:189–196

    CAS  Google Scholar 

  • Cherr CM, Scholberg JMS, McSorely R (2006) Green manure approaches to crop production: a synthesis. Agron J 98:302–319

    Google Scholar 

  • Clarkson DT (1985) Factors affecting mineral acquisition by plants. Ann Rev Plant Physiol 36:77–115

    CAS  Google Scholar 

  • Condron LM (2004) Phosphorus—surplus and deficiency. In: Schjønning P, Christensen BT, Elmholt S (eds) Managing Soil Quality—challenges in modern agriculture. CAB International, Wallingford, pp 69–84

    Google Scholar 

  • Cordell D, Drangert JO, White S (2009) The story of phosphorus: Global food security and food for thought. Global Environ Chang 19:292–305

    Google Scholar 

  • Costa R, Salles, JF, Berg G, Smalla K (2006) Cultivation-independent analysis of Pseudomonas species in soil and in the rhizosphere of field-grown Verticillium dahliae host plants. Environ Microbiol 8:2136–2149

    PubMed  CAS  Google Scholar 

  • Crush JR, Boulesteix-Coutelier ARL, Ouyang L (2008) Phosphate uptake by white clover (Trifolium repens L.) genotypes with contrasting root morphology. New Zeal J Agric Res 51:279–285

    CAS  Google Scholar 

  • Cunningham JE, Kuiack C (1992) Production of citric and oxalic acids and solubilization of calcium phosphate by Penicillium billai. Appl Environ Microbiol 52:1451–1458

    Google Scholar 

  • De Groot CC, Marcelis LFM, Van Den Boogaard R, Lambers H (2001) Growth and dry-mass partitioning in tomato as affected by phosphorus nutrition and light. Plant Cell Environ 24:1309–1317

    Google Scholar 

  • De Groot CC, Van den Boogaard R, Marcelis LFM, Harbinson J, Lambers H (2003) Contrasting effects of N and P deprivation on the regulation of photosynthesis in tomato plants in relation to feedback limitation. J Exp Bot 54:1957–1967

    PubMed  Google Scholar 

  • de la Fuente JM, Ramírez-Rodríguez V, Cabrera-Ponce JL, Herrera-Estrella L (1997) Aluminum tolerance in transgenic plants by alteration of citrate synthesis. Science 276:1566–1568

    PubMed  Google Scholar 

  • De Marco DG (1990) Effect of seed weight, and seed phosphorus and nitrogen concentrations on the early growth of wheat seedlings. Aust J Exp Agric 30:545–549

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Delhaize E, Ryan PR, Hocking PJ, Richardson AE (2003) Effects of altered citrate synthase and isocitrate dehydrogenase expression on internal citrate concentrations and citrate efflux from tobacco (Nicotiana tabacum L.) roots. Plant Soil 248:137–144

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Delhaize E, Gruber BD, Ryan PR (2007) The roles of organic anion permeases in aluminium tolerance and mineral nutrition. FEBS Letters 581:2255–2262

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Denton MD, Veneklaas EJ, Freimoser FM, Lambers H (2007) Banksia species (Proteaceae) from severely phosphorus-impoverished soils exhibit extreme efficiency in the use and re-mobilization of phosphorus. Plant Cell Environ 30:1557–1565

    PubMed  CAS  Google Scholar 

  • Dessureault-Rompre J, Nowack B, Schulin R, Luster J (2007) Spatial and temporal variation in organic acid anion exudation and nutrient anion uptake in the rhizosphere of Lupinus albus L. Plant Soil 301:123–134

    CAS  Google Scholar 

  • Dinkelaker B, Romheld BV, Marschner H (1989) Citric acid excretion and precipitation of Ca citrate in the rhizosphere of white lupin (Lupinus albus L.). Plant Cell Environ 12:285–292

    CAS  Google Scholar 

  • Dinkelaker B, Hengeler C, Marschner H (1995) Distribution and function of proteoid roots and other root clusters. Botanica Acta 108:183–200

    Google Scholar 

  • Downey J, van Kessel C (1990) Dual inoculation of Pisum sativum with Rhizobium leguminosarum and Penicillium bilaji. Biol Fert Soils 10:194–196

    Google Scholar 

  • Drew MC, He CJ, Morgan PN (1989) Decreased ethylene biosynthesis, and induction of aerenchyma, by nitrogen- or phosphate-starvation in adventitious roots of Zea mays L. Plant Physiol 91:266–271

    PubMed  CAS  Google Scholar 

  • Duff SMG, Sarath G, Plaxton WC (1994) The role of acid phosphatases in plant phosphorus metabolism. Physiol Plantarum 90:791–800

    CAS  Google Scholar 

  • Durrett TP, Gassmann W, Rogers EE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol 144:197–205

    PubMed  CAS  Google Scholar 

  • Edel-Hermann V, Gautheron N, Alabouvette C, Steinberg C (2008) Fingerprinting methods to approach multitrophic interactions among microflora and microfauna communities in soil. Biol Fert Soils 44:975–984

    CAS  Google Scholar 

  • Elliot DE, Reuter DJ, Reddy GD, Abbott RJ (1997) Phosphorus nutrition of spring wheat (Triticum aestivum L.) 1. Effects of phosphorus supply on plant symptoms, yield, components of yield, and plant phosphorus uptake. Aust J Agric Res 48:855–867

    Google Scholar 

  • El-Tarabily KA, Nassar AH, Sivasithamparam K (2008) Promotion of growth of bean (Phaseolus vulgaris L.) in a calcareous soil by a phosphate-solubilizing, rhizosphere-competent isolate of Micromonospora endolithica. Appl Soil Ecol 39:161–171

    Google Scholar 

  • Eshel A, Nielsen KL, Lynch JP (1995) Response of bean root systems to low level of P. In: Plant roots—from cells to systems. 14th Long Ashton International Symposium. IACR-Long Ashton Research Station Bristol, England, p 63

  • Fageria NK (2007) Green manuring in crop production. J Plant Nutr 30:691–719

    CAS  Google Scholar 

  • Fan MS, Zhu JM, Richards C, Brown KM, Lynch JP (2003) Physiological roles for aerenchyma in phosphorus-stressed roots. Func Plant Biol 30:493–506

    Google Scholar 

  • Fay P, Mitchell DT, Osborne BA (1996) Photosynthesis and nutrient-use efficiency of barley in response to low arbuscular mycorrhizal colonization and addition of phosphorus. New Phytol 132:425–433

    CAS  Google Scholar 

  • Fox TR, Comerford NB, McFee WW (1990) Phosphorus and aluminium release fom a spodic horizon mediated by organic acids. Soil Sci Soc Am J 54:1763–1767

    CAS  Google Scholar 

  • Foyer C, Spencer C (1986) The relationship between phosphate status and photosynthesis in leaves. Planta 167:369–375

    Google Scholar 

  • Freer M, Dove H, Nolan JV (2007) Nutrient requirements of domesticated ruminants. CSIRO Publishing, Collingwood

    Google Scholar 

  • Gadd GM (1999) Fungal production of citric and oxalic acid: Importance in metal speciation, physiology and biogeochemical processes. Advan Microbial Physiol 41:47–92

    CAS  Google Scholar 

  • 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 143:185–191

    CAS  Google Scholar 

  • Gahoonia TS, Nielsen NE (1997) Variation in root hairs of barley cultivars doubled soil phosphorus uptake. Euphytica 98:177–182

    Google Scholar 

  • Gahoonia TS, Nielsen NE (1998) Direct evidence on participation of root hairs in phosphorus (P-32) uptake from soil. Plant Soil 19:147–152

    Google Scholar 

  • Gahoonia TS, Nielsen NE (2003) Phosphorus (P) uptake and growth of a root hairless barley mutant (bald root barley, brb) and wild type in low- and high-P soils. Plant Cell Environ 26:1759–1766

    CAS  Google Scholar 

  • Gahoonia TS, Nielsen NE (2004) Barley genotypes with long root hairs sustain high grain yields in low-P field. Plant Soil 262:55–62

    CAS  Google Scholar 

  • Gahoonia TS, Nielsen NE, Lyshede OB (1999) Phosphorus (P) acquisition of cereal cultivars in the field at three levels of P fertilization. Plant Soil 211:269–281

    CAS  Google Scholar 

  • Gardner WK, Parbery DG, Barber DA (1981) Proteoid root morphology and function in Lupinus albus. Plant Soil 60:143–147

    CAS  Google Scholar 

  • Gardner WK, Barber DA, Parbery DG (1983) The acquisition of phosphorus by Lupinus albus L. III. The probable mechanism by which phosphorus movement in the soil-root interface is enhanced. Plant Soil 70:107–124

    CAS  Google Scholar 

  • Ge ZY, Rubio G, Lynch JP (2000) The importance of root gravitropism for inter-root competition and phosphorus acquisition efficiency: results from a geometric simulation model. Plant Soil 218:159–171

    PubMed  CAS  Google Scholar 

  • George TS, Richardson AE (2008) Potential and limitations to improving crops for enhanced phosphorus utilisation. In: White PJ, Hammond JP (eds) The ecophysiology of plant-phosphorus interactions. Plant Ecophysiology, vol. 7. Springer, Dordrecht, pp 247–270

    Google Scholar 

  • George TS, Gregory PJ, Robinson JS, Buresh RJ (2002a) Changes in phosphorus concentrations and pH in the rhizosphere of some agroforestry and crop species. Plant Soil 246:65–73

    CAS  Google Scholar 

  • George TS, Gregory PJ, Robinson JS, Buresh RJ, Jama B (2002b) Utilisation of soil organic P by agroforestry and crop species in the field, western Kenya. Plant Soil 246:53–63

    CAS  Google Scholar 

  • George TS, Richardson AE, Hadobas PA, Simpson RJ (2004) Characterisation of transgenic Trifolium subterraneum L. which expresses phyA and releases extracellular phytase: Growth and phosphorus nutrition in laboratory media and soil. Plant Cell Environ 27:1351–1361

    CAS  Google Scholar 

  • George TS, Richardson AE, Simpson RJ (2005a) Behaviour of plant-derived extracellular phytase upon addition to soil. Soil Biol Biochem 37:977–988

    CAS  Google Scholar 

  • George TS, Richardson AE, Smith JB, Hadobas PA, Simpson J (2005b) Limitations to the potential of transgenic Trifolium subterraneum L. plants that exude phytase, when grown in soils with a range of organic phosphorus content. Plant Soil 278:263–274

    CAS  Google Scholar 

  • George TS, Simpson RJ, Hadobas PA, Richardson AE (2005c) Expression of a fungal phytase gene in Nicotiana tabacum improves phosphorus nutrition in plants grown in amended soil. Plant Biotechnol J 3:129–140

    PubMed  CAS  Google Scholar 

  • George TS, Gregory PJ, Simpson RJ, Richardson AE (2007a) Differential interactions of Aspergillus niger and Peniophora lycii phytases with soil particles affects the hydrolysis of inositol phosphates. Soil Biol Biochem 39:793–803

    CAS  Google Scholar 

  • George TS, Simpson RJ, Hadobas PA, Marshall DJ, Richardson AE (2007b) Accumulation and phosphatase-lability of organic phosphorus in fertilized pasture soils. Aust J Agric Res 58:47–55

    CAS  Google Scholar 

  • George TS, Hocking PJ, Gregory PJ, Richardson AE (2008) Variation of root-associated phosphatase in wheat cultivars explains their ability to utilise organic P substrates in-vitro, but does not effectively predict P-nutrition in a range soils. Environ Exp Bot 64:239–249

    CAS  Google Scholar 

  • George TS, Brown LK, Newton AC, Hallett PD, Sun BH, Thomas WTB, White PJ (2011) Impact of soil tillage on the robustness of the genetic component of variation in phosphorus (P) use efficiency in barley (Hordeum vulgare L.). Plant Soil 339:113–123

    CAS  Google Scholar 

  • Gerke J (1992) Phosphate, aluminium and iron in the soil solution of three different soils in relation to varying concentrations of citric acid. Z Pflanz Bodenkunde 155:339–343

    CAS  Google Scholar 

  • Gerke J (1994) Kinetics of soil phosphate desorption as affected by citric acid. Z Pflanz Bodenkunde 157:17–22

    CAS  Google Scholar 

  • Giaveno C, Celi L, Richardson AE, Simpson RJ, Barberis E (2010) Interaction of phytases with soil minerals and availability of substrate affects the hydrolysis of inositol phosphates. Soil Biol Biochem 42:491–498

    CAS  Google Scholar 

  • Gilbert GA, Knight JD, Vance CP, Allan DL (1999) Acid phosphatase activity in phosphorus-deficient white lupin roots. Plant Cell Environ 22:801–810

    CAS  Google Scholar 

  • Glassop D, Smith SE, Smith FW (2005) Cereal phosphate transporters associated with the mycorrhizal pathway of phosphate uptake into roots. Planta 222:688–698

    PubMed  CAS  Google Scholar 

  • Godwin DC, Wilson EJ (1976) Prospects for selecting plants with increased P efficiency. In: Blair GJ (ed) Reviews in rural science. Ill. The efficiency of phosphorus utilization. University of New England Press, Armidale, pp 131–139

    Google Scholar 

  • Goos RJ, Johnson BE, Stack RW (1994) Penicillium bilaji and phosphorus fertilization effects on the growth, development yield and common root rot severity of spring wheat. Fert Res 39:97–103

    CAS  Google Scholar 

  • Górny AG, Sodkiewicz T (2001) Genetic analysis of the nitrogen and phosphorus utilization efficiencies in mature spring barley plants. Plant Breeding 120:129–132

    Google Scholar 

  • Grace EJ, Smith FA, Smith SE (2009) Deciphering the arbuscular mycorrhizal pathway of P uptake in non-responsive host plant species. In: Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson (eds) Functional processes and ecological impact. Springer, Heidelberg, pp 89–106

    Google Scholar 

  • Graham JH, Miller RM (2005) Mycorrhizas: gene to function. Plant Soil 274:79–100

    CAS  Google Scholar 

  • Gruber BD, Ryan PR, Richardson AE, Tyerman SD, Ramesh S, Hebb DM, Howitt SM, Delhaize E (2010) HvALMT1 from barley is involved in the transport of organic anions. J Exp Bot 61:1455–1467

    PubMed  CAS  Google Scholar 

  • Gruber BD, Delhaize E, Richardson AE, Roessner U, James RA, Howitt SM, Ryan PR (2011) Characterisation of HvALMT1 function in transgenic barley plants. Func Plant Biol 38:163–175

    CAS  Google Scholar 

  • Gulden RH, Vessey JK (2000) Penicillium bilaii inoculation increases root hair production in field pea. Can J Plant Sci 80:801–804

    Google Scholar 

  • Guttieri M, Bowen D, Dorsch JA, Raboy V, Souza E (2004) Identification and characterization of a low phytic acid wheat. Crop Sci 44:418–424

    CAS  Google Scholar 

  • Gyaneshwar P, Naresh Kumar G, Parekh LJ, Poole PS (2002) Role of soil microorganisms in improving P nutrition of plants. Plant Soil 245:83–93

    CAS  Google Scholar 

  • 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 architecture traits. J Exp Bot 60:1953–1968

    PubMed  CAS  Google Scholar 

  • Harvey PR, Warren RA, Wakelin SA (2009) Potential to improve root access to phosphorus: the role of non-symbiotic microbial inoculants in the rhizosphere. Crop Pasture Sci 60:144–151

    CAS  Google Scholar 

  • Haugland RA, Varma M, Wymer LJ, Vesper SJ (2004) Quantitative PCR analysis of selected Aspergillus, Penicillium and Paecilomyces species. Syst Appl Microbiol 27:198–210

    PubMed  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Hayes JE, Richardson AE, Simpson RJ (2000a) Components of organic phosphorus in soil extracts that are hydrolysed by phytase and acid phosphatase. Biol Fert Soils 32:279–286

    CAS  Google Scholar 

  • Hayes JE, Simpson RJ, Richardson AE (2000b) The growth and utilisation of plants in sterile media when supplied with inositol hexaphosphate, glucose 1-phosphate or inorganic phosphate. Plant Soil 220:165–174

    CAS  Google Scholar 

  • Helyar KR (1998) Efficiency of nutrient utilization and sustaining soil fertility with particular reference to phosphorus. Field Crops Res 56:187–195

    Google Scholar 

  • Henry A, Chaves NF, Kleinman PJA, Lynch JP (2010a) Will nutrient-efficient genotypes mine the soil? Effects of genetic differences in root architecture in common bean (Phaseolus vulgaris L.) on soil phosphorus depletion in a low-input agro-ecosystem in Central America. Field Crops Res 115:67–78

    Google Scholar 

  • Henry A, Rosas JC, Beaver JS, Lynch JP (2010b) Multiple stress response and below ground competition in multilines of common bean (Phaseolus vulgaris L.). Field Crops Res 117:209–218

    Google Scholar 

  • Hetrick BAD (1991) Mycorrhizas and root architecture. Experientia 47:355–362

    Google Scholar 

  • Hetrick BAD, Wilson GWT, Todd TC (1996) Mycorrhizal response in wheat cultivars: relationship to phosphorus. Can J Bot 74:19–25

    CAS  Google Scholar 

  • Hill JO, Simpson RJ, Wood JT, Moore AD, Chapman DF (2005) The phosphorus and nitrogen requirements of temperate pasture species and their influence on grassland botanical composition. Aust J Agric Res 56:1027–1039

    CAS  Google Scholar 

  • Ho M, Rosas J, Brown K, Lynch J (2005) Root architectural tradeoffs for water and phosphorus acquisition. Func Plant Biol 32:737–748

    CAS  Google Scholar 

  • Hocking PJ, Jeffery S (2004) Cluster-root production and organic anion exudation in a group of old-world lupins and a new-world lupin. Plant Soil 258:135–150

    CAS  Google Scholar 

  • 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 environment. Kluwer Academic Publishers, Dordrecht, pp 305–308

    Google Scholar 

  • Hocking AD, Whitelaw M, Harden TJ (1998) Penicillium radicum sp. nov. from the rhizosphere of Australian wheat. Mycol Res 102:801–806

    Google Scholar 

  • Horst WJ, Kamh M, Jibrin JM, Chude VO (2001) Agronomic measures for increasing P availability to crops. Plant Soil 237:211–223

    CAS  Google Scholar 

  • Huyghe C (1997) White lupin (Lupinus albus L). Field Crops Res 53:147–160

    Google Scholar 

  • Itoh S, Barber SA (1983) Phosphorus uptake by six plant species as related to root hairs. Agron J 75:457–461

    Google Scholar 

  • Jakobsen I, Chen BD, Munkvold L, Lundsgaard T, Zhu Y-G (2005a) Contrasting phosphate acquisition of mycorrhizal fungi with that of root hairs using the root hairless barley mutant. Plant Cell Environ 28:928–938

    CAS  Google Scholar 

  • Jakobsen I, Leggett ME, Richardson AE (2005b) Rhizosphere microorganisms and plant phosphorus uptake. In: Sims JT, Sharpley AN (eds) Phosphorus, agriculture and the environment. American Society for Agronomy, Madison, pp 437–494

    Google Scholar 

  • Javot H, Pumplin N, Harrison MJ (2007) Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ 30:310–322

    PubMed  CAS  Google Scholar 

  • Jeschke WD, Pate JS (1995) Mineral nutrition and transport in xylem and phloem of Banksia prionotes (Proteaceae), a tree with dimorphic root morphology. J Exp Bot 46:895–905

    CAS  Google Scholar 

  • Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–585

    Google Scholar 

  • Jones DL (1998) Organic acids in the rhizosphere—a critical review. Plant Soil 205:25–44

    CAS  Google Scholar 

  • Jones DL, Darrah PR (1994) Role of root-derived organic acids in the mobilisation of nutrients from the rhizosphere. Plant Soil 166:247–257

    CAS  Google Scholar 

  • Jones DL, Dennis PG, Owen AG, van Hees PAW (2003) Organic acid behaviour in soils—misconceptions and knowledge gaps. Plant Soil 248:31–41

    CAS  Google Scholar 

  • Jungk A (2001) Root hairs and the acquisition of plant nutrients from soil. J Plant Nutr Soil Sci 164:121–129

    CAS  Google Scholar 

  • Karamanos RE, Flore NA, Harapiak JT (2010) Re-visiting use of Penicillium bilaii with phosphorus fertilization of hard red spring wheat. Can J Plant Sci 90:265–277

    Google Scholar 

  • Khademi Z, Jones DL, Malakouti MJ, Asadi F, Ardebili M (2009) Organic acid mediated nutrient extraction efficiency in three calcareous soils. Aust J Soil Res 47:213–220

    CAS  Google Scholar 

  • Khademi Z, Jones DL, Malakouti MJ, Asadi F (2010) Organic acids differ in enhancing phosphorus uptake by Triticum aestivum L.- effects of rhizosphere concentration and counterion. Plant Soil 334:151–159

    CAS  Google Scholar 

  • Khan SA, Hamayun M, Yoon M, Kim H-Y, Suh S-Y, Hwang S-K, Kim J-M, Lee I-Y, Choo Y-S, Yoon U-H, Kong W-S, Lee B-M, Kim J-G (2008) Plant growth promotion and Penicillium citrinum. BMC Microbiol 8:231–40

    PubMed  Google Scholar 

  • Khan MS, Zaidi A, Ahemad M, Oves M, Wani PA (2010) Plant growth promotion by phosphate solubilizing fungi—current perspective. Arch Agron Soil Sci 56:73–98

    CAS  Google Scholar 

  • Kirk GJD (1999) A model for phosphate solubilization by organic anion excretion from plant roots. Eur J Soil Sci 50:369–378

    CAS  Google Scholar 

  • Kochian LV, Hoekenga OA, Pineros MA (2004) How do crop plants tolerate acid soils?—Mechanisms of aluminum tolerance and phosphorous efficiency. Ann Rev Plant Biol 55:459–493

    CAS  Google Scholar 

  • Konings H, Verschuren G (1980) Formation of aerenchyma in roots of Zea mays in aerated solutions, and its relation to nutrient supply. Physiol Plant 49:265–279

    CAS  Google Scholar 

  • Kothari SK, Marschner H, George E (1990) Effect of VA mycorrhizal fungi and rhizosphere microorganisms on root and shoot morphology, growth and water relations in maize. New Phytol 116:303–311

    Google Scholar 

  • Kovermann P, Meyer S, Hortensteiner S, Picco C, Scholz-Starke J, Ravera S, Lee Y, Martinoia E (2007) The Arabidopsis vacuolar malate channel is a member of the ALMT family. Plant J 52:1169–1180

    PubMed  CAS  Google Scholar 

  • Koyama H, Takita E, Kawamura A, Hara T, Shibata D (1999) Over expression of mitochondrial citrate synthase gene improves the growth of carrot cells in Al-phosphate medium. Plant Cell Physiol 40:482–488

    PubMed  CAS  Google Scholar 

  • 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 41:1030–1037

    PubMed  CAS  Google Scholar 

  • Kucey RMN (1983) Phosphate-solubilizing bacteria and fungi in various cultivated and virgin Alberta soils. Can J Soil Sci 63:671–678

    CAS  Google Scholar 

  • Kucey RMN (1987) Increased phosphorus uptake by wheat and field beans inoculated with a phosphorus-solubilizing Penicillium bilaji strain and with vesicular-arbuscular mycorrhizal fungi. Appl Environ Microbiol 53:2699–2703

    PubMed  CAS  Google Scholar 

  • Kucey RMN (1988) Effect of Penicillium bilaji on solubility and uptake of P and micronutrients from soil by wheat. Can J Soil Sci 68:261–270

    CAS  Google Scholar 

  • Kucey RMN, Leggett ME (1989) Increased yields and phosphorus uptake by Westar canola (Brassica napus L.) inoculated with a phosphate-solubilizing isolate of Penicillium bilaji. Can J Soil Sci 69:425–432

    Google Scholar 

  • Kucey RMN, Janzen HH, Leggett ME (1989) Microbially mediated increases in plant-available phosphorus. Adv Agron 42:199–228

    CAS  Google Scholar 

  • Kumar V, Sinha AK, Makkar HPS, Becker K (2010) Dietary roles of phytate and phytase in human nutrition: A review. Food Chem 120:945–959

    CAS  Google Scholar 

  • Lambers H, Poorter H (1992) Inherent variation in growth-rate between higher-plants—a search for physiological causes and ecological consequences. Adv Ecol Res 23:187–261

    CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103

    PubMed  Google Scholar 

  • Lambers H, Brundrett MC, Raven JA, Hopper SD (2010) Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant Soil 334:11–31

    CAS  Google Scholar 

  • Lambers H, Finnegan PM, Laliberté E, Pearse SJ, Ryan MH, Shane MW, Veneklaas EJ (2011) Phosphorus nutrition of proteaceae in severely phosphorus-impoverished soils: Are there lessons to be learned for future crops? Plant Physiol 156:1058–1066

    PubMed  CAS  Google Scholar 

  • Lamont B (1973) Factors affecting the distribution of proteoid roots within the root systems of two Hakea species. Aust J Bot 21:165–187

    CAS  Google Scholar 

  • Leggett M, Cross J, Hnatowich G, Holloway G (2007) Challenges in commercializing a phosphate-solubilizing microorganisms: Penicillium bilaiae, a case history. In: Velázquez E, Rodríguez-Barrueco C, Velázquez E, Rodríguez-Barrueco C (eds) First international meeting on microbial phosphate solubilization. Springer, Dordrecht, pp 215–222

    Google Scholar 

  • Lewis DG, Quirk JP (1967) Phosphate diffusion in soil and uptake by plants. Plant Soil 26:445–453

    CAS  Google Scholar 

  • Li MG, 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

    Google Scholar 

  • Li L, Tang CX, Rengel Z, Zhang FS (2003) Chickpea facilitates phosphorus uptake by intercropped wheat from an organic phosphorus source. Plant Soil 248:297–303

    CAS  Google Scholar 

  • Li SM, Li L, Zhang FS, Tang CX (2004) Acid phosphatase role in chickpea/maize intercropping. Ann Bot 94:297–303

    PubMed  CAS  Google Scholar 

  • Li HY, Smith SE, Holloway RE, Zhu Y-G, Smith FA (2006) Arbuscular mycorrhizal fungi contribute to phosphorus uptake by wheat grown in a phosphorus-fixing soil even in the absence of positive growth responses. New Phytol 172:536–543

    PubMed  CAS  Google Scholar 

  • Li HY, Smith FA, Dickson S, Holloway RE, Smith SE (2008) Plant growth depressions in arbuscular mycorrhizal symbiosis: not just caused by carbon drain? New Phytol 178:852–862

    PubMed  Google Scholar 

  • Liao H, Rubio G, Yan XL, Cao AQ, Brown KM, Lynch JP (2001) Effect of phosphorus availability on basal root shallowness in common bean. Plant Soil 232:69–79

    PubMed  CAS  Google Scholar 

  • 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 31:959–970

    CAS  Google Scholar 

  • Liao M, Hocking PJ, Dong B, Delhaize E, Richardson AE, Ryan PR (2008) Genotypic variation in phosphorus efficiency among wheat genotypes grown on two contrasting Australian soils. Aust J Agr Res 59:157–166

    CAS  Google Scholar 

  • López-Bucio J, de la Vega OM, Guevara-García A, Herrera-Estrella L (2000) Enhanced phosphorus uptake in transgenic tobacco plants that overproduce citrate. Nat Biotechnol 18:450–453

    PubMed  Google Scholar 

  • Lung S-C, Lim BL (2006) Assimilation of phytate-phosphours by the extracellualr phytase activity of tobacco (Nicotiana tabaccum) is affected by the availabiliyt of souluble phytate. Plant Soil 279:187–199

    CAS  Google Scholar 

  • Lung S-C, Chan WL, Yip W, Wang L, Yeung EC, Lim BL (2005) Secretion of beta-propeller phytase from tobacco and Arabidopsis roots ehnances phosphorus utilization. Plant Sci 169:341–349

    CAS  Google Scholar 

  • Lynch JP (2007) Roots of the second green revolution. Aust J Bot 55:1–20

    Google Scholar 

  • Lynch JP, Brown KM (1998) Regulation of root architecture by phosphorus availability. In: Lynch JP, Deikman J (eds) Phosphorus in plant biology: Regulatory roles in molecular, cellular, organismic and ecosystem processes. American Society of Plant Biologists, Rockville, pp 148–156

    Google Scholar 

  • Lynch JP, Brown KM (2001) Topsoil foraging—an architectural adaptation of plants to low phosphorus availability. Plant Soil 237:225–237

    CAS  Google Scholar 

  • Lynch JP, Brown KM (2006) Whole plant adaptations to low phosphorus availability. In: Huang B (ed) Plant-environment interactions. CRC, Boca Raton, pp 209–242

    Google Scholar 

  • Lynch JP, Brown KM (2008) Root strategies for phosphorus acquisition. In: White PJ, Hammond JP (eds) The ecophysiology of plant-phosphorus interactions. Plant Ecophysiology, vol. 7. Springer, Dordrecht, pp 83–116

    Google Scholar 

  • Lynch JP, Ho MD (2005) Rhizoeconomics: Carbon costs of phosphorus acquisition. Plant Soil 269:45–56

    CAS  Google Scholar 

  • Lynch JP, St Clair SB (2004) Mineral stress: the missing link in understanding how global climate change will affect plants in real world soils. Field Crops Res 90:101–115

    Google Scholar 

  • Lynch JP, Nielsen KL, Davis RD, Jablokow AG (1997) SimRoot: modelling and visualization of root systems. Plant Soil 188:139–151

    CAS  Google Scholar 

  • Ma Z, Bielenberg DG, Brown KM, Lynch JP (2001a) Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant Cell Environ 24:459–467

    CAS  Google Scholar 

  • Ma Z, Walk TC, Marcus A, Lynch JP (2001b) Morphological synergism in root hair length, density, initiation and geometry for phosphorus acquisition in Arabidopsis thaliana: A modeling approach. Plant Soil 236:221–35

    CAS  Google Scholar 

  • Ma X-F, Wright E, Ge Y, Bell J, Xi Y, Bouton JH, Wang Z-Y (2009) Improving phosphorus acquistion of white clover (Trifolium repens L.) by transgenic expression of plant-derived phytase and acid phosphatase genes. Plant Sci 176:479–488

    CAS  Google Scholar 

  • Magid J, Tiessen H, Condron LM (1996) Dynamics of organic phosphorus in soils under natural and agricultural ecosystems. In: Piccolo A (ed) Humic substances in terrestrial ecosystems. Elsevier Science, Amsterdam, pp 429–466

    Google Scholar 

  • Mano Y, Omori F, Takamizo T, Kindiger B, Bird RM, Loaisiga CH, Takahashi H (2007) QTL mapping of root aerenchyma formation in seedlings of a maize x rare teosinte Zea nicaraguensis cross. Plant Soil 295:103–113

    CAS  Google Scholar 

  • Manske GGB, Ortiz-Monasterio JI, Van Ginkel M, Gonzalez RM, Rajaram S, Molina E, Vlek PLG (2000) Traits associated with improved P-uptake efficiency in CIMMYT’s semidwarf spring bread wheat grown on acid Andisols in Mexico. Plant Soil 221:189–204

    CAS  Google Scholar 

  • Matzek V, Vitousek PM (2009) N:P stoichiometry and protein:RNA ratios in vascular plants: an evaluation of the growth-rate hypothesis. Ecol Lett 12:765–771

    PubMed  Google Scholar 

  • McIvor JG, Guppy C, Probert ME (2011) Phosphorus requirements of tropical grazing systems: the northern Australian experience. Plant Soil (Special Issue S43—Phosphorus. doi:10.1007/s11104-011-0906-8)

  • McLaughlin MJ, Fillery IR, Till AR (1992) Operation of the phosphorus, sulphur and nitrogen cycles. In: Australia’s renewable resources: sustainability and global change. Bureau Rural Res Proc 14:67–116

  • McLaughlin MJ, McBeath TM, Smernik R, Stacey SP, Ajiboye B. Guppy, C (2011) The chemical nature of P accumulation in agricultural soils—implications for fertiliser management and design: an Australian perspective. Plant Soil (Special Issue S43—Phosphorus. doi:10.1007/s11104-011-0907-7)

  • Miguel MA (2004) Genotypic variation in root hairs and phosphorus efficiency in common bean (Phaseolus vulgaris L.). MS thesis. Pennsylvania State University, University Park

    Google Scholar 

  • Miguel MA (2011) Functional role and synergistic effect of root traits for phosphorus acquisition efficiency and their genetic basis in common bean (Phaseolus vulgaris L.). PhD thesis. Pennsylvania State University, University Park

    Google Scholar 

  • Miller CR, Ochoa I, Nielsen KL, Beck D, Lynch JP (2003) Genetic variation for adventitious rooting in response to low phosphorus availability: potential utility for phosphorus acquisition from stratified soils. Func Plant Biol 30:973–985

    CAS  Google Scholar 

  • Mollier A, Pellerin S (1999) Maize root system growth and development as influenced by phosphorus deficiency. J Exp Bot 50:487–497

    CAS  Google Scholar 

  • Morrow de la Riva L (2010) Root etiolation as a strategy for phosphorus acquisition in common bean, MS thesis. Pennsylvania State University, University Park

    Google Scholar 

  • Neumann G, Martinoia E (2002) Cluster roots—an underground adaptation for survival in extreme environments. Trends Plant Sci 7:162–167

    PubMed  CAS  Google Scholar 

  • Nielsen KL, Bouma TJ, Lynch JP, Eissenstat DM (1998) Effects of phosphorus availability and vesicular-arbuscular mycorrhizas on the carbon budget of common bean (Phaseolus vulgaris). New Phytol 139:647–656

    Google Scholar 

  • Nielsen KL, Eshel A, Lynch JP (2001) The effect of phosphorus availability on the carbon economy of contrasting common bean (Phaseolus vulgaris L.) genotypes. J Exp Bot 52:329–339

    PubMed  CAS  Google Scholar 

  • Nuruzzaman M, Lambers H, Bolland MDA, Veneklaas EJ (2005) Phosphorus benefits of different legume crops to subsequent wheat grown in different soils of Western Australia. Plant Soil 271:175–187

    CAS  Google Scholar 

  • Nye PH (1973) The relation between the radius of a root and its nutrient absorbing power. J Exp Bot 24:783–786

    Google Scholar 

  • 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

    Google Scholar 

  • Oberson A, Besson JM, Maire N, Sticher H (1996) Microbiological processes in soil organic phosphorus transformations in conventional and biological cropping systems. Biol Fert Soils 21:138–148

    CAS  Google Scholar 

  • Oburger E, Kirk GJD, Wenzel WW, Puschenreiter M, Jones DL (2009) Interactive effects of organic acids in the rhizosphere. Soil Biol Biochem 41:449–457

    CAS  Google Scholar 

  • Oburger E, Jones DL, Wenzel WW (2011) Phosphorus saturation and pH differentially regualte the efficiency of organcic acid anion-mediated P solubilization mechanims in soil. Plant Soil (on line: doi 10.1007/s11104-010-0659-5)

  • Ochoa I, Blair M, Lynch J (2006) QTL Analysis of adventitious root formation in common bean (Phaseolus vulgaris L.) under contrasting phosphorus availability. Crop Sci 46:1609–1621

    CAS  Google Scholar 

  • Osorio NW, Habte M (2001) Synergistic influence of an arbuscular mycorrhizal fungus and a P solubilizing fungus on growth and P uptake of Leucaena leucocephala in an oxisol. Arid Land Res Manage 15:263–274

    CAS  Google Scholar 

  • Ozanne PG (1980) Phosphate nutrition of plants—a general treatise. In: Khasawneh FE, Sample EC, Kamprath EJ (eds) The role of phosphorus in agriculture. American Society of Agronomy, Madison, pp 559–616

    Google Scholar 

  • 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 269:69–80

    CAS  Google Scholar 

  • Pang J, Ryan MH, Tibbett M, Cawthray GR, Siddique KHM, Bolland MDA, Denton MD, Lambers H (2010) Variation in morphological and physiological parameters in herbaceous perennial legumes in response to phosphorus supply. Plant Soil 331:241–255

    CAS  Google Scholar 

  • Pate JS, Verboom WH, Galloway PD (2001) Co-occurrence of Proteaceae, laterite and related oligotrophic soils: coincidental associations or causative inter-relationships? Aust J Bot 49:529–560

    CAS  Google Scholar 

  • Pearse SJ, Veneklaas EJ, Cawthray GR, Bolland MDA, Lambers H (2006) Carboxylate release of wheat, canola and 11 grain legume species as affected by phosphorus status. Plant Soil 288:127–139

    CAS  Google Scholar 

  • Pearse SJ, Veneklaas EJ, Cawthray GR, 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 173:181–190

    PubMed  CAS  Google Scholar 

  • Peix A, Rivas-Boyero AA, Mateos PF, Rodriguez-Barrueco C, Martínez-Molina E, Velazquez E (2001) Growth promotion of chickpea and barley by a phosphate solubiliizing strain of Mesorhizobium mediterraneum under growth chamber conditions. Soil Biol Biochem 33:103–110

    CAS  Google Scholar 

  • Perry RP (2007) Balanced production of ribosomal proteins. Gene 401:1–3

    PubMed  CAS  Google Scholar 

  • Peterson RL, Farquhar ML (1996) Root hairs: specialized tubular cells extending root surfaces. Botanical Rev 62:1–40

    Google Scholar 

  • Pinkerton A, Smith FW, Lewis DC (1997) Pasture species. In: Reuter DJ, Robinson JB (eds) Plant analysis: An interpretation manual. CSIRO Publishing, Collingwood, pp 287–346

    Google Scholar 

  • Polglase PJ, Attiwill PM, Adams MA (1992) Nitrogen and phosphorus cycling in relation to standage of Eucalyptus regans F.Muell. 3. Labile inorganic and organic P, phosphatase-activity and P-availability. Plant Soil 142:177–185

    CAS  Google Scholar 

  • Postma JA, Lynch JP (2011) Theoretical evidence for the functional benefit of root cortical aerenchyma in soils with low phosphorus availability. Ann Bot 107:829–841

    Google Scholar 

  • Raboy V (2003) myo-Inositol-1,2,3,4,5,6-hexakisphosphate. Phytochem 64:1033–1043

    CAS  Google Scholar 

  • Raboy V (2009) Approaches and challenges to engineering seed phytate and total phosphorus. Plant Sci 177:281–296

    CAS  Google Scholar 

  • Rao IM, Terry N (1989) Leaf phosphate status, photosynthesis, and carbon partitioning in sugar beet: I. Changes in growth, gas exchange, and Calvin cycle enzymes. Plant Physiol 90:814–819

    PubMed  CAS  Google Scholar 

  • Rasmussen SK, Ingvardsen CR, Torp AM (2010) Mutations in genes controlling the biosynthesis and accumulation of inositol phosphates in seeds. Biochem Soc Trans 38:689–694

    PubMed  CAS  Google Scholar 

  • Ray JD, Kindiger B, Sinclair TR (1999) Introgressing root aerenchyma into maize. Maydica 44:113–117

    Google Scholar 

  • Reddell P, Yun Y, Shipton WA (1997) Cluster roots and mycorrhizae in Casuarina cunninghamiana: Their occurrence and formation in relation to phosphorus supply. Aust J Bot 45:41–51

    Google Scholar 

  • Relwani L, Krishna P, Reddy MS (2008) Effect of carbon and nitrogen sources on phosphate solubilisation by a wild-type strain and UV-induced mutants of Aspergillus tubigensis. Curr Microbiol 57:401–406

    PubMed  CAS  Google Scholar 

  • Rice WA, Lupwayi NZ, Olsen PE, Schlechte D, Gleddie SC (2000) Field evaluation of dual inoculation of alfalfa with Sinorhizobium meliloti and Penicillium bilaii. Can J Plant Sci 80:303–308

    Google Scholar 

  • Richardson AE (1994) Soil microorganisms and phosphorus availablility. In: Pankhurst CE, Doube BM, Gupta VVSR, Grace PR (eds) Management of the soil biota in sustainable farming systems. CSIRO Publishing, Collingwood, pp 50–62

    Google Scholar 

  • Richardson AE, Hadobas PA (1997) Soil isolates of Pseudomonas spp. that utilise inositol phosphates. Can J Microbiol 43:509–516

    PubMed  CAS  Google Scholar 

  • Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability. Plant Physiol 156:989–996

    PubMed  CAS  Google Scholar 

  • Richardson AE, Hadobas PA, Hayes JE (2001a) Extracellular secretion of Aspergillus phytase from Arabidopsis roots enables plants to obtain phosphorus from phytate. Plant J 25:641–649

    PubMed  CAS  Google Scholar 

  • 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 229:47–56

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Richardson AE, George TS, Jackobsen I, Simpson RJ (2007) Plant access to inositol phosphates in soil. In: Turner BL, Richardson AE, Mullaney EJ (eds) Inositol phosphates: Linking agriculture and the environment. CABI Publishing, Wallingford, pp 242–260

    Google Scholar 

  • Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009a) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339

    CAS  Google Scholar 

  • Richardson AE, Hocking PJ, Simpson RJ, George TS (2009b) Plant mechanisms to optimise access to soil phosphorus. Crop Pasture Sci 60:124–143

    CAS  Google Scholar 

  • Robinson D (2005) Integrated root responses to variations in nutrient supply. In: BassiriRad H (ed) Nutrient acquisition by plants: an ecological perspective. Springer, Berlin, pp 43–62

    Google Scholar 

  • Robson AD, Abbott LK, Malajczuk N (1994) Management of mycorrhizas in agriculture, horticulture and forestry. Developments in Plant and Soil Sciences, Vol. 56. Kluwer Academic Publishers

  • Rodríguez H, Fraga R, Gonzalez T, Bashan Y (2006) Genetics of phosphate solubilisation and its potential applications for improving plant growth-promoting bacteria. Plant Soil 287:15–21

    Google Scholar 

  • Roelofs RFR, Rengel Z, Cawthray GR, Dixon KW, Lambers H (2001) Exudation of carboxylates in Australian Proteaceae: chemical composition. Plant Cell Environ 24:891–903

    CAS  Google Scholar 

  • Rose TJ, Rengel Z, Qn M, Bowden JW (2007) Differential accumulation patterns of phosphorus and potassium by canola cultivars compared to wheat. Z Pflanz Bodenkunde 170:404–411

    CAS  Google Scholar 

  • Rose TJ, Pariasca-Tanaka J, Rose MT, Fukuta Y, Wissuwa M (2010) Genotypic variation in grain phosphorus concentration, and opportunities to improve P-use efficiency in rice. Field Crops Res 119:154–160

    Google Scholar 

  • Rubio G, Walk T, Ge ZY, Yan XL, Liao H, Lynch JP (2001) Root gravitropism and below-ground competition among neighbouring plants: A modelling approach. Ann Bot 88:929–940

    Google Scholar 

  • 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

    Google Scholar 

  • Ryan MH, Angus JF (2003) Arbuscular mycorrhizae in wheat and field pea crops on a low P soil: increased Zn-uptake but no increase in P-uptake or yield. Plant Soil 250:225–239

    CAS  Google Scholar 

  • Ryan MH, Graham JH (2002) Is there a role for arbuscular mycorrhizal fungi in production agriculture? Plant Soil 244:263–271

    CAS  Google Scholar 

  • Ryan PR, Delhaize E (2010) The convergent evolution of aluminium resistance in plants exploits a convenient currency. Func Plant Biol 37:275–284

    CAS  Google Scholar 

  • Ryan MH, Small DR, Ash JE (2000) Phosphorus controls the level of colonisation by arbuscular mycorrhizal fungi in conventional and biodynamic irrigated dairy pastures. Aust J Exp Agric 40:663–670

    Google Scholar 

  • Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Ann Rev Plant Physiol Plant Molec Biol 52:527–560

    CAS  Google Scholar 

  • Ryan PR, Delhaize E, Randall PJ (1995) Characterisation of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196:103–111

    CAS  Google Scholar 

  • Ryan MH, McInerney JK, Record IR, Angus JF (2008) Zinc bioavailability in wheat grain in relation to phosphorus fertiliser, crop sequence and mycorrhizal fungi. J Sci Food Agric 88:1208–1216

    CAS  Google Scholar 

  • Ryan MH, van Herwaarden AF, Angus JF, Kirkegaard JA (2005) Reduced growth of autumn-sown wheat in a low-P soil is associated with high colonisation by arbuscular mycorrhizal fungi. Plant Soil 270:275–286

    CAS  Google Scholar 

  • Sampson RA, Seifert KA, Kuijpers AFA, Houbraken JAMP, Frisvad JC (2004) Phylogenetic analyses of Penicillium subgenus Penicillium, using partial using partial β-tubulin sequences. Stud Mycol 49:175–200

    Google Scholar 

  • Sánchez PA (2010) Tripling crop yields in tropical Africa. Nature Geosci 3:299–300

    Google Scholar 

  • Santonoceto C, Hocking PJ, Braschkat J, Randall PJ (2002) Mineral nutrient uptake and removal by canola, Indian mustard, and Linola in two contrasting environments, and implications for carbon cycle effects on soil acidification. Aust J Agric Res 53:459–470

    CAS  Google Scholar 

  • Sas L, Rengel Z, Tang C (2001) Excess cation uptake, and extrusion of protons and organic acid anions by Lupinus albus under phosphorus deficiency. Plant Sci 160:1191–1198

    PubMed  CAS  Google Scholar 

  • Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Delhaize E, Matsumoto H (2004) A wheat gene encoding an aluminum-activated malate transporter. Plant J 37:645–653

    PubMed  CAS  Google Scholar 

  • Sasaki T, Mori IC, Furuichi T, Munemasa S, Toyooka K, Matsuoka K, Murata Y, Yamamoto Y (2010) Closing plant stomata requires a homolog of an Aluminum-activated malate transporter. Plant Cell Physiol 51:354–365

    PubMed  CAS  Google Scholar 

  • Savard ME, Miller JD, Blais LA, Seifert KA, Sampson RA (1994) Secondary metabolites of Penicillium bilaii strain PB-50. Mycopathologica 127:19–27

    CAS  Google Scholar 

  • Schweiger PF, Jakobsen I (1999) Direct measurement of arbuscular mycorrhizal phosphorus uptake into field-grown winter wheat. Agron J 91:998–1002

    Google Scholar 

  • Schweiger PF, Robson AD, Barrow NJ (1995) Root hair length determines beneficial effect of a Glomus species on shoot growth of some pasture species. New Phvtol 131:247–254

    Google Scholar 

  • Seifert KA, Sampson RA, de Waard JR, Houbraken J, Levesque AC, Moncalvo J-M, Louis-Selze G, Hebet PDM (2007) Prospects for fungus identification using CO1 DNA barcodes, with Penicillium as a test case. Proc Nat Acad Sci USA 104:3901–3906

    PubMed  CAS  Google Scholar 

  • Sekiya N, Yano K (2010) Seed P-enrichment as an effective P supply to wheat. Plant Soil 327:347–354

    CAS  Google Scholar 

  • Setter TL, Waters I (2003) Review of prospects for germplasm improvement for waterlogging tolerance in wheat, barley and oats. Plant Soil 253:1–34

    CAS  Google Scholar 

  • Shane MW, Lambers H (2005) Cluster roots: A curiosity in context. Plant Soil 274:101–125

    CAS  Google Scholar 

  • Shane MW, De Vos M, De Roock S, Cawthray GR, Lambers H (2003a) Effect of external phosphorus supply on internal phosphorus concentration and the initiation, growth and exudation of cluster roots in Hakea prostrata R.Br. Plant Soil 248:209–219

    CAS  Google Scholar 

  • Shane MW, De Vos M, De Roock S, Lambers H (2003b) 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

    CAS  Google Scholar 

  • Shane MW, Dixon KW, Lambers H (2005) The occurrence of dauciform roots amongst Western Australian reeds, rushes and sedges, and the impact of phosphorus supply on dauciform-root development in Schoenus unispiculatus (Cyperaceae). New Phytol 165:887–898

    PubMed  CAS  Google Scholar 

  • Shane MW, Cawthray GR, Cramer MD, Kuo J, Lambers H (2006) Specialized ‘dauciform’ roots of Cyperaceae are structurally distinct, but functionally analogous with ‘cluster’ roots. Plant Cell Environ 29:1989–1999

    PubMed  CAS  Google Scholar 

  • Shang C, Stewart JWB, Huang PM (1992) pH effect on kinetics of adsorption of organic and inorganic phophates by short-range ordered aluminium and iron precipitates. Geoderma 53:1–14

    CAS  Google Scholar 

  • Shu LZ, Shen JB, Rengel Z, Tang CX, Zhang FS (2007a) Cluster root formation by Lupinus albus is modified by stratified application of phosphorus in a split-root system. J Plant Nutr 30:1–3

    Google Scholar 

  • Shu LZ, Shen JB, Rengel Z, Tang CX, Zhang FS, Cawthray GR (2007b) Formation of cluster roots and citrate exudation by Lupinus albus in response to localized application of different phosphorus sources. Plant Sci 172:1017–1024

    CAS  Google Scholar 

  • Silberbush M, Barber SA (1983) Sensitivity of simulated phosphorus uptake to parameters used by a mechanistic-mathematical model. Plant Soil 74:93–100

    CAS  Google Scholar 

  • Simpson RJ, Oberson A, Culvenor RA, Ryan MH, Veneklaas EJ, Lambers H, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Richardson AE (2011) Strategies and agronomic interventions to improve the phosphorus-use efficiency of farming systems. Plant Soil (Special Issue S43—Phosphorus. doi:10.1007/s11104-011-0880-1)

  • Singh SP, Urrea CA, Gutiérrez JA, Garcia J (1989) Selection for yield at two fertilizer levels in small-seeded common bean. Can J Plant Sci 69:1011–1017

    Google Scholar 

  • Skene KR (1998) Cluster roots: some ecological considerations. J Ecol 86:1062–1066

    Google Scholar 

  • Smernik RJ, Dougherty WJ (2007) Identification of phytate in phosphorus-31 nuclear magnetic resonance spectra: The need for spiking. Soil Sci Soc Am J 71:1045–1050

    CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal Symbiosis. Academic, London

    Google Scholar 

  • Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Ann Rev Plant Biol 62:227–250

    CAS  Google Scholar 

  • Smith SE, Jakobsen I, Grønlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: Interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–1057

    PubMed  CAS  Google Scholar 

  • Ström L, Owen AG, Godbold DL, Jones DL (2002) Organic acid mediated mobilization in the rhizosphere and uptake by maize. Soil Biol Biochem 34:703–710

    Google Scholar 

  • Syers JK, Johnston AE, Curtin D (2008). Efficiency of soil and fertilizer phosphorus use—reconciling changing concepts of soil phosphorus behaviour with agronomic information. FAO Fertilizer and Plant Nutrition Bulletin 18. FAO, United Nations, Rome

  • Tadano T, Ozawa K, Sakai H, Osaki M, Matsui H (1993) Secretion of acid phosphatase be 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

    Google Scholar 

  • Takeda M, Knight JD (2006) Enhanced solubilisation of rock phosphate by Penicillium bilaiae in pH-buffered solution culture. Can J Microbiol 52:1121–1129

    PubMed  CAS  Google Scholar 

  • Tang J, Leung A, Leung C, Lim BL (2006) Hydrolyis of precipiatated phytate by three distinct families of phytases. Soil Biol Biochem 38:1316–1324

    CAS  Google Scholar 

  • 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 Fert Soils 5:308–312

    CAS  Google Scholar 

  • Tarafdar JC, Jungk A (1987) Phosphatase activity in the rhizosphere and its relation to the depletion of soil organic phosphorus. Biol Fert Soils 3:199–204

    CAS  Google Scholar 

  • Taurian T, Anzuay MS, Angelini JG, Tonelli ML, Luduena L, Pena D, Ibanez F, Fabra A (2010) Phosphate-solubilizing peanut associated bacteria: screening for plant growth-promoting activities. Plant Soil 329:421–431

    CAS  Google Scholar 

  • 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 aluminium. Plant Physiol 127:1836–1844

    PubMed  CAS  Google Scholar 

  • Thompson JP (1987) Decline of vesicular-arbuscular mycorrhizae in long fallow disorder of field crops and its expression in phosphorus deficiency of sunflower. Aust J Agric Res 38:847–867

    CAS  Google Scholar 

  • Thompson JP (1991) Improving the mycorrhizal condition of the soil through cultural practices and effects on growth and phosphorus uptake in plants. In: Johansen C, Lee KK, Sahrawat KL (eds) Phosphorus nutrition of grain legumes in the semi-arid tropics. ICRISAT, Hyderabad, Andra Pradesh, pp 117–137

  • Thomson CJ, Bolger TP (1993) Effects of seed phosphorus concentration on the emergence and growth of subterranean clover (Trifolium subterraneum). Plant Soil 155(156):285–288

    Google Scholar 

  • Thomson BD, Robson AD, Abbott LK (1986) Effects of phosphorus on the formation of mycorrhizas by Gigaspora calospora and Glomus fasciculatum in relation to root carbohydrates. New Phytol 103:751–765

    Google Scholar 

  • Trachsel S, Kaeppler SM, Brown KM, Lynch JP (2011) Shovelomics: high throughput phenotyping of maize (Zea mays L.) root architecture in the field. Plant Soil 341:75–87

    Google Scholar 

  • Turner BL (2007) Inositol phosphates in soil: amounts, forms and significance of the phosphorylated inositol stereoismoers. In: Turner BL, Richardson AE, Mullaney EJ (eds) Inositol phosphates: Linking agriculture and the environment. CABI Publishing, Wallingford, pp 186–206

    Google Scholar 

  • Turner BL, Papházy MJ, Haygarth PM, McKelvie ID (2002) Inositol phosphates in the environment. Philos T Roy Soc B 357:449–469

    CAS  Google Scholar 

  • Tye AJ, Siu KY, Leung YC, Lim BL (2002) Molecular cloning and the biochemical characterisation of two novel phytases from B. subtilis 168 and B. licheniformis. Appl Microbiol Biotechnol 59:190–197

    PubMed  CAS  Google Scholar 

  • Unno Y, Okubo K, Wasaki J, Shinano T, Osaki M (2005) Plant growth promotion abilities and microscale bacterial dynamics in the rhizosphere of Lupin analysed by phytate utilization ability. Environ Microbiol 7:396–404

    PubMed  Google Scholar 

  • Van den Berg MA, Albang R, Albermann K, Badger JH, Daran JM, Driessen AJ, Garcia-Estrada C, Fedorova ND, Harris DM, Heijne WH, Joardar V, Kiel JA, Kovalchuk A, Martin JF, Nierman WC, Nijland JG, Pronk JT, Roubos JA, van der Klei IJ, van Peij NN, Veenhuis M, von Dohren H, Wagner C, Wortman J, Bovenberg RA (2008) Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nature Biotech 26:1161–1168

    CAS  Google Scholar 

  • Van Kauwenbergh SJ (2010) World phosphate rock reserves and resources. International Fertilizer Development Center, Muscle Shoals

    Google Scholar 

  • Van Veen JA, Leonard S, van Overbeek LS, Van Elsas JD (1997) Fate and activity of micro-organisms introduced into soil. Microbiol Mol Biol Rev 61:121–135

    PubMed  Google Scholar 

  • Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a non-renewable resource. New Phytol 157:423–447

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Vessey JK, Heisinger KG (2001) Effect of Penicillium bilaii inoculation and phosphorus fertilisation on root and shoot parameters of field-grown pea. Can J Plant Sci 81:361–366

    Google Scholar 

  • Vesterager JM, Nielsen NE, Høgh-Jensen H (2006) Variation in phosphorus uptake and use efficiencies between pigeonpea genotypes and cowpea. J Plant Nutr 29:1869–1888

    CAS  Google Scholar 

  • Wakelin SA, Warren RA, Harvey PR, Ryder MH (2004) Phosphate solubilization by Penicillium spp. closely associated with wheat roots. Biol Fert Soils 40:36–43

    CAS  Google Scholar 

  • Wakelin SA, Gupta VVSR, Harvey PR, Ryder MH (2007) The effect of Penicillium fungi on plant growth and P mobilisation in neutral to alkaline soils from southern Australia. Can J Microbiol 53:106–115

    PubMed  CAS  Google Scholar 

  • Walk TC, Jaramillo R, Lynch JP (2006) Architectural tradeoffs between adventitious and basal roots for phosphorus acquisition. Plant Soil 279:347–366

    CAS  Google Scholar 

  • Wang LD, Liao H, Yan XL, Zhuang BC, Dong YS (2004) Genetic variability for root hair traits as related to phosphorus status in soybean. Plant Soil 261:77–84

    CAS  Google Scholar 

  • Wang X, Wang Y, Tian J, Lim BL, Yan X, Liao H (2009) Overexpressing AtPAP15 enhances phosphorus efficiency in soybean. Plant Physiol 151:233–240

    PubMed  CAS  Google Scholar 

  • Warner JR, Vilardell J, Sohn JH (2001) Economics of ribosome biosynthesis. Cold Spring Harbor Symposia on Quantitative Biology 66:567–574

    PubMed  CAS  Google Scholar 

  • Wasaki J, Maruyama H, Tanaka M, Yamamura T, Dateki H, Shinano T, Ito S, Osaki M (2009) Overexpression of the LaSAP2 gene for secretory acid phosphatase in white lupin improves the phosphorus uptake and growth of tobacco plants. Soil Sci Plant Nutr 55:107–113

    CAS  Google Scholar 

  • Watt RG, Dykes J, Sheiham A (2001) Socio-economic determinants of selected dietary indicators in British pre-school children. Public Health Nutr 4:1229–1233

    PubMed  CAS  Google Scholar 

  • Weaver DM, Wong MTF (2011) Phosphorus balance efficiency and P status in crop and pasture soils with contrasting P buffer indices: scope for improvement. Plant Soil (Special Issue S43—Phosphorus; submitted)

  • Wei LL, Chen CR, Xu ZH (2010) Citric acid enhances the mobilization of organic phosphorus in subtropical and tropical forest soils. Biol Fert Soils 46:765–769

    CAS  Google Scholar 

  • Weisskopf L, Abou-Mansour E, Fromin N, Tomasi N, Santelia D, Edelkott I, Neumann G, Aragno M, Tabacchi R, Martinoia E (2006) White lupin has developed a complex strategy to limit microbial degradation of exuded citrate required for phosphate acquisition. Plant Cell Environ 29:919–927, wheat under drought conditions in South Australia. Aust J Exp Agric 39:721–732

    PubMed  CAS  Google Scholar 

  • Wherrett T, Ryan PR, Delhaize E, Shabala S (2005) Effect of aluminium on membrane potential and ion fluxes at the apices of wheat roots. Func Plant Biol 32:199–208

    CAS  Google Scholar 

  • Whitelaw MA (2000) Growth promotion of plants inoculated with phosphate-solubilizing fungi. Adv Agron 69:99–151

    CAS  Google Scholar 

  • Whitelaw MA, Harden TJ, Bender GL (1997) Plant growth promotion of wheat inoculated with Penicillium radicum sp. nov. Aust J Soil Res 35:291–300

    Google Scholar 

  • Whitelaw MA, Harden TJ, Helyar KR (1999) Phosphate solubilisation in solution culture by the soil fungus Penicillium radicum. Soil Biol Biochem 31:655–665

    CAS  Google Scholar 

  • World Bank (2004) World development indicators. The World Bank, Washington

    Google Scholar 

  • Wouterlood M, Lambers H, Veneklaas EJ (2005) Plant phosphorus status has a limited influence on the concentration of phosphorus-mobilising carboxylates in the rhizosphere of chickpea. Func Plant Biol 32:153–159

    CAS  Google Scholar 

  • Xu JP (2006) Microbial ecology in the age of genomics and metagenomics: concepts, tools and recent advances. Mol Ecol 15:1713–1731

    PubMed  CAS  Google Scholar 

  • Yadav RS, Tarafdar JC (2003) Phytase and phosphatase producing fungi in arid and semi-arid soils and their efficiency in hydrolyzing different organic P compounds. Soil Biol Biochem 35:745–751

    CAS  Google Scholar 

  • Yan F, Zhu YY, Müller C, Zörb C, Schubert S (2002) Adaptation of H+-pumping and plasma membrane H+ ATPase activity in proteoid roots of white lupin under phosphorus deficiency. Plant Physiol 129:50–63

    PubMed  CAS  Google Scholar 

  • Yan XL, Liao H, Beebe SE, Blair MW, Lynch JM (2004) QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant Soil 265:17–29

    CAS  Google Scholar 

  • Yao Q, Li XL, Feng G, Christie P (2001) Mobilization of sparingly soluble inorganic phosphates by the external mycelium of an abuscular mycorrhizal fungus. Plant Soil 230:279–285

    CAS  Google Scholar 

  • Yokosho K, Yamaji N, Ueno D, Mitani N, Ma JF (2009) OsFRDL1 Is a citrate transporter required for efficient translocation of iron in rice. Plant Physiol 149:297–305

    PubMed  CAS  Google Scholar 

  • Yuen K-Y, Pascal G, Wong SSY, Glaser P, Woo PCY, Kunst F, Cai JJ, Cheung EYL, Médigue C, Danchin A (2003) Exploring the Penicillium marneffei genome. Arch Microbiol 179:339–353

    PubMed  CAS  Google Scholar 

  • Zhu JM, Lynch JP (2004) The contribution of lateral rooting to phosphorus acquisition efficiency in maize (Zea mays L.) seedlings. Func Plant Biol 31:949–958

    CAS  Google Scholar 

  • Zhu JM, Kaeppler SM, Lynch JP (2005a) Topsoil foraging and phosphorus acquisition efficiency in maize (Zea mays L.). Func Plant Biol 32:749–762

    CAS  Google Scholar 

  • Zhu JM, Kaeppler SM, Lynch JP (2005b) Mapping of QTL for lateral root branching and length in maize (Zea mays L.) under differential phosphorus supply. Theor Appl Genet 111:688–695

    PubMed  CAS  Google Scholar 

  • Zhu JM, Kaeppler SM, Lynch JP (2005c) Mapping of QTL controlling root hair length in maize (Zea mays L.) under phosphorus deficiency. Plant Soil 270:299–310

    CAS  Google Scholar 

  • Zhu YY, Yan F, Zörb C, Schubert S (2005d) A link between citrate and proton release by proteoid roots of white lupin (Lupinus albus L.) grown under phosphorus-deficient conditions. Plant Cell Physiol 46:892–901

    PubMed  CAS  Google Scholar 

  • Zhu JM, Zhang CC, Lynch JP (2010a) The utility of phenotypic plasticity for root hair length for phosphorus acquisition. Func Plant Biol 37:313–322

    Google Scholar 

  • Zhu JM, Brown KM, Lynch JP (2010b) Root cortical aerenchyma improves the drought tolerance of maize (Zea mays L.). Plant Cell Environ 33:740–749

    Google Scholar 

  • Zinn KE, Liu J, Allan DL, Vance CP (2009) White lupin (Lupinus albus) response to phosphorus stress: evidence for complex regulation of LaSAP1. Plant Soil 322:1–15

    CAS  Google Scholar 

  • Zubaidi A, McDonald GK, Hollamby GJ (1999) Nutrient uptake and distribution by bread and durum wheat under drought conditions in South Australia. Aust J Exp Agric 39:721–732

    CAS  Google Scholar 

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Acknowledgements

The authors thank Mark Conyers, Peter Cornish, Keith Helyar and Peter Randall for critical discussion of the ideas expressed in this paper. FAS and SES wish to acknowledge the Australian Research Council, the South Australian Grain Industry Trust and the Waite Research Institute for research support and AO thanks Else Bünemann and Emmanuel Frossard for stimulating discussions. Preparation of the review was funded in part by Meat and Livestock Australia Ltd and CSIRO’s National Research Flagships Program’s Flagship Collaboration Fund which aims to enhance collaboration between CSIRO’s Flagships, Australian universities and other publicly-funded research agencies.

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  1. CSIRO Sustainable Agriculture National Research Flagship/CSIRO Plant Industry, GPO Box 1600, Canberra, ACT, 2601, Australia

    Alan E. Richardson, Richard A. Culvenor & Richard J. Simpson

  2. Department of Horticulture, The Pennsylvania State University, University Park, PA, 16802, USA

    Jonathan P. Lynch

  3. CSIRO Plant Industry, GPO Box 1600, Canberra, ACT, 2601, Australia

    Peter R. Ryan & Emmanuel Delhaize

  4. Soils Group, School of Agriculture, Food and Wine, The University of Adelaide, Waite Campus DX 650 636, Adelaide, 5005, Australia

    F. Andrew Smith & Sally E. Smith

  5. CSIRO Sustainable Agriculture National Research Flagship/CSIRO Ecosystem Sciences, PMB 2, Glen Osmond, SA, 5064, Australia

    Paul R. Harvey

  6. School of Plant Biology, Faculty of Natural and Agricultural Sciences, and Institute of Agriculture, The University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

    Alan E. Richardson, Megan H. Ryan, Erik J. Veneklaas, Hans Lambers & Richard J. Simpson

  7. Group of Plant Nutrition, Research Station Eschikon, ETH Zurich, Institute of Agricultural Sciences, Lindau, Switzerland

    Astrid Oberson

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Richardson, A.E., Lynch, J.P., Ryan, P.R. et al. Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349, 121–156 (2011). https://doi.org/10.1007/s11104-011-0950-4

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