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Phosphorus mobilization in agroforestry: Organic anions, phosphatase activity and phosphorus fractions in the rhizosphere

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Abstract

In agroforestry systems on Ferralsols in the tropics, maize crop yields are low owing to a lack of P. However, some agroforestry tree species adapted to P-fixing soils may be able to utilize less available P sources and concurrently increase P availability to adjacent crops. Adaptations for enhanced P acquisition from P-fixing soils include exudation of low molecular weight (LMW) organic anions (OA) and phosphatase enzymes. We identified major organic anions, and measured acid phosphatase activity and P fractions in the rhizosphere soil of maize (Zea mays L.), as well as in the perennial species Grevillea robusta A. Cunn., Cassia spectabilis DC. (syn. Senna spectabilis (DC.) H.S. Irwin and R.C. Barneby), Tithonia diversifolia (Hemsl.) A. Gray, Eucalyptus grandis W. Hill ex Maiden and Cedrella serrata Royle. Maize and trees were grown simultaneously at field sites and in large pots. Rhizosphere soil of C. spectabilis contained at least 29 μmol oxalate g−1 soil, derived from a high exudation rate in the range of at least 5–10 μmol oxalate m−1 root day−1. Incubation of Ferralsols with much lower concentrations of citrate increased labile P fractions, but there was no clear relation between OA concentration and an increase in labile P fractions in rhizosphere soils, where P mobilization and P uptake occur at the same time. Acid phosphatase activity in rhizosphere soil of all species was two to five times greater in rhizosphere soil compared with bulk soil, and correlated in rhizosphere soil of G. robusta with a shift from organic P to inorganic P in soil P fractions. We conclude that organic anion exudation and acid phosphatase activity of tree roots may increase mobilization of P in the rhizosphere, the extent of which depends on the species, the organic anion and pH. However, it is unlikely that the extent of P mobilization will benefit adjacent crop plants unless crop roots exert insufficient P-mobilization effects themselves, and grow in the rhizosphere of tree roots.

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References

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

    Google Scholar 

  • Anderson J M and Ingram J S 1989 Tropical Soil Biology and Fertility: A Handbook of Methods. CAB International, Wallingford. 171 pp.

    Google Scholar 

  • Barber S A 1971 Influence of the plant root on ion movement in soil. In The Plant Root and its Environment. Ed. E W Carson. pp. 525–563. University Press of Virginia, Charlottesville.

    Google Scholar 

  • Baziramakenga R, Simard R R and Leroux G D 1995 Determination of organic acids in soil extracts by ion chromatography. Soil Biol. Biochem. 27, 349–356.

    Google Scholar 

  • Boero G and Thien S 1979 Phosphatase Activity and Phosphorus Availability in the Rhizosphere of Corn Roots. In The Soil Root Interface. Eds. J L Harley and R Scott Russell. pp. 231–242. Academic Press, London.

    Google Scholar 

  • Bolan N S, Naidu R, Mahimairaja S and Baskaran S 1994 Influence of low-molecular-weight organic acids on the solubilization of phosphates. Biol. Fert. Soils 18, 311–319.

    Google Scholar 

  • Bowen G D and Rovira A D 1999 The rhizosphere and its management to improve plant growth. Adv. Agron. 66, 1–102.

    Google Scholar 

  • Chapin F S III 1980 The mineral nutrition of wild plants. Ann. Rev. Ecol. Syst. 11, 233–260.

    Google Scholar 

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

    Google Scholar 

  • Eivazi F and Tabatabai M A 1977 Phosphatases in soils. Soil Biol. Biochem. 9, 167–172.

    Google Scholar 

  • Filius J, Hiemstra T and van Riemsdijk W 1997 Adsorption of small weak organic acids on goethite: Modeling of mechanisms. J. Colloid Interface Sci. 195, 368–380.

    Google Scholar 

  • Findenegg G R and J A Nelemans 1993 The effect of phytase on the availability of P from myo-inositol hexaphosphate (phytate) for maize roots. Plant Soil 154, 189–196.

    Google Scholar 

  • Fox T R and N B Comerford 1990 Low-molecular-weight organic acids in selected forest soils of the Southeastern USA. Soil Sci. Soc. Am. J. 54, 1139–1144.

    Google Scholar 

  • Fox T R and N B Comerford 1992 Influence of Oxalate loading on phosphorus and aluminum solubility in spodosols. Soil Sci. Soc. Am. J. 56, 290–294.

    Google Scholar 

  • Gardner W K, Barber D A and Parbery D G 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.

    Google Scholar 

  • Geelhoed J S, Hiemstra T and van Riemsdijk W H 1998 Competitive interaction between phosphate and citrate on goethite. Environ. Sci. Technol. 32, 2119–2123.

    Google Scholar 

  • Genstat 2000 Genstat for Windows, fifth edition. VSN International, Oxford.

    Google Scholar 

  • Gerke J 1995 Phosphate, Fe and Mn uptake of N2 fixing red clover and ryegrass from an Oxisol as affected by P and model humic substances application. 2. Phosphate and aluminium species distribution as modified by plant roots. Z. Pflanzenernähr. Bodenk. 158, 445–451.

    Google Scholar 

  • Gerke J, Römer W and Jungk A 1994 The excretion of citric and malic acid by proteoid roots of Lupinus albus L.: Effects on soil solution concentrations of phosphate, iron, and aluminium in the proteoid rhizosphere in samples of an oxisol and a luvisol. Z. Pflanzenernähr. Bodenk. 157, 289–294.

    Google Scholar 

  • Gilbert G A, Knight J D, Vance C P and Allan D L 1999 Acid phosphatase activity in phosphorus-deficient white lupin roots. Plant Cell Environ. 22, 801–810.

    Google Scholar 

  • Grierson P F and Adams M A 1999 Growth and nutrient cycling in native ecosystems of southern Australia: Application to the development of sustainable agriculture. Agroforest. Syst. 45, 215–244.

    Google Scholar 

  • Grierson P F and Attiwill P M 1989 Chemical characteristics of the proteoid root mat of Banksia integrifolia L.f.. Aust. J. Bot. 37, 137–143.

    Google Scholar 

  • Hendrix J E 1967 The effect of pH on the uptake and accumulation of phosphate and sulphate ions by bean plants. Am. J. Bot. 54, 560–564.

    Google Scholar 

  • Hiemstra T and van Riemsdijk W 1996 A surface structure approach to ion adsorption: The charge distribution (CD) model. J. Colloid Interface Sci. 179, 488–508.

    Google Scholar 

  • 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.

    Google Scholar 

  • Hoffland E, Findenegg G R and Nelemans J A 1989 Solubilization of rock phosphate by rape II. Local root exudation of organic acids as a response to P-starvation. Plant Soil 113, 161–165.

    Google Scholar 

  • Hue N V 1991 Effects of Organic Acids/Anions on P sorption and Phytoavailability in Soils with Different Mineralogies. Soil Sci. 152, 463–471.

    Google Scholar 

  • ISFEIP 1972 International Soil Fertility Evaluation and Improvement Program. Ann. Rep. North Carolina State Univ. Dept. of Soil Sci., Raleigh, USA.

    Google Scholar 

  • Jama B, Palm C A, Buresh R J, Niang A, Gachengo C, Nziguheba G and Amadalo B 2000 Tithonia diversifolia as a green manure for soil fertility improvement in Western Kenya: A review. Agroforest. Syst. 49, 201–221.

    Google Scholar 

  • Jones D L and Darrah P R 1995 Influx and efflux of organic acids across the soil-root interface of Zea mays L. and its implications in rhizosphere C flow. Plant Soil 173, 103–109.

    Google Scholar 

  • Kpomblekou-a K and Tabatabai M A 1994 Effect of organic acids on release of phosphorus from phosphate rocks. Soil Sci. 158, 442–453.

    Google Scholar 

  • Kuo S 1996 Phosphorus. In Methods of Soil Analysis Part 3 — Chemical Methods. Ed. D L Sparks. pp. 869–919. Soil Science Society of America, Madison.

    Google Scholar 

  • Marschner H, Römheld V and Cakmak I 1987 Root-induced changes of nutrient availability in the rhizosphere. J. Plant Nutr. 10, 1175–1184.

    Google Scholar 

  • Mc Lachlan K D 1980 Acid phosphatase activity of intact roots and phosphorus nutrition of plants. I. Assay conditions and phosphatase activity. Aust. J. Agr. Res. 31, 429–440.

    Google Scholar 

  • Nagarajah S, Posner A M and Quirk J P 1970 Competitive adsorption of phosphate with polygalacturonate and other organic anions on kaolinite and oxide surfaces. Nature 228, 83–84.

    Google Scholar 

  • Palm C A 1995 Contribution of agroforestry trees to nutrient requirements of intercropped plants. Agroforest. Syst. 30, 105–124.

    Google Scholar 

  • Radersma S 2002 Tree effects on crop growth on a phosphorus-fixing Ferralsol. PhD Thesis, Wageningen University, Wageningen.

    Google Scholar 

  • Ridge E H and Rovira A D 1971 Phosphatase activity of intact young wheat roots under sterile and non-sterile conditions. New Phytol. 70, 1017–1026.

    Google Scholar 

  • Sanchez P A 1976 Properties and Management of Soils in the Tropics. John Wiley and Sons, New York. 618 pp.

    Google Scholar 

  • Shepherd K D, Swinkels R, Muturi W M, Ohlsson E and Ndufa J K 1992 Evaluation of hedgerow intercropping on farms in Western Kenya I. Diagnosis of technology potential and farmers interest. In AFRENA Report no. 50. pp. 1–29. ICRAF, Nairobi, Kenya.

    Google Scholar 

  • Tabatabai M A and Bremmer J M 1969 Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol. Biochem. 1, 301–307.

    Google Scholar 

  • Tadano T, Ozawa K, Sakai H, Osaki M and 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.

    Google Scholar 

  • Tarafdar J C and Chhonkar P K 1978 Status of phosphatases in the root-soil interface of leguminous and non-leguminous plants. Z. Pflanzenernähr. Bodenk. 141, 347–351.

    Google Scholar 

  • Tiessen H and J O Moir 1993 Characterization of available P by sequential extraction. In Soil sampling and Methods of Analysis. Ed. M R Carter. pp. 75–86. Boca Rato, Lewis.

    Google Scholar 

  • Van Noordwijk M and Ong C K 1999 Can the ecosystem mimic hypotheses be applied to farms in African savannahs? Agroforest. Syst. 45, 131–158.

    Google Scholar 

  • Van Noordwijk M, Radersma S and Lusiana B 1999 Modeling root architecture and phosphorus uptake in agroforestry. Agroforestry Forum 9, 28–30.

    Google Scholar 

  • Veneklaas E J, Stevens J, Cawthray G R, Turner S, Grigg A M and Lambers H 2003 Chickpea and white lupin rhizosphere carboxylates vary with soil properties and enhance phosphorus uptake. Plant Soil 248, 187–197.

    Google Scholar 

  • Violante A, Colombo C and Buondonno A 1991 Competitive adsorption of phosphate and oxalate by aluminum oxides. Soil Sci. Soc. Am. J. 55, 65–70.

    Google Scholar 

  • Whitehead D C, Dibb H and Hartley R D 1981 Extractant pH and the release of phenolic compounds from soils, plant roots and leaf litter. Soil Biol. Biochem. 13, 343–348.

    Google Scholar 

Download references

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Radersma, S., Grierson, P.F. Phosphorus mobilization in agroforestry: Organic anions, phosphatase activity and phosphorus fractions in the rhizosphere. Plant and Soil 259, 209–219 (2004). https://doi.org/10.1023/B:PLSO.0000020970.40167.40

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