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Elevated CO2 temporally enhances phosphorus immobilization in the rhizosphere of wheat and chickpea

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Abstract

Aims

The efficient management of phosphorus (P) in cropping systems remains a challenge due to climate change. We tested how plant species access P pools in soils of varying P status (Olsen-P 3.2–17.6 mg kg−1), under elevated atmosphere CO2 (eCO2).

Methods

Chickpea (Cicer arietinum L.) and wheat (Triticum aestivum L.) plants were grown in rhizo-boxes containing Vertosol or Calcarosol soil, with two contrasting P fertilizer histories for each soil, and exposed to ambient (380 ppm) or eCO2 (700 ppm) for 6 weeks.

Results

The NaHCO3-extractable inorganic P (Pi) in the rhizosphere was depleted by both wheat and chickpea in all soils, but was not significantly affected by CO2 treatment. However, NaHCO3-extractable organic P (Po) accumulated, especially under eCO2 in soils with high P status. The NaOH-extractable Po under eCO2 accumulated only in the Vertosol with high P status. Crop species did not exhibit different eCO2-triggered capabilities to access any P pool in either soil, though wheat depleted NaHCO3-Pi and NaOH-Pi in the rhizosphere more than chickpea. Elevated CO2 increased microbial biomass C in the rhizosphere by an average of 21 %. Moreover, the size in Po fractions correlated with microbial C but not with rhizosphere pH or phosphatase activity.

Conclusion

Elevated CO2 increased microbial biomass in the rhizosphere which in turn temporally immobilized P. This P immobilization was greater in soils with high than low P availability.

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References

  • Achat DL, Morel C, Bakker MR, Augusto L, Pellerin S, Gallet-Budynek A, Gonzalez M (2010) Assessing turnover of microbial biomass phosphorus: combination of an isotopic dilution method with a mass balance model. Soil Biol Biochem 42:2231–2240

    Article  CAS  Google Scholar 

  • Armstrong RD, Helyar KR (1992) Changes in soil phosphate fractions in the rhizosphere of semiarid pasture grasses. Aust J Soil Res 30:131–143

    Article  CAS  Google Scholar 

  • Attiwill PM, Adams MA (1993) Nutrient cycling in forests. New Phytol 124:561–582

    Article  CAS  Google Scholar 

  • Barrett DJ, Richardson AE, Gifford RM (1998) Elevated atmospheric CO2 concentrations increase wheat root phosphatase activity when growth is limited by phosphorus. Aust J Plant Physiol 25:87–93

    Article  CAS  Google Scholar 

  • BassiriRad H, Gutschick VP, Lussenhop J (2001) Root system adjustments: regulation of plant nutrient uptake and growth responses to elevated CO2. Oecologia 126:305–320

    Article  Google Scholar 

  • Beck MA, Sanchez PA (1994) Soil-phosphorus fraction dynamics during 18 years of cultivation on a Typic Paleudult. Soil Sci Soc Am J 58:1424–1431

    Article  CAS  Google Scholar 

  • Binkley D, Giardina C, Bashkin MA (2000) Soil phosphorus pools and supply under the influence of Eucalyptus saligna and nitrogen-fixing Albizia facaltaria. Forest Ecol Manag 128:241–247

    Article  Google Scholar 

  • Blagodatskaya E, Blagodatsky S, Dorodnikov M, Kuzyakov Y (2010) Elevated atmospheric CO2 increases microbial growth rates in soil: results of three CO2 enrichment experiments. Glob Change Biol 16:836–848

    Article  Google Scholar 

  • Butterly CR, Buenemann EK, McNeill AM, Baldock JA, Marschner P (2009) Carbon pulses but not phosphorus pulses are related to decreases in microbial biomass during repeated drying and rewetting of soils. Soil Biol Biochem 41:1406–1416

    Article  CAS  Google Scholar 

  • Campbell CD, Sage RF (2002) Interactions between atmospheric CO2 concentration and phosphorus nutrition on the formation of proteoid roots in white lupin (Lupinus albus L.). Plant Cell Environ 25:1051–1059

    Article  Google Scholar 

  • Conyers MK, Poile GJ, Oates AA, Waters D, Chan KY (2011) Comparison of three carbon determination methods on naturally occurring substrates and the implication for the quantification of ‘soil carbon’. Aust J Soil Res 49:27–33

    Article  CAS  Google Scholar 

  • Dai XY, Ping CL, Michaelson GJ (2002) Characterizing soil organic matter in Arctic tundra soils by different analytical approaches. Org Geochem 33:407–419

    Article  CAS  Google Scholar 

  • FAO-UNESCO (1976) Soil Map of the World, 1:5 000 000, vol X. UNESCO, Paris

    Google Scholar 

  • George TS, Gregory PJ, Wood M, Read D, Buresh RJ (2002) Phosphatase activity and organic acids in the rhizosphere of potential agroforestry species and maize. Soil Biol Biochem 34:1487–1494

    Article  CAS  Google Scholar 

  • Gerke J, Beissner L, Romer W (2000) The quantitative effect of chemical phosphate mobilization by carboxylate anions on P uptake by a single root. I. The basic concept and determination of soil parameters. J Plant Nutr Soil Sc 163:207–212

    Article  CAS  Google Scholar 

  • Grinsted MJ, Hedley MJ, White RE, Nye PH (1982) Plant-induced changes in the rhizosphere of rape (Brassica Napus Var. Emerald) seedlings I. pH change and the increase in P concentration in the soil solution. New Phytol 91:19–29

    Article  CAS  Google Scholar 

  • Guppy CN, Menzies NW, Moody PW, Compton BL, Blamey FPC (2000) A simplified, sequential, phosphorus fractionation method. Commun Soil Sci Plan 31:1981–1991

    Article  CAS  Google Scholar 

  • Heanes DL (1984) Determination of total organic-C in soils by an improved chromic-acid digestion and spectrophotometric procedure. Commun Soil Sci Plan 15:1191–1213

    Article  CAS  Google Scholar 

  • Hinsinger P, Betencourt E, Bernard L, Brauman A, Plassard C, Shen J, Tang X, Zhang F (2011) P for two, sharing a scarce resource: soil phosphorus acquisition in the rhizosphere of intercropped species. Plant Physiol 156:1078–1086

    Article  PubMed  CAS  Google Scholar 

  • Hodge A, Millard P (1998) Effect of elevated CO2 on carbon partitioning and exudate release from Plantago lanceolata seedlings. Physiol Plant 103:280–286

    Article  CAS  Google Scholar 

  • Hütsch BW, Augustin J, Merbach W (2002) Plant rhizodeposition—an important source for carbon turnover in soils. J Plant Nutr Soil Sc 165:397–407

    Article  Google Scholar 

  • Isbell RF (1996) The Australian soil classification. CSIRO Publishing, Melbourne

    Google Scholar 

  • Jin J, Tang C, Armstrong R, Sale P (2012) Phosphorus supply enhances the response of legumes to elevated CO2 (FACE) in a phosphorus-deficient Vertisol. Plant Soil 358:91–104. doi:10.1007/s11104-012-1270-z

    Article  CAS  Google Scholar 

  • Joergensen RG (1996) The fumigation-extraction method to estimate soil microbial biomass: calibration of the k(EC) value. Soil Biol Biochem 28:25–31

    Article  CAS  Google Scholar 

  • Johnson DW, Ball JT, Walker RF (1997) Effects of CO2 and nitrogen fertilization on vegetation and soil nutrient content in juvenile ponderosa pine. Plant Soil 190:29–40

    Article  CAS  Google Scholar 

  • Johnson DW, Hungate BA, Dijkstra P, Hymus G, Hinkle CR, Stiling P, Drake BG (2003) The effects of elevated CO2 on nutrient distribution in a fire-adapted scrub oak forest. Ecol Appl 13:1388–1399

    Article  Google Scholar 

  • Johnson DW, Cheng W, Joslin JD, Norby RJ, Edwards NT, Todd DE (2004) Effects of elevated CO2 on nutrient cycling in a sweetgum plantation. Biogeochem 69:379–403

    Article  CAS  Google Scholar 

  • Khan FN, Lukac M, Turner G, Godbold DL (2008) Elevated atmospheric CO2 changes phosphorus fractions in soils under a short rotation poplar plantation (EuroFACE). Soil Biol Biochem 40:1716–1723

    Article  CAS  Google Scholar 

  • Laby RJ, Kincaid MS, Kim DG, Gibson SI (2000) The Arabidopsis sugar-insensitive mutants sis4 and sis5 are defective in abscisic acid synthesis and response. Plant J 23:587–596

    Article  PubMed  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-London 98:693–713

    Article  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academic, London

    Google Scholar 

  • McBeath TM, Lombi E, McLaughlin MJ, Buenemann EK (2007) Pyrophosphate and orthophosphate addition to soils: sorption, cation concentrations, and dissolved organic carbon. Aust J Soil Res 45:237–245

    Article  CAS  Google Scholar 

  • Montealegre CM, van Kessel C, Russelle MP, Sadowsky MJ (2002) Changes in microbial activity and composition in a pasture ecosystem exposed to elevated atmospheric carbon dioxide. Plant Soil 243:197–207

    Article  CAS  Google Scholar 

  • Moorhead DL, Linkins AE (1997) Elevated CO2 alters belowground exoenzyme activities in tussock tundra. Plant Soil 189:321–329

    Article  CAS  Google Scholar 

  • Motomizu S, Wakimoto T, Toei K (1983) Spectrophotometric determination of phosphate in river waters with molybdite and malachite green. Analyst 108:361–367

    Article  CAS  Google Scholar 

  • Overdieck D (1986) Long-term effects of an increased CO2 concentration on terrestrial plants in model ecosystems. Morphology and reproduction of Trifolium repens L and Lolium perenne L. Int J Biometeorol 30:323–332

    Article  Google Scholar 

  • Paterson E, Hall JM, Rattray EAS, Griffiths BS, Ritz K, Killham K (1997) Effect of elevated CO2 on rhizosphere carbon flow and soil microbial processes. Glob Change Biol 3:363–377

    Article  Google Scholar 

  • Pearse SJ, Veneklaas EJ, Cawthray G, Bolland MDA, Lambers H (2006) Triticum aestivum shows a greater biomass response to a supply of aluminium phosphate than Lupinus albus, despite releasing fewer carboxylates into the rhizosphere. New Phytol 169:515–524

    Article  PubMed  CAS  Google Scholar 

  • Pheav S, Bell RW, White PF, Kirk GJD (2003) Fate of applied fertilizer phosphorus in a highly weathered sandy soil under lowland rice cropping, and its residual effect. Field Crops Res 81:1–16

    Article  Google Scholar 

  • Pitelka LF (1994) Ecosystem response to elevated CO2. Trends Ecol Evol 9:204–207

    Article  PubMed  CAS  Google Scholar 

  • Prior SA, Rogers HH, Runion GB, Mauney JR (1994) Effects of tree-air CO2 enrichment on cotton root growth. Agr Forest Meteorol 70:69–86

    Article  Google Scholar 

  • Rayment GE, Higginson FR (1992) Australian laboratory handbook of soil and water chemical methods. Inkata Press, Melbourne

    Google Scholar 

  • Rice CW, Garcia FO, Hampton CO, Owensby CE (1994) Soil microbial response in tall grass prairie to elevated CO2. Plant Soil 165:67–74

    Article  CAS  Google Scholar 

  • Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Aust J Plant Physiol 28:897–906

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Richardson AE, Lynch JP, Ryan PR, Delhaize E, Smith FA, Smith SE, Harvey PR, Ryan MH, Veneklaas EJ, Lambers H, Oberson A, Culvenor RA, Simpson RJ (2011) Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349:121–156

    Article  CAS  Google Scholar 

  • Roitsch T (1999) Source-sink regulation by sugar and stress. Curr Opin Plant Biol 2:198–206

    Article  PubMed  CAS  Google Scholar 

  • Schortemeyer M, Dijkstra P, Johnson DW, Drake BG (2000) Effects of elevated atmospheric CO2 concentration on C and N pools and rhizosphere processes in a Florida scrub oak community. Glob Change Biol 6:383–391

    Article  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 349:89–120

    Article  CAS  Google Scholar 

  • Skujins JJ, Braal L, McLaren AD (1962) Characterization of phosphatase in a terrestrial soil sterilized with an electron beam. Enzymologia 25:125–133

    CAS  Google Scholar 

  • Steel RG, Torrie JH (1980) Principles and procedures of statistics: A biometrical approach, 2nd edn. McGraw-Hill, New York

    Google Scholar 

  • Stöcklin J, Körner C (1999) Interactive effects of elevated CO2, P availability and legume presence on calcareous grassland: results of a glasshouse experiment. Funct Ecol 13:200–209

    Article  Google Scholar 

  • Swinnen J, van Veen JA, Merckx R (1994) 14C pulse-labelling of field-grown spring wheat, an evaluation of its use in rhizosphere carbon budget estimations. Soil Biol Biochem 26:161–170

    Article  Google Scholar 

  • Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307

    Article  CAS  Google Scholar 

  • Tang C, Robson AD, Dilworth MJ (1990) A split-root experiment shows that iron is required for nodule initiation in Lupinus angustifolius L. New Phytol 115:61–67

    Article  CAS  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass-C. Soil Biol Biochem 19:703–707

    Article  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

    Article  CAS  Google Scholar 

  • Vu DT, Tang C, Armstrong RD (2008) Changes and availability of P fractions following 65 years of P application to a calcareous soil in a Mediterranean climate. Plant Soil 304:21–33

    Article  CAS  Google Scholar 

  • Vu DT, Tang C, Armstrong RD (2009) Tillage system affects phosphorus form and depth distribution in three contrasting Victorian soils. Aust J Soil Res 47:33–45

    Article  CAS  Google Scholar 

  • Vu DT, Tang C, Armstrong RD (2010) Transformations and availability of phosphorus in three contrasting soil types from native and farming systems: a study using fractionation and isotopic labeling techniques. J Soils Sediments 10:18–29

    Article  CAS  Google Scholar 

  • Wang X, Lester DW, Guppy CN, Lockwood PV, Tang C (2007) Changes in phosphorus fractions at various soil depths following long-term P fertilizer application on a black vertosol from south-eastern Queensland. Aust J Soil Res 45:524–532

    Article  Google Scholar 

  • Wang X, Tang C, Guppy CN, Sale PWG (2010) Cotton, wheat and white lupin differ in phosphorus acquisition from sparingly soluble sources. Environ Exp Bot 69:267–272

    Article  CAS  Google Scholar 

  • Wang X, Guppy CN, Watson L, Sale PWG, Tang C (2011) Availability of sparingly soluble phosphorus sources to cotton (Gossypium hirsutum L.), wheat (Triticum aestivum L.) and white lupin (Lupinus albus L.) with different forms of nitrogen as evaluated by a 32P isotopic dilution technique. Plant Soil 348:85–98

    Article  CAS  Google Scholar 

  • Watt M, Evans JR (1999) Linking development and determinacy with organic acid efflux from proteoid roots of white lupin grown with low phosphorus and ambient or elevated atmospheric CO2 concentration. Plant Physiol 120:705–716

    Article  PubMed  CAS  Google Scholar 

  • White ME (1986) The greening of Gondwana. The 400 million year story of Australian plants. Reed Books, Frenchs Forest

    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. Funct Plant Biol 32:153–159

    Article  CAS  Google Scholar 

  • Yuen SH, Pollard AG (1954) Determination of nitrogen in agricultural materials by the Nessler Reagent. II. Micro-determination of plant tissue and soil extracts. J Sci Food Agr 5:364–369

    Article  CAS  Google Scholar 

  • Zanetti S, Hartwig UA, Luscher A, Hebeisen T, Frehner M, Fischer BU, Hendrey GR, Blum H, Nosberger J (1996) Stimulation of symbiotic N2 fixation in Trifolium repens L. under elevated atmospheric pCO2 in a grassland ecosystem. Plant Physiol 112:575–583

    PubMed  CAS  Google Scholar 

  • Zhang TQ, MacKenzie AF, Liang BC, Drury CF (2004) Soil test phosphorus and phosphorus fractions with long-term phosphorus addition and depletion. Soil Sci Soc Am J 68:519–528

    Article  CAS  Google Scholar 

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Acknowledgments

This research was supported by an Australian Research Council Linkage Project (LP100200757), and utilised the SoilFACE facility of the Department of Primary Industries, Victoria at Horsham. We thank anonymous reviewers for their comments on the manuscript.

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Authors and Affiliations

  1. Department of Agricultural Sciences, La Trobe University, Melbourne Campus, Bundoora, VIC, 3086, Australia

    Jian Jin, Caixian Tang, Clayton Butterly & Peter Sale

  2. Department of Primary Industries, PMB 260, Horsham, VIC, 3401, Australia

    Roger Armstrong

  3. Key Laboratory of Black Soil Ecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Harbin, 150081, China

    Jian Jin

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  1. Jian Jin
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Correspondence to Caixian Tang.

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Jin, J., Tang, C., Armstrong, R. et al. Elevated CO2 temporally enhances phosphorus immobilization in the rhizosphere of wheat and chickpea. Plant Soil 368, 315–328 (2013). https://doi.org/10.1007/s11104-012-1516-9

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