Biology and Fertility of Soils

, Volume 51, Issue 3, pp 289–298 | Cite as

Liming of anthropogenically acidified soil promotes phosphorus acquisition in the rhizosphere of wheat

  • Ljiljana Kostic
  • Nina Nikolic
  • Jelena Samardzic
  • Mira Milisavljevic
  • Vuk Maksimović
  • Dragan Cakmak
  • Dragan Manojlovic
  • Miroslav NikolicEmail author
Original Paper


We studied the effect of liming and P fertilization of extremely acid soil (accidently acidified by sulfidic mining waste) on P availability and the subsequent adaptive responses of wheat roots. The wheat plants were grown in rhizoboxes allowing precise sampling of rhizosphere and bulk soil for sequential extraction of P fractions and determination of exchangeable Al. Root exudates were collected by pieces of paper for electrophoresis and subjected to HPLC analysis. Expression of organic anions and Pi transporter genes was analyzed by a real-time quantitative PCR. The concomitant application of lime with P fertilization increased the concentrations of plant-available P fractions in both rhizosphere and bulk compartments. The applied soil amendments strongly affected plant growth, biomass partitioning and shoot P accumulation. Liming enhanced root exudation of citrate in P unfertilized plants, while the high malate efflux was maintained until both P deficiency and Al toxicity were eliminated by the amendments. We showed the importance of liming for recovering of P acquisition potential of wheat roots, which can be strongly impaired in acid soils. Our results clearly demonstrated that P-deficient roots not subjected to Al stress in the limed soil can maintain high efflux of malate and even increase efflux of citrate along with the enhanced expression of related anion transporters (TaMATE1 and TaALMT1).


Liming Phosphorus deficiency Polluted acid soil Rhizosphere Root exudates Wheat 



The paper is dedicated to the memory of Prof. Volker Römheld. This work was supported by the Serbian Ministry for Education, Science and Technological Development projects OI-173028 and OI-173005. We thank Prof. Zed Rengel (University of Western Australia) for stimulating discussion and critical reading of the manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Annaheim KE, Rufener CB, Frossard E, Bünemann EK (2013) Hydrolysis of organic phosphorus in soil water suspensions after addition of phosphatase enzymes. Biol Fertil Soils 49:1203–1213CrossRefGoogle Scholar
  2. Bashan Y, Levanony H (1989) Effect of root environment on proton efflux in wheat roots. Plant Soil 119:191–197CrossRefGoogle Scholar
  3. Catarecha P, Segura MD, Franco-Zorrilla JM, García-Ponce B, Lanza M, Solano R, Paz-Ares J, Leyva A (2007) A mutant of the Arabidopsis phosphate transporter PHT1; 1 displays enhanced arsenic accumulation. Plant Cell 19:1123–1133CrossRefPubMedCentralPubMedGoogle Scholar
  4. Cesco S, Mimmo T, Tonon G, Tomasi N, Pinton R, Terzano R, Neumann G, Weisskopf L, Renella G, Landi L, Nannipieri P (2012) Plant-borne flavonoids released into the rhizosphere: impact on soil bio-activities related to plant nutrition. A review. Biol Fertil Soils 48:123–149CrossRefGoogle Scholar
  5. Chang SC, Jackson ML (1957) Fractionation of soil phosphorus. Soil Sci 84:133–144CrossRefGoogle Scholar
  6. Clemente R, Walker D, Bernal M (2005) Uptake of heavy metals and As by Brassica juncea grown in a contaminated soil in Azñalcóllar (Spain): the effect of soil amendments. Environ Pollut 138:46–58CrossRefPubMedGoogle Scholar
  7. Darke AK, Walbridge MR (2000) Al and Fe biogeochemistry in a floodplain forest: implications for P retention. Biogeochemistry 51:1–32CrossRefGoogle Scholar
  8. Davies TGE, Ying J, Xu Q, Li ZS, Li J, Gordon-Weeks R (2002) Expression analysis of putative high-affinity phosphate transporters in Chinese winter wheats. Plant Cell Environ 25:1325–1339CrossRefGoogle Scholar
  9. Delgado A, Scalenghe R (2008) Aspects of phosphorus transfer from soils in Europe. J Plant Nutr Soil Sci 171:552–575CrossRefGoogle Scholar
  10. Delhaize E, Ryan PR, Randall PJ (1993) Aluminum tolerance in wheat (Triticum aestivum L.) II. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiol 103:695–702PubMedCentralPubMedGoogle Scholar
  11. 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 7:391–400CrossRefPubMedGoogle Scholar
  12. Domínguez M, Marañón T, Murillo JM, Schulin R, Robinson B (2010) Nutritional status of mediterranean trees growing in a contaminated and remediated area. Water Air Soil Pollut 205:305–321CrossRefGoogle Scholar
  13. Egner H, Riehm H, Domingo W (1960) Untersuchungen über die chemische Bodenanalyse als Grundlage für die Beurteilung des Nährstoffzustandes der Böden. II. Chemische Extraktionsmethoden zur Phosphor und Kaliumbestimmung. K. Lantbrukshoegskolans Annaler 26:199–215Google Scholar
  14. Fageria NK (2001) Adequate and toxic levels of copper and manganese in upland rice, common bean, corn, soybean, and wheat grown on an oxisol. Commun Soil Sci Plant Anal 32:1659–1676CrossRefGoogle Scholar
  15. Gerrard J (1987) Alluvial soils, 1st edn. Van Nostrand Reinhold Co., New YorkGoogle Scholar
  16. HilleRisLambers J, Ettinger AK, Ford KR, Haak DC, Horwith M, Miner BE, Rogers HS, Sheldon KS, Tewksbury JJ, Waters SM, Yang S (2013) Accidental experiments: ecological and evolutionary insights and opportunities derived from global change. Oikos 122:1649–1661CrossRefGoogle Scholar
  17. Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195CrossRefGoogle Scholar
  18. Hinsinger P, Gilkes RJ (1996) Mobilization of phosphate from phosphate rock and alumina-sorbed phosphate by the roots of ryegrass and clover as related to rhizosphere pH. Eur J Soil Sci 47:533–544CrossRefGoogle Scholar
  19. Huang CY, Shirley N, Genc Y, Shi BJ, Langridge P (2011) Phosphate utilization efficiency correlates with expression of low affinity phosphate transporters and noncoding RNA, IPS1, in barley. Plant Physiol 156:1217–1229CrossRefPubMedCentralPubMedGoogle Scholar
  20. Kochian LV, Hoekenga OA, Piñeros MA (2004) How do crop plants tolerate acid soil? Mechanisms of aluminum tolerance and phosphorus efficiency. Annu Rev Plant Biol 55:459–493CrossRefPubMedGoogle Scholar
  21. Li H, Shen J, Zhang F, Clairotte M, Drevon JJ, Le Cadre E, Hinsinger P (2008) Dynamics of phosphorus fractions in the rhizosphere of common bean (Phaseolus vulgaris L.) and durum wheat (Triticum turgidum durum L.) grown in monocropping and intercropping systems. Plant Soil 312:139–150CrossRefGoogle Scholar
  22. Liang CA, Piñeros MA, Tian J, Yao Z, Sun L, Liu J, Shaff J, Coluccio A, Kochian LV, Liao H (2013) Low pH, aluminum, and phosphorus coordinately regulate malate exudation through GmALMT1 to improve soybean adaptation to acid soils. Plant Physiol 161:1347–1361CrossRefPubMedCentralPubMedGoogle Scholar
  23. Madejón P, Murillo JM, Marañón T, Cabrera F, Soriano M (2003) Trace element and nutrient accumulation in sunflower plants two years after the Azñalcóllar mine spill. Sci Total Environ 307:239–257CrossRefPubMedGoogle Scholar
  24. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, LondonGoogle Scholar
  25. Meyer S, De Angeli A, Fernie AR, Martinoia E (2010) Intra- and extra-cellular excretion of carboxylates. Trends Plant Sci 15:40–47CrossRefPubMedGoogle Scholar
  26. Miao J, Sun J, Liu D, Li B, Zhang A, Li Z, Tong Y (2009) Characterization of the promoter of phosphate transporter TaPHT1.2 differentially expressed in wheat varieties. J Genet Genomics 36:455–466CrossRefPubMedGoogle Scholar
  27. Murillo JM, Marañón T, Cabrera F, López R (1999) Accumulation of heavy metals in sunflower and sorghum plants affected by the Guadiamar spill. Sci Total Environ 242:281–292CrossRefPubMedGoogle Scholar
  28. Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bünemann EK, Oberson A, Frossardet E (eds) Phosphorus in action. Soil Biology 26. Springer Verlag, Heidelberg, pp 215–241Google Scholar
  29. Neumann G, Römheld V (2007) The release of root exudates as affected by the plant physiological status. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere. Biochemistry and organic substances at the soil-plant interface, 2nd edn. CRC Press, Boca Raton, pp 23–72CrossRefGoogle Scholar
  30. Nikolic N, Kostic L, Djordjevic A, Nikolic M (2011) Phosphorus deficiency is the major limiting factor for wheat on alluvium polluted by the copper mine pyrite tailings: a black box approach. Plant Soil 339:485–498CrossRefGoogle Scholar
  31. Nuruzzaman M, Lambers H, Bolland MDA, Veneklaas EJ (2006) Distribution of carboxylates and acid phosphatase and depletion of different phosphorus fractions in the rhizosphere of a cereal and three grain legumes. Plant Soil 28:109–120CrossRefGoogle Scholar
  32. Oberson A, Friesen DK, Rao IM, Bühler S, Frossard E (2001) Phosphorus transformations in an oxisol under contrasting land-use systems: the role of the soil microbial biomass. Plant Soil 237:197–210CrossRefGoogle Scholar
  33. Osborne LD, Rengel Z (2002) Genotypic differences in wheat for uptake and utilization of P from iron phosphate. Aust J Agric Res 53:837–844CrossRefGoogle Scholar
  34. Pearse SJ (2011) Why does the musketeer approach to phosphorus acquisition from sparingly soluble forms fail: all for one, but not one for all? Plant Soil 348:81–83CrossRefGoogle Scholar
  35. Pearse SJ, Veneklaas EJ, Cawthray GR, Barber MDA, Lambers H (2006) Triticum aestivum shows a greater biomass response to a supply of aluminium phosphate than Lupinus albus, despite releasing less carboxylates into the rhizosphere. New Phytol 169:515–524CrossRefPubMedGoogle Scholar
  36. 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 173:181–190CrossRefPubMedGoogle Scholar
  37. Pellet DM, Papernik LA, Jones DL, Darrah PR, Grunes DL, Kochian LV (1997) Involvement of multiple aluminum exclusion mechanisms in aluminum resistance in wheat. Plant Soil 192:63–68CrossRefGoogle Scholar
  38. Piňeros MA, Cancado GMA, Kochian LV (2008) Novel properties of the wheat aluminum tolerance organic acid transporter (TaALMT1) revealed by electrophysiological characterization in xenopus oocytes: functional and structural implications. Plant Physiol 147:2131–2146CrossRefPubMedCentralPubMedGoogle Scholar
  39. Reddy DD, Rao AS, Takar PN (1999) Effects of repeated manure and fertilizer phosphorus additions on soil phosphorus dynamics under soybean–wheat rotation. Biol Fertil Soils 28:150–155CrossRefGoogle Scholar
  40. Rose TJ, Hardiputra B, Rengel Z (2010) Wheat, canola and grain legume access to soil phosphorus fractions differs in soils with contrasting phosphorus dynamics. Plant Soil 326:159–170CrossRefGoogle Scholar
  41. Ryan PR, Delhaize E, Randall PJ (1995a) Characterisation of Al stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196:103–110CrossRefGoogle Scholar
  42. Ryan PR, Delhaize E, Randall PJ (1995b) Malate efflux from root apices and tolerance to aluminium are highly correlated in wheat. Aust J Plant Physiol 22:531–536CrossRefGoogle Scholar
  43. Ryan PR, Skerrett M, Findlay GP, Delhaize E, Tyerman SD (1997) Aluminium activates an anion channel in the apical cells of wheat roots. Proc Natl Acad Sci U S A 94:6547–6552CrossRefPubMedCentralPubMedGoogle Scholar
  44. Ryan PR, Raman H, Gupta S, Horst WJ, Delhaize E (2009) A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots. Plant Physiol 149:340–351CrossRefPubMedCentralPubMedGoogle Scholar
  45. Ryan PR, James RA, Weligama C, Delhaize E, Rattey A, Lewis DC, Bovill WD, McDonald G, Rathjen TM, Wang E, Fettell NA, Richardson AE (2014) Can citrate efflux from roots improve phosphorus uptake by plants? Testing the hypothesis with near-isogenic lines of wheat. Physiol Plant 151:230–242CrossRefPubMedGoogle Scholar
  46. 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 37:645–653CrossRefPubMedGoogle Scholar
  47. Shen J, Yuan L, Zhang J, Li H, Bai Z, Chen X, Zhang W, Zhang F (2011) Phosphorus dynamics: from soil to plant update on phosphorus dynamics in the soil-plant continuum. Plant Physiol 156:997–1005CrossRefPubMedCentralPubMedGoogle Scholar
  48. Stass A, Smit I, Eticha D, Oetter G, Horst WJ (2008) The significance of organic-anion exudation for the aluminum resistance of primary triticale derived from wheat and rye parents differing in aluminum resistance. J Plant Nutr Soil Sci 171:634–642CrossRefGoogle Scholar
  49. Teng W, Deng Y, Chen XP, Xu XF, Chen RY, Lv Y, Zhao YY, Zhao XQ, He X, Li B, Tong YP, Zhang FS, Li ZS (2013) Characterization of root response to phosphorus supply from morphology to gene analysis in field-grown wheat. J Exp Bot 64:1403–1411CrossRefPubMedCentralPubMedGoogle Scholar
  50. Tiessen H, Moir JO (1993) Characterization of available P by sequential extraction. In: Carter MR (ed) Soil sampling and methods of analysis. Canadian Society of Soil Science. Lewis Publishers, Boca Raton, pp 75–86Google Scholar
  51. Tittarelli A, Milla L, Vargas F, Morales A, Neupert C, Meisel LA, Salvo GH, Peñaloza E, Muñoz G, Corcuera LJ, Silva H (2007) Isolation and comparative analysis of the wheat TaPT2 promoter: identification in silico of new putative regulatory motifs conserved between monocots and dicots. J Exp Bot 58:2573–2582CrossRefPubMedGoogle Scholar
  52. Veneklaas EJ, Stevens T, Cawthray GR, Turner NC, Grigg AM, Lambers H (2003) Chickpea and white lupin rhizosphere carboxylates vary with soil properties and enhance phosphorus uptake. Plant Soil 248:187–197CrossRefGoogle Scholar
  53. Verma S, Subehia SK, Sharma SP (2005) Phosphorus fractions in an acid soil continuously fertilized with mineral and organic fertilizers. Biol Fertil Soils 41:295–300CrossRefGoogle Scholar
  54. Vu DT, Armstrong RD, Sale PWG, Tang C (2010) Phosphorus availability for three crop species as a function of soil type and fertilizer history. Plant Soil 337:497–510CrossRefGoogle Scholar
  55. Waldrip HM, He Z, Erich SM (2011) Effects of poultry manure amendment on phosphorus uptake by ryegrass, soil phosphorus fractions and phosphatases activity. Biol Fertil Soils 47:407–418CrossRefGoogle Scholar
  56. Wang X, Tang C, Guppy CN, Sale PWG (2010) Cotton, wheat and white lupin differ in phosphorus acquisition from sparingly soluble P sources. Environ Exp Bot 69:267–272CrossRefGoogle Scholar
  57. 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 348:85–98CrossRefGoogle Scholar
  58. Wang E, Ridoutt BG, Luo Z, Probert ME (2013) Using systems modelling to explore the potential for root exudates to increase phosphorus use efficiency in cereal crops. Environ Model Softw 46:50–60CrossRefGoogle Scholar
  59. White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511CrossRefPubMedCentralPubMedGoogle Scholar
  60. Yang X, Post WM (2011) Phosphorus transformations as a function of pedogenesis: a synthesis of soil phosphorus data using Hedley fractionation method. Biogeosciences 8:2907–2916CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Ljiljana Kostic
    • 1
  • Nina Nikolic
    • 1
  • Jelena Samardzic
    • 2
  • Mira Milisavljevic
    • 2
  • Vuk Maksimović
    • 1
  • Dragan Cakmak
    • 3
  • Dragan Manojlovic
    • 4
  • Miroslav Nikolic
    • 1
    Email author
  1. 1.Institute for Multidisciplinary ResearchUniversity of BelgradeBelgradeSerbia
  2. 2.Institute of Molecular Genetics and Genetic EngineeringUniversity of BelgradeBelgradeSerbia
  3. 3.Institute of Soil ScienceBelgradeSerbia
  4. 4.Faculty of ChemistryUniversity of BelgradeBelgradeSerbia

Personalised recommendations