Journal of Soils and Sediments

, Volume 19, Issue 1, pp 198–210 | Cite as

Dynamic influence of S fertilizer on Cu bioavailability in rice (Oryza sativa L.) rhizosphere soil during the whole life cycle of rice plants

  • Lijuan Sun
  • Qinglin Liu
  • Yong Xue
  • Chen Xu
  • Cheng Peng
  • Xiaofeng Yuan
  • Jiyan Shi
Soils, Sec 3 • Remediation and Management of Contaminated or Degraded Lands • Research Article



Addition of S fertilizer influences the behavior of metals in soil, the mechanism of which has not been extensively studied to date. We explored the dynamic influence of S fertilizer (S0 and Na2SO4) applied in paddy soils on Cu bioavailability in rice rhizosphere soil during the life cycle of rice plants.

Materials and methods

Through a microcosm experiment, the speciation of Cu and S in rhizosphere soil was explored by traditional chemical extraction methods and advanced synchrotron-based X-ray absorption near-edge spectroscopy (XANES) techniques.

Results and discussion

In the vegetative stages of rice plants, sulfur fertilization increased the concentration of bioavailable Cu, as well as the dissolved organic carbon (DOC) concentration in rhizosphere soil. Meanwhile, a higher proportion of Cu-humic substances was found in soil treated with S than that in control soil. However, extended flooding conditions led to the reduction of S fertilizer to sulfide, which provided the substrate for Cu2S formation. Thus, in the reproductive stages of rice plants, a higher proportion of Cu2S formation from +S treatments led to a relatively lower concentration of bioavailable Cu in rice rhizosphere soil than in control soil.


The influence of S fertilizer on Cu bioavailability depended on the growth stage of rice plants. Both the DOC and redox potential (Eh) were changed by S fertilization in paddy soils and are critical factors that control Cu speciation in rice rhizosphere soil.


Bioavailability Cu Paddy rice Speciation S fertilizer 


Funding information

The work was supported by the National Natural Science Foundation of China (11179025, 41422107, U1532103), National Key Research and Development Program of China (2016YFD0800401), Shanghai Sailing Program (18YF1421100), and Excellent Team Program of Shanghai Academy of Agricultural Sciences (Nongkechuang 2017(A-03)). We would like to express our great gratitude to Lirong Zheng at the beamline 1W1B and Lei Zheng at beamline 4B7A of Beijing Synchrotron Radiation Facility, Institute of High Energy Physics, Chinese Academy of Sciences for their generous help in Cu and S K-edge XANES collection and analysis, respectively.

Supplementary material

11368_2018_2009_MOESM1_ESM.docx (313 kb)
ESM 1 (DOCX 313 kb)


  1. Aulakh MS, Wassmann R, Bueno C, Kreuzwieser J, Rennenberg H (2001) Characterization of root exudates at different growth stages of ten rice (Oryza sativa L.) cultivars. Plant Biol 3:139–148CrossRefGoogle Scholar
  2. Borch T, Kretzschmar R, Kappler A, Cappellen PV, Ginder-Vogel M, Voegelin A, Campbell K (2009) Biogeochemical redox processes and their impact on contaminant dynamics. Environ Sci Technol 44:15–23CrossRefGoogle Scholar
  3. Burkhead JL, Gogolin Reynolds KA, Abdel-Ghany SE, Cohu CM, Pilon M (2009) Copper homeostasis. New Phytol 182:799–816CrossRefGoogle Scholar
  4. Capaldi FR, Gratão PL, Reis AR, Lima LW, Azevedo RA (2015) Sulfur metabolism and stress defense responses in plants. Trop Plant Biol 8:60–73CrossRefGoogle Scholar
  5. Chien SH, Gearhart MM, Villagarcía S (2011) Comparison of ammonium sulfate with other nitrogen and sulfur fertilizers in increasing crop production and minimizing environmental impact: a review. Soil Sci 176:327–335CrossRefGoogle Scholar
  6. Coles CA, Yong RN (2006) Humic acid preparation, properties and interactions with metals lead and cadmium. Eng Geol 85:26–32CrossRefGoogle Scholar
  7. Cui Y, Dong Y, Li H, Wang Q (2004) Effect of elemental sulphur on solubility of soil heavy metals and their uptake by maize. Environ Int 30:323–328CrossRefGoogle Scholar
  8. De Kok LJ (2005) Proceedings of the 1st Sino-German Workshop on Aspects of Sulfur Nutrition of Plants: 23–27 May 2004 in Shenyang, China (Bundesforsch.-Anst. f. Landwirtschaft)Google Scholar
  9. Du Y, Hu XF, Wu XH, Shu Y, Jiang Y, Yan XJ (2013) Affects of mining activities on Cd pollution to the paddy soils and rice grain in Hunan province, Central South China. Environ Monit Assess 185:9843–9856CrossRefGoogle Scholar
  10. Flemming C, Trevors J (1989) Copper toxicity and chemistry in the environment: a review. Water Air Soil Pollut 44:143–158CrossRefGoogle Scholar
  11. Fulda B, Voegelin A, Ehlert K, Kretzschmar R (2013) Redox transformation, solid phase speciation and solution dynamics of copper during soil reduction and reoxidation as affected by sulfate availability. Geochim Cosmochim Acta 123:385–402CrossRefGoogle Scholar
  12. Hong S, Candelone JP, Soutif M, Boutron CF (1996) A reconstruction of changes in copper production and copper emissions to the atmosphere during the past 7000 years. Sci Total Environ 188:183–193CrossRefGoogle Scholar
  13. Hu ZY, Zhao FJ, McGrath SP (2005) Sulphur fractionation in calcareous soils and bioavailability to plants. Plant Soil 268:103–109CrossRefGoogle Scholar
  14. Jalilehvand F (2006) Sulfur: not a “silent” element any more. Chem Soc Rev 35:1256–1268CrossRefGoogle Scholar
  15. Jia Y, Bao P, Zhu YG (2015) Arsenic bioavailability to rice plant in paddy soil: influence of microbial sulfate reduction. J Soils Sediments 15:1960–1967CrossRefGoogle Scholar
  16. Karlsson T, Persson P, Skyllberg U (2006) Complexation of copper (II) in organic soils and in dissolved organic matter-EXAFS evidence for chelate ring structures. Environ Sci Technol 40:2623–2628CrossRefGoogle Scholar
  17. Kayser A, Wenger K, Keller A, Attinger W, Felix H, Gupta S, Schulin R (2000) Enhancement of phytoextraction of Zn, Cd, and Cu from calcareous soil: the use of NTA and sulfur amendments. Environ Sci Technol 34:1778–1783CrossRefGoogle Scholar
  18. Krishnamurti G, Cieslinski G, Huang P, Van Rees K (1997) Kinetics of cadmium release from soils as influenced by organic acids: implication in cadmium availability. J Enviro Qual 26:271–277CrossRefGoogle Scholar
  19. Lakanen E, Erviö R (1971) A comparison of eight extractants for the determination of plant available micronutrients in soils. Helsingin yliopiston rehtorin professori Erkki Kivisen juhlajulkaisu: Jubilee issue in honour of professor Erkki Kivinen Rector of Helsinki UniversityGoogle Scholar
  20. Li QK (1992) Acidity of paddy soils. In: Chen PL, Fan SQ, Wang HJ (eds) Paddy soils of China, pp 274–288Google Scholar
  21. Li Z, Ma Z, Van der Kuijp TJ, Yuan Z, Huang L (2014) A review of soil heavy metal pollution from mines in China: pollution and health risk assessment. Sci Total Environ 468:843–853CrossRefGoogle Scholar
  22. Lin HR, Shi JY, Wu B, Yang JJ, Chen YX, Zhao Y, Hu TD (2010) Speciation and biochemical transformations of sulfur and copper in rice rhizosphere and bulk soil—XANES evidence of sulfur and copper associations. J Soils Sediments 10:907–914CrossRefGoogle Scholar
  23. Liu WJ, Zhu YG, Hu Y, Williams PN, Gault AG, Meharg AA, Charnock JM, Smith FA (2006) Arsenic sequestration in iron plaque, its accumulation and speciation in mature rice plants (Oryza Sativa L.). Environ Sci Technol 40:5730–5736CrossRefGoogle Scholar
  24. Lu Y, Wassmann R, Neue HU, Huang C (2000) Dynamics of dissolved organic carbon and methane emissions in a flooded rice soil. Soil Sci Soc Am J 64:2011–2017CrossRefGoogle Scholar
  25. Luo L, Xu C, Ma YB, Zheng L, Liu LJ, Lv JT, Zhang SZ (2014) Sulfur speciation in an arable soil as affected by sample pretreatments and sewage sludge application. Soil Sci Soc Am J 78:1615–1623CrossRefGoogle Scholar
  26. Marschner H (2011) Marschner’s mineral nutrition of higher plants (Academic press)Google Scholar
  27. McGrath SP, Zhao FJ, Withers, PJA (1996) Development of sulphur deficiency in crops and its treatment. Proceedings-Fertiliser Society (United Kingdom). NO. 379Google Scholar
  28. Murase J, Kimura M (1997) Anaerobic reoxidation of Mn2+, Fe2+, S0 and S2− in submerged paddy soils. Biol Fertil Soils 25:302–306CrossRefGoogle Scholar
  29. Pattrick R, Mosselmans J, Charnock J, England K, Helz G, Garner C, Vaughan D (1997) The structure of amorphous copper sulfide precipitates: an X-ray absorption study. Geochim Cosmochim Ac 61:2023–2036CrossRefGoogle Scholar
  30. Qian YZ, Chen C, Zhang Q, Li Y, Chen ZC, Li M (2010) Concentrations of cadmium, lead, mercury and arsenic in Chinese market milled rice and associated population health risk. Food Control 21:1757–1763CrossRefGoogle Scholar
  31. Qin F, Shan XQ, Wei B (2004) Effects of low-molecular-weight organic acids and residence time on desorption of Cu, Cd, and Pb from soils. Chemosphere 57:253–263CrossRefGoogle Scholar
  32. Quevauviller P (1998) Operationally defined extraction procedures for soil and sediment analysis I. Standardization. TrAC-Trends Anal Chem 17:289–298CrossRefGoogle Scholar
  33. Ravel á, Newville M (2005) ATHENA, ARTEMIS, HEPHAESTUS: data analysis for X-ray absorption spectroscopy using IFEFFIT. J Synchrotron Radiat 12:537–541CrossRefGoogle Scholar
  34. Spark K, Wells J, Johnson B (1997) The interaction of a humic acid with heavy metals. Aust J of Soil Res 35:89–101CrossRefGoogle Scholar
  35. Strawn DG, Baker LL (2007) Speciation of Cu in a contaminated agricultural soil measured by XAFS, μ-XAFS, and μ-XRF. Environ Sci Techno 42:37–42CrossRefGoogle Scholar
  36. Sun LJ, Zheng CQ, Yang JJ, Peng C, Xu C, Wang Y, Feng JB, Shi JY (2016) Impact of sulfur (S) fertilization in paddy soils on copper (Cu) accumulation in rice (Oryza sativa L.) plants under flooding conditions. Biol Fertil Soils 52:31–39CrossRefGoogle Scholar
  37. Tang WW, Zeng GM, Gong JL, Liang J, Xu P, Zhang C, Huang BB (2014) Impact of humic/fulvic acid on the removal of heavy metals from aqueous solutions using nanomaterials: a review. Sci Total Environ 468:1014–1027CrossRefGoogle Scholar
  38. Vega FA, Covelo EF, Andrade M (2006) Competitive sorption and desorption of heavy metals in mine soils: influence of mine soil characteristics. J Colloid Interf Sci 298:582–592CrossRefGoogle Scholar
  39. Wang S, Mulligan CN (2013) Effects of three low-molecular-weight organic acids (LMWOAs) and pH on the mobilization of arsenic and heavy metals (Cu, Pb, and Zn) from mine tailings. Environ Geochem Health 35:111–118CrossRefGoogle Scholar
  40. Wang YP, Li QB, Hui W, Shi JY, Lin Q, Chen XC, Chen YX (2008) Effect of sulphur on soil Cu/Zn availability and microbial community composition. J Hazard Mater 159:385–389CrossRefGoogle Scholar
  41. Weber FA, Voegelin A, Kaegi R, Kretzschmar R (2009) Contaminant mobilization by metallic copper and metal sulphide colloids in flooded soil. Nat Geosci 2:267–271CrossRefGoogle Scholar
  42. Wu Z, Gu Z, Wang X, Evans L, Guo H (2003) Effects of organic acids on adsorption of lead onto montmorillonite, goethite and humic acid. Environ Pollut 121:469–475CrossRefGoogle Scholar
  43. Yang JJ, Zhu SH, Zheng CQ, Sun LJ, Liu J, Shi JY (2015) Impact of S fertilizers on pore-water cu dynamics and transformation in a contaminated paddy soil with various flooding periods. J Hazard Mater 286:432–439CrossRefGoogle Scholar
  44. Yoshida S, Forno DA, Cock JH (1971) Laboratory manual for physiological studies of rice. Laboratory manual for physiological studies of rice, International Rice Research InstituteGoogle Scholar
  45. Yu HY, Li FB, Liu CS, Huang W, Liu TX, Yu WM (2016) Iron redox cycling coupled to transformation and immobilization of heavy metals: implications for paddy rice safety in the red soil of South China. Adv Agron 137:279–317CrossRefGoogle Scholar
  46. Zhou W, Wan M, He P, Li ST, Lin B (2002) Oxidation of elemental sulfur in paddy soils as influenced by flooded condition and plant growth in pot experiment. Biol Fertil Soils 36:384–389CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.MOE Key Laboratory of Environment Remediation and Ecological Health, College of Environmental & Resource ScienceZhejiang UniversityHangzhouChina
  2. 2.Department of Environmental Engineering, College of Environmental and Resource SciencesZhejiang UniversityHangzhouChina
  3. 3.Institute of ECO-Environment and Plant ProtectionShanghai Academy of Agricultural SciencesShanghaiChina
  4. 4.Bestwa Environmental Protection Sci-Tech Co. LtdHangzhouChina
  5. 5.College of Environmental Science and EngineeringDonghua UniversityShanghaiChina
  6. 6.College of Life ScienceZhejiang Chinese Medical UniversityHangzhouChina

Personalised recommendations