Skip to main content
SpringerLink
Log in

Impact of sulfur (S) fertilization in paddy soils on copper (Cu) accumulation in rice (Oryza sativa L.) plants under flooding conditions

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

As the biogeochemical cycling of S in soil is closely associated with the mobility and bioavailability of heavy metals, in this study, we investigated the influence of S fertilization (S0 and SO4 2−) in paddy soils on rice growth, iron plaque formation over root surface, and Cu speciation of rice rhizosphere soil under flooding conditions. The dry weight and height of rice plants increased significantly after S fertilization, indicating that S fertilization of Cu-contaminated paddy soils can enhance rice growth. Sulfur fertilization (less than 500 mg/kg) promoted the formation of iron plaque, thus sequestering a large amount of Cu on root surface and decreasing the bioavailability of Cu by inducing transformation of Cu bioavailable fractions (exchangeable, carbonate oxides, or iron and manganese oxide bound to Cu) to Cu bound to organic matter. Copper K-edge X-ray absorption near-edge structure (XANES) revealed that S fertilization increased the percentage of Cu present as Cu2S and Cu–cysteine in rice rhizosphere soil, thus reducing Cu mobility. As Cu concentration in rice plants decreased and the biomass of rice plants increased after S fertilization, it can be suggested that S fertilization may be an effective approach for managing Cu-contaminated paddy soils.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

SSE:

Selective sequential extraction

XANES:

X-ray absorption near-edge structure

DTPA:

Diethylenetriaminepentaacetic acid

References

  • Ahsan N, Lee DG, Lee SH, Kang KY, Lee JJ, Kim PJ, Yoon HS, Kim JS, Lee BH (2007) Excess copper induced physiological and proteomic changes in germinating rice seeds. Chemosphere 67:1182–1193. doi:10.1016/j.chemosphere.2006.10.075

    Article  PubMed  CAS  Google Scholar 

  • Armstrong W (1964) Oxygen diffusion from the roots of some British bog plants. Nature 204:801–802. doi:10.1038/204801b0

    Article  CAS  Google Scholar 

  • Astolfi S, Zuchi S (2013) Adequate S supply protects barley plants from adverse effects of salinity stress by increasing thiol contents. Acta Physiol Plant 35:175–181. doi:10.1007/s11738-012-1060-5

    Article  CAS  Google Scholar 

  • Barnett MO, Harris LA, Turner RR, Stevenson RJ, Henson TJ, Melton RC, Hoffman DP (1997) Formation of mercuric sulfide in soil. Environ Sci Technol 31:3037–3043. doi:10.1021/es960389j

    Article  CAS  Google Scholar 

  • Chen Z, Zhu YG, Liu WJ, Meharg AA (2005) Direct evidence showing the effect of root surface iron plaque on arsenite and arsenate uptake into rice (Oryza sativa L.) roots. New Phytol 165:91–97. doi:10.1111/j.1469-8137.2004.01241.x

    Article  PubMed  CAS  Google Scholar 

  • Chen GC, Chen XC, Yang YQ, Hay AG, Yu XH, Chen YX (2011) Sorption and distribution of copper in unsaturated Pseudomonas putida CZ1 biofilms as determined by X-ray fluorescence microscopy. Appl Environ Microbiol 77:4719–4727. doi:10.1128/AEM.00125-11

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cheng H, Wang MY, Wong MH, Ye ZH (2014) Does radial oxygen loss and iron plaque formation on roots alter Cd and Pb uptake and distribution in rice plant tissues? Plant Soil 375:137–148. doi:10.1007/s11104-013-1945-0

    Article  CAS  Google Scholar 

  • Chien SH, Prochnow LI, Cantarella H (2009) Recent developments of fertilizer production and use to improve nutrient efficiency and minimize environmental impacts. In: Donald LS (ed) Adv agron. Academic Press, London, pp 267–322. doi:10.1016/S0065-2113(09)01008-6

    Google Scholar 

  • Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182. doi:10.1146/annurev.arplant.53.100301.135154

    Article  PubMed  CAS  Google Scholar 

  • DalCorso G, Manara A, Furini A (2013) An overview of heavy metal challenge in plants: from roots to shoots. Metallomics 5:1117–1132. doi:10.1039/C3MT00038A

    Article  PubMed  CAS  Google Scholar 

  • Elguindi J, Hao XL, Lin YB, Alwathnani HA, Wei GH, Rensing C (2011) Advantages and challenges of increased antimicrobial copper use and copper mining. Appl Microbiol Biotehnol 91:237–249. doi:10.1007/s00253-011-3383-3

    Article  CAS  Google Scholar 

  • Fan MX, Messick DL (2005) Advances in sulfur fertilizer requirement and research for Chinese agriculture: summary of field trial data from TSI’s China project from 1997 to 2003. In: Aspects of sulfur nutrition of plants; evaluation of China’s current, future and available resources to correct plant nutrient sulfur deficiencies–report of the first Sino-German Sulfur Workshop, pp 15-21.

  • Fan JL, Hu ZY, Ziadi N, Xia X, Wu CYH (2010) Excessive sulfur supply reduces cadmium accumulation in brown rice (Oryza sativa L.). Environ Pollut 158:409–415. doi:10.1016/j.envpol.2009.08.042

    Article  PubMed  CAS  Google Scholar 

  • Fan J, Xia X, Hu Z, Ziadi N, Liu C (2013) Excessive sulfur supply reduces arsenic accumulation in brown rice. Plant Soil Environ 59:169–174

    CAS  Google Scholar 

  • Fisher JC, Wallschläger D, Planer Friedrich B, Hollibaugh JT (2007) A new role for sulfur in arsenic cycling. Environ Sci Technol 42:81–85. doi:10.1021/es0713936

    Article  CAS  Google Scholar 

  • Flemming C, Trevors J (1989) Copper toxicity and chemistry in the environment: a review. Water Air Soil Pollut 44:143–158

    Article  CAS  Google Scholar 

  • 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 123:385–402. doi:10.1016/j.gca.2013.07.017

    Article  CAS  Google Scholar 

  • Gao MX, Wang G, Dong, Hu ZY (2007) Effect of elemental sulfur supply on cadmium uptake into rice seedlings when cultivated in low and excess cadmium soils. Commun Soil Sci Plan 41:013. doi:10.1080/00103621003646071

    Google Scholar 

  • Hesterberg D, Chou JW, Hutchison KJ, Sayers DE (2001) Bonding of Hg (II) to reduced organic sulfur in humic acid as affected by S/Hg ratio. Environ Sci Technol 35:2741–2745. doi:10.1021/es001960o

    Article  PubMed  CAS  Google Scholar 

  • Hu ZY, Zhu YG, Li M, Zhang LG, Cao ZH, Smith FA (2007) Sulfur (S)-induced enhancement of iron plaque formation in the rhizosphere reduces arsenic accumulation in rice (Oryza sativa L.) seedlings. Environ Pollut 147:387–393. doi:10.1016/j.envpol.2006.06.014

    Article  PubMed  CAS  Google Scholar 

  • Huang JH, Hsu SH, Wang SL (2011) Effects of rice straw ash amendment on Cu solubility and distribution in flooded rice paddy soils. J Hazard Mater 186:1801–1807. doi:10.1016/j.jhazmat.2010.12.066

    Article  PubMed  CAS  Google Scholar 

  • 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 40:2623–2628. doi:10.1021/es052211f

    Article  PubMed  CAS  Google Scholar 

  • 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 34:1778–1783. doi:10.1021/es990697s

    Article  CAS  Google Scholar 

  • Kögel KI, Amelung W, Cao ZH, Fiedler S, Frenzel P, Jahn R, Kalbitz K, Kölbl A, Schloter M (2010) Biogeochemistry of paddy soils. Geoderma 157:1–14. doi:10.1016/j.geoderma.2010.03.009

    Article  CAS  Google Scholar 

  • Li QK (1992) Paddy soils of China. Chinese Science Press, Beijing, pp 380–432

    Google Scholar 

  • Li ZY, Ma ZW, van der Kuijp TJ, Yuan ZW, Huang L (2014) A review of soil heavy metal pollution from mines in China: pollution and health risk assessment. Sci Total Environ 468:843–853. doi:10.1016/j.scitotenv.2013.08.090

    Article  PubMed  CAS  Google Scholar 

  • Lin YF, Aarts MG (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69:3187–3206. doi:10.1007/s00018-012-1089-z

    Article  PubMed  CAS  Google Scholar 

  • Lin HR, Shi JY, Chen XC, Yang JJ, Chen YX, Zhao YD, Hu TD (2010a) Effects of lead upon the actions of sulfate-reducing bacteria in the rice rhizosphere. Soil Biol Biochem 42:1038–1044. doi:10.1016/j.soilbio.2010.02.023

    Article  CAS  Google Scholar 

  • Lin HR, Shi JY, Wu B, Yang JJ, Chen YX, Zhao YD, Hu TD (2010b) Speciation and biochemical transformations of sulfur and copper in rice rhizosphere and bulk soil-XANES evidence of sulfur and copper associations. J Soil Sediments 10:907–914. doi:10.1007/s11368-010-0204-8

    Article  CAS  Google Scholar 

  • Liu WJ, Zhu YG, Smith FA, Smith SE (2004) Do iron plaque and genotypes affect arsenate uptake and translocation by rice seedlings (Oryza sativa L.) grown in solution culture? J Exp Bot 55:1707–1713. doi:10.1093/jxb/erh205

    Article  PubMed  CAS  Google Scholar 

  • Liu WJ, Zhu YG, Hu Y, Williams P, Gault A, Meharg AA, Charnock J, Smith FA (2006) Arsenic sequestration in iron plaque, its accumulation and speciation in mature rice plants (Oryza sativa L.). Environ Sci Technol 40:5730–5736. doi:10.1021/es060800v

    Article  PubMed  CAS  Google Scholar 

  • Mei XQ, Wong MH, Yang Y, Dong HY, Qiu RL, Ye ZH (2012) The effects of radial oxygen loss on arsenic tolerance and uptake in rice and on its rhizosphere. Environ Pollut 165:109–117. doi:10.1016/j.envpol.2012.02.018

    Article  PubMed  CAS  Google Scholar 

  • Peng C, Duan DC, Xu C, Chen YS, Sun LJ, Zhang H, Yuan XF, Zheng LR, Yang YQ, Yang JJ, Zhen XJ, Chen YX, Shi JY (2015) Translocation and biotransformation of CuO nanoparticles in rice (Oryza sativa L.) plants. Environ Pollut 197:99–107. doi:10.1016/j.envpol.2014.12.008

    Article  PubMed  CAS  Google Scholar 

  • Quevauviller P (1998) Operationally defined extraction procedures for soil and sediment analysis I. Standardization. Trac-Trend Anal Chem 17:289–298. doi:10.1016/S0165-9936(97)00119-2

    Article  CAS  Google Scholar 

  • Ravel á, Newville M (2005) Athena, Artemis, Hephaestus: data analysis for X-ray absorption spectroscopy using IFEFFIT. J Synchrotron Radiat 12:537–541. doi:10.1107/S0909049505012719

    Article  PubMed  CAS  Google Scholar 

  • Shi JY, Wu B, Yuan XF, Cao YY, Chen XC, Chen YX, Hu TD (2008) An X-ray absorption spectroscopy investigation of speciation and biotransformation of copper in Elsholtzia splendens. Plant Soil 302:163–174. doi:10.1007/s11104-007-9463-6

    Article  CAS  Google Scholar 

  • Strawn DG, Baker LL (2008) Speciation of Cu in a contaminated agricultural soil measured by XAFS, mu-XAFS, and mu-XRF. Environ Sci Technol 42:37–42. doi:10.1021/es071605z

    Article  PubMed  CAS  Google Scholar 

  • Takahashi H, Kopriva S, Giordano M, Saito K, Hell R (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol 62:157–184. doi:10.1146/annurev-arplant-042110-103921

    Article  PubMed  CAS  Google Scholar 

  • Tessier A, Campbell PG, Bisson M (1979) Sequential extraction procedure for the speciation of particulate trace metals. Anal Chem 51:844–851. doi:10.1021/ac50043a017

    Article  CAS  Google Scholar 

  • Tripathi RD, Tripathi P, Dwivedi S, Kumar A, Mishra A, Chauhan PS, Norton GJ, Nautiyal CS (2014) Roles for root iron plaque in sequestration and uptake of heavy metals and metalloids in aquatic and wetland plants. Metallomics 6:1789–1800. doi:10.1039/C4MT00111G

    Article  PubMed  CAS  Google Scholar 

  • 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 159:385–389. doi:10.1016/j.jhazmat.2008.02.029

    Article  PubMed  CAS  Google Scholar 

  • Weber FA, Voegelin A, Kaegi R, Kretzschmar R (2009) Contaminant mobilization by metallic copper and metal sulphide colloids in flooded soil. Nat Geosci 2:267–271. doi:10.1038/ngeo476

    Article  CAS  Google Scholar 

  • Wenger K, Kayser A, Gupta S, Furrer G, Schulin R (2002) Comparison of NTA and elemental sulfur as potential soil amendments in phytoremediation. Soil Sediment Contam 11:655–672. doi:10.1080/20025891107023

    Article  CAS  Google Scholar 

  • Wu C, Ye ZH, Li H, Wu SC, Deng D, Zhu YG, Wong MH (2012) Do radial oxygen loss and external aeration affect iron plaque formation and arsenic accumulation and speciation in rice? J Exp Bot 63:2961–2970. doi:10.1093/jxb/ers017

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang JJ, Liu J, Dynes JJ, Peak D, Regier T, Wang J, Zhu SH, Shi JY, John ST (2014a) Speciation and distribution of copper in a mining soil using multiple synchrotron-based bulk and microscopic techniques. Environ Sci Pollut Res 21:2943–2954. doi:10.1007/s11356-013-2214-8

    Article  CAS  Google Scholar 

  • Yang JX, Tam NFY, Ye ZH (2014b) Root porosity, radial oxygen loss and iron plaque on roots of wetland plants in relation to zinc tolerance and accumulation. Plant Soil 374:815–828. doi:10.1007/s11104-013-1922-7

    Article  CAS  Google Scholar 

  • 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 286:432–439. doi:10.1016/j.jhazmat.2015.01.035

    Article  PubMed  CAS  Google Scholar 

  • Yoshida S, Forno DA, Cock JH (1971) Laboratory manual for physiological studies of rice

  • 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 36:384–389. doi:10.1007/s00374-002-0547-4

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The work was supported by the National Natural Science Foundation of China (11179025, 41422107, 21207114) and the Fundamental Research Funds for the Central Universities. We would like to express our sincere gratitude to Lirong Zheng and Jing Zhang at the beam line 1W1B of Beijing Synchrotron Radiation Facility (BSRF) for their generous help in XAFS experiments.

Author information

Authors and Affiliations

  1. Department of Environmental Engineering, College of Environmental and Resource Sciences, Zijingang Campus, Zhejiang University, Hangzhou, 310058, People’s Republic of China

    Lijuan Sun, Cuiqing Zheng, Jianjun Yang, Cheng Peng, Chen Xu, Yi Wang, Jiabei Feng & Jiyan Shi

Authors
  1. Lijuan Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cuiqing Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jianjun Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cheng Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chen Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yi Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jiabei Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jiyan Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jiyan Shi.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Figure S1

(DOCX 1688 kb)

Figure S2

(DOCX 1688 kb)

Figure S3

(DOCX 1688 kb)

Figure S4

(DOCX 1688 kb)

Figure S5

(DOCX 1688 kb)

Figure S6

(DOCX 1688 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, L., Zheng, C., Yang, J. et al. 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, 31–39 (2016). https://doi.org/10.1007/s00374-015-1050-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-015-1050-z

Keywords

Search

Navigation