Journal of Soils and Sediments

, Volume 20, Issue 1, pp 320–329 | Cite as

Nitrogen fertilizer enhances zinc and cadmium uptake by hyperaccumulator Sedum alfredii Hance

  • Ziwen Lin
  • Chunying Dou
  • Yongfu LiEmail author
  • Hailong Wang
  • Nabeel Khan Niazi
  • Shaobo Zhang
  • Dan Liu
  • Keli Zhao
  • Weijun Fu
  • Yongchun Li
  • Zhengqian YeEmail author
Soils, Sec 3 • Remediation and Management of Contaminated or Degraded Lands • Research Article



Nitrogen (N) fertilization is known to have a substantial effect on heavy metal uptake in plants. However, the impact of N fertilization on plant growth and heavy metal uptake of hyperaccumulator plants remains unclear. This study examined the effect of N fertilization on growth and uptake of zinc (Zn) and cadmium (Cd) in Zn/Cd-hyperaccumulating plants species, Sedum alfredii (S. alfredii) Hance (Crassulaceae).

Materials and methods

Plants of S. alfredii were grown for 60 days in nutrient solution with 100 μmol Cd L−1 and 0–10 mmol N L−1, and in a Cd-contaminated soil receiving N fertilizer and composted pig manure amendment. Biomass production, nutrient uptake, and concentrations and accumulation of Zn and Cd in plant parts were measured.

Results and discussion

In the hydroponic experiment, both low (< 1 mmol L−1) and high (> 5 mmol L−1) N supply decreased the growth and Zn and Cd accumulation in the whole plants. The 2.5 mmol N L−1 is an optimal N dosage for shoot biomass production and Zn accumulation in shoots, while the 1.0 mmol N L−1 is an optimal N dosage for Cd accumulation in shoots, which was 68.1% higher than the control. The N doses of 1 to 2.5 mmol L−1 N represented optimal conditions for Zn and Cd accumulation in the shoots of S. alfredii seedlings. In the soil pot experiment, shoot dry weight decreased with increasing N fertilization rate, while composted pig manure decreased biomass production. Both Zn and Cd accumulation in the shoots of S. alfredii decreased along with the addition of higher N fertilization rate. However, the composted pig manure amendment increased the accumulation of Zn, but not Cd in the shoots.


The application of N at appropriate amount enhanced the phytoremediation efficiency by S. alfredii in Zn/Cd-polluted fields, but the effectiveness of phytoextraction technology needs to be validated in the field trials.


Cadmium Hyperaccumulator Phytoextraction Sedum alfredii Hance Zinc 


Funding information

The National Natural Science Foundation of China (31670617, 21577131), the National Key Research and Development Project (2017YFD0801302), the Key Research and Development Project of Science Technology Department of Zhejiang Province (2018C03028), and Guangdong Provincial Natural Science Foundation, China (2017A030311019), supported this study.


  1. Agnello AC, Bagard M, Van Hullebusch ED, Esposito G, Huguenot D (2016) Comparative bioremediation of heavy metals and petroleum hydrocarbons co-contaminated soil by natural attenuation, phytoremediation, bioaugmentation and bioaugmentation-assisted phytoremediation. Sci Total Environ 563:693–703Google Scholar
  2. Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals-concepts and applications. Chemosphere 91:869–881Google Scholar
  3. Arnamwong S, Wu LH, Hu PJ, Yuan C, Thiravetyan P, Luo YM, Christie P (2015) Phytoextraction of cadmium and zinc by Sedum plumbizincicola using different nitrogen fertilizers, a nitrification inhibitor and a urease inhibitor. Int J Phytoremediat 17:382–390Google Scholar
  4. Arnesen AKM, Singh BR (1998) Plant uptake and DTPA-extractability of Cd, Cu, Ni and Zn in a Norwegian alum shale soil as affected by previous addition of dairy and pig manures and peat. Can J Soil Sci 78:531–539Google Scholar
  5. Ayangbenro A, Babalola O (2017) A new strategy for heavy metal polluted environments: a review of microbial biosorbents. Int J Env R Pub He 14:94Google Scholar
  6. Bao SD (2000) Soil and agricultural chemistry analysis. Chinese Agriculture Press, BeijingGoogle Scholar
  7. Bolan N, Kunhikrishnan A, Thangarajan R, Kumpiene J, Park J, Makino T, Krikham MB, Scheckel K (2014) Remediation of heavy metal (loid)s contaminated soils-to mobilize or to immobilize? J Hazard Mater 266:141–166Google Scholar
  8. Burges A, Alkorta I, Epelde L, Garbisu C (2018) From phytoremediation of soil contaminants to phytomanagement of ecosystem services in metal contaminated sites. Int J Phytoremediat 20:384–397Google Scholar
  9. Carignan R, Tessier A (1988) The co-diagenesis of sulfur and iron in acid lake sediments of southwestern Québec. Geochim Cosmochim Ac 52:1179–1188Google Scholar
  10. Chaffei C, Pageau K, Suzuki A, Gouia H, Ghorbel MH, Masclaux-Daubresse C (2004) Cadmium toxicity induced changes in nitrogen management in Lycopersicon esculentum leading to a metabolic safeguard through an amino acid storage strategy. Plant Cell Physiol 45:1681–1693Google Scholar
  11. Chang YS, Chang YJ, Lin CT, Lee MC, Wu CW (2013) Nitrogen fertilization promotes the phytoremediation of cadmium in Pentas lanceolata. Int Biodeterior Biodegradation 85:709–714Google Scholar
  12. Cheng MM, Wang AN, Tang CX (2017) Ammonium-based fertilizers enhance cd accumulation in Carpobrotus rossii grown in two soils differing in pH. Chemosphere 188:689–696Google Scholar
  13. Dai W, Zhao KL, Fu WJ, Jiang PK, Li YF, Zhang CS, Gielen G, Gong X, Li YH, Wang HL, Wu JS (2018) Spatial variation of organic carbon density in topsoils of a typical subtropical forest, southeastern China. Catena 167:181–189Google Scholar
  14. Garbisu C, Alkorta I (2001) Phytoextraction: a cost-effective plant-based technology for the removal of metals from the environment. Bioresour Technol 77:229–236Google Scholar
  15. Giansoldati V, Tassi E, Morelli E, Gabellieri E, Pedron F, Barbafieri M (2012) Nitrogen fertilizer improves boron phytoextraction by Brassica juncea grown in contaminated sediments and alleviates plant stress. Chemosphere 87:1119–1125Google Scholar
  16. Guo JM, Lei M, Yang JX, Yang J, Wan XM, Chen TB, Zhou XY, Gu SP, Guo GH (2017) Effect of fertilizers on the Cd uptake of two sedum species (Sedum spectabile Boreau and Sedum aizoon L.) as potential Cd accumulators. Ecol Eng 106:409–414Google Scholar
  17. Gupta DK, Chatterjee S, Datta S, Veer V, Walther C (2014) Role of phosphate fertilizers in heavy metal uptake and detoxification of toxic metals. Chemosphere 108:134–144Google Scholar
  18. Hao HL, Wei YZ, Yang XE, Feng Y, Wu CY (2007) Effects of different nitrogen fertilizer levels on Fe, Mn, Cu and Zn concentrations in shoot and grain quality in rice (Oryza sativa). Rice Sci 14:289–294Google Scholar
  19. Hrynkiewicz K, Złoch M, Kowalkowski T, Baum C, Buszewski B (2018) Efficiency of microbially assisted phytoremediation of heavy-metal contaminated soils. Environ Rev 26:316–332Google Scholar
  20. Hu PJ, Yin YG, Ishikawa S, Suzui N, Kawachi N, Fujimaki S, Igura M, Yuan C, Huang JX, Li Z, Makino T, Luo YM, Christie P, Wu LH (2013) Nitrate facilitates cadmium uptake, transport and accumulation in the hyperaccumulator Sedum plumbizincicola. Environ Sci Pollut Res 20:6306–6316Google Scholar
  21. Jacobs A, De Brabandere L, Drouet T, Sterckeman T, Noret N (2018) Phytoextraction of Cd and Zn with Noccaea caerulescens for urban soil remediation: influence of nitrogen fertilization and planting density. Ecol Eng 16:178–187Google Scholar
  22. Kelly JJ, Häggblom MM, Tate RL (2003) Effects of heavy metal contamination and remediation on soil microbial communities in the vicinity of a zinc smelter as indicated by analysis of microbial community phospholipid fatty acid profiles. Biol Fertil Soils 38:65–71Google Scholar
  23. Kumar PBAN, Dushenkov V, Motto H, Raskin I (1995) Phytoextraction: the use of plants to remove heavy metals from soils. Environ Sci Technol 29:1232–1238Google Scholar
  24. Li NY, Fu QL, Zhuang P, Guo B, Zou B, Li ZA (2012) Effect of fertilizers on Cd uptake of Amaranthus hypochondriacus, a high biomass, fast growing and easily cultivated potential Cd hyperaccumulator. Int J phytoremediat 14:162–173Google Scholar
  25. Li S, Chen JR, Islam E, Wang Y, Wu JS, Ye ZQ, Yan WB, Peng DL, Liu D (2016) Cadmium-induced oxidative stress, response of antioxidants and detection of intracellular cadmium in organs of moso bamboo (Phyllostachys pubescens) seedlings. Chemosphere 153:107–114Google Scholar
  26. Li YC, Li YF, Chang SX, Yang YF, Fu SL, Jiang PK, Luo Y, Yang M, Chen ZH, Hu SD, Zhao MX, Liang X, Xu QF, Zhou GM, Zhou JZ (2018a) Biochar reduces soil heterotrophic respiration in a subtropical plantation through increasing soil organic carbon recalcitrancy and decreasing carbon-degrading microbial activity. Soil Biol Biochem 122:173–185Google Scholar
  27. Li YF, Hu SD, Chen JH, Müller K, Li YC, Fu WJ, Lin ZW, Wang HL (2018b) Effects of biochar application in forest ecosystems on soil properties and greenhouse gas emissions: a review. J Soils Sediments 18:546–563Google Scholar
  28. Li YF, Zhang JJ, Scott X, Chang, Jiang PK, Zhou GM, Fu SL, Yan ER, Wu JS, Lin L (2013) Long-term intensive management effects on soil organic carbon pools and chemical composition in Moso bamboo (Phyllostachys pubescens) forests in subtropical China. Forest Ecol Manag 303:121–131Google Scholar
  29. Liu H, Ding Y, Zhang Q, Liu X, Xu J, Li Y, Di H (2018) Heterotrophic nitrification and denitrification are the main sources of nitrous oxide in two paddy soils. Plant Soil. Google Scholar
  30. Liu WX, Wang QL, Wang BB, Hou JY, Luo YM, Tang CX, Franks AE (2015) Plant growth-promoting rhizobacteria enhance the growth and Cd uptake of Sedum plumbizincicola in a Cd-contaminated soil. J Soils Sediments 15:1191–1199Google Scholar
  31. Liu WX, Zhang CJ, Hu PJ, Luo YM, Wu LH, Sale P, Tang CX (2016) Influence of nitrogen form on the phytoextraction of cadmium by a newly discovered hyperaccumulator Carpobrotus rossii. Environ Sci Pollut Res 23:1246–1253Google Scholar
  32. Liu YL, Ge TD, Jun Y, Liu SL, Shibistova O, Wang P, Wang JK, Li Y, Guggenberger G, Kuzyakov Y, Wu JS (2019) Initial utilization of rhizodeposits with rice growth in paddy soils: rhizosphere and N fertilization effects. Geoderma 338:30–39Google Scholar
  33. Luo BF, Du ST, Lu KX, Liu JW, Lin XY, Jin CW (2012) Iron uptake system mediates nitrate-facilitated cadmium accumulation in tomato (Solanum lycopersicum) plants. J Exp Bot 63:3127–3136Google Scholar
  34. Luo Y, Zhu Z, Liu S, Peng P, Xu J, Brookes P, Ge T, Wu J (2018) Nitrogen fertilization increases rice rhizodeposition and its stabilization in soil aggregates and the humus fraction. Plant Soil. Google Scholar
  35. Mahar A, Wang P, Ali A, Awasthi MK, Lahori AH, Wang Q, Li RH, Zhang ZQ (2016) Challenges and opportunities in the phytoremediation of heavy metals contaminated soils: a review. Ecotox Environ Safe 126:111–121Google Scholar
  36. Marques AP, Rangel AOSS, Castro PML (2009) Remediation of heavy metal contaminated soils: phytoremediation as a potentially promising clean-up technology. Crit Rev Environ Sci Technol 39:622–654Google Scholar
  37. Monsant AC, Tang C, Baker AJM (2008) The effect of nitrogen form on rhizosphere soil pH and zinc phytoextraction by Thlaspi caerulescens. Chemosphere 73:635–642Google Scholar
  38. Monsant AC, Wang YL, Tang CX (2010) Nitrate nutrition enhances zinc hyperaccumulation in Noccaea caerulescens (Prayon). Plant Soil 336:391–404Google Scholar
  39. Murphy J, Riley J (1962) A modified single solution method for the determination of PO% in natural waters. Anal Chim Acta 27:31–36Google Scholar
  40. Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216Google Scholar
  41. Nedjimi B, Daoud Y (2009) Cadmium accumulation in Atriplex halimus subsp. schweinfurthii and its influence on growth, proline, root hydraulic conductivity and nutrient uptake. Flora-Morphology Dist Func Ecol Plants 204:316–324Google Scholar
  42. Nelson DW, Sommers LE (1982) Total carbon, organic carbon and organic matter. In: Methods of soil analysis part 2. Chemical and Microbial Properties. Am. Soc. Agron. Soil Sci. Soc. Am Madison, WI, pp 408–411Google Scholar
  43. Padmavathiamma PK, Li LY (2007) Phytoremediation technology: hyper-accumulation metals in plants. Water Air Soil Pollut 184:105–126Google Scholar
  44. Paz-Ferreiro J, Lu H, Fu S, Méndez A, Gascó G (2014) Use of phytoremediation and biochar to remediate heavy metal polluted soils: a review. Solid Earth 5:65–75Google Scholar
  45. Pandey VC, Pandey DN, Singh N (2015) Sustainable phytoremediation based on naturally colonizing and economically valuable plants. J Clean Prod 86:37–39Google Scholar
  46. Pan H, Xie K, Zhang Q, Jia Z, Xu J, Di H, Li Y (2018) Archaea and bacteria respectively dominate nitrification in lightly and heavily grazed soil in a grassland system. Biol Fertil Soils 54:41–54Google Scholar
  47. Schwartz C, Echevarria G, Morel JL (2003) Phytoextraction of cadmium with Thlaspi caerulescens. Plant Soil 249:27–35Google Scholar
  48. Sessitsch A, Kuffner M, Kidd P, Vangronsveld J, Wenzel WW, Fallmann K, Puschenreiter M (2013) The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils. Soil Biol Biochem 60:182–194Google Scholar
  49. Simard RR (1993) Ammonium acetate extractable elements. In: Martin R, Carter S (eds) Soil sampling and methods of analysis. Lewis Publisher, FL, pp 39–43Google Scholar
  50. Wang X, Chen C, Wang JL (2017) Cs phytoremediation by Sorghum bicolor cultivated in soil and in hydroponic system. Int J Phytoremediat 19:402–412Google Scholar
  51. Wei SH, Wang SS, Zhou QX, Zhan J, Ma LH, Wu ZJ, Sun TH, Prasad MNV (2010) Potential of Taraxacum mongolicum Hand-Mazz for accelerating phytoextraction of cadmium in combination with eco-friendly amendments. J Hazard Mater 181:480–484Google Scholar
  52. Wiszniewska A, Hanus-Fajerska E, Muszyńska E, Ciarkowska K (2016) Natural organic amendments for improved phytoremediation of polluted soils: a review of recent progress. Pedosphere 26:1–12Google Scholar
  53. Xiao ML, Zang HD, Liu SL, Ye RZ, Zhu ZK, Su YR, Wu JS, Ge TD (2019) Nitrogen fertilization alters the distribution and fates of photosynthesized carbon in rice–soil systems: a 13C-CO2 pulse labeling study. Plant Soil. Google Scholar
  54. Xiao WD, Li D, Ye XZ, Xu HZ, Yao GH, Wang JW, Zhang Q, Hu J, Gao N (2017) Enhancement of Cd phytoextraction by hyperaccumulator Sedum alfredii using electrical field and organic amendments. Environ Sci Pollut Res 24:5060–5067Google Scholar
  55. Yan WB, Mahmood Q, Peng DL, Fu WJ, Chen T, Wang Y, Li S, Chen JR, Liu D (2015) The spatial distribution pattern of heavy metals and risk assessment of moso bamboo forest soil around lead–zinc mine in Southeastern China. Soil Till Res 153: 120-130Google Scholar
  56. Yang W, Dai HP, Dou XK, Zhang QR, Wei SH (2019) Effect and mechanism of commonly used four nitrogen fertilizers and three organic fertilizers on Solanum nigrum L. hyperaccumulating Cd. Environ Sci Pollut Res 26:12940–12947Google Scholar
  57. Yang XE, Long XX, Ye HB, He ZL, Calvert DV, Stoffella PJ (2004) Cadmium tolerance and hyperaccumulation in a new Zn-hyperaccumulating plant species (Sedum alfredii Hance). Plant Soil 259:181–189Google Scholar
  58. Yang XE, Ye HB, Long XX, He B, He ZL, Stoffella PJ, Calvert DV (2005) Uptake and accumulation of cadmium and zinc by Sedum alfredii Hance at different Cd/Zn supply levels. J Plant Nutr 27:1963–1977Google Scholar
  59. Yang ZB, Liu LX, Lv YF, Cheng Z, Xu XX, Xian JR, Zhu XM, Yang YX (2018) Metal availability, soil nutrient, and enzyme activity in response to application of organic amendments in Cd-contaminated soil. Environ Sci Pollut Res 25:2425–2435Google Scholar
  60. Yavari S, Malakahmad A, Sapari NB, Yavari S (2018) Nutrients balance for improvement of phytoremediation ability of teak seedlings (Tectona grandis). J Plant Nutr 41:545–551Google Scholar
  61. Zaccheo P, Crippa L, Pasta VDM (2006) Ammonium nutrition as a strategy for cadmium mobilisation in the rhizosphere of sunflower. Plant Soil 283:43–56Google Scholar
  62. Zhang RR, Liu Y, Xue WL, Chen RX, Du ST, Jin CW (2016) Slow-release nitrogen fertilizers can improve yield and reduce Cd concentration in pakchoi (Brassica chinensis L.) grown in Cd-contaminated soil. Environ Sci Pollut Res 23:25074–25083Google Scholar
  63. Zhao KL, Fu WJ, Qiu QZ, Ye ZQ, Li YF, Tunney H, Dou CY, Zhou KN, Qian XB (2019) Spatial patterns of potentially hazardous metals in paddy soils in a typical electrical waste dismantling area and their pollution characteristics. Geoderma 337:453–462Google Scholar
  64. Zhou GD, Guo JM, Yang J, Yang JX (2018) Effect of fertilizers on Cd accumulation and subcellular distribution of two cosmos species (Cosmos sulphureus and Cosmos bipinnata). Int J Phytoremediat 20:930–938Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.State Key Laboratory of Subtropical Silviculture, Zhejiang Provincial Key Laboratory of Carbon Cycling in Forest Ecosystems and Carbon SequestrationZhejiang A & F UniversityLin’anChina
  2. 2.Key Laboratory of Soil Contamination Bioremediation of Zhejiang ProvinceZhejiang A & F UniversityHangzhouChina
  3. 3.Biochar Engineering Technology Research Center of Guangdong Province, School of Environment and Chemical EngineeringFoshan UniversityFoshanChina
  4. 4.Institute of Soil and Environmental SciencesUniversity of Agriculture FaisalabadFaisalabadPakistan
  5. 5.School of Civil Engineering and SurveyingUniversity of Southern QueenslandToowoombaAustralia

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