Plant and Soil

, Volume 443, Issue 1–2, pp 401–411 | Cite as

Stem aqueous extracts of accumulator Bidens tripartita L. strongly promoted Solanum nigrum L. Cd hyperaccumulation from soil

  • Ran Han
  • Huiping DaiEmail author
  • Lidia Skuza
  • Jie Zhan
  • Shuhe WeiEmail author
Regular Article



The effects of aqueous extracts from bio-resources on Solanum nigrum L. Cd hyperaccumulation were determined with EDTA as control.


Soil pot culture experiment and Leaching experiment were arranged and conducted.


The results showed that stem extracts of Bidens tripartita L. (BT-S) significantly increased (by 61.0%) Cd shoot concentration in S. nigrum, which was higher compared (p < 0.05) to EDTA addition (32.4%), and the plants grew well. However, S. nigrum shoot biomass significantly decreased by 23.9% (p < 0.05) in the case of EDTA addition. The extraction rate of BT-S was 56.2% in the soil leaching experiment, and the extractable Cd concentration in soil in BT-S treatment was 69.7% higher compared to control. The concentrations of soluble polysaccharides, total organic acids and reducing sugars in the BT-S treatment were much higher than for other extracts, which may partly be the reason for it strong stimulation of S. nigrum Cd hyperaccumulation from the soil.


The aqueous extracts of B. tripartita stems (BT-S) significantly increased (p < 0.05) S. nigrum hyperaccumulating Cd. This new chelator that can replace EDTA is of great significance for phytoremediation.


Bidens tripartita L. Extracts Strengthen Hyperaccumulation 



This work was supported by the Special Plan in the Major Research & Development of the 13rd Five-Year Plan of China (2018YFC1800501, 2016YFD0800802), the National Natural Science Foundation of China (31870488, 41571300, 31270540, 31070455), Projects of Shaanxi Province (2019JM-413, 15JK1121, 17JS023, 2018SZS-27-07), and the project of Foreign Experts Bureau of Shaanxi province (G20190241001, GDT20186100430B).


  1. Alamri SA, Siddiqui MH, Al-Khaishany MYY, Khan MN, Ali HM, Alaraidh IA, Alsahli AA, Al-Rabiah H, Mateen MJ (2018) Ascorbic acid improves the tolerance of wheat plants to lead toxicity. Plant Interact 13:409–419CrossRefGoogle Scholar
  2. Aznar Ò, Checa A, Oliver R, Hernández-Cassou S, Saurina J (2015) Determination of polyphenols in wines by liquid chromatography with UV spectrophotometric detection. J Sep Sci 34:527–535CrossRefGoogle Scholar
  3. Bvenura C, Afolayan AJ (2014) Growth and physiological response of Solanum nigrum L. to organic and/or inorganic fertilisers. J Appl Bot Food Qual 87:168–174Google Scholar
  4. Carrasco-Pancorbo A, Cerretani L, Bendini A, Lorenzo C, Fernández-Gutiérrez A (2015) Analytical determination of polyphenols in olive oils. J Sep Sci 28:837–858CrossRefGoogle Scholar
  5. Chen B, Ma XX, Liu GQ, Xu XM, Pan FS, Zhang J, Tian SK, Feng Y, Yang XE (2015a) An endophytic bacterium Acinetobacter calcoaceticus Sasm3-enhanced phytoremediation of nitrate-cadmium compound polluted soil by intercropping Sedum alfredii with oilseed rape. Environ Sci Pollut Res 22:17625–17635CrossRefGoogle Scholar
  6. Chen JW, Sun YM, Wang FY, Zhang XQ, Yang ZN, Liu YH, Sun M (2015b) Induction and accumulation of cadmium and lead by hairy root of Bidens pilosa. Acta Sci Circumst 35:1596–1602Google Scholar
  7. Dai HP, Wei SH, Twardowska I, Han R, Xu L (2017) Hyperaccumulating potential of Bidens pilosa L. for Cd and elucidation of its translocation behavior based on cell membrane permeability. Environ Sci Pollut Res 24:23161–23167CrossRefGoogle Scholar
  8. Dobrowolska-Iwanek J (2015) Simple method for determination of short-chain organic acid in Mead. Food Anal Methods 8:2356–2359CrossRefGoogle Scholar
  9. Durand A, Piutti S, Rue M, Morel JL, Echevarria G, Benizri E (2016) Improving nickel phytoextraction by co-cropping hyperaccumulator plants inoculated by plant growth promoting rhizobacteria. Plant Soil 399:179–192CrossRefGoogle Scholar
  10. Eissa MA (2017) Phytoextraction mechanism of cd by, Atriplex lentiformis, using some mobilizing agents. Ecol Eng 108:220–226CrossRefGoogle Scholar
  11. El-Jendoubi H, Javier A, Anunciación A (2013) Assessment of nutrient removal in bearing peach trees (Prunus persica L. Batsch) based on whole tree analysis. Plant Soil 369:421–437CrossRefGoogle Scholar
  12. Gao Y, Miao CY, Mao L, Zhou P, Jin ZG, Shi WJ (2010) Improvement of phytoextraction and antioxidative defense in Solanum nigrum L. under cadmium stress by application of cadmium-resistant strain and citric acid. J Hazard Mater 181:771–777CrossRefPubMedGoogle Scholar
  13. Guo D, Amjad A, Ren CY, Du J, Li RH, Altaf HL, Xiao R, Zhang ZY, Zhang ZQ (2019) EDTA and organic acids assisted phytoextraction of Cd and Zn from a smelter contaminated soil by potherb mustard (Brassica juncea,coss) and evaluation of its bioindicators. Ecotox Environ Safety 167:396–403CrossRefGoogle Scholar
  14. Huang YM, Zhang YX, Liu QL, Hung SL, Liu P (2015) Research on allelopathy of aqueous extract from Tagetes patula to four garden plants. Acta Pratacul Sin 24:150–158Google Scholar
  15. Huo WM, Zou R, Wang L, Guo W, Zhang DJ, Fan HL (2018) Effect of different forms of N fertilizers on the hyperaccumulator Solanum nigrum L. and maize in intercropping mode under Cd stress. RSC Adv 8:40210–40218CrossRefGoogle Scholar
  16. Kong Y, Zhang LL, Sun Y, Zhang YY, Sun BG, Chen HT (2017) Determination of the free amino acid, organic acid, and nucleotide in commercial vinegars. J Food Sci 82:336–345CrossRefGoogle Scholar
  17. Kováˇcik J, Rotková G, Bujdoˇs M, Babula P, Peterková V, Matúˇs P (2017) Ascorbic acid protects Coccomyxa subellipsoidea against metal toxicity through modulation of ROS/NO balance and metal uptake. J Hazard Mater 339:200–207CrossRefGoogle Scholar
  18. Li JT, Baker AJM, Ye ZH, Wang HB, Shu WS (2012) Phytoextraction of cd-contaminated soils: current status and future challenges. Critical Reviews Environ Sci Tech 42:2113–2152CrossRefGoogle Scholar
  19. Li TQ, Tao Q, Liang CF, Yang XE (2014) Elevated CO2 concentration increase the obility of Cd and Zn in the rhizosphere of hyperaccumulator Sedum alfredii. Environ Sci Pollut Res 21:5899–5908CrossRefGoogle Scholar
  20. Li TQ, Tao Q, Shohag MJI, Yang XE, Sparks DL, Liang Y (2015) Root cell wall polysaccharides are involved in cadmium hyperaccumulation insedum alfredii. Plant Soil 389:387–399CrossRefGoogle Scholar
  21. Lingua G, Todeschini V, Grimaldi M, Baldantoni D, Proto A, Cicatelli A (2014) Polyaspartate, a biodegradable chelant that improves the phytoremediation potential of poplar in a highly metal-contaminated agricultural soil. J Environ Manag 132:9–15CrossRefGoogle Scholar
  22. Liu WT, Liang LC, Zhang X, Zhou QX (2015) Cultivar variations in cadmium and lead accumulation and distribution among 30 wheat (Triticum aestivum L.) cultivars. Environ Sci Pollut Res 22:8432–8441CrossRefGoogle Scholar
  23. Liu L, Ma Q, Lin L, Tang Y, Wang J, Lv X, Liao MA, Xia H, Chen SX, Li JH, Wang X, Lai YS, Liang D (2017) Effects of exogenous abscisic acid on cadmium accumulation in two ecotypes of hyperaccumulator, Bidens pilosa. Environ Progress Sustai Energy 36:1643–1649CrossRefGoogle Scholar
  24. Lopez S, van der Ent A, Erskine PD, Echevarria G, Morel JL, Lee G, Permana E, Benizri E (2019) Rhizosphere chemistry and above-ground elemental fractionation of nickel hyperaccumulator species from Weda Bay (Indonesia). Plant Soil 436:543–563CrossRefGoogle Scholar
  25. Luo SL, Wan Y, Xiao X, Guo HJ, Chen L, Xi Q, Zeng GM, Liu CB, Chen JL (2011) Isolation and characterization of endophytic bacterium LRE07 from cadmium hyperaccumulator Solanum nigrum L. and its potential for remediation. Appl Microbiol Biotechnol 89:1637–1644CrossRefPubMedGoogle Scholar
  26. Naghipour D, Gharibi H, Taghavi K, Jaafari J (2016) Influence of EDTA and NTA on heavy metal extraction from sandy-loam contaminated soils. J Environ Chemical Engineering 4:3512–3518CrossRefGoogle Scholar
  27. Pan FS, Meng Q, Luo S, Shen J, Chen B, Khan KY, Japenga J, Ma X, Yang X, Feng Y (2017) Enhanced Cd extraction of oilseed rape (Brassica napus) by plant growth promoting bacteria isolated from Cd hyperaccumulator Sedum alfredii Hance. Int J Phytoremediat 19:281–289CrossRefGoogle Scholar
  28. Prado FE, González JA, Boero C (2015) A simple and sensitive method for determining reducing sugars in plant tissues. Application to quantify the sugar content in quinoa (chenopodium quinoa willd.) seedlings. Phytochem Anal 9:58–62CrossRefGoogle Scholar
  29. Radziemska M, Gusiatin ZM, Bilgin A (2017) Potential of using immobilizing agents in aided phytostabilization on simulated contamination of soil with lead. Ecol Eng 102:490–500CrossRefGoogle Scholar
  30. Sharma VK, Li XY, Wu GL, Bai WX, Parmar S, White JF, Li HY (2019) Endophytic community of Pb-Zn hyperaccumulator Arabis alpina and its role in host plants metal tolerance. Plant Soil 437:397–411CrossRefGoogle Scholar
  31. Sheel R, Anand M, Nisha K (2015) Phytoremediation of heavy metals (Zn and Pb) and its toxicity on Azolla filiculoides. Inter J Sci Res 4:1238–1241Google Scholar
  32. Sun RL, Zhou QX, Jin CX (2006) Cadmium accumulation in relation to organic acids in leaves of Solanum nigrum L. as a newly found cadmium hyperaccumulator. Plant Soil 285:125–134CrossRefGoogle Scholar
  33. Vigliotta G, Matrella S, Cicatelli A, Guarino F, Castiglione S (2016) Effects of heavy metals and chelants on phytoremediation capacity and on rhizobacterial communities of maize. J Environ Manag 179:93–102CrossRefGoogle Scholar
  34. Wang S, Liu J (2014) The effectiveness and risk comparison of EDTA with EGTA in enhancing Cd phytoextraction by mirabilis jalapa L. Environ Monit Assess 186:751–759CrossRefPubMedGoogle Scholar
  35. Wang SQ, Wei SH, Ji DD, Bai JY (2015) Co-planting Cd contaminated field using hyperaccumulator Solanum nigrum L. through interplant with low accumulation welsh onion. Inter J Phytoremediat 17:879–884Google Scholar
  36. Wang J, Liu C, Zhang X, Lin L, Liang D (2016) Effects of applying hyperaccumulator straw in soil on growth and cadmium accumulation of galinsoga parviflora. Environ Progress Sust Energy 35:618–623Google Scholar
  37. Wang G, Zhang S, Zhong Q, Xu X, Li T, Jia Y (2018) Effect of soil washing with biodegradable chelators on the toxicity of residual metals and soil biological properties. Sci Total Environ 625:1021–1029CrossRefPubMedGoogle Scholar
  38. Wei SH, Twardowska I (2013) Main rhizosphere characteristics of the Cd hyperaccumulator Rorippa globosa (Turcz.) Thell. Plant Soil 372:669–681CrossRefGoogle Scholar
  39. Wei SH, Zhou QX (2008) Screen of Chinese weed species for cadmium tolerance and accumulation characteristics. Int J Phytoremediat 10:584–597CrossRefGoogle Scholar
  40. Wei SH, Zhou QX, Wang X, Zhang KS, Guo GL, Ma LN (2005) A newly-discovered Cd-hyperaccumulator Solanum nigrum L. Chin Sci Bull 50:33–38CrossRefGoogle Scholar
  41. Wei SH, Niu RC, Srivastava M, Zhou QX, Wu ZJ, Sun TH, Hu YH (2009) Bidens tripartite L.: a Cd-accumulator confirmed by pot culture and site sampling experiment. J Hazard Mater 170:1269–1272CrossRefPubMedGoogle Scholar
  42. Wu JL, Chen AQ, Peng SL, Wei ZG, Liu GC (2013) Identification and application of amino acids as chelators in phytoremediation of rare earth elements lanthanum and yttrium. Plant Soil 373:329–338CrossRefGoogle Scholar
  43. Wu DT, Lam SC, Cheong KL (2016) Simultaneous determination of molecular weights and contents of water-soluble polysaccharides and their fractions from Lycium barbarum collected in China. J Pharm Biome Analysis 129:210–218CrossRefGoogle Scholar
  44. Yang QW, Ke HM, Liu SJ, Zeng Q (2018) Phytoremediation of Mn-contaminated paddy soil by two hyperaccumulators (Phytolacca americana and Polygonum hydropiper) aided with citric acid. Environ Sci Pollut Res 25:25933–25941CrossRefGoogle Scholar
  45. Yin Y, Wang Y, Zeng G, Hu X, Zhou L, Guo Y, Li J (2015) Cadmium accumulation and apoplastic and symplastic transport in Boehmeria nivea (l). Gaudich on cadmium-contaminated soil with the addition of EDTA or NTA. RSC Adv 5:47584–47591CrossRefGoogle Scholar
  46. Zhan J, Twardowska I, Wang SQ, Wei SH, Chen YQ, Ljupco M (2019) Prospective sustainable production of safe food for growing population based on the soybean (Glycine max L. Merr.) crops under Cd soil contamination stress. J Clean Prod 212:22–36CrossRefGoogle Scholar
  47. Zhang YP, Wu Y, Shi Z (2017) Study on Cd and Pb pollution of soil in Xiangyang, Hubei province. Resources Environ Engine 31:713–716Google Scholar
  48. Zhao J, Hai LU, Lai M (2016) Separation and determination of angiotensin converting enzyme inhibitory peptide from salt-soluble protein solution fermented with lactic acid bacteria. Food Sci, 37. 170–178Google Scholar
  49. Zhou QX, Song YF (2004) Remediation of contaminated soils: principles and methods. Science Press, China, BeijingGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Pollution Ecology and Environmental Engineering, Institute of Applied EcologyChinese Academy of SciencesShenyangChina
  2. 2.College of Biological Science & Engineering, Shaanxi Province Key Laboratory of Bio-resourcesShaanxi University of TechnologyHanzhongChina
  3. 3.Department of Molecular Biology and Cytology, Institute for Research on BiodiversityUniversity of SzczecinSzczecinPoland
  4. 4.College of Liaoning Professional Hygiene TechnologyShenyangChina
  5. 5.University of Chinese Academy of SciencesBeijingChina

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