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Phytoextraction of cobalt (Co)-contaminated soils by sweet alyssum (Lobularia maritima (L.) Desv.) is enhanced by biodegradable chelating agents

  • Soils, Sec 1 • Soil Organic Matter Dynamics and Nutrient Cycling • Research Article
  • Published:
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Abstract

Purpose

Combining biodegradable chelating agents with phytoextraction is an efficient technique to amend metal-contaminated soils, but most studies have addressed remediation efficiency rather than a comprehensive understanding of the interactions among plant stress, metal accumulation, and metal bioavailability. This study aimed to investigate the effects of biodegradable chelating agents on improving the efficiency of phytoextraction for cobalt (Co)-contaminated soil by sweet alyssum (Lobularia maritima (L.)) and to explore the interrelationships among plant stress, Co accumulation, and Co bioavailability.

Materials and methods

Sweet alyssum (three plants per pot) was grown in pots containing soil with Co added at 0, 40, and 60 mg kg−1, respectively. After 70 days of growth, we added four biodegradable chelating agents (EDDS, NTA, CA, and OA) at various concentrations (0, 2.5, 5.0, and 7.5 mmol kg−1). The plants were harvested after 7 days, and the biomass, reactive oxygen species (ROS) parameters, Co concentrations of the shoot and root, and available Co content in the soil were analyzed.

Results and discussion

The results demonstrate that chelating agents significantly (p < 0.05) improved the phytoextraction capability of sweet alyssum and influenced plant growth and stress. The capability of EDDS to activate Co was higher than that of other chelating agents at identical concentrations in Co-contaminated soils. Furthermore, we observed that a moderate concentration (40 mg kg−1) of Co could promote plant growth and that high concentrations of Co (60 mg kg−1) and EDDS (7.5 mmol kg−1) cause enhanced stress to plant growth, even resulting in lower shoot Co accumulation than that in the moderate EDDS treatment (5.0 mmol kg−1).

Conclusions

The present study demonstrates that the application of EDDS may be a better choice for Co phytoextraction than NTA, CA, and OA; nevertheless, a high concentration of EDDS may enhance the negative effects on plant growth, physiological traits, and Co accumulation.

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Abbreviations

Co:

Cobalt

EDDS:

Ethylenediamine-N,N′-disuccinic acid

EDTA:

Ethylenediaminetetraacetic acid

DTPA:

Diethylenetriaminepentaacetic acid

CA:

Citric acid

OA:

Oxalic acid

TA:

Tartaric acid

NTA:

Nitrilotriacetic acid

TF:

Translocation factor

LMWOAs:

Low molecular organic acids

APCAs:

Aminopolycarboxylate chelating agents

SOM:

Soil organic matter

CEC:

Cation exchange capacity

N:

Nitrogen

K:

Potassium

P:

Phosphorus

References

  • Adiloglu S (2016) Using phytoremediation with canola to remove cobalt from agricultural soils. Pol J Environ Stud 25:2251–2254

    Article  CAS  Google Scholar 

  • Ali B, Hayat S, Hayat Q, Ahmad A (2010) Cobalt stress affects nitrogen metabolism, photosynthesis and antioxidant system in chickpea (Cicer arietinum L.). J Plant Interact 5:223–231

    Article  CAS  Google Scholar 

  • Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals-concepts and applications. Chemosphere 91:869–881

    Article  CAS  Google Scholar 

  • Almaroai YA, Usman RA, Ahmad M, Kim KR, Moon DH, Lee SS, Ok YS (2012) Effects of synthetic chelators and low-molecular-weight organic acids on chromium, copper, and arsenic uptake and translocation in maize (Zea mays L.). Soil Sci 177:655–663

    Article  CAS  Google Scholar 

  • Amari T, Ghnaya T, Debez A, Taamali M, Youssef NB, Lucchini G, Sacchi GA, Abdelly C (2014) Comparative Ni tolerance and accumulation potentials between Mesembryanthemum crystallinum (halophyte) and Brassica juncea: metal accumulation, nutrient status and photosynthetic activity. J Plant Physiol 171:1634–1644

    Article  CAS  Google Scholar 

  • Anwar S, Khan S, Hussain I, Bashir R, Fahad S (2019) Chelators induced uptake of cadmium and modulation of water relation, antioxidants, and photosynthetic traits of maize. Environ Sci Pollut R 26:17577–17590

    Article  CAS  Google Scholar 

  • Ashraf S, Ali Q, Zahir ZA, Ashraf S, Asghar HN (2019) Phytoremediation: environmentally sustainable way for reclamation of heavy metal polluted soils. Ecotox Environ Saf 174:714–727

    Article  CAS  Google Scholar 

  • Bauddh K, Singh RP (2015) Assessment of metal uptake capacity of castor bean and mustard for phytoremediation of nickel from contaminated soil. Bioremediation J 19:124–138

    Article  CAS  Google Scholar 

  • Bhagawatilal J, Anubha S (2013) Optimization of chelators to enhance uranium uptake from tailings for phytoremediation. Chemosphere 91:692–696

    Article  CAS  Google Scholar 

  • Bian XG, Cui J, Tang BP, Yang L (2018) Chelant-induced phytoextraction of heavy metals from contaminated soils: a review. Pol J Environ Stud 27:2417–2424

    Article  CAS  Google Scholar 

  • Chen J, Liu YQ, Yan XW, Wei GH, Zhang JH, Fang LC (2018) Rhizobium inoculation enhances copper tolerance by affecting copper uptake and regulating the ascorbate-glutathione cycle and phytochelatin biosynthesis-related gene expression in Medicago sativa seedlings. Ecotoxicol Environ Saf 162:312–323

    Article  CAS  Google Scholar 

  • Chen L, Wang D, Zeng C, Long C (2019) Improving cobalt phytoextraction by Astragalus Sinicus L. grown in co-contaminated soils using biodegradable chelators. Soil Sediment Contam 28:461–472

    Article  CAS  Google Scholar 

  • Chen L, Long C, Wang D, Yang J (2020) Phytoremediation of cadmium (Cd) and uranium (U) contaminated soils by Brassica juncea L. enhanced with exogenous application of plant growth regulators. Chemosphere 242:125112

    Article  CAS  Google Scholar 

  • Choppala G, Saifullah BN, Bibi S, Iqbal M, Rengel Z, Kunhikrishnan A, Ashwath N, Ok YS (2014) Cellular mechanisms in higher plants governing tolerance to cadmium toxicity. Crit Rev Plant Sci 33:374–391

    Article  CAS  Google Scholar 

  • Duan C, Fang L, Yang C, Chen W, Cui Y, Li S (2018) Reveal the response of enzyme activities to heavy metals through in situ zymography. Ecotoxicol Environ Saf 156:106–115

    Article  CAS  Google Scholar 

  • Elrashidi MA, Seybold CA, Wysocki DA (2015) Effects of annual precipitation on heavy metals in runoff from soils in the US Great Plains. Water Air Soil Pollut 226:417

    Article  CAS  Google Scholar 

  • Evangelou MWH, Ebel M, Schaeffer A (2007) Chelate assisted phytoextraction of heavy metals from soil. Effect, mechanism, toxicity, and fate of chelating agents. Chemosphere 68:989–1003

    Article  CAS  Google Scholar 

  • Fabbricino M, Ferraro A, Del Giudice G, Antonio L (2013) Current views on EDDS use for ex situ washing of potentially toxic metal contaminated soils. Rev Environ Sci Biotechnol 12:391–398

    Article  CAS  Google Scholar 

  • Fang L, Wang M, Cai L, Cang L (2017) Deciphering biodegradable chelant-enhanced phytoremediation through microbes and nitrogen transformation in contaminated soils. Environ Sci Pollut R 24:14627–14636

    Article  CAS  Google Scholar 

  • Fang L, Ju W, Yang C, Duan C, Cui Y, Han F, Shen G, Zhang C (2019) Application of signaling molecules in reducing metal accumulation in alfalfa and alleviating metal-induced phytotoxicity in Pb/Cd-contaminated soil. Ecotoxicol Environ Saf 182:109459

    Article  CAS  Google Scholar 

  • Farooq MA, Niazi AK, Akhtar J, Saifullah FM, Souri Z, Karimi N, Rengel Z (2019) Acquiring control: the evolution of ROS-induced oxidative stress and redox signaling pathways in plant stress responses. Plant Physiol Biochem 141:353–369

    Article  CAS  Google Scholar 

  • Ferraz P, Fidalgo F, Almeida A, Teixeira J (2012) Phytostabilization of nickel by the zinc and cadmium hyperaccumulator Solanum nigrum L. Are metallothioneins involved? Plant Physiol Biochem 57:254–260

    Article  CAS  Google Scholar 

  • Gad N (2006) Increasing the efficiency of nitrogen fertilization through cobalt application to pea plant. Res J Agric Biol Sci 2:433–442

    Google Scholar 

  • Gad N, Kandil H (2010) Influence of cobalt on phosphorus uptake, growth and yield of tomato. Agric Biol J N Am 1:1069–1075

    Article  CAS  Google Scholar 

  • González Á, García-Gonzalo P, Gil-Díaz MM, Alonso J, Lobo MC (2019) Compost-assisted phytoremediation of As-polluted soil. J Soils Sediments 19:2971–2983

    Article  CAS  Google Scholar 

  • Guo B, Liu C, Liang Y, Li N, Fu Q (2019) Salicylic acid signals plant defence against cadmium toxicity. Int J Mol Sci 20:2960

    Article  CAS  Google Scholar 

  • Hu X, Liu X, Zhang X, Cao L, Chen J, Yu H (2017) Increased accumulation of Pb and Cd from contaminated soil with Scirpus triqueter by the combined application of NTA and APG. Chemosphere 188:397–402

    Article  CAS  Google Scholar 

  • Jahani M, Khavari-Nejad RA, Mahmoodzadeh H, Saadatmand S (2019) Effects of foliar application of cobalt oxide nanoparticles on growth, photosynthetic pigments, oxidative indicators, non-enzymatic antioxidants and compatible osmolytes in canola (Brassica napus L.). Acta Biol Cracov Ser Bot 61:29–42

    CAS  Google Scholar 

  • Jiang M, Liu S, Li Y, Li X, Luo Z, Song H, Chen Q (2019) EDTA-facilitated toxic tolerance, absorption and translocation and phytoremediation of lead by dwarf bamboos. Ecotox Environ Safe 170:502–512

    Article  CAS  Google Scholar 

  • Ju W, Liu L, Fang L, Cui Y, Duan C, Wu H (2019) Impact of co-inoculation with plant-growth-promoting rhizobacteria and rhizobium on the biochemical responses of alfalfa-soil system in copper contaminated soil. Ecotoxicol Environ Saf 167:218–226

    Article  CAS  Google Scholar 

  • Kim GN, Lee SS, Shon DB, Lee KW, Chung US (2010) Development of pilot-scale electrokinetic remediation technology to remove 60Co and 137Cs from soil. J Ind Eng Chem 16:986–991

    Article  CAS  Google Scholar 

  • Ko CH, Chang FC, Wang YN, Chung CY (2014) Extraction of heavy metals from contaminated soil by two Amaranthus spp. Clean Soil Air Water 42:635–640

    Article  CAS  Google Scholar 

  • Kosiorek M, Wyszkowski M (2019) Remediation of cobalt-polluted soil after application of selected substances and using oat (Avena sativa L.). Environ Sci Pollut R 26:16762–16780

    Article  CAS  Google Scholar 

  • Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323–330

    Article  CAS  Google Scholar 

  • Li HF, Gray C, Mico C, Zhao FJ, Mcgrath SP (2009) Phytotoxicity and bioavailability of cobalt to plants in a range of soils. Chemosphere 75:979–986

    Article  CAS  Google Scholar 

  • Li Z, Zhang R, Zhang H (2018) Effects of plant growth regulators (DA-6 and 6-BA) and EDDS chelator on phytoextraction and detoxification of cadmium by Amaranthus hybridus Linn. Int J Phytoremediat 20:1121–1128

    Article  CAS  Google Scholar 

  • Liang Y, Wang X, Guo Z, Xiao X, Peng C, Yang J, Zhou C, Zeng P (2019) Chelator-assisted phytoextraction of arsenic, cadmium and lead by Pteris vittata L. and soil microbial community structure response. Int J Phytoremediat 21:1–9

    Article  CAS  Google Scholar 

  • Liu S, Yang R, Tripathi DK, Li X, He W, Wu M, Ali S, Ma MD, Cheng QS, Pan YZ (2018) The interplay between reactive oxygen and nitrogen species contributes in the regulatory mechanism of the nitro-oxidative stress induced by cadmium in Arabidopsis. J Hazard Mater 344:1007–1024

    Article  CAS  Google Scholar 

  • Mahdavian K, Ghaderian SM, Torkzadeh M (2017) Accumulation and phytoremediation of Pb, Zn, and Ag by plants growing on Koshk lead–zinc mining area, Iran. J Soils Sediments 17:1310–1320

    Article  CAS  Google Scholar 

  • Michael WE, Mathias E, Andreas S (2007) Chelate assisted phytoextraction of heavy metals from soil. Effect, mechanism, toxicity, and fate of chelating agents. Chemosphere 68:989–1003

    Article  CAS  Google Scholar 

  • Mohtadi A, Ghaderian SM, Schat H (2013) The effect of EDDS and citrate on the uptake of lead in hydroponically grown Matthiola flavida. Chemosphere 93:986–989

    Article  CAS  Google Scholar 

  • Moslehi A, Feizian M, Higueras P, Eisvand HR (2019) Assessment of EDDS and vermicompost for the phytoextraction of Cd and Pb by sunflower (Helianthus annuus L.). Int J Phytoremediat 21:191–199

    Article  CAS  Google Scholar 

  • Nörtemann B (2005) Biodegradation of chelating agents: EDTA, DTPA, PDTA, NTA, and EDDS. In: Nowack B, VanBriesen JM (eds) Biogeochemistry of Chelating Agents, vol 910. American Chemical Society, Washington, D.C., pp 150–170

    Chapter  Google Scholar 

  • Pandey SK, Bhattacharya T (2018) Effect of two biodegradable chelates on metals uptake, translocation and biochemical changes of Lantana Camara growing in fly ash amended soil. Int J Phytoremediat 20:214–224

    Article  CAS  Google Scholar 

  • Pilon-Smits EA, Quinn CF, Tapken W, Malagoli M, Schiavon M (2009) Physiological functions of beneficial elements. Curr Opin Plant Biol 12:267–274

    Article  CAS  Google Scholar 

  • Rehman MZ, Rizwan M, Ali S, Ok YS, Ishaque W, Saifullah NMF, Akmal F, Waqar M (2017) Remediation of heavy metal contaminated soils by using Solanum nigrum: a review. Ecotox Environ Safe 143:236–248

    Article  CAS  Google Scholar 

  • Riedel T, Hennessy P, Iden SC, Koschinsky A (2015) Leaching of soil-derived major and trace elements in an arable topsoil after the addition of biochar. Eur J Soil Sci 66:823–834

    Article  CAS  Google Scholar 

  • Robinson BH, Anderson CWN, Dickinson NM (2015) Phytoextraction: where’s the action? Geochem Explor 151:34–40

    Article  CAS  Google Scholar 

  • Selvakumara R, Ramadossa G, Menona M, Rajendrana K, Thavamanib P, Naidub R, Megharaj M (2018) Challenges and complexities in remediation of uranium contaminated soils: a review. J Envion Radioact 18:1–10

    Google Scholar 

  • Sidhu GPS, Bali AS, Singh HP, Batish DR, Kohli RK (2018) Ethylenediamine disuccinic acid enhanced phytoextraction of nickel from contaminated soils using Coronopus didymus (L.) Sm. Chemosphere 205:234–243

    Article  CAS  Google Scholar 

  • Sillanpa MET, Kurniawan TA, Lo WH (2011) Degradation of chelating agents in aqueous solution using advanced oxidation process (AOP). Chemosphere 83:1443–1460

    Article  CAS  Google Scholar 

  • Smičiklas I, Dimović S, Jović M, Milenković A, Šljivić-Ivanović M (2015) Evaluation study of cobalt(II) and strontium(II) sorption–desorption behavior for selection of soil remediation technology. Int J Environ Sci Technol 12:3853–3862

    Article  CAS  Google Scholar 

  • Song Y, Ammami MT, Benamar A, Mezazigh S, Wang H (2016) Effect of EDTA, EDDS, NTA and citric acid on electrokinetic remediation of As, Cd, Cr, Cu, Ni, Pb and Zn contaminated dredged marine sediment. Environ Sci Pollut R 23:10577–10586

    Article  CAS  Google Scholar 

  • Tandy S, Schulin R, Nowack B (2006) Uptake of metals during chelant-assisted phytoextraction with EDDS related to the solubilized metal concentration. Environ Sci Technol 40:2753–2758

    Article  CAS  Google Scholar 

  • Tsang DC, Yip TC, Lo IM (2009) Kinetic interactions of EDDS with soils. 2. Metal-EDDS complexes in uncontaminated and metal contaminated soils. Environ Sci Technol 43:837–842

    Article  CAS  Google Scholar 

  • Tsang D, Lo I, Surampalli RY (2012) Chelating agents for land decontamination technologies. Am Soc Civil Eng:198–209

  • Vandevivere PC, Saveyn H, Verstraete W, Feijte TC, Schowanek DR (2001) Biodegradation of metal-[S,S]-EDDS complexes. Environ Sci Technol 35:1765–1770

    Article  CAS  Google Scholar 

  • Wa Lwalaba JL, Zvogbo G, Mulembo M, Mundende M, Zhang G (2017) The effect of cobalt stress on growth and physiological traits and its association with cobalt accumulation in barley genotypes differing in cobalt tolerance. J Plant Nutr 40:2192–2199

    Article  CAS  Google Scholar 

  • Wang YD, Cui AX, An HX, Guo XL, Feng WD, Yang WB, Guo XB (2017) Removal of cobalt in simulated wastewater from nuclear power plant by complexation enhanced adsorption process. Atom Energ Sci Technol 51:404–410

    Google Scholar 

  • Wu M, Luo Q, Zhao Y, Long Y, Liu S, Pan Y (2017) Physiological and biochemical mechanisms preventing Cd toxicity in the new hyperaccumulator Abelmoschus manihot. J Plant Growth Regul 37:709–718

    Article  CAS  Google Scholar 

  • Yan X, Luo X (2015) Radionuclides distribution, properties, and microbial diversity of soils in uranium mill tailings from southeastern China. J Environ Radioact 139:85–90

    Article  CAS  Google Scholar 

  • Ye M, Guo H, Xiong R, Yu Q (2018) A double-scale and adaptive particle filter-based online parameter and state of charge estimation method for lithium-ion batteries. Energy 144:789–799

    Article  Google Scholar 

  • Zhang T, Liu JM, Huang XF, Bing X, Sub CY, Luo GF, Xu YW, Wu YX, Mao ZW, Qiu RL (2013) Chelant extraction of heavy metals from contaminated soils using new selective EDTA derivatives. J Hazard Mater 262:464–471

    Article  CAS  Google Scholar 

  • Zhang HZ, Guo QJ, Yang JX, Ma J, Chen G, Chen TB, Zhu GX, Wang J, Zhang GX, Wang X, Shao CY (2016) Comparison of chelates for enhancing Ricinus communis L. phytoremediation of Cd and Pb contaminated soil. Ecotoxicol Environ Saf 133:57–62

    Article  CAS  Google Scholar 

  • Zhao SL, Lian F, Duo L (2011) EDTA-assisted phytoextraction of heavy metals by turfgrass from municipal solid waste compost using permeable barriers and associated potential leaching risk. Bioresour Technol 102:621–626

    Article  CAS  Google Scholar 

  • Zhu C, Ma Y, Zang W, Guan C, Liu X, Pennycook SJ, Wang J, Huang W (2019) Conformal dispersed cobalt nanoparticles in hollow carbon nanotube arrays for flexible Zn-air and Al-air batteries. Chem Eng J 369:988–995

    Article  CAS  Google Scholar 

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Funding

The study was funded by the Sichuan Science and Technology Program, China (No. 2018HH0137).

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Authors and Affiliations

  1. College of Life Science and Engineering, Southwest University of Science and Technology, Mianyang, 621010, China

    Li Chen, Chao Zeng & Dan Wang

  2. College of Architecture and Environment, Sichuan University, Chengdu, 610065, China

    Li Chen & Jin-yan Yang

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  1. Li Chen
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  2. Chao Zeng
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  3. Dan Wang
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Correspondence to Dan Wang.

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Chen, L., Zeng, C., Wang, D. et al. Phytoextraction of cobalt (Co)-contaminated soils by sweet alyssum (Lobularia maritima (L.) Desv.) is enhanced by biodegradable chelating agents. J Soils Sediments 20, 1931–1942 (2020). https://doi.org/10.1007/s11368-020-02592-5

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