Skip to main content
SpringerLink
Log in

Effect of pH and citric acid on the growth, arsenic accumulation, and phytochelatin synthesis in Eupatorium cannabinum L., a promising plant for phytostabilization

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Heavy-metal contamination of soils has increased in the last decades due to anthropogenic and industrial activities. Arsenic is one of the pollutants that is commonly found in industrial soils and is toxic for both plants and humans. The pH of the soil or the culture medium is one of the most important factors that interferes with the bioavailability of this metalloid to the plant. The addition of chelating agents, such as citric acid (CA), can increase the absorption of As by plants. Therefore, the objective of this work is to study the effect of the pH and the exogenous addition of citric acid on the growth, As accumulation, and thiol compounds in Eupatorium cannabinum; this plant grows naturally in contaminated soils in Asturias, Spain, and has a potential use in phytoremediation. The results showed that E. cannabinum was able to tolerate As stress even at extreme pH values and accumulated a high amounts of As in its roots, which makes it a promising species for the phytostabilization of soils polluted with this metalloid. An addition of 20 mg CA L−1 led to increased biomass and As accumulation at acidic pH. In order to determine if thiolic compounds, such as phytochelatins, are involved in As accumulation and detoxification in E. cannabinum, we analyzed the synthesis of these compounds in the presence and absence of As and/or citric acid. Our results suggest that these thiolic compounds play a major role in As detoxification, since the presence of CA as a chelating agent reduced the amount of thiols necessary to cope with the toxicity caused by As.

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

Similar content being viewed by others

References

  • Abioye OP (2011) Biological remediation of hydrocarbon and heavy metals contaminated soil. In: Pascucci S (ed) Soil contamination. InTech, Rijeka, pp 127–142

    Google Scholar 

  • Afshan S, Ali S, Bharwana SA, Rizwan M, Farid M, Abbas F, Ibrahim M, Medmood MA, Abbasi GH (2015) Citric acid enhances the phytoextraction of chromium, plant growth, and photosynthesis by alleviating the oxidative damages in Brassica napus L. Environ Sci Pollut Res 22(15):11679–11689

    Article  CAS  Google Scholar 

  • Akhter MF, McGarvey B, Macfie SM (2012) Reduced translocation of cadmium from roots is associated with increased production of phytochelatins and their precursors. J Plant Physiol 169(18):1821–1829

    Article  CAS  Google Scholar 

  • Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals: concepts and applications. Chemosphere 91(7):869–881

    Article  CAS  Google Scholar 

  • Almaroai YA, Usman AR, 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.). Appl Environ Soil Sci 177(11):655–663

    Article  CAS  Google Scholar 

  • Almaroai YA, Usman AR, Ahmad M, Kim KR, Vithanage M, Ok YS (2013) Role of chelating agents on release kinetics of metals and their uptake by maize from chromated copper arsenate-contaminated soil. Envirotech 34(6):747–755

    CAS  Google Scholar 

  • Andra SS, Datta R, Sarkar D, Saminathan SKM, Mullens CP, Bach SBH (2009) Analysis of phytochelatin complexes in the lead tolerant vetiver grass [Vetiveria zizanioides (L.)] using liquid chromatography and mass spectrometry. Environ Pollut 157:2173–2183

    Article  CAS  Google Scholar 

  • Anjum NA, Hasanuzzaman M, Hossain MA, Thangavel P, Roychoudhury A, Gill SS, Rodrigo MAM, Adam V, Fujita M, Kizek R, Duarte AC, Pereira E, Ahmad I (2015) Jacks of metal/metalloid chelation trade in plants—an overview. Front Plant Sci 6:192

    Google Scholar 

  • Anwer S, Yasin Ashraf M, Hussain M, Ashraf M, Jamil A (2012) Citric acid mediated phytoextraction of cadmium by maize (Zea mays L.). Pak J Bot 44(6):1831–1836

    CAS  Google Scholar 

  • Benavides MP, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17(1):21–34

    Article  CAS  Google Scholar 

  • Chen YX, Lin Q, Luo YM, He YF, Zhen SJ, Yu YL, Tian GM, Wong MH (2003) The role of citric acid on the phytoremediation of heavy metal contaminated soil. Chemosphere 50(6):807–811

    Article  CAS  Google Scholar 

  • Chen A, Komives EA, Schroeder JI (2006) An improved grafting technique for mature Arabidopsis plants demonstrates long-distance shoot-to-root transport of phytochelatins in Arabidopsis. Plant Physiol 141(1):108–120

    Article  CAS  Google Scholar 

  • Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88(11):1707–1719

    Article  CAS  Google Scholar 

  • Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53(1):159–182

    Article  CAS  Google Scholar 

  • Duarte B, Delgado M, Caçador I (2007) The role of citric acid in cadmium and nickel uptake and translocation, in Halimione portulacoides. Chemosphere 69(5):836–840

    Article  CAS  Google Scholar 

  • Ehsan S, Ali S, Noureen S, Mahmood K, Farid M, Ishaque W, Shakoor MB, Rizwan M (2014) Citric acid assisted phytoremediation of cadmium by Brassica napus L. Ecotoxicol Environ Saf 106:164–172

    Article  CAS  Google Scholar 

  • Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82(1):70–77

    Article  CAS  Google Scholar 

  • Evangelou MW, Ebel M, Schaeffer A (2007) Chelate assisted phytoextraction of heavy metals from soil. Effect, mechanism, toxicity, and fate of chelating agents. Chemosphere 68(6):989–1003

    Article  CAS  Google Scholar 

  • Farid M, Ali S, Rizwan M, Ali Q, Abbas F, Bukhari SAH, Saeed R, Wu L (2017) Citric acid assisted phytoextraction of chromium by sunflower; morpho-physiological and biochemical alterations in plants. Ecotoxicol Environ Saf 145:90–102

    Article  CAS  Google Scholar 

  • Farid M, Ali S, Zubair M, Saeed R, Rizwan M, Sallah-Ud-Din R, Azan A, Ashraf R, Ashraf W (2018) Glutamic acid assisted phyto-management of silver-contaminated soils through sunflower; physiological and biochemical response. Environ Sci Pollut Res 25(25):25390–25400

    Article  CAS  Google Scholar 

  • Farooq MA, Li L, Ali B, Gill RA, Wang J, Ali S, Gill MB, Zhou W (2015) Oxidative injury and antioxidant enzymes regulation in arsenic-exposed seedlings of four Brassica napus L. cultivars. Environ Sci Pollut Res 22(14):10699–10712

    Article  CAS  Google Scholar 

  • Fernández R, Bertrand A, Casares A, García R, González A, Tamés RS (2008) Cadmium accumulation and its effect on the in vitro growth of woody fleabane and mycorrhized white birch. Environ Pollut 152(3):522–529

    Article  CAS  Google Scholar 

  • Fernández R, Carballo I, Nava H, Sánchez-Tamés R, Bertrand A, González A (2011) Looking for native hyperaccumulator species useful in phytoremediation. In: Golubevia (ed) Handbook of phytoremediation. Nova Science Publisher, New York, pp 297–330

    Google Scholar 

  • Fernández R, Bertrand A, García JI, Tamés RS, González A (2012) Lead accumulation and synthesis of non-protein thiolic peptides in selected clones of Melilotus alba and Melilotus officinalis. Environ Exp Bot 78:18–24

    Article  CAS  Google Scholar 

  • Fernández R, Fernández-Fuego D, Bertrand A, González A (2014a) Strategies for Cd accumulation in Dittrichia viscosa (L.) Greuter: role of the cell wall, non-protein thiols and organic acids. Plant Physiol Biochem 78:63–70

    Article  CAS  Google Scholar 

  • Fernández R, Fernández-Fuego D, Rodríguez-González P, Alonso JG, Bertrand A, González A (2014b) Cd-induced phytochelatin synthesis in Dittrichia viscosa (L.) Greuter is determined by the dilution of the culture medium. Environ Sci Pollut Res 21(2):1133–1145

    Article  CAS  Google Scholar 

  • Fernández-Fuego D, Bertrand A, González A (2017) Metal accumulation and detoxification mechanisms in mycorrhizal Betula pubescens. Environ Pollut 231:1153–1162

    Article  CAS  Google Scholar 

  • Finnegan P, Chen W (2012) Arsenic toxicity: the effects on plant metabolism. Front Physiol 3:182

    Article  CAS  Google Scholar 

  • Francesconi K, Visoottiviseth P, Sridokchan W, Goessler W (2002) Arsenic species in an arsenic hyperaccumulating fern, Pityrogramma calomelanos: a potential phytoremediator of arsenic-contaminated soils. Sci Total Environ 284(1):27–35

    Article  CAS  Google Scholar 

  • Gaber SE, Rizk MS, Yehia MM (2011) Extraction of certain heavy metals from sewage sludge using different types of acids. Biokemistri 23(1):41–48

    Google Scholar 

  • Gallego JR, Rodríguez-Valdés E, Esquinas N, Fernández-Braña A, Afif E (2016) Insights into a 20-ha multi-contaminated brownfield megasite: an environmental forensics approach. Sci Total Environ 563:683–692

    Article  CAS  Google Scholar 

  • Gogoi P, Adhikari P, Maji TK (2017) Bioremediation of arsenic from water with citric acid cross-linked water hyacinth (E. crassipes) root powder. Environ Monit Assess 189(8):383

    Article  CAS  Google Scholar 

  • Gupta M, Sharma P, Sarin NB, Sinha AK (2009) Differential response of arsenic stress in two varieties of Brassica juncea L. Chemosphere 74(9):1201–1208

    Article  CAS  Google Scholar 

  • Gupta DK, Huang HG, Yang XE, Razafindrabe BHN, Inouhe M (2010) The detoxification of lead in Sedum alfredii H. is not related to phytochelatins but the glutathione. J Hazard Mat 177:437–444

    Article  CAS  Google Scholar 

  • Gusmão R, Ariño C, Díaz-Cruz JM, Esteban M (2010) Electrochemical survey of the chain length influence in phytochelatins competitive binding by cadmium. Anal Biochem 406(1):61–69

    Article  CAS  Google Scholar 

  • Harada E, Yamaguchi Y, Koizumi N, Hiroshi S (2002) Cadmium stress induces production of thiol compounds and transcripts for enzymes involved in sulfur assimilation pathways in Arabidopsis. J Plant Physiol 159(4):445–448

    Article  CAS  Google Scholar 

  • Hernández LE, Sobrino-Plata J, Montero-Palmero MB, Carrasco-Gil S, Flores-Cáceres ML, Ortega-Villasante C, Escobar C (2015) Contribution of glutathione to the control of cellular redox homeostasis under toxic metal and metalloid stress. J Exp Bot 66(10):2901–2911

    Article  CAS  Google Scholar 

  • Kabata-Pendias A (2010) Trace elements in soils and plants, 4ª edn. CRC press, Florida

    Book  Google Scholar 

  • Kühnlenz T, Westphal L, Schmidt H, Scheel D, Clemens S (2015) Expression of Caenorhabditis elegans PCS in the AtPCS1-deficient Arabidopsis thaliana cad1-3 mutant separates the metal tolerance and non-host resistance functions of phytochelatin synthases. Plant Cell Environ 38(11):2239–2247

    Article  CAS  Google Scholar 

  • Kwak JH, Park K, Chang PC, Liu W, Kim JY, Kim KW (2013) Influence of phosphate and citric acid on the phytoextraction of As from contaminated soils. Int J Environ Waste 11(1):1–12

    Article  CAS  Google Scholar 

  • Liang L, Liu W, Sun Y, Huo X, Li S, Zhou Q (2016) Phytoremediation of heavy metal contaminated saline soils using halophytes: current progress and future perspectives. Environ Rev 25(3):269–281

    Article  CAS  Google Scholar 

  • Liu CC, Lin YC (2013) Reclamation of copper-contaminated soil using EDTA or citric acid coupled with dissolved organic matter solution extracted from distillery sludge. Environ Pollut 178:97–101

    Article  CAS  Google Scholar 

  • McGrath SP, Zhao FJ, Lombi (2001) Plant and rhizosphere processes involved in phytoremediation of metal-contaminated soils. Plant Soil 232(1-2):207–214

    Article  CAS  Google Scholar 

  • Mesa V, Navazas A, González-Gil R, González A, Weyens N, Lauga B, Gallego JL, Sánchez J, Peláez AI (2017) Use of endophytic and rhizosphere bacteria to improve phytoremediation of arsenic-contaminated industrial soils by autochthonous Betula celtiberica. Appl Environ Microbiol 83(8):03411–03416

    Article  Google Scholar 

  • Mishra S, Srivastava S, Tripathi RD, Trivedi PK (2008) Thiol metabolism and antioxidant systems complement each other during arsenate detoxification in Ceratophyllum demersum L. Aquat Toxicol 86(2):205–215

    Article  CAS  Google Scholar 

  • Montaser A (1998) Inductively coupled plasma mass spectrometry. John Wiley-VCH, New York

    Google Scholar 

  • Moreno-Jimenez E, Vazquez S, Carpena-Ruiz RO, Esteban E, Penalosa JM (2011) Using Mediterranean shrubs for the phytoremediation of a soil impacted by pyritic wastes in Southern Spain: a field experiment. J Environ Manage 92(6):1584–1590

    Article  Google Scholar 

  • Mubarak H, Mirza N, Chai LY, Yang ZH, Yong W, Tang CJ, Mahmood Q, Pervez A, Farooq U, Fahad S, Nasim W, Siddique KHM (2016) Biochemical and Metabolic Changes in Arsenic Contaminated Boehmeria nivea L. Biomed Res Int 2016 ID 1423828:1–8

    Article  CAS  Google Scholar 

  • Muhammad D, Chen F, Zhao J, Zhang G, Wu F (2009) Comparison of EDTA-and citric acid-enhanced phytoextraction of heavy metals in artificially metal contaminated soil by Typha angustifolia. Int J Phytoremediation 11(6):558–574

    Article  CAS  Google Scholar 

  • Mumthas S, Chidambaram AA, Sundaramoorthy P, Ganesh KS (2010) Effect of arsenic and manganese on root growth and cell division in root tip cells of green gram (Vigna radiata L.). Emir J Food Agric 22(4):285–297

    Article  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15(3):473–497

    Article  CAS  Google Scholar 

  • Mykolenko S, Liedienov V, Kharytonov M, Makieieva N, Kuliush T, Queralt I, Marguí E, Hidalgo M, Pardini G, Gispert M (2018) Presence, mobility and bioavailability of toxic metal (oids) in soil, vegetation and water around a Pb-Sb recycling factory (Barcelona, Spain). Environ Pollut 237:569–580

    Article  CAS  Google Scholar 

  • Najeeb U, Jilani G, Ali S, Sarwar M, Xu LZW (2011) Insights into cadmium induced physiological and ultra-structural disorders in Juncus effusus L. and its remediation through exogenous citric acid. J Hazard Mater 186(1):565–574

    Article  CAS  Google Scholar 

  • Ordóñez A, Álvarez R, Loredo J (2013) Asturian mercury mining district (Spain) and the environment: a review. Environ Sci Pollut Res 20(11):7490–7508

    Article  CAS  Google Scholar 

  • Otones V, Álvarez-Ayuso E, García-Sánchez A, Santa Regina I, Murciego A (2011) Mobility and phytoavailability of arsenic in an abandoned mining area. Geoderma 166(1):153–161

    Article  CAS  Google Scholar 

  • Oven M, Grill E, Golan-Goldhirsh A, Kutchan TM, Zenk MH (2002) Increase of free cysteine and citric acid in plant cells exposed to cobalt ions. Phytochem 60(5):467–474

    Article  CAS  Google Scholar 

  • Pérez-Sirvent C, Martínez-Sánchez MJ, Martínez-López S, Bech J, Bolan N (2012) Distribution and bioaccumulation of arsenic and antimony in Dittrichia viscosa growing in mining-affected semiarid soils in southeast Spain. J Geochem Explor 123:128–135

    Article  CAS  Google Scholar 

  • Piechalak A, Tomaszewska B, Baralkiewicz D, Malecka A (2002) Accumulation and detoxification of lead ions in legumes. Phytochem 60:153–162

    Article  CAS  Google Scholar 

  • Pistelli L, D’Angiolillo F, Morelli E, Basso B, Rosellini I, Posarelli M, Barbafieri M (2017) Response of spontaneous plants from an ex-mining site of Elba island (Tuscany, Italy) to metal (loid) contamination. Environ Sci Pollut Res 24(8):7809–7820

    Article  CAS  Google Scholar 

  • Shakoor MB, Ali S, Hameed A, Farid M, Hussain S, Yasmeen T, Najeeb U, Bharwana SA, Abbasi GH (2014) Citric acid improves lead (Pb) phytoextraction in Brassica napus L. by mitigating Pb-induced morphological and biochemical damages. Ecotoxicol Environ Saf 109:38–47

    Article  CAS  Google Scholar 

  • Shri M, Kumar S, Chakrabarty D, Trivedi PK, Mallick S, Misra P, Shukla D, Mishra S, Srisvastaba S, Tripathi RD, Tuli R (2009) Effect of arsenic on growth, oxidative stress, and antioxidant system in rice seedlings. Ecotoxicol Environ Saf 72(4):1102–1110

    Article  CAS  Google Scholar 

  • Shukla D, Trivedi PK, Nath P, Tuteja N (2016) Metallothioneins and phytochelatins: role and perspectives in heavy metal(loid)s stress tolerance in crop plants. In: Tuteja N, Gill S (eds) Abiotic stress response in plants, 1st edn. Wiley-VCH, Weinheim, pp 237–264

    Chapter  Google Scholar 

  • Stoeva N, Berova M, Zlatev Z (2005) Effect of arsenic on some physiological parameters in bean plants. Biol plant 49(2):293–296

    Article  CAS  Google Scholar 

  • Suanon F, Sun Q, Dimon B, Mama D, Yu CP (2016) Heavy metal removal from sludge with organic chelators: comparative study of N, N-bis (carboxymethyl) glutamic acid and citric acid. J Environ Manage 166:341–347

    Article  CAS  Google Scholar 

  • Tripathi RD, Srivastava S, Mishra S, Singh N, Tuli R, Gupta DK, Maathuis FJ (2007) Arsenic hazards: strategies for tolerance and remediation by plants. Trends Biotechnol 25(4):158–165

    Article  CAS  Google Scholar 

  • Van der Ent A, Baker AJ, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362(1-2):319–334

    Article  CAS  Google Scholar 

  • Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12(3):364–372

    Article  CAS  Google Scholar 

  • Vurro E, Ruotolo R, Ottonello S, Elviri L, Maffini M, Falasca G, Zanella L, Altamira MM, di Toppi LS (2011) Phytochelatins govern zinc/copper homeostasis and cadmium detoxification in Cuscuta campestris parasitizing Daucus carota. Environ Exp Bot 72(1):26–33

    Article  CAS  Google Scholar 

  • White PJ, Brown PH (2010) Plant nutrition for sustainable development and global health. Ann Bot 105(7):1073–1080

    Article  CAS  Google Scholar 

  • Wuana RA, Okieimen FE, Imborvungu JA (2010) Removal of heavy metals from a contaminated soil using organic chelating acids. Int J Environ Sci Technol 7(3):485–496

    Article  CAS  Google Scholar 

  • Xu XY, McGrath SP, Zhao FJ (2007) Rapid reduction of arsenate in the medium mediated by plant roots. New Phytol 176(3):590–599

    Article  CAS  Google Scholar 

  • Zagorchev L, Seal CE, Kranner I, Odjakova M (2013) A central role for thiols in plant tolerance to abiotic stress. Int J Mol Sci 14(4):7405–7432

    Article  CAS  Google Scholar 

  • Zaheer IE, Ali S, Rizwan M, Farid M, Shakoor MB, Gill RA, Najeeb U, Iqbal N, Ahmad R (2015) Citric acid assisted phytoremediation of copper by Brassica napus L. Ecotoxicol Environ Saf 120:310–317

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the project LIFE 11 ENV/ES/547. Fernández-Fuego D. was funded by fellowship Foundation for the promotion of Applied Scientific Research and Technology (FICYT).

Author information

Authors and Affiliations

  1. Departamento de Biología de Organismos y Sistemas, Facultad de Biología, Universidad de Oviedo, C/ Catedrático Rodrigo Uría s/n, 33071, Oviedo, Spain

    Héctor González, Daniel Fernández-Fuego, Ana Bertrand & Aída González

  2. Instituto Universitario de Biotecnología de Asturias, Oviedo, Spain

    Daniel Fernández-Fuego, Ana Bertrand & Aída González

Authors
  1. Héctor González
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel Fernández-Fuego
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ana Bertrand
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Aída González
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aída González.

Additional information

Responsible editor: Elena Maestri

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

González, H., Fernández-Fuego, D., Bertrand, A. et al. Effect of pH and citric acid on the growth, arsenic accumulation, and phytochelatin synthesis in Eupatorium cannabinum L., a promising plant for phytostabilization. Environ Sci Pollut Res 26, 26242–26253 (2019). https://doi.org/10.1007/s11356-019-05657-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-05657-2

Keywords

Search

Navigation