Skip to main content

Advertisement

SpringerLink
Log in

Accumulation of arsenic, lead, copper, and zinc, and synthesis of phytochelatins by indigenous plants of a mining impacted area

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

Abstract

Several native plants, able to grow in an unconfined mining impacted area that is now in close vicinity with urban areas, were evaluated for their ability to accumulate heavy metals. The main soil contaminants were As, Pb, Cu, and Zn. Sampling of the rhizospheric metal polluted soil showed that Euphorbia prostrata Aiton, Parthenium incanum Kunth, and Zinnia acerosa (DC.) A. Gray were able to grow in the presence of high amounts of mixtures of these elements. The plants accumulated the metals in the above ground parts and increased the synthesis of thiol molecules. E. prostrata showed the highest capacity for accumulation of the mixture of elements (588 μg g DW−1). Analysis of the thiol-molecules profile showed that these plants synthesized high amounts of long-chain phytochelatins, accompanied by low amounts of monothiol molecules, which may be related to their higher resistance to As and heavy metals. The three plants showed translocation factors from roots to leaves >1 for As, Pb, Cu, and Zn. Thus, by periodically removing aerial parts, these plants could be useful for the phytoremediation of semi-arid and arid mining impacted areas, in which metal hyper-accumulator plants are not able to grow.

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

References

  • Aldrich MV, Gardea-Torresdey JL, Peralta-Videa JR, Parsons JG (2003) Uptake and reduction of Cr(VI) to Cr(III) by mesquite (Prosopis spp.): an X-ray absorption spectroscopic study. Environ Sci Technol 37:1859–1864

    Article  CAS  Google Scholar 

  • Antosiewics DM (1992) Adaptation of plants to an environment polluted with metals. Acta Soc Bot Pol 61:281–299

    Article  Google Scholar 

  • Arnetoli M, Vooijs R, Bookum W, Galardi F, Gonnelli C, Gabbrielli R, Schat H, Verkleij JAC (2008) Arsenate tolerance in Silene paradoxa does not rely on phytochelatin-dependent sequestration. Environ Pollut 152:585–591

    Article  CAS  Google Scholar 

  • Baker AJM (1981) Accumulators and excluders—strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654

    Article  CAS  Google Scholar 

  • Barazani O, Sathiyamoorthy P, Manandhar U, Vulkan R, Golan-Goldhirsh A (2004) Heavy metal accumulation by Nicotiana glauca Graham in a solid waste disposal site. Chemosphere 54:867–872

    Article  CAS  Google Scholar 

  • Barman SC, Sahu RK, Bhargava SK, Chaterjee C (2000) Distribution of heavy metals in wheat, mustard, and weed grown in field irrigated with industrial effluents. Bull Environ Contam Toxicol 64:489–496

    Article  CAS  Google Scholar 

  • Cai Y, Ma LQ (2003) Metal tolerance, accumulation, and detoxification in plants with emphasis on arsenic in terrestrial plants. In: Cai Y, Braids O (eds) Biogeochemistry of environmentally important trace elements. University Press, London, pp 95–114

    Google Scholar 

  • Carrillo-González R, González-Chávez MCA (2006) Metal accumulation in wild plants surrounding mining wastes. Environ Pollut 144:84–92

    Article  Google Scholar 

  • Castro J, Kramar U, Pulchet H (1997) 200 years of mining activities at La Paz/San Luis Potosí/México—consequences for environment and geochemical exploration. J Geochem Explor 58:81–91

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Cobbett CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123:825–832

    Article  CAS  Google Scholar 

  • Delhaize E, Jackson PJ, Lujan LD, Robinson NJ (1989) Poly(y-glutamylcysteinyl)glycine synthesis in Datura innoxia and binding with cadmium. Role in cadmium tolerance. Plant Physiol 89:700–706

    Article  CAS  Google Scholar 

  • Flores-Tavizón E, Alarcón-Herrera MT, González-Elizondo S, Olguín EJ (2003) Arsenic tolerating plants from mine sites and hot springs in the semi-arid region of Chihuahua, Mexico. Acta Biotechnol 23:113–119

    Article  Google Scholar 

  • García-García JD, Rodríguez-Zavala JS, Jasso-Chávez R, Mendoza-Cózat D, Moreno-Sánchez R (2009) Chromium uptake, retention and reduction in photosynthetic Euglena gracilis. Arch Microbiol 191:431–440

    Article  Google Scholar 

  • Gardea-Torresdey JL, Peralta-Videa JR, De la Rosa G, Parsons JG (2005) Phytoremediation of heavy metals and study of the metal coordination by X-ray absorption spectroscopy. Coord Chem Rev 249:1797–1810

    Article  CAS  Google Scholar 

  • González DJ (2006) Riesgo ecológico en la zona minera de Villa de la Paz, San Luis Potosí. Dissertation, Universidad Autónoma de San Luis Potosí

  • Grill E, Winnacker EL, Zenk MH (1987) Phytochelatins, a class of heavy-metal-binding peptides from plants, are functionally analogous to metallothioneins. Proc Natl Acad Sci USA 84:439–443

    Article  CAS  Google Scholar 

  • Gulz PA, Gupta S-K, Schulin R (2005) Arsenic accumulation of common plants from contaminated soils. Plant Soil 272:337–347

    Article  CAS  Google Scholar 

  • Gupta DK, Tripathi RD, Mishra S, Srivastava S, Dwivedi S, Rai UN, Yang XE, Huanj H, Inouhe M (2008) Arsenic accumulation in root and shoot vis-a-vis its effects on growth and level of phytochelatins in seedlings of Cicer arietinum L. J Environ Biol 29:281–286

    CAS  Google Scholar 

  • Gustin JL, Loureiro ME, Kim D, Na G, Tikhonova M, Salt DE (2009) MTP1-dependent Zn sequestration into shoot vacuoles suggests dual roles in Zn tolerance and accumulation in Zn-hyperaccumulating plants. Plant J 57:1116–1127

    Article  CAS  Google Scholar 

  • Haque N, Peralta-Videa JR, Duarte-Gardea M, Gardea-Torresdey JL (2009) Differential effects of metals/metalloids on the growth and element uptake of mesquite plants obtained from plants grown at a copper mining tailing and commercial seeds. Bioresour Technol 100:6177–6182

    Article  CAS  Google Scholar 

  • Haydon MJ, Cobbett CS (2007) Transporters of ligands for essential metal ions in plants. New Phytol 174:499–506

    Article  CAS  Google Scholar 

  • Jamil S, Abhilash PC, Singh N, Sharma PM (2009) Jatropha curcas: a potential crop for phytoremediation of coal fly ash. J Hazard Mater 172:269–275

    Article  CAS  Google Scholar 

  • Jarüp L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182

    Article  Google Scholar 

  • Jasso-Pineda Y, Espinoza-Reyes G, González-Mille D, Razo-Soto I, Carrizales L, Torres-Dosal A, Mejía-Saavedra J, Monroy M, Ize AI, Yarto M, Díaz-Barriga F (2007) An integrated health risk assessment approach to the study of mining sites contaminated with arsenic and lead. Integr Environ Assess Manag 3:344–350

    Article  CAS  Google Scholar 

  • Jomova K, Valko M (2011) Advances in metal-induced oxidative stress and human disease. Toxicology 283:65–87

    Article  CAS  Google Scholar 

  • Kishinami I, Widholm JM (1987) Characterization of Cu and Zn resistant Nicotiana plumbaginifolia suspension cultures. Plant Cell Physiol 28:203–210

    CAS  Google Scholar 

  • Leavitt SW, Dueser RD, Goodell HG (1979) Plant regulation of essential and non-essential heavy metals. J Appl Ecol 16:203–212

    Article  CAS  Google Scholar 

  • LeDuc DL, Tarun AS, Montes-Bayon M, Meija J, Malit MF, Wu CP, AbdelSamie M, Chiang C-Y, Tagmount A, de Souza M, Neuhierl B, Böck A, Caruso J, Terry N (2004) Overexpression of selenocysteine methyltransferase in Arabidopsis and Indian mustard increases selenium tolerance and accumulation. Plant Physiol 135:377–383

    Article  CAS  Google Scholar 

  • Lizama K, Fletcher TD, Sun G (2011) Removal processes for arsenic in constructed wetlands. Chemosphere 84:1032–1043

    Article  Google Scholar 

  • Ma LQ, Komar KM, Tu C, Zhang WH, Cai Y, Kennelley ED (2001) A fern that hyperaccumulates arsenic. A hardy, versatile, fast-growing plant helps to remove arsenic from contaminated soils. Nature 409:579

    Article  CAS  Google Scholar 

  • Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environ Exp Bot 68:1–13

    Article  CAS  Google Scholar 

  • Mejía J, Carrizales L, Rodríguez VM, Jiménez-Capdeville ME, Díaz-Barriga F (1999) Un método para la evaluación de riesgos para la salud en zonas mineras. Salud Pública Méx 41:132–140 (in Spanish)

    Article  Google Scholar 

  • Mendoza-Cózatl D, Moreno-Sánchez R (2005) Cd2+ transport and storage in the chloroplast of Euglena gracilis. Biochim Biophys Acta 1706:88–97

    Article  Google Scholar 

  • Mendoza-Cózatl D, Rangel-González E, Moreno-Sánchez R (2006a) Simultaneous Cd2+, Zn2+ and Pb2+ uptake and accumulation by photosynthetic Euglena gracilis. Arch Environ Contam Toxicol 51:521–528

    Article  Google Scholar 

  • Mendoza-Cózatl D, Rodríguez-Zavala JS, Rodríguez-Enrıquez S, Mendoza-Hernández G, Briones-Gallardo R, Moreno-Sánchez R (2006b) Phytochelatin–cadmium–sulfide high molecular weight complexes of Euglena gracilis. FEBS J 273:5703–5713

    Article  Google Scholar 

  • Mills RF, Francini A, Ferreira da Rocha PS, Baccarini PJ, Aylett M, Krijger GC, Williams LE (2005) The plant P1B-type ATPase AtHMA4 transports Zn and Cd and plays a role in detoxification of transition metals supplied at elevated levels. FEBS Lett 579:783–791

    Article  CAS  Google Scholar 

  • Milner MJ, Kochian LV (2008) Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Ann Bot 102:3–13

    Article  CAS  Google Scholar 

  • Moreno-Jiménez E, Peñalosa JM, Manzano R, Carpena-Ruiz RO, Gamarra R, Esteban E (2009) Heavy metals distribution in soils surrounding an abandoned mine in NW Madrid (Spain) and their transference to wild flora. J Hazard Mater 162:854–859

    Article  Google Scholar 

  • Mueller-Dombois D, Ellengerg H (1974) Aims and methods of vegetation ecology. Wiley, New York

    Google Scholar 

  • Peralta-Videa JR, Lopez ML, Narayan M, Saupe G, Gardea-Torresdey J (2009) The biochemistry of environmental heavy metal uptake by plants: implications for the food chain. Int J Biochem Cell Biol 41:1665–1677

    Article  CAS  Google Scholar 

  • Rauser WE (1999) Structure and function of metal chelators produced by plants. The case for organic acids, amino acids, phytin, and metallothioneins. Cell Biochem Biophys 31:19–48

    Article  CAS  Google Scholar 

  • Razo I, Carrizales L, Castro J, Díaz-Barriga F, Monroy M (2004) Arsenic and heavy metal pollution of soil, water and sediments in a semi-arid climate mining area in México. Water Air Soil Pollut 152:129–152

    Article  CAS  Google Scholar 

  • Reisinger S, Schiavon M, Terry N, Pilon-Smits EA (2008) Heavy metal tolerance and accumulation in Indian mustard (Brassica juncea L.) expressing bacterial gamma-glutamylcysteine synthetase or glutathione synthetase. Int J Phytoremediation 10:440–454

    Article  CAS  Google Scholar 

  • Rodríguez VM, Dufour L, Carrizales L, Díaz-Barriga F, Jiménez-Capdeville ME (1998) Effects of oral exposure to a mining waste on in vivo dopamine release from rat striatum. Environ Health Perspect 106:487–491

    Article  Google Scholar 

  • Rodríguez-Zavala JS, García-García JD, Ortiz-Cruz MA, Moreno-Sánchez R (2007) Molecular mechanisms of resistance to heavy metals in the protist Euglena gracilis. J Environ Sci Health A 42:1365–1378

    Article  Google Scholar 

  • Sagner S, Kneer R, Wanner G, Cosson J-P, Dues-Neumann B, Zenk MH (1998) Hyperaccumulation, complexation and distribution of nickel in Sebertia accuminata. Phytochemistry 47:339–347

    Article  CAS  Google Scholar 

  • Salt DE, Blaylock M, Kumar PB, Dushenkov AN, Ensly V, Chet I (1998) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Biotechnology 13:468–474

    Google Scholar 

  • Salt DE, Prince RC, Baker AJM, Raskin I, Pickering JI (1999) Zinc ligands in the metal hyperaccumulator Thlaspi caerulescens as determined using X-ray absorption spectroscopy. Environ Sci Technol 33:713–717

    Article  CAS  Google Scholar 

  • Satofuka H, Amano S, Atomi H, Takagi M, Hirata K, Miyamoto K, Imanaka T (1999) Rapid method for detection and detoxification of heavy metal ions in water environments using phytochelatin. J Biosci Bioeng 88:287–292

    Article  CAS  Google Scholar 

  • Scheerer U, Haensch R, Mendel RR, Kopriva S, Rennenberg H, Herschbach C (2010) Sulphur flux through the sulphate assimilation pathway is differently controlled by adenosine 5′-phosphosulphate reductase under stress and in transgenic poplar plants overexpressing γ-ECS, SO, or APR. J Exp Bot 61:609–622

    Article  CAS  Google Scholar 

  • Soghoian S, Sinert R (2011) Heavy Metals Toxicity http://emedicine.medscape.com/article/814960-overview [accessed February 2011]

  • Tian D, Zhu F, Yan W, Fang X, Xiang W, Deng X, Wang G, Peng C (2009) Heavy metal accumulation by panicled goldenrain tree (Koelreuteria paniculata) and common elaeocarpus (Elaeocarpus decipens) in abandoned mine soils in southern China. J Environ Sci 21:340–345

    Article  CAS  Google Scholar 

  • United States Environmental Protection Agency (U.S. EPA) (1990) Record of Decision (ROD) Abstract ROD Number: EPA/ROD/R08-90/028 ROD Date: 03/30/90 Site: Whitewood Creek. EPA ID Number: SDD980717136. Location: Whitewood, SD. Operable Unit: 01. Environmental Protection Agency, United States

    Google Scholar 

  • United States Environmental Protection Agency (U.S. EPA) (1993) Standards for the use or disposal of sewage sludge final rules. 40 CFR Part 257. Fed Regist 58(32):9248e9415

    Google Scholar 

  • Wang J, Zhao FJ, Meharg AA, Raab A, Feldmann J, McGrath S (2002) Mechanisms of arsenic hyperaccumulation in Pteris vittata. Uptake, kinetics, interactions with phosphate, and arsenic speciation. Plant Physiol 130:1552–1561

    Article  CAS  Google Scholar 

  • Wangeline AL, Burkhead JL, Hale KL, Lindblom SD, Terry N, Pilon M, Pilon-Smits EAH (2004) Overexpression of ATP sulfurylase in Indian mustard: effects on tolerance and accumulation of twelve metals. J Environ Qual 33:54–60

    Article  CAS  Google Scholar 

  • Wu C, Ye Z, Shu W, Zhu Y, Wong M (2011) Arsenic accumulation and speciation in rice are affected by root aeration and variation of genotypes. J Exp Bot 62:2889–2898

    Article  CAS  Google Scholar 

  • Xiong ZT (1998) Lead uptake and effects on seed germination and plant growth in a Pb hyperaccumulator Brassica pekinensis. Bull Environ Contam Toxicol 60:285–291

    Article  CAS  Google Scholar 

  • Yañez L, García-Nieto E, Rojas E, Carrizales L, Mejía J, Calderón J, Razo I, Díaz-Barriga F (2003) DNA damage in blood cells from children exposed to arsenic and lead in a mining area. Environ Res 93:231–240

    Article  Google Scholar 

  • Zenk MH (1996) Heavy metal detoxification in higher plants—a review. Gene 179:21–30

    Article  CAS  Google Scholar 

  • Zhang XH, Liu J, Huang HT, Chen J, Zhu JN, Wang DQ (2007) Chromium accumulation by the hyperaccumulator plant Leersia hexandra Swartz. Chemosphere 67:1138–1143

    Article  CAS  Google Scholar 

Download references

Acknowledgment

The present work was partially supported by grants from CONACyT-México Nos. 78775, 80534, 102926, 166463, J 37584-M, ICyTDF grant PICS08-5, and CONACyT fellowship 181460.

Author information

Authors and Affiliations

  1. Departamento de Toxicología Ambiental, Universidad Autónoma de San Luis Potosí, San Luis Potosí, México

    Blenda Machado-Estrada & Jaqueline Calderón

  2. Departamento de Bioquímica, Instituto Nacional de Cardiología, Juan Badiano No. 1, Seccion XVI, Tlalpan, México, D.F., 14080, México

    Rafael Moreno-Sánchez & José S. Rodríguez-Zavala

Authors
  1. Blenda Machado-Estrada
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jaqueline Calderón
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rafael Moreno-Sánchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. José S. Rodríguez-Zavala
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to José S. Rodríguez-Zavala.

Additional information

Responsible editor: Zhihong Xu

Rights and permissions

Reprints and permissions

About this article

Cite this article

Machado-Estrada, B., Calderón, J., Moreno-Sánchez, R. et al. Accumulation of arsenic, lead, copper, and zinc, and synthesis of phytochelatins by indigenous plants of a mining impacted area. Environ Sci Pollut Res 20, 3946–3955 (2013). https://doi.org/10.1007/s11356-012-1344-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-012-1344-8

Keywords

Search

Navigation