Abstract
Copper (Cu) is one of the micronutrients needed by living organisms. In plants, Cu plays key roles in chlorophyll formation, photosynthesis, respiratory electron transport chains, oxidative stress protection as well as protein, carbohydrate, and cell wall metabolism. Therefore, deficiency of Cu can alter various functions of plant metabolism. However, Cu-based agrochemicals have traditionally been used in agriculture and being excessively released into the environment by anthropogenic activities. Continuous and extensive release of Cu is an imperative issue with various documented cases of phytotoxicity by the overproduction of reactive oxygen species (ROS) and damage to carbohydrates, lipids, proteins, and DNA. The mobility of Cu from soil to plant tissues has several concerns including its adverse effects on humans. In this review, we have described about importance and occurrence of Cu in environment, Cu homeostasis and toxicity in plants as well as remediation and progress in research so far done worldwide in the light of previous findings. Furthermore, present review provides a comprehensive ecological risk assessment on Cu in soils and thus provides insights for agricultural soil management and protection.
References
Adriano DC (2001) Trace elements in terrestrial environments. Biogeochemistry, bioavailability and risks of metals, 2nd edn. Springer, New York
Akinnifesi TA, Asubiojo OI, Amusan AA (2006) Effects of fungicide residues on the physico-chemical characteristics of soils of a major cocoa-producing area of Nigeria. Sci Total Environ 366:876–879
Aksu A (2015) Sources of metal pollution in the urban atmosphere (a case study: Tuzla, Istanbul). Aksu Journal of Environmental Health Science & Engineering 13:79
Al Naggar Y, Khalil MS, Ghorab MA (2018) Environmental pollution by heavy metals in the aquatic ecosystems of Egypt. Open Acc J of Toxicol 3:555603
Al-Bayati MA, Jamil DA, Al-Aubaidy HA (2015) Cardiovascular effects of copper deficiency on activity of superoxide dismutase in diabetic nephropathy. N Am J Med Sci 7:41–46
Alloway BJ (2013) Heavy Metals and Metalloids as Micronutrients for Plants and Animals. In: Alloway B (ed) Heavy Metals in Soils. Environmental Pollution, vol 22. Springer, Dordrecht
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress and signal transduction. Annual Review of Plant Biology 55:373–399
ATSDR (2002) Toxicological profile for copper (draft for public comment). Atlanta, GA, US Department of Health and Human Services, Public Health Service, Agency for Toxic Substances and Disease Registry (Subcontract No. ATSDR-205-1999-00024)
Ballabio C, Panagos P, Lugato E, Huang J-H, Orgiazzi A, Jones A, Fernández-Ugalde O, Borrelli P, Montanarella L (2018) Copper distribution in European topsoils: an assessment based on LUCAS soil survey. Science of The Total Environment 636:282–298
Basta NT, Gradwohl R, Snethen KL, Schroder JL (2001) Chemical immobilization of lead, zinc and cadmium in smelter-contaminated soils using bio solids and rock phosphate. J Environ Qual 30:1222–1230
Beer W, Jepsen E, Roth J (2003) Atmospheric contamination of a national forest near a copper smelter in Northern Michigan. Developments in Environmental Science 3:315–327
Bradl H (2005) Heavy Metals in the Environment: Origin, Interaction and Remediation. Elsevier/Academic Press, London
Branzini A, Zubillaga MS (2013) Phytostabilization as Soil Remediation Strategy. Plant-Based Remediation Processes. In: Gupta D (ed) Plant-Based Remediation Processes. Soil Biology, vol 35. Springer, Berlin
Brun LA, Corff JLE, Maillet J (2003) Effects of elevated soil copper on henology, growth and reproduction of five ruderal plant species. Environ Pollut 122:361–368
Cambrollé J, Mancilla-Leytón JM, Muñoz-Vallés S, Figueroa-Luque E, Luque T, Figueroa ME (2013) Effects of copper sulfate on growth and physiological responses of Limoniastrum monopetalum. Environ Sci Pollut Res Int 20:8839–8847
CFL (1983) Soil Analysis Service Interpretation Charts. Consolidated Fertilizers Limited, Morningside, Queensland, Australia.
Chaffai R, Elhammadi MA, Seybou TN, Tekitek B, Marzouk B, Ferjani e E (2007) Altered fatty acid profile of polar lipids in maize seedlings in response to excess copper. J Agron Crop Sci 193:207–217
Chaignon V, Hinsinger P (2003) A biotest for evaluating copper bioavailability to plants in a contaminated soil. J Enviro Qual 32:824–833
Chandrasekhar C, Ray JG (2017) Copper accumulation, localization and antioxidant response in Eclipta alba L. in relation to quantitative variation of the metal in soil. Acta Physiol Plant 39:205
Chen J, Wei F, Zheng C, Wu Y, C. Adriano D. (1991) Background concentrations of elements in Chinese soils. Water Air Soil Pollut 57-58:699–712. https://doi.org/10.1007/BF00282934
Chen J, Shafi M, Li S, Wang Y, Wu J, Ye Z, Peng D, Yan W, Liu D (2015) Copper induced oxidative stresses, antioxidant responses and phytoremediation potential of Moso bamboo (Phyllostachys pubescens). Sci Rep 5:13554
Chen L-M, Lin CC, Kao CH (2000) Copper toxicity in rice seedlings: changes in antioxidative enzyme activities, H2O2 level and cell wall peroxidase activity in roots. Bot Bull Acad Sin 41:99–103
Chen X, Chen G, Chen L, Chen Y, Lehmann J, McBride MB, Hay AG (2011) Adsorption of copper and zinc by biochars produced from pyrolysis of hardwood and corn straw in aqueous solution. Bioresour Technol 102:8877–8884
Chen YF, Randlett MD, Findell JL, Schaller GE (2002) Localization of the ethylene receptor ETR1 to the endoplamic reticulum of Arabidopsis. J Biol Chem 277:19861–19866
Cheng J, Song J, Ding C, Li X, Wang X (2014) Eco-toxicity of benzo [a] pyrene assessed by soil microbial indicators. Environ Toxicol Chem 33:1930–1936
Chinmayee MD, Mahesh B, Pradesh S, Mini I, Swapna TS (2012) The assessment of phytoremediation potential of invasive weed Amaranthus spinosus L. Appl Biochem Biotech 167:1550–1559
Cohu CM, Pilon M (2007) Regulation of superoxide dismutase expression by copper availability. Physiol Plant 129:747–755
Ebbs SD, Kochian LV (1997) Toxicity of zinc and copper to Brassica species: implications for phytoremediation. J Environ Qual 26:776–781
Elleuch A, CHaâbene Z, Douglas CG, Drira N, Mejdoub H, Khemakhem B (2013) Morphological and biochemical behavior of fenugreek (Trigonella foenum-graecum) under copper stress. Ecotox Environ Safe 98:46–53
EU (2008) European Union risk assessment report. Voluntary risk assessment of copper, copper II sulphate pentahydrate, copper(I) oxide, copper (II) oxide, dicopper chloride trihydroxide. http://echa.europa.eu/chem_data/transit_measures/vrar_en.asp
Festa RA, Thiele DJ (2011) Copper: an essential metal in biology. Curr Biol 21:R877–R883. https://doi.org/10.1016/j.cub.2011.09.040
Fifield FW, Haines PJ (2000) Environmental analytical chemistry. Wiley-Blackwell, Hoboken
Gaetke LM, Chow CK (2003) Copper toxicity, oxidative stress, and antioxidant nutrients. Toxicology 189:147–163
Gallego SM, Pena LB, Barcia RA, Azpilicueta CE, Iannone MF, Rosales EP, Benavides MP (2012) Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms. Environ Exp Bot 83:33–46
Gharbi F, Rejeb S, Ghorbal MH, Morel JL (2005) Plant response to copper toxicity as affected by plant species and soil type. Journal of Plant Nutrition 28:379–392
Goswami S, Das S (2016) Copper phytoremediation potential of Calandula officinalis L. and the role of antioxidant enzymes in metal tolerance. Ecotoxicology and Environmental Safety 126:211–218
Grotz N, Guerinot ML (2006) Molecular aspects of Cu, Fe and Zn homeostasis in plants. Biochimica et Biophysica Acta 1763:595–608
Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322
Hammond CR (2004) The Elements, in Handbook of Chemistry and Physics (81st ed.). CRC press. ISBN 0-8493-0485-7
He ZL, Yang XE, Stoffella PJ (2005) Trace elements in agroecosystems and impacts on the environment. J Trace Elem Med Bio 19:125–140
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198
Himelblau E, Mira H, Lin S-J, Culotta VC, Peñarrubia L, Amasino RM (1998) Identification of a functional homolog of the yeast copper homeostasis gene ATX1 from Arabidopsis. Plant Physiol 117:1227–1234
Holleman AF, Wiberg N (2001) Inorganic Chemistry. Academic Press, San Diego ISBN 978-0-12-352651-9
Hrynkiewicz K, Złoch M, Kowalkowski T, Baum C, Buszewski B (2018). Efficiency of microbially assisted phytoremediation of heavy-metal-contaminated soils. Environmental Reviews. 26. https://doi.org/10.1139/er-2018-0023
Husak V (2015) Copper and copper-containing pesticides: metabolism, toxicity and oxidative stress. Journal of Vasyl Stefanyk Precarpathian National University 2:38-50
Imtiaz M, Rizwan MS, Xiong S, Li H, Ashraf M, Shahzad SM, Shahzad M, Rizwan M, Tu S (2015) Vanadium, recent advancements and research prospects: a review. Environment International 80:79–88
Kabata-Pendias A (2010) Trace Elements in Soils and Plants (fourth ed). CRC Press, Boca Raton
Kabata-Pendias A, Pendias H (1993) Biogeochemia pier-wiastków śladowych‘ PWN, Warszawa
Khalil AH, Alquzweeni SS, Modhloom HM (2015) Removal of copper ions from contaminated soil by enhanced soil washing. Int J Environ Res 9:1141–1146
Kidd P, Barceló J, Bernal MP, Navari-Izzo F, Poschenrieder C, Shilev S, Clemente R, Monterroso C (2009) Trace element behaviour at the root–soil interface: implications in phytoremediation. Environmental and Experimental Botany 67:243–259
Landon JR (1991) Booker tropical soil manual: a handbook for soil survey and agricultural land evaluation in the tropics and subtropics. Longman, Essex
Li L, Zhang K, Gill RA, Islam F, Farooq MA, Wang J, Zhou W (2018) “Ecotoxicological and interactive effects of copper and chromium on physiochemical, ultrastructural, and molecular profiling in Brassica napus L.,” BioMed Research International, vol. 2018, Article ID 9248123, 17 pages, 2018. https://doi.org/10.1155/2018/9248123
Li Z, Tang L, Zheng Y, Tian D, Su M, Zhang F et al (2017) Characterizing the mechanisms of lead immobilization via bioapatite and various clay minerals. ACS Earth and Space Chemistry 1:152–157
Li Z, Wang F, Bai T, Tao J, Guo J, Yang M et al (2016) Lead immobilization by geological fluorapatite and fungus Aspergillus niger. J Hazard Mater 320:386–392
Lide DR (ed) (2009) CRC handbook of chemistry and physics. 89th Edition (CD-ROM version). CRC Press/Taylor and Francis, Boca Raton
Lidon FC, Henriques FS (1994) Subcellular localisation of copper and partial isolation of copper proteins in roots from rice plants exposed to excess copper. Aust J Plant Physiol 21:427–436
Liu J, Wang J, Lee S, Wen R (2018) Copper-caused oxidative stress triggers the activation of antioxidant enzymes via ZmMPK3 in maize leaves. PLOS ONE 13:e0203612. https://doi.org/10.1371/journal.pone.0203612
Luo L, Ma Y, Zhang S, Wei D, Zhu YG (2009) Inventory of trace element inputs to agricultural soils in China. J Environ Manag 90:2524–2530
Ma JF, Yamaji N, Motani N, Xu XY, Su YH, McGrath SP, Zhao FJ (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci USA 105:9931–9935
Ma Y, Du X, Shi Y, Hou D, Dong B, Xu Z et al (2016) Engineering practice of mechanical soil aeration for the remediation of volatile organic compound-contaminated sites in China: advantages and challenges. Front Environ Sci Eng 10:6
Mahmud S, Hassan MM, Moniruzzaman M, Biswas N, Rahman MM, Haque ME (2013) Study on the accumulation of copper from soil by shoots and roots of some selective plant species. International Journal of Biosciences 3:68–75
Mahurpawar M (2015) Effects of heavy metals on human health. International Journal of Research-GRANTHAALAYAH. [Social Issues and Environmental Problems: September]
Maier R, Pepper I, Gerba C (2000) Environmental Microbiology. Academic Press, San Diego
Manousaki E, Kadukova J, Papadantonakis N, Kalogerakis N (2008) Phytoextraction and phytoexcretion of Cd by the leaves of Tamarix smyrnensis growing on contaminated non-saline and saline soils. Environ Res 106:326–332
Marques DM, Júnior VV, da Silva AB, Mantovani JR, Magalhães PC, de Souza TC (2018) Copper toxicity on photosynthetic responses and root morphology of Hymenaea courbaril L. (Caesalpinioideae). Water Air Soil Pollut 229:138
Marschner H (1995) Mineral nutrition of higher plants. London, Academic Press
Martins L, Mourato M (2006) Effect of excess copper on tomato plants: growth parameters, enzyme activities, chlorophyll, and mineral content. J Plant Nutr 29:2179–2198
Meng Q, Zou M, Zou J, Jiang JH, W. S, Liu DH (2007) Effect of Cu2+ concentration on growth, antioxidant enzyme activity and malondialdehyde content in garlic (Allium sativum L.). Acta Biol Cracov Bot 49:95-101
Mengel K, Kirkby EA, Kosegarten H, Appel T (2001) Principles of plant nutrition. Kluwer Academic, Dordrecht
Merrington G (2018) The good, the bad and the ugly: copper and arsenic in soils. Soil health: the foundation of sustainable agriculture
Mira H, Sancenón V, Peñarrubia L (2002) Copper Homeostasis in Plants. In: Massaro EJ (ed) Handbook of Copper Pharmacology and Toxicology. Humana Press, Totowa. https://doi.org/10.1007/978-1-59259-288-3_33
Mocquot B, Vangronsveld J, Clijsters H, Mench M (1996) Copper toxicity in young maize (Zea mays L.) plants: effects on growth, mineral and chlorophyll contents, and enzyme activities. Plant Soil 182:287–300
Mostofa MG, Fujita M (2013) Salicylic acid alleviates copper toxicity in rice (Oryza sativa L.) seedlings by up-regulating antioxidative and glyoxalase systems. Ecotoxicology 22:959–973
Murakami M, Ae M (2009) Potential for phytoextraction of copper, lead, and zinc by rice (Oryza sativa L.), soybean (Glycine max [L.] Merr.), and maize (Zea mays L.). J Hazard Mater 162:1185–1192
Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216
Nason JA, Bloomquist DJ, Sprick MS (2012) Factors influencing dissolved copper concentrations in oregon highway storm water runoff. J Environ Eng 138:734–742
Nicholson FA, Chambers BJ, Williams JR, Unwin RJ (1999) Heavy metal contents of livestock feeds and animal manures in England and Wales. Bioresour Technol 70:23–31
Nicholson FA, Smith SR, Alloway BJ, Carlton-Smith C, Chambers BJ (2003) An inventory of heavy metals inputs to agricultural soils in England and Wales. Sci Total Environ 311:205–219
Olawoyin R, Oyewole SA, Grayson RL (2012) Potential risk effect from elevated levels of soil heavy metals on human health in the Niger delta. Ecotoxicol Environ Saf 85:120–130
Oorts K (2013) Copper. In: Alloway B (ed) Heavy Metals in Soils. Environmental Pollution, vol 22. Springer, Dordrecht
Panda SK, Upadhyay SK (2009) Copper-induced growth inhibition, oxidative stress and ultrastructural alterations in freshly grown water lettuce (Pistia stratiotes L.). C R Biol 332:623–632
Pedersen MB, Kjaer C, Elmegaard N (2000) Toxicity and bioaccumulation of copper to black bindweed (Fallopia convolvulus) in relation to bioavailability and the age of soil contamination. Arch Environ Contam Toxicol 39:431–439
Percival, S.S. 1998. Copper and immunity. Am. J. Clin. Nutr. 67(5 Suppl.): 1064S-1068S.
Petris MJ (2004) The SLC31 (Ctr) copper transporter family. Eur J Physiol 447:752–755
Pietrzak U, Uren NC (2011) Remedial options for copper-contaminated vineyard soils. Soil Res 49:44–55
Pilon M, Abdel-Ghany SE, Cohu C, Gogolin KA, Ye H (2006) Copper cofactor delivery in plant cells. Curr Opin Plant Biol 9:256–263
Puig S, Thiele DJ (2002) Molecular mechanisms of copper uptake and distribution. Curr Opin Chem Biol 6:171–180
Quartacci MF, Pinzino C, Sgherri CLM, Vecchia FD, Navari - Izzo F (2000) Growth in excess copper induces changes in the lipid composition and fluidity of PSII-enriched membranes in wheat. Physiol Plant 108:87–93
Race M, Marotta R, Fabbricino M, Pirozzi F, Andreozzi R, Cortese L, Giudicianni P (2016) Copper and zinc removal from contaminated soils through soil washing process using ethylenediaminedisuccinic acid as a chelating agent: A modeling investigation. J Environ Chem Eng:4. https://doi.org/10.1016/j.jece.2016.05.031
Radwan MA, Salama AK (2006) Market basket survey for some heavy metals in Egyptian fruits and vegetables. Food Chem. Toxicol 44:1273–1278
Rehman M, Liu L, Bashir S, Saleem MH, Chen C, Peng D, Siddique KHM (2019b) Influence of rice straw biochar on growth, antioxidant capacity and copper uptake in ramie (Boehmeria nivea L.) grown as forage in aged copper-contaminated soil. Plant Physiol Biochem. https://doi.org/10.1016/j.plaphy.2019.02.021
Rehman M, Maqbool Z, Peng D, Lijun L (2019a) Morpho-physiological traits, antioxidant capacity and phytoextraction of copper by ramie (Boehmeria nivea L.) grown as fodder in copper-contaminated soil. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-018-4015-6
Rizwan M, Ali S, Adrees M, Rizvi H, Zia-ur-Rehman M, Hannan F, Qayyum MF, Hafeez F, Ok YS (2016) Cadmium stress in rice: toxic effects, tolerance mechanisms, and management: a critical review. Environ Sci Pollut Res 23:17859–17879
Rosenzweig AC (2002) Metallochaperones: bind and deliver. Chem Biol 9:673–677
Savithri P, Biju J, Poongothai S (2003) Effect of Copper Fungicide Sprays on the Status of Micronutrient in Soils of Hot Semi-Arid Region of India. Tamil Nadu Agricultural University, Coimbatore 641:003
Seigneurin-Berny D, Gravot A, Auroy P, Mazard C, Kraut A, Finazzi G, Grunwald D, Rappaport F, Vavasseur A, Joyard J, Richaud P, Rolland N (2006) HMA1, a new Cu-ATPase of the chloroplast envelope, is essential for growth under adverse light conditions. J Biol Chem 281:2882–2892
Sheldon A, Menzies NW (2004) The effect of copper toxicity on the growth and morphology of Rhodes grass (Chloris gayana) in solution culture. School of Land and Food Sciences, University of Queensland, St Lucia, Qld, 4072, Australia. 3rd Australian New Zealand Soils Conference, 5-9 December 2004, University of Sydney, Australia. Published on CDROM. Website www.regional.org.au/au/asssi/
Singh OV, Labana S, Pandey G, Budhiraja R, Jain RK (2003) Phytoremediation: an overview of metallic ion decontamination from soil. Appl Microbiol Biotechnol 61:405–412
Singh VP (2005) Metal toxicity and tolerance in plants and animals. Sarup & Sons, New Delphi
Sonmez S, Kaplan M, Sonmez NK, Kaya H, Uz I (2006) High level of copper application to soil and leaves reduce the growth and yield of tomato plants. Scientia Agricola 63:213–218
Stern BR, Solioz M, Krewski D, Aggett P, Aw TC, Baker S, Crump K, Dourson M, Haber L, Hertzberg R, Keen C, Meek B, Rudenko L, Schoeny R, Slob W, Starr T (2007) Copper and human health: biochemistry, genetics, and strategies for modeling dose-response relationships. Toxicol Enp Heal B 10:157–222
Stojek M (2013) The concentration of molybdenum and copper in rocks, soils and plants in the area of Jabłonki (Eastern Beskids Mts.). Environmental Protection and Natural Resources 24:13–17
Thounaojam TC, Panda P, Mazumdar P, Kumar D, Sharma GD, Sahoo L, Sanjib P (2012) Excess copper induced oxidative stress and response of antioxidants in rice. Plant Physiol Bioch 53:33–39
Tie SG, Tang ZJ, Zhao YM, Li W (2014) Oxidative damage and antioxidant response caused by excess copper in leaves of maize. Afr J Biotechnol 11:4378–4384
Tye AM, Young S, Crout NMJ, Zhang H, Preston S, Zhao FJ, McGarth SP (2004) Speciation and solubility of Cu, Ni and Pb in contaminated soils. Eur J Soil Sci 55:579–590
Uchimiya M, Lima IM, Klasson KT, Chang SC, Wartelle LH, Rodgers JE (2010) Immobilization of heavy metal ions (Cu (II), Cd (II), Ni (II), and Pb (II)) by broiler litter-derived biochars in water and soil. J Agr Food Chem 58:5538–5544
Urekli F, Porgali ZB (2006) The effect of excessive exposure to copper in bean plants. Acta Biologica Cracoviensia Series Botanica 48:7–13
US NRC (2000) Copper in drinking water. DC, National Research Council, National Academy Press, Washington
Vassilev A, Lidon FC, Ramalho JC, Do Ceu Matos M, Da Graca M (2003) Effects of excess copper on growth and photosynthesis of barley plants. Implication with a screening test for Cu tolerance. J Cent Eur Agric 4:225–236
Wagg C, Bender SF, Widmer F, van der Heijden MG (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci 111:5266–5270
Wang R, Shafi M, Ma J, Zhong B, Guo J, Hu X, Xu W, Yang Y, Ruan Z, Wang Y, Ye Z, Liu D (2018) Effect of amendments on contaminated soil of multiple heavy metals and accumulation of heavy metals in plants. Environ Sci Pollut Res 25:28695–28704
Wang S, Zhang P, Kong X, Xie S, Li Q, Li Z, Zhou Z (2017) Delicate changes of bioapatite mineral in pig femur with addition of dietary xylooligosaccharide: evidences from Raman spectroscopy and ICP. Anim Sci J 88:1820–1826
Wang X, Wang C, Bao L, Xie S (2015) Impact of carbon source amendment on ammonia-oxidizing microorganisms in reservoir riparian soil. Ann Microbiol 65:1411–1418
Waseem A, Arshad J, Iqbal F, Sajjad A, Mehmood Z, Murtaza G (2014) Pollution status of Pakistan: a retrospective review on heavy metal contamination of water, soil, and vegetables,” BioMed Research International, vol. 2014, Article ID 813206, 29 pages, https://doi.org/10.1155/2014/813206
Waters BM, Armbrust LC (2013) Optimal copper supply is required for normal plant iron deficiency responses. Plant Signal Behav 8:e26611
Williams DM (1983) Copper deficiency in humans. Semin Hematol 20:118–128
Wuana RA, Okieimen FE (2011) Heavy Metals in Contaminated Soils: A Review of Sources, Chemistry, Risks and Best Available Strategies for Remediation. ISRN Ecology https://doi.org/10.5402/2011/402647
Xiong X, Li YX, Li W, Lin CY, Han W (2010) Copper content in animal manures and potential risk of soil copper pollution with animal manure use in agriculture. Resour. Conserv. Recycl 54:985–990
Xu J, Yang L, Wang Z, Dong G, Huang J, Wang Y (2006) Toxicity of copper on rice growth and accumulation of copper in rice grain in copper contaminated soil. Chemosphere 62:602–607
Xu X, Cao X, Zhao L, Wang H, Yu H, Gao B (2013) Removal of Cu, Zn, and Cd from aqueous solutions by the dairy manure-derived biochar. Environ Sci Pollut Res 20:358–368
Yaghi B, Abdul-Wahab SA (2003) Assessment of lead, zinc, copper, nickel and chromium in total suspended particulate matter from the workplace in Al-Rusayl Industrial Estate, Oman. J Environ Monit 5:950–952
Yang B, Zhou M, Shu WS, Lan CY, Ye ZH, Qiu RL, Jie YC, Cui GX, Wong MH (2010) Constitutional tolerance to heavy metals of a fiber crop, ramie (Boehmeria nivea), and its potential usage. Environ Pollut 158:551–558
Yang W, Wang Y, Zhao F, Ding Z, Zhang X, Zhu Z, Yang X (2014) Variation in copper and zinc tolerance and accumulation in 12 willow clones: implications for phytoextraction. J Zhejiang Univ Sci B 15:788–800
Yang X, Liu J, McGrouther K, Huang H, Lu K, Guo X, He L, Lin X, Che L, Ye Z, Wang H (2016) Effect of biochar on the extractability of heavy metals (Cd, Cu, Pb, and Zn) and enzyme activity in soil. Environ Sci Pollut Res 23:974–984
Yruela I (2005) Copper in plants. Braz J Plant Physiol 17:145–156
Yruela I (2009) Copper in plants: acquisition, transport and interactions. Funct Plant Biol 36:409–430
Zatta P, Frank A (2007) Copper deficiency and neurological disorders in man and animals. Brain Res Rev 54:19–33
Zhao SL, Liu Q, Qi YT, Duo L (2010) Responses of root growth and protective enzymes to copper stress in turfgrass. Acta Biol Cracov Bot 52:7–11
Zvezdanovic J, Markovic D, Nikolic G (2007) Different possibilities for the formation of complexes of copper and zinc with chlorophyll inside photosynthetic organelles: chloroplasts and thylakoids. J Serv Chem Soc 72:1053–1062
Funding
This work was financially supported by the National Natural Science Foundation of China (31571717) and China Agriculture Research System project (CARS-16-E12).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Philippe Garrigues
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Rehman, M., Liu, L., Wang, Q. et al. Copper environmental toxicology, recent advances, and future outlook: a review . Environ Sci Pollut Res 26, 18003–18016 (2019). https://doi.org/10.1007/s11356-019-05073-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-019-05073-6