Skip to main content

Advertisement

Log in

The effect of excess copper on growth and physiology of important food crops: a review

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

Abstract

In recent years, copper (Cu) pollution in agricultural soils, due to arbitrary use of pesticides, fungicides, industrial effluent and wastewater irrigation, present a major concern for sustainable agrifood production especially in developing countries. The world’s major food requirement is fulfilled through agricultural food crops. The Cu-induced losses in growth and yield of food crops probably exceeds from all other causes of food safety and security threats. Here, we review the adverse effects of Cu excess on growth and yield of essential food crops. Numerous studies reported the Cu-induced growth inhibition, oxidative damage and antioxidant response in agricultural food crops such as wheat, rice, maize, sunflower and cucumber. This article also describes the toxic levels of Cu in crops that decreased plant growth and yield due to alterations in mineral nutrition, photosynthesis, enzyme activities and decrease in chlorophyll biosynthesis. The response of various crops to elevated Cu concentrations varies depending upon nature of crop and cultivars used. This review could be helpful to understand the Cu toxicity and the mechanism of its tolerance in food crops. We recommend that Cu-tolerant crops should be grown on Cu-contaminated soils in order to ameliorate the toxic effects for sustainable farming systems and to meet the food demands of the intensively increasing population.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adhikari T, Kundu S, Biswas AK, Tarafdar JC, Rao AS (2012) Effect of copper oxide nano particle on seed germination of selected crops. J Agric Sci Technol A 2:815–823

    CAS  Google Scholar 

  • Adriano DC (2001) Trace elements in terrestrial environments: biogeochemistry, bioavailability, and risks of metals, 2nd edn. Springer, New York

    Google Scholar 

  • Ahsan N, Lee DG, Lee SH, Kang KY, Lee JJ, Kim PJ, Lee BH (2007) Excess copper induced physiological and proteomic changes in germinating rice seeds. Chemosphere 67:1182–1193

    CAS  Google Scholar 

  • Akeel H, AL-Assie A (2014) Assessment of genotoxic effects of copper on cucumber plant (Cucumis sativus L.) using random amplified polymorphic DNA (RAPD-PCR) markers. J Biotechnol Res Center 8:12–19

    Google Scholar 

  • Alaoui-Sossé B, Genet P, Vinit-Dunand F, Toussaint ML, Epron D, Badot PM (2004) Effect of copper on growth in cucumber plants and its relationships with carbohydrate accumulation and changes in ion contents. Plant Sci 166:1213–1218

    Google Scholar 

  • Al-Hakimi ABM, Hamada AM (2011) Ascorbic acid, thiamine or salicylic acid induced changes in some physiological parameters in wheat grown under copper stress. Plant Prot Sci 47:92–108

    CAS  Google Scholar 

  • Ali NA, Bernal MP, Ater M (2002) Tolerance and bioaccumulation of copper in Phragmites australis and Zea mays. Plant Soil 239:103–111

    CAS  Google Scholar 

  • Ali S, Shahbaz M, Shahzad AN, Fatima A, Khan HAA, Anees M, Haider MS (2015) Impact of copper toxicity on stone-head cabbage (Brassica oleracea var. capitata) in hydroponics. PeerJ PrePrints 3:e1029. doi:10.7287/peerj.preprints.830v1

    Google Scholar 

  • Allan DL, Jarrell WM (1989) Proton and copper adsorption to maize and soybean root cell walls. Plant Physiol 89:823–832

    CAS  Google Scholar 

  • Alloway BJ (1995) Heavy metals in soils (Ed.). Blackie Academic and Professional, London

  • Aly AA, Mohamed AA (2012) The impact of copper ion on growth, thiol compounds and lipid peroxidation in two maize cultivars (Zea mays L.) grown in vitro. Aust J Crop Sci 6:541–549

    CAS  Google Scholar 

  • An YJ (2006) Assessment of comparative toxicities of lead and copper using plant assay. Chemosphere 62:1359–1365

    CAS  Google Scholar 

  • Ando Y, Nagata S, Yanagisawa S, Yoneyama T (2013) Copper in xylem and phloem saps from rice (Oryza sativa): the effect of moderate copper concentrations in the growth medium on the accumulation of five essential metals and a speciation analysis of copper-containing compounds. Funct Plant Biol 40:89–100

    CAS  Google Scholar 

  • Ansari MKA, Oztetik E, Ahmad A, Umar S, Iqbal M, Owens G (2013) Identification of the phytoremediation potential of Indian mustard genotypes for copper, evaluated from a hydroponic experiment. Clean: Soil Air Water 41:789–796

    CAS  Google Scholar 

  • Arnon DI, Stout PR (1939) The essentiality of certain elements in minute quantity for plants with special reference to copper. Plant Physiol 14:371–375

    CAS  Google Scholar 

  • Ashagre H, Shelema M, Kedir R, Ebsa S (2013) Seed germination and seedling growth of haricot bean (Phaseolus vulgaris L.) cultivars as influenced by copper sulphate. World J Agric Sci 1:312–317

    Google Scholar 

  • Atha DH, Wang H, Petersen EJ, Cleveland D, Holbrook RD, Jaruga P, Nelson BC (2012) Copper oxide nanoparticle mediated DNA damage in terrestrial plant models. Environ Sci Technol 46:1819–1827

    CAS  Google Scholar 

  • ATSDR (2004) Agency for Toxic Substances and Disease Registry www.atsdr.cdc.gov/toxprofiles/tp.asp?id=206&tid=37. Accessed 10 Jan 2015

  • Azeez MO, Adesanwo OO, Adepetu JA (2015) Effect of Copper (Cu) application on soil available nutrients and uptake. Afr J Agric Res 10:359–364

    Google Scholar 

  • Azmat R, Riaz S (2012) The inhibition of polymerization of glucose in carbohydrate under Cu stress in Vigna radiata. Pak J Bot 44:95–98

    CAS  Google Scholar 

  • Azooz MM, Abou-Elhamd MF, Al-Fredan MA (2012) Biphasic effect of copper on growth, proline, lipid peroxidation and antioxidant enzyme activities of wheat (Triticum aestivum’cv. Hasaawi) at early growing stage. Aust J Crop Sci 6:688–694

    CAS  Google Scholar 

  • Baize D (1997) Teneurs Totales en Eléments Traces Métalliques dans les Sols Français. Références et Stratégies d’Interprétation. INRA Editions, Paris

    Google Scholar 

  • Barbosa RH, Tabaldi LA, Miyazaki FR, Pilecco M, Kassab SO, Bigaton D (2013) Foliar copper uptake by maize plants: effects on growth and yield. Cienc Rural 43:1561–1568

    CAS  Google Scholar 

  • Benimali CS, Medina A, Navarro CM, Medina RB, Amoroso MJ, Gómez MI (2010) Bioaccumulation of copper by Zea mays: impact on root, shoot and leaf growth. Water Air Soil Pollut 210:365–370

    Google Scholar 

  • Borkert CM, Cox FR, Tucker M (1998) Zinc and copper toxicity in peanut, soybean, rice, and corn in soil mixtures. Commun Soil Sci Plant Anal 29:2991–3005

    CAS  Google Scholar 

  • Bravin MN, Marti AL, Clairotte M, Hinsinger P (2009) Rhizosphere alkalisation—a major driver of copper bioavailability over a broad pH range in an acidic, copper-contaminated soil. Plant Soil 318:257–268

    CAS  Google Scholar 

  • Bravin MN, Le Merrer B, Denaix L, Schneider A, Hinsinger P (2010) Copper uptake kinetics in hydroponically-grown durum wheat (Triticum turgidum durum L.) as compared with soil’s ability to supply copper. Plant Soil 331:91–104

    CAS  Google Scholar 

  • Bravin MN, Garnier C, Lenoble V, Gérard F, Dudal Y, Hinsinger P (2012) Root-induced changes in pH and dissolved organic matter binding capacity affect copper dynamic speciation in the rhizosphere. Geochim Cosmochim Acta 84:256–268

    CAS  Google Scholar 

  • Brun LA, Maillet J, Richarte J, Herrmann P, Remy JC (1998) Relationships between extractable copper, soil properties and copper uptake by wild plants in vineyard soils. Environ Pollut 102:151–161

    CAS  Google Scholar 

  • Brun LA, Maillet J, Hinsinger P, Pépin M (2001) Evaluation of copper availability to plants in copper-contaminated vineyard soils. Environ Pollut 111:293–302

    CAS  Google Scholar 

  • Cao ZH, Hu ZY (2000) Copper contamination in paddy soils irrigated with wastewater. Chemosphere 41:3–6

    CAS  Google Scholar 

  • Caspi V, Droppa M, Horvath G, Malkin S, Marder JB, Raskin VI (1999) The effect of copper on chlorophyll organization during greening of barley leaves. Photosynth Res 62:165–174

    CAS  Google Scholar 

  • Chaignon V, Bedin F, Hinsinger P (2002) Copper bioavailability and rhizosphere pH changes as affected by nitrogen supply for tomato and oil seed rape cropped on an acidic and a calcareous soil. Plant Soil 243:219–228

    CAS  Google Scholar 

  • Chaignon V, Quesnoit M, Hinsinger P (2009) Copper availability and bioavailability are controlled by rhizosphere pH in rape grown in an acidic Cu-contaminated soil. Environ Pollut 157:3363–3369

    CAS  Google Scholar 

  • Chatterjee J, Chatterjee C (2000) Phytotoxicity of cobalt, chromium and copper in cauliflower. Environ Pollut 109:69–74

    CAS  Google Scholar 

  • Chen LM, 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

    CAS  Google Scholar 

  • Ciscato M, Valcke R, Loven K, Clijsters H, Navari‐Izzo F (1997) Effects of in vivo copper treatment on the photosynthetic apparatus of two Triticum durum cultivars with different stress sensitivity. Physiol Plant 100:901–908

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Colzi I, Arnetoli M, Gallo A, Doumett S, Del Bubba M, Pignattelli S, Gabbrielli R, Gonnelli C (2012) Copper tolerance strategies involving the root cell wall pectins in Silene paradoxa L. Environ Exp Bot 78:91–98

    CAS  Google Scholar 

  • Cook CM, Vardaka E, Lanaras T (1997) Concentrations of Cu, growth, and chlorophyll content of field-cultivated wheat growing in naturally enriched Cu soil. Bull Environ Contam Toxicol 58:248–253

    CAS  Google Scholar 

  • Dimkpa CO, McLean JE, Britt DW, Anderson AJ (2015) Nano-CuO and interaction with nano-ZnO or soil bacterium provide evidence for the interference of nanoparticles in metal nutrition of plants. Ecotoxicology 24:119–129

    CAS  Google Scholar 

  • Dresler S, Hanaka A, Bednarek W, Maksymiec W (2014) Accumulation of low-molecular-weight organic acids in roots and leaf segments of Zea mays plants treated with cadmium and copper. Acta Physiol Plant 36:1565–1575

    CAS  Google Scholar 

  • Droppa M, Terry N, Horvath G (1984) Effects of Cu deficiency on photosynthetic electron transport. Proc Natl Acad Sci U S A 81:2369–2373

    CAS  Google Scholar 

  • EL-Metwally AE, Abdalla FE, El-Saady AM, Safina SA, EI-Sawy SS (2010) Response of wheat to magnesium and copper foliar feeding under sandy soil condition. J Am Sci 6:818–823

    Google Scholar 

  • Epstein E, Bloom JA (2005) Mineral nutrition of plants: principles and perspective, 2nd edn. Sinauer, Sunderland

    Google Scholar 

  • FAO (2009) www.fao.org/ “How to Feed the World in 2050”. Accessed 10 Jan 2015

  • Feigl G, Kumar D, Lehotai N, Kolbert Z (2013) Physiological and morphological responses of the root system of Indian mustard (Brassica juncea L. Czern.) and rapeseed (Brassica napus L.) to copper stress. Ecotoxicol Environ Saf 94:179–189

    CAS  Google Scholar 

  • Feigl G, Kumar D, Lehotai N, Pető A, Molnár Á, Rácz É, Ördög A, Erdei L, Kolbert Zs, Laskay G (2015) Comparing the effects of excess copper in the leaves of Brassica juncea (L. Czern) and Brassica napus (L.) seedlings: growth inhibition, oxidative stress and photosynthetic damage. Acta Biol Hungarica

  • Fidalgo F, Azenha M, Silva AF, Sousa A, Santiago A, Ferraz P, Teixeira J (2013) Copper-induced stress in Solanum nigrum L. and antioxidant defense system responses. Food Energy Secur 2:70–80

    Google Scholar 

  • Gajewska E, SkŁodowska M (2010) Differential effect of equal copper, cadmium and nickel concentration on biochemical reactions in wheat seedlings. Ecotoxicol Environ Saf 73:996–1003

    CAS  Google Scholar 

  • Gang A, Vyas A, Vyas H (2013) Toxic effect of heavy metals on germination and seedling growth of wheat. J Environ Res Develop 8:206–213

  • Ginocchio R, Rodriguez PH, Badilla-Ohlbaum R, Allen HE, Lagos GE (2002) Effect of soil copper content and pH on copper uptake of selected vegetables grown under controlled conditions. Environ Toxicol Chem 21:1736–1744

    CAS  Google Scholar 

  • Guan TX, He HB, Zhang XD, Bai Z (2011) Cu fractions, mobility and bioavailability in soil-wheat system after Cu-enriched livestock manure applications. Chemosphere 82:215–222

    CAS  Google Scholar 

  • Gupta M, Cuypers A, Vangronsveld J, Clijsters H (1999) Copper affects the enzymes of the ascorbate-glutathione cycle and its related metabolites in the roots of Phaseolus vulgaris. Physiol Plant 106:262–267

    CAS  Google Scholar 

  • Hänsch R, Mendel RR (2009) Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr Opin Plant Biol 12:259–266

    Google Scholar 

  • Hattab S, Chouba L, Ben Kheder M, Mahouachi T, Boussetta H (2009) Cadmium- and copper-induced DNA damage in Pisum sativum roots and leaves as determined by the comet assay. Plant Biosys 143(sup 1):S6–S11

    Google Scholar 

  • Hinsinger P (1998) How do plant roots acquire mineral nutrients chemical processes involved in the rhizosphere? Adv Agron 64:225–265

    CAS  Google Scholar 

  • Hinsinger P, Bengough AG, Vetterlein D, Young IM (2009) Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321:117–152

    CAS  Google Scholar 

  • Hong J, Rico CM, Zhao L, Adeleye AS, Keller AA, Peralta-Videa JR, Gardea-Torresdey JL (2015) Toxic effects of copper-based nanoparticles or compounds to lettuce (Lactuca sativa) and alfalfa (Medicago sativa). Environ Sci Processes Impacts 17:177–185

    CAS  Google Scholar 

  • Hristozkova M, Geneva M, Stancheva I (2006) Response of pea plants (Pisum sativum L.) to reduced supply with molybdenum and copper. Int J Agric Biol 8:218–220

    CAS  Google Scholar 

  • Hussain S, Peng S, Fahad S, Khaliq A, Huang J, Cui K, Nie L (2015) Rice management interventions to mitigate greenhouse gas emissions: a review. Environ Sci Pollut Res 22:3342–3360

    Google Scholar 

  • Inceer H, Ayaz S, Beyazoğlu O, Sentürk E (2003) Cytogenetic effects of copper chloride on the root tip cells of Helianthus annuus L. Turk J Biol 27:43–46

    CAS  Google Scholar 

  • Işeri OD, Korpe DA, Yurtcu E, Sahin FI, Haberal M (2011) Copper-induced oxidative damage, antioxidant response and genotoxicity in Lycopersicum esculentum Mill. and Cucumis sativus L. Plant Cell Rep 30:1713–1721

    Google Scholar 

  • Ivanova EM, Kholodova VP, Kuznetsov VV (2010) Biological effects of high copper and zinc concentrations and their interaction in rapeseed plants. Russ J Plant Physiol 57:806–814

    CAS  Google Scholar 

  • Jiang W, Liu D, Liu X (2001) Effects of copper on root growth, cell division, and nucleolus of Zea mays. Biol Plant 44:105–109

    CAS  Google Scholar 

  • Jiang J, Qin C, Shu X, Chen R, Song H, Li Q, Xu H (2015) Effects of copper on induction of thiol-compounds and antioxidant enzymes by the fruiting body of Oudemansiella radicata. Ecotoxicol Environ Saf 111:60–65

    CAS  Google Scholar 

  • Kabata-Pendias A, Pendias H (1992) Trace elements in soils and plants, 2nd edn. CRC Press, Boca Raton

    Google Scholar 

  • Kabata-Pendias A, Pendias H (2001) Trace elements in soils and plants, 3rd edn. CRC Press, Boca Raton

    Google Scholar 

  • Kang W, Bao J, Zheng J, Hu H, Du J (2015) Distribution and chemical forms of copper in the root cells of castor seedlings and their tolerance to copper phytotoxicity in hydroponic culture. Environ Sci Pollut Res. doi:10.1007/s11356-014-4030-1

    Google Scholar 

  • Keller C, Rizwan M, Davidian JC, Pokrovsky OS, Bovet N, Chaurand P, Meunier JD (2014) Effect of silicon on wheat seedlings (Triticum turgidum L.) grown in hydroponics and exposed to 0 to 30 μM Cu. Planta. doi:10.1007/s00425-014-2220-1

    Google Scholar 

  • Kim S, Lee S, Lee I (2012) Alteration of phytotoxicity and oxidant stress potential by metal oxide nanoparticles in Cucumis sativus. Water Air Soil Pollut 223:2799–2806

    CAS  Google Scholar 

  • Kopittk PM, Menzies NW (2006) Effect of Cu toxicity on growth of cowpea (Vigna unguiculata). Plant Soil 279:287–296

    Google Scholar 

  • Kopittke PM, Menzies NW, de Jonge MD, McKenna BA, Donner E, Webb RI, Paterson DJ, Howard DL, Ryan CG, Glover CJ et al (2011) In-situ distribution and speciation of toxic copper, nickel, and zinc in hydrated roots of cowpea. Plant Physiol 156:663–673

    CAS  Google Scholar 

  • Krzeslowska M (2011) The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiol Plant 33:35–51

    CAS  Google Scholar 

  • Kumar P, Tewari RK, Sharma PN (2008) Modulation of copper toxicity-induced oxidative damage by excess supply of iron in maize plants. Plant Cell Rep 27:399–409

    CAS  Google Scholar 

  • Kumar R, Mehrotra NK, Nautiyal BD, Kumar P, Singh PK (2009) Effect of copper on growth, yield and concentration of Fe, Mn, Zn and Cu in wheat plants (Triticum aestivum L.). J Environ Biol 30:485–488

    CAS  Google Scholar 

  • Kumar S, Kumar S, Prakash P, Singh M (2014) Antioxidant defense mechanisms in chickpea (Cicer arietinum L.) under copper and arsenic toxicity. Int J Plant Physiol Biochem 6:40–43

    CAS  Google Scholar 

  • Legros S, Chaurand P, Rose J, Masion A, Briois V, Ferrasse JH, Macary HS, Bottero JY, Doelsch E (2010) Investigation of copper speciation in pig slurry by a multitechnique approach. Environ Sci Technol 44:6926–6932

    CAS  Google Scholar 

  • Lin J, Jiang W, Liu D (2003) Accumulation of copper by roots, hypocotyls, cotyledons and leaves of sunflower (Helianthus annuus L.). Bioresour Technol 86:151–155

    CAS  Google Scholar 

  • Lin CY, Trinh NN, Fu SF, Hsiung YC, Chia LC, Lin CW, Huang HJ (2013) Comparison of early transcriptome responses to copper and cadmium in rice roots. Plant Mol Biol 81:507–522

    CAS  Google Scholar 

  • Liu DH, Jiang WS, Hou WQ (2001) Uptake and accumulation of copper by roots and shoots of maize (Zea mays L.). J Environ Sci 13:228–232

    CAS  Google Scholar 

  • Liu JJ, Wei Z, Li JH (2014) Effects of copper on leaf membrane structure and root activity of maize seedling. Bot Stud 55:1–6

    Google Scholar 

  • Lopez-Alonso ML, Benedito JL, Miranda M, Castillo C, Hernández J, Shore RF (2000) The effect of pig farming on copper and zinc accumulation in cattle in Galicia (North-Western Spain). Vet J 160:259–266

    CAS  Google Scholar 

  • Lukatkin A, Egorova I, Michailova I, Malec P, Strzałka K (2014) Effect of copper on pro-and antioxidative reactions in radish (Raphanus sativus L.) in vitro and in vivo. J Trace Elem Med Biol 28:80–86

    CAS  Google Scholar 

  • Luo Y, Jiang X, Wu L, Song J, Wu S, Lu R, Christie P (2003) Accumulation and chemical fractionation of Cu in a paddy soil irrigated with Cu-rich wastewater. Geoderma 115:113–120

    CAS  Google Scholar 

  • Mackie KA, Müller T, Kandeler E (2012) Remediation of copper in vineyards—a mini review. Environ Pollut 167:16–26

    CAS  Google Scholar 

  • Mahmood T, Islam KR, Muhammad S (2007) Toxic effects of heavy metals on early growth and tolerance of cereal crops. Pak J Bot 39:451–462

    Google Scholar 

  • Manivasagaperumal R, Vijayarengan P, Balamurugan S, Thiyagarajan G (2011) Effect of copper on growth, dry matter yield and nutrient content of Vigna radiata (L) Wilczek. J Phytol 3:53–62

    CAS  Google Scholar 

  • Mantovi P, Bonazzi G, Maestri E, Marmiroli N (2003) Accumulation of copper and zinc from liquid manure in agricultural soils and crop plants. Plant Soil 250:249–257

    CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, San Diego

    Google Scholar 

  • McBride MS, Sauve S, Hendershot W (1997) Solubility control of Cu, Zn, Cd and Pb in contaminated soils. Eur J Soil Sci 48:337–346

    CAS  Google Scholar 

  • Mediouni C, Houlné G, Chabouté ME, Ghorbel MH, Jemal F (2008) Cadmium and copper genotoxicity in plants. In: Biosaline Agriculture and High Salinity Tolerance (pp. 325–333). Birkhäuser Basel

  • Mei L, Daud MK, Ullah N, Ali S, Khan M, Malik Z, Zhu SJ (2015) Pretreatment with salicylic acid and ascorbic acid significantly mitigate oxidative stress induced by copper in cotton genotypes. Environ Sci Pollut Res. doi:10.1007/s11356-015-4075-9

    Google Scholar 

  • Mench M (1990) Transfert des oligo-éléments du sol à la racine et absorption. Compte Rendu de l’Académie d’Agriculture Française 76:17–30

  • Meng QM, Zou J, Zou JH, Jiang WS, 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

    Google Scholar 

  • Metwali MR, Gowayed SM, Al-Maghrabi OA, Mosleh YY (2013) Evaluation of toxic effect of copper and cadmium on growth, physiological traits and protein profile of wheat (Triticum aestivum L.), maize (Zea mays L.) and sorghum (Sorghum bicolor L.). World Appl Sci J 21:301–304

    CAS  Google Scholar 

  • Michaud AM, Bravin MN, Galleguillos M, Hinsinger P (2007) Copper uptake and phytotoxicity as assessed in situ for durum wheat (Triticum turgidum durum L.) cultivated in Cu-contaminated, former vineyard soils. Plant Soil 298:99–111

    CAS  Google Scholar 

  • Michaud AM, Chappellaz C, Hinsinger P (2008) Copper phytotoxicity affects root elongation and iron nutrition in durum wheat (Triticum turgidum durum L.). Plant Soil 310:151–165

    CAS  Google Scholar 

  • Micó C, Recatala L, Peris M, Sanchez J (2006) Assessing heavy metal sources in agricultural soils of an European Mediterranean area by multivariate analysis. Chemosphere 65:863–872

    Google Scholar 

  • Mishra S, Dubey RS (2005) Heavy metal toxicity induced alterations in photosynthetic metabolism in plants. Handbook of Photosynthesis 2:845–863

  • Miyazawa M, Giminez SMN, Yabe MJS, Oliveira EL, Kamogawa MY (2002) Absorption and toxicity of copper and zinc in bean plants cultivated in soil treated with chicken manure. Water Air Soil Pollut 138:211–222

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Morales JML, Rodríguez-Monroy M, Sepúlveda-Jiménez G (2012) Betacyanin accumulation and guaiacol peroxidase activity in Beta vulgaris L. leaves following copper stress. Acta Soc Bot Pol 81:193–201

    CAS  Google Scholar 

  • Mourato MP, Martins LL, Cuypers A (2009) Effect of copper on antioxidant enzyme activities and mineral nutrition of white lupin plants grown in nutrient solution. J Plant Nutr 32:1882–1900

    CAS  Google Scholar 

  • Muccifora S, Bellani LM (2013) Effects of copper on germination and reserve mobilization in Vicia sativa L. seeds. Environ Pollut 179:68–74

    CAS  Google Scholar 

  • Nan Z, Cheng G (2001) Copper and zinc uptake by spring wheat (Triticum aestivum L.) and corn (Zea Mays L.) grown in Baiyin region. Bull Environ Contam Toxicol 67:83–90

    CAS  Google Scholar 

  • Olteanu Z, Truta E, Oprica L, Zamfirache MM, Rosu CM, Vochita G (2013) Copper-induced changes in antioxidative response and soluble protein level in Triticum aestivum cv. beti seedlings. Rom Agric Res 30:2012–2190

    Google Scholar 

  • Ouzounidou G, Ciamporova M, Moustakas M, Karataglis S (1995) Responses of maize (Zea mays L.) plants to copper stress. Growth, mineral content and ultrastructure of roots. Environ Exp Bot 35:167–176

    CAS  Google Scholar 

  • Ouzounidou G, Ilias I, Tranopoulou H, Karataglis S (1998) Amelioration of copper toxicity by iron on spinach physiology. J Plant Nutr 21:2089–2101

    CAS  Google Scholar 

  • Pantola RC, Shekhawat GS (2012) Copper induced antioxidative enzyme indices in leaves of Brassica juncea seedlings. J Pharm Biomed Sci 15:1–6

    Google Scholar 

  • Patsikka E, Kairavuo M, Sersen F, Aro EM, Tyystjarvi E (2002) Excess copper predisposes photosystem II to photoinhibition in vivo by outcompeting iron and causing decrease in leaf chlorophyll. Plant Physiol 129:1359–1367

    CAS  Google Scholar 

  • Posmyk M, Kontek R, Janas K (2009) Antioxidant enzymes activity and phenolic compounds content in red cabbage seedlings exposed to copper stress. Ecotoxicol Environ Saf 72:596–602

    CAS  Google Scholar 

  • Rizwan M (2012) Silicon-mediated heavy metal tolerance in durum wheat: evidences of combined effects at the plant and soil levels (Doctoral dissertation, Aix-Marseille France)

  • Ryan BM, Kirby JK, Degryse F, Harris H, McLaughlin MJ, Scheiderich K (2013) Copper speciation and isotopic fractionation in plants: uptake and translocation mechanisms. New Phytol 199:367–378

    CAS  Google Scholar 

  • Sancenon V, Puig S, Mateu-Andres I, Dorcey E, Thiele DJ, Peñarrubia L (2004) The Arabidopsis copper transporter COPT1 functions in root elongation and pollen development. J Biol Chem 279:15348–15355

    CAS  Google Scholar 

  • Sánchez-Pardo B, Fernández-Pascual M, Zornoza P (2012) Copper microlocalisation, ultrastructural alterations and antioxidant responses in the nodules of white lupin and soybean plants grown under conditions of copper excess. Environ Exp Bot 84:52–60

    Google Scholar 

  • Sanchez-Pardo B, Fernandez-Pascual M, Zornoza P (2014) Copper microlocalisation and changes in leaf morphology, chloroplast ultrastructure and antioxidative response in white lupin and soybean grown in copper excess. J Plant Res 127:119–129

    CAS  Google Scholar 

  • Sauvé S, McBride MB, Norvell WA, Hendershot WH (1997) Copper solubility and speciation of in situ contaminated soils: effects of copper level, pH and organic matter. Water Air Soil Pollut 100:133–149

    Google Scholar 

  • Scheck HJ, Pscheidt JW (1998) Effect of Cu bactericides on Cu-resistant and -sensitive strains of Pseudomonas syringae pv. syringae. Plant Dis 82:397–406

    CAS  Google Scholar 

  • Shahbaz M, Tseng MH, Stuiver CEE, De Kok LJ (2010) Copper exposure interferes with the regulation of the uptake, distribution and metabolism of sulfate in Chinese cabbage. J Plant Physiol 167:438–446

    CAS  Google Scholar 

  • Shahid M, Pourrut B, Dumat C, Nadeem M, Aslam M, Pinelli E (2014) Heavy-metal-induced reactive oxygen species: phytotoxicity and physicochemical changes in plants. Rev Environ Contamin Toxicol 232:1–44

    CAS  Google Scholar 

  • Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726

    CAS  Google Scholar 

  • Sharma A, Singh G (2013) Studies on the effect of Cu (II) ions on the antioxidant enzymes in chickpea (Cicer arietinum L) cultivars. J Stress Physiol Biochem 9:5–13

    Google Scholar 

  • Sheldon AR, Menzies NW (2005) The effect of copper toxicity on the growth and root morphology of Rhodes grass (Chloris gayana Knuth.) in resin buffered solution culture. Plant Soil 278:341–349

    CAS  Google Scholar 

  • Shi J, Wu B, Yuan XF, Cao YY, Chen X, Chen Y, Hu T (2008) An X-ray absorption spectroscopy investigation of speciation and biotransformation of copper in Elsholtzia splendens. Plant Soil 302:163–174

    CAS  Google Scholar 

  • Singh D, Nath K, Sharma YK (2007) Response of wheat seed germination and seedling growth under copper stress. J Environ Biol 28:409–414

    CAS  Google Scholar 

  • Sommer AL (1931) Copper as an essential for plant growth. Plant Physiol 6:339–345

    CAS  Google Scholar 

  • Song Y, Zhang H, Chen C, Wang G, Zhuang K, Cui J, Shen Z (2014) Proteomic analysis of copper-binding proteins in excess copper-stressed rice roots by immobilized metal affinity chromatography and two-dimensional electrophoresis. BioMetals 27:265–276

    CAS  Google Scholar 

  • Szollosi R, Kalman E, Medvegy A, Peto A, Varga IS (2011) Studies on oxidative stress caused by Cu and Zn excess in germinating seeds of Indian mustard (Brassica juncea L.). Acta Biol Szegediensis 55:175–178

    Google Scholar 

  • Tanyolac D, Ekmekçi Y, Ünalan Ş (2007) Changes in photochemical and antioxidant enzyme activities in maize (Zea mays L.) leaves exposed to excess copper. Chemosphere 67:89–98

    CAS  Google Scholar 

  • Thomas DJ, Avenson TJ, Thomas JB, Herbert SK (1998) A cyanobacterium lacking iron superoxide dismutase is sensitized to oxidative stress induced with methyl viologen but not sensitized to oxidative stress induced with norflurazon. Plant Physiol 116:1593–1602

    CAS  Google Scholar 

  • Thounaojam TC, Panda P, Mazumdar P, Kumar D, Sharma G, Sahoo L, Panda S (2012) Excess copper induced oxidative stress and response of antioxidants in rice. Plant Physiol Biochem 53:33–39

    CAS  Google Scholar 

  • Trujillo-Reyes J, Majumdar S, Botez CE, Peralta-Videa JR, Gardea-Torresdey JL (2014) Exposure studies of core–shell Fe/Fe 3 O 4 and Cu/CuO NPs to lettuce (Lactuca sativa) plants: are they a potential physiological and nutritional hazard? J Hazard Mater 267:255–263

    CAS  Google Scholar 

  • Truta E, Vochita G, Zamfirache MM, Olteanu Z, Rosu CM (2013) Copper-induced genotoxic effects in root meristems of Triticum aestivum L. cv. beti. Carp J Earth Environ Sci 8:83–92

    Google Scholar 

  • Vassilev A, Lidon FC, do Céu Matos M, Ramalho JC, Yordanov I (2002) Photosynthetic performance and some nutrients content in cadmium– and copper–treated barley plants. J Plant Nutr 25:2343–2360

    CAS  Google Scholar 

  • Vassilev A, Lidon F, Campos PS, Ramalho JC, Barreiro MG, Yordanov I (2003) Cu-induced changes in chloroplast lipids and photosystem 2 activity in barley plants. Bulg J Plant Physiol 29:33–43

    Google Scholar 

  • Verma JP, Singh V, Yadav J (2011) Effect of copper sulphate on seed germination, plant growth and peroxidase activity of Mung bean (Vigna radiata). Int J Bot 7:200–204

    CAS  Google Scholar 

  • Vinit-Dunand F, Epron D, Alaoui-Sossè B, Badot PM (2002) Effects of copper on growth and on photosynthesis of mature and expanding leaves in cucumber plants. Plant Sci 163:53–58

    CAS  Google Scholar 

  • Vinod K, Awasthi G, Chauhan PK (2012) Cu and Zn tolerance and responses of the biochemical and physiochemical system of wheat. J Stress Physiol Biochem 8:203–213

    Google Scholar 

  • Wang QY, Liu JS, Wang Y, Yu HW (2015) Accumulations of copper in apple orchard soils: distribution and availability in soil aggregate fractions. J Soils Sediments. doi:10.1007/s11368-015-1065-y

    Google Scholar 

  • Wani PA, Khan MS, Zaidi A (2007) Effect of metal tolerant plant growth promoting Bradyrhizobium sp. (vigna) on growth, symbiosis, seed yield and metal uptake by greengram plants. Chemosphere 70:36–45

    CAS  Google Scholar 

  • Wani PA, Khan MS, Zaidi A (2008) Chromium-reducing and plant growth-promoting Mesorhizobium improves chickpea growth in chromium-amended soil. Biotechnol Lett 30:159–163

    CAS  Google Scholar 

  • Wheeler DM, Power IL (1995) Comparison of plant uptake and plant toxicity of various ions in wheat. Plant Soil 172:167–173

    CAS  Google Scholar 

  • White MC, Baker FD, Chaney RL, Decker AM (1981) Metal complexation in xylem fluid. 2. Theoretical equilibrium-model and computational computer-program. Plant Physiol 67:301–310

    CAS  Google Scholar 

  • Wodala B, Eitel G, Gyula TN, Ördög A, Horváth F (2012) Monitoring moderate Cu and Cd toxicity by chlorophyll fluorescence and P700 absorbance in pea leaves. Photosynthetica 50:380–386

    CAS  Google Scholar 

  • Wu C, Mosher BP, Zeng T (2006) One-step green route to narrowly dispersed copper nanocrystals. J Nanoparticle Res 8:965–969

    CAS  Google Scholar 

  • Wu J, Zhao FJ, Ghandilyan A, Logoteta B, Guzman MO, Schat H, Wang X, Aarts MGM (2009) Identification and functional analysis of two ZIP metal transporters of the hyperaccumulator Thlaspi caerulescens. Plant Soil 325:79–95

    CAS  Google Scholar 

  • Wu C, Luo Y, Zhang L (2010) Variability of copper availability in paddy fields in relation to selected soil properties in southeast China. Geoderma 156:200–206

    CAS  Google Scholar 

  • Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecol doi:10.5402/2011/402647. Article ID 402647

  • Xiong J, Wang Y, Xue Q, Wu X (2011) Synthesis of highly stable dispersions of nanosized copper particles using L-ascorbic acid. Green Chem 13:900–904

    CAS  Google Scholar 

  • Xu JK, Yang LX, Wang ZQ, Dong GC, Huang JY, Wang YL (2005) Effects of soil copper concentration on growth, development and yield formation of rice (Oryza sativa). Rice Sci 12:125–132

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179

    CAS  Google Scholar 

  • Yan YP, He JY, Zhu C, Cheng C, Pan XB, Sun ZY (2006) Accumulation of copper in brown rice and effect of copper on rice growth and grain yield in different rice cultivars. Chemosphere 65:1690–1696

    CAS  Google Scholar 

  • Yıldız M, Cigerci IH, Konuk M, Fidan AF, Terzi H (2009) Determination of genotoxic effects of copper sulphate and cobalt chloride in Allium cepa root cells by chromosome aberration and comet assays. Chemosphere 75:934–938

  • Yruela I (2005) Copper in plants. Braz J Plant Physiol 17:145–156

    CAS  Google Scholar 

  • Yruela I (2009) Copper in plants: acquisition, transport and interactions. Funct Plant Biol 36:409–430

    CAS  Google Scholar 

  • Yruela I (2013) Transition metals in plant photosynthesis. Metallomics 5:1090–1109

    CAS  Google Scholar 

  • Zengin FK, Kirbag S (2007) Effects of copper on chlorophyll, proline, protein and abscisic acid level of sunflower (Helianthus annuus L.) seedlings. J Environ Biol 28:561–566

    CAS  Google Scholar 

  • Zheng YB, Wang LP, Dixon MA (2004) Response to copper toxicity for three ornamental crops in solution culture. Hortic Sci 39:1116–1120

    CAS  Google Scholar 

  • Zheng Y, Wang L, Cayanan DF, Dixon M (2010) Greenhouse cucumber growth and yield response to copper application. Hortic Sci 45:771–774

    Google Scholar 

  • Zlobin IE, Kholodova VP, Rakhmankulova ZF, Kuznetsov VV (2014) Brassica napus responses to short-term excessive copper treatment with decrease of photosynthetic pigments, differential expression of heavy metal homeostasis genes including activation of gene NRAMP4 involved in photosystem II stabilization. Photosynth Res. doi:10.1007/s11120-014-0054-0

    Google Scholar 

Download references

Acknowledgments

Financial support from the Government College University Faisalabad and HEC (Higher Education Commission) of Pakistan is gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Muhammad Rizwan.

Additional information

Responsible editor: Elena Maestri

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Adrees, M., Ali, S., Rizwan, M. et al. The effect of excess copper on growth and physiology of important food crops: a review. Environ Sci Pollut Res 22, 8148–8162 (2015). https://doi.org/10.1007/s11356-015-4496-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-015-4496-5

Keywords

Navigation