Advertisement

Environmental Science and Pollution Research

, Volume 22, Issue 11, pp 8148–8162 | Cite as

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

  • Muhammad Adrees
  • Shafaqat Ali
  • Muhammad RizwanEmail author
  • Muhammad Ibrahim
  • Farhat Abbas
  • Mujahid Farid
  • Muhammad Zia-ur-Rehman
  • Muhammad Kashif Irshad
  • Saima Aslam Bharwana
Review Article

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.

Keywords

Copper Growth Mineral nutrition Photosynthesis Yield 

Notes

Acknowledgments

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

References

  1. 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 2:815–823Google Scholar
  2. Adriano DC (2001) Trace elements in terrestrial environments: biogeochemistry, bioavailability, and risks of metals, 2nd edn. Springer, New YorkGoogle Scholar
  3. 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 67:1182–1193Google Scholar
  4. 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 8:12–19Google Scholar
  5. 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 166:1213–1218Google Scholar
  6. 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 47:92–108Google Scholar
  7. Ali NA, Bernal MP, Ater M (2002) Tolerance and bioaccumulation of copper in Phragmites australis and Zea mays. Plant Soil 239:103–111Google Scholar
  8. 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
  9. Allan DL, Jarrell WM (1989) Proton and copper adsorption to maize and soybean root cell walls. Plant Physiol 89:823–832Google Scholar
  10. Alloway BJ (1995) Heavy metals in soils (Ed.). Blackie Academic and Professional, LondonGoogle Scholar
  11. 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 6:541–549Google Scholar
  12. An YJ (2006) Assessment of comparative toxicities of lead and copper using plant assay. Chemosphere 62:1359–1365Google Scholar
  13. 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 40:89–100Google Scholar
  14. 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 41:789–796Google Scholar
  15. Arnon DI, Stout PR (1939) The essentiality of certain elements in minute quantity for plants with special reference to copper. Plant Physiol 14:371–375Google Scholar
  16. 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 1:312–317Google Scholar
  17. 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 46:1819–1827Google Scholar
  18. ATSDR (2004) Agency for Toxic Substances and Disease Registry www.atsdr.cdc.gov/toxprofiles/tp.asp?id=206&tid=37. Accessed 10 Jan 2015
  19. Azeez MO, Adesanwo OO, Adepetu JA (2015) Effect of Copper (Cu) application on soil available nutrients and uptake. Afr J Agric Res 10:359–364Google Scholar
  20. Azmat R, Riaz S (2012) The inhibition of polymerization of glucose in carbohydrate under Cu stress in Vigna radiata. Pak J Bot 44:95–98Google Scholar
  21. 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 6:688–694Google Scholar
  22. Baize D (1997) Teneurs Totales en Eléments Traces Métalliques dans les Sols Français. Références et Stratégies d’Interprétation. INRA Editions, ParisGoogle Scholar
  23. 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 43:1561–1568Google Scholar
  24. 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 210:365–370Google Scholar
  25. 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 29:2991–3005Google Scholar
  26. 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 318:257–268Google Scholar
  27. 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 331:91–104Google Scholar
  28. 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 84:256–268Google Scholar
  29. 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 102:151–161Google Scholar
  30. Brun LA, Maillet J, Hinsinger P, Pépin M (2001) Evaluation of copper availability to plants in copper-contaminated vineyard soils. Environ Pollut 111:293–302Google Scholar
  31. Cao ZH, Hu ZY (2000) Copper contamination in paddy soils irrigated with wastewater. Chemosphere 41:3–6Google Scholar
  32. 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 62:165–174Google Scholar
  33. 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 243:219–228Google Scholar
  34. 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 157:3363–3369Google Scholar
  35. Chatterjee J, Chatterjee C (2000) Phytotoxicity of cobalt, chromium and copper in cauliflower. Environ Pollut 109:69–74Google Scholar
  36. 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 41:99–103Google Scholar
  37. 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 100:901–908Google Scholar
  38. Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719Google Scholar
  39. 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 78:91–98Google Scholar
  40. 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 58:248–253Google Scholar
  41. 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 24:119–129Google Scholar
  42. 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 36:1565–1575Google Scholar
  43. Droppa M, Terry N, Horvath G (1984) Effects of Cu deficiency on photosynthetic electron transport. Proc Natl Acad Sci U S A 81:2369–2373Google Scholar
  44. 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 6:818–823Google Scholar
  45. Epstein E, Bloom JA (2005) Mineral nutrition of plants: principles and perspective, 2nd edn. Sinauer, SunderlandGoogle Scholar
  46. FAO (2009) www.fao.org/ “How to Feed the World in 2050”. Accessed 10 Jan 2015
  47. 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 94:179–189Google Scholar
  48. 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 HungaricaGoogle Scholar
  49. 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 2:70–80Google Scholar
  50. Gajewska E, SkŁodowska M (2010) Differential effect of equal copper, cadmium and nickel concentration on biochemical reactions in wheat seedlings. Ecotoxicol Environ Saf 73:996–1003Google Scholar
  51. Gang A, Vyas A, Vyas H (2013) Toxic effect of heavy metals on germination and seedling growth of wheat. J Environ Res Develop 8:206–213Google Scholar
  52. 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 21:1736–1744Google Scholar
  53. 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 82:215–222Google Scholar
  54. 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 106:262–267Google Scholar
  55. Hänsch R, Mendel RR (2009) Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr Opin Plant Biol 12:259–266Google Scholar
  56. 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–S11Google Scholar
  57. Hinsinger P (1998) How do plant roots acquire mineral nutrients chemical processes involved in the rhizosphere? Adv Agron 64:225–265Google Scholar
  58. Hinsinger P, Bengough AG, Vetterlein D, Young IM (2009) Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321:117–152Google Scholar
  59. 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 17:177–185Google Scholar
  60. 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 8:218–220Google Scholar
  61. 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 22:3342–3360Google Scholar
  62. 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 27:43–46Google Scholar
  63. 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 30:1713–1721Google Scholar
  64. 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 57:806–814Google Scholar
  65. Jiang W, Liu D, Liu X (2001) Effects of copper on root growth, cell division, and nucleolus of Zea mays. Biol Plant 44:105–109Google Scholar
  66. 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 111:60–65Google Scholar
  67. Kabata-Pendias A, Pendias H (1992) Trace elements in soils and plants, 2nd edn. CRC Press, Boca RatonGoogle Scholar
  68. Kabata-Pendias A, Pendias H (2001) Trace elements in soils and plants, 3rd edn. CRC Press, Boca RatonGoogle Scholar
  69. 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
  70. 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
  71. 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 223:2799–2806Google Scholar
  72. Kopittk PM, Menzies NW (2006) Effect of Cu toxicity on growth of cowpea (Vigna unguiculata). Plant Soil 279:287–296Google Scholar
  73. 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 156:663–673Google Scholar
  74. Krzeslowska M (2011) The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiol Plant 33:35–51Google Scholar
  75. 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 27:399–409Google Scholar
  76. 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 30:485–488Google Scholar
  77. 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 6:40–43Google Scholar
  78. 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 44:6926–6932Google Scholar
  79. Lin J, Jiang W, Liu D (2003) Accumulation of copper by roots, hypocotyls, cotyledons and leaves of sunflower (Helianthus annuus L.). Bioresour Technol 86:151–155Google Scholar
  80. 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 81:507–522Google Scholar
  81. Liu DH, Jiang WS, Hou WQ (2001) Uptake and accumulation of copper by roots and shoots of maize (Zea mays L.). J Environ Sci 13:228–232Google Scholar
  82. Liu JJ, Wei Z, Li JH (2014) Effects of copper on leaf membrane structure and root activity of maize seedling. Bot Stud 55:1–6Google Scholar
  83. 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 160:259–266Google Scholar
  84. 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 28:80–86Google Scholar
  85. 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 115:113–120Google Scholar
  86. Mackie KA, Müller T, Kandeler E (2012) Remediation of copper in vineyards—a mini review. Environ Pollut 167:16–26Google Scholar
  87. Mahmood T, Islam KR, Muhammad S (2007) Toxic effects of heavy metals on early growth and tolerance of cereal crops. Pak J Bot 39:451–462Google Scholar
  88. 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 3:53–62Google Scholar
  89. 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 250:249–257Google Scholar
  90. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, San DiegoGoogle Scholar
  91. McBride MS, Sauve S, Hendershot W (1997) Solubility control of Cu, Zn, Cd and Pb in contaminated soils. Eur J Soil Sci 48:337–346Google Scholar
  92. 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 BaselGoogle Scholar
  93. 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
  94. Mench M (1990) Transfert des oligo-éléments du sol à la racine et absorption. Compte Rendu de l’Académie d’Agriculture Française 76:17–30Google Scholar
  95. 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 49:95–101Google Scholar
  96. 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 21:301–304Google Scholar
  97. 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 298:99–111Google Scholar
  98. Michaud AM, Chappellaz C, Hinsinger P (2008) Copper phytotoxicity affects root elongation and iron nutrition in durum wheat (Triticum turgidum durum L.). Plant Soil 310:151–165Google Scholar
  99. 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 65:863–872Google Scholar
  100. Mishra S, Dubey RS (2005) Heavy metal toxicity induced alterations in photosynthetic metabolism in plants. Handbook of Photosynthesis 2:845–863Google Scholar
  101. 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 138:211–222Google Scholar
  102. 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 182:287–300Google Scholar
  103. 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 81:193–201Google Scholar
  104. 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 32:1882–1900Google Scholar
  105. Muccifora S, Bellani LM (2013) Effects of copper on germination and reserve mobilization in Vicia sativa L. seeds. Environ Pollut 179:68–74Google Scholar
  106. 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 67:83–90Google Scholar
  107. 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 30:2012–2190Google Scholar
  108. 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 35:167–176Google Scholar
  109. Ouzounidou G, Ilias I, Tranopoulou H, Karataglis S (1998) Amelioration of copper toxicity by iron on spinach physiology. J Plant Nutr 21:2089–2101Google Scholar
  110. Pantola RC, Shekhawat GS (2012) Copper induced antioxidative enzyme indices in leaves of Brassica juncea seedlings. J Pharm Biomed Sci 15:1–6Google Scholar
  111. 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 129:1359–1367Google Scholar
  112. 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 72:596–602Google Scholar
  113. 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)Google Scholar
  114. 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 199:367–378Google Scholar
  115. 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 279:15348–15355Google Scholar
  116. 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 84:52–60Google Scholar
  117. 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 127:119–129Google Scholar
  118. 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 100:133–149Google Scholar
  119. Scheck HJ, Pscheidt JW (1998) Effect of Cu bactericides on Cu-resistant and -sensitive strains of Pseudomonas syringae pv. syringae. Plant Dis 82:397–406Google Scholar
  120. 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 167:438–446Google Scholar
  121. 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 232:1–44Google Scholar
  122. 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 57:711–726Google Scholar
  123. 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 9:5–13Google Scholar
  124. 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 278:341–349Google Scholar
  125. 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 302:163–174Google Scholar
  126. Singh D, Nath K, Sharma YK (2007) Response of wheat seed germination and seedling growth under copper stress. J Environ Biol 28:409–414Google Scholar
  127. Sommer AL (1931) Copper as an essential for plant growth. Plant Physiol 6:339–345Google Scholar
  128. 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 27:265–276Google Scholar
  129. 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 55:175–178Google Scholar
  130. 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 67:89–98Google Scholar
  131. 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 116:1593–1602Google Scholar
  132. 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 53:33–39Google Scholar
  133. 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 267:255–263Google Scholar
  134. 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 8:83–92Google Scholar
  135. 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 25:2343–2360Google Scholar
  136. 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 29:33–43Google Scholar
  137. 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 7:200–204Google Scholar
  138. 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 163:53–58Google Scholar
  139. 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 8:203–213Google Scholar
  140. 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
  141. 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 70:36–45Google Scholar
  142. Wani PA, Khan MS, Zaidi A (2008) Chromium-reducing and plant growth-promoting Mesorhizobium improves chickpea growth in chromium-amended soil. Biotechnol Lett 30:159–163Google Scholar
  143. Wheeler DM, Power IL (1995) Comparison of plant uptake and plant toxicity of various ions in wheat. Plant Soil 172:167–173Google Scholar
  144. White MC, Baker FD, Chaney RL, Decker AM (1981) Metal complexation in xylem fluid. 2. Theoretical equilibrium-model and computational computer-program. Plant Physiol 67:301–310Google Scholar
  145. 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 50:380–386Google Scholar
  146. Wu C, Mosher BP, Zeng T (2006) One-step green route to narrowly dispersed copper nanocrystals. J Nanoparticle Res 8:965–969Google Scholar
  147. 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 325:79–95Google Scholar
  148. Wu C, Luo Y, Zhang L (2010) Variability of copper availability in paddy fields in relation to selected soil properties in southeast China. Geoderma 156:200–206Google Scholar
  149. 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
  150. Xiong J, Wang Y, Xue Q, Wu X (2011) Synthesis of highly stable dispersions of nanosized copper particles using L-ascorbic acid. Green Chem 13:900–904Google Scholar
  151. 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 12:125–132Google Scholar
  152. 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 62:602–607Google Scholar
  153. 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 76:167–179Google Scholar
  154. 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 65:1690–1696Google Scholar
  155. 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 75:934–938Google Scholar
  156. Yruela I (2005) Copper in plants. Braz J Plant Physiol 17:145–156Google Scholar
  157. Yruela I (2009) Copper in plants: acquisition, transport and interactions. Funct Plant Biol 36:409–430Google Scholar
  158. Yruela I (2013) Transition metals in plant photosynthesis. Metallomics 5:1090–1109Google Scholar
  159. 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 28:561–566Google Scholar
  160. Zheng YB, Wang LP, Dixon MA (2004) Response to copper toxicity for three ornamental crops in solution culture. Hortic Sci 39:1116–1120Google Scholar
  161. Zheng Y, Wang L, Cayanan DF, Dixon M (2010) Greenhouse cucumber growth and yield response to copper application. Hortic Sci 45:771–774Google Scholar
  162. 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

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Muhammad Adrees
    • 1
  • Shafaqat Ali
    • 1
  • Muhammad Rizwan
    • 1
    Email author
  • Muhammad Ibrahim
    • 1
  • Farhat Abbas
    • 1
  • Mujahid Farid
    • 1
  • Muhammad Zia-ur-Rehman
    • 2
  • Muhammad Kashif Irshad
    • 1
  • Saima Aslam Bharwana
    • 1
  1. 1.Department of Environmental Sciences and EngineeringGovernment College UniversityFaisalabadPakistan
  2. 2.Institute of Soil and Environmental SciencesUniversity of AgricultureFaisalabadPakistan

Personalised recommendations