Skip to main content

Advertisement

Log in

Copper: uptake, toxicity and tolerance in plants and management of Cu-contaminated soil

  • Published:
BioMetals Aims and scope Submit manuscript

Abstract

Copper (Cu) is an essential mineral nutrient for the proper growth and development of plants; it is involved in myriad morphological, physiological, and biochemical processes. Copper acts as a cofactor in various enzymes and performs essential roles in photosynthesis, respiration and the electron transport chain, and is a structural component of defense genes. Excess Cu, however, imparts negative effects on plant growth and productivity. Many studies have summarized the adverse effects of excess Cu on germination, growth, photosynthesis, and antioxidant response in agricultural crops. Its inhibitory influence on mineral nutrition, chlorophyll biosynthesis, and antioxidant enzyme activity has been verified. The current review focuses on the availability and uptake of Cu by plants. The toxic effects of excess Cu on seed germination, plant growth and development, photosynthesis, and antioxidant response in plants are discussed. Plant tolerance mechanisms against Cu stress, and management of Cu-contaminated soils are presented.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

  • Abraham K, Sridevi R, Suresh B, Damodharam T (2013) Effect of heavy metals (Cd, Pb, Cu) on seed germination of Arachis hypogeae L. Asian J Plant Sci 3:10–12

    CAS  Google Scholar 

  • Adeleke R, Nwangburuka C, Oboirien B (2017) Origins, roles and fate of organic acids in soils: a review. S Afr J Bot 108:393–406

    Article  CAS  Google Scholar 

  • Adrees M et al (2015) The effect of excess copper on growth and physiology of important food crops: a review. Environ Sci Pollut Res 22:8148–8162

    Article  CAS  Google Scholar 

  • Aghajanzadeh TA, Prajapati DH, Burow M (2020) Copper toxicity affects indolic glucosinolates and gene expression of key enzymes for their biosynthesis in Chinese cabbage. Arch Agron Soil Sci 66:1288–1301

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  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 (Cucumis sativus) and its relationships with carbohydrate accumulation and changes in ion contents. Plant Sci 166:1213–1218

    Article  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. https://doi.org/10.1023/A:1014995321560

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Ambrosini VG, Rosa DJ, Basso A, Borghezan M, Pescador R, Miotto A, Melo GWBD, Soares CRFDS, Comin JJ, Brunetto G (2017) Liming as an ameliorator of copper toxicity in black oat (Avena strigosa Schreb.). J Plant Nutr 40:404–416

    Article  CAS  Google Scholar 

  • Ambrosini VG, Rosa DJ, de Melo GWB, Zalamena J, Cella C, Simão DG, da Silva LS, dos Santos HP, Toselli M, Tiecher TL, Brunetto G (2018) High copper content in vineyard soils promotes modifications in photosynthetic parameters and morphological changes in the root system of ‘Red Niagara’ plantlets. Plant Physiol Bioch 128:89–98

    Article  CAS  Google Scholar 

  • Apodaca SA, Tan W, Dominguez OE, Hernandez-Viezcas JA, Peralta-Videa JR, Gardea-Torresdey JL (2017) Physiological and biochemical effects of nanoparticulate copper, bulk copper, copper chloride, and kinetin in kidney bean (Phaseolus vulgaris) plants. Sci Total Environ 599:2085–2094

    Article  PubMed  CAS  Google Scholar 

  • Apori OS, Hanyabui E, Asiamah YJ (2018) Remediation technology for copper contaminated soil: a review. Asian J Agric Res 1–7.

  • 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

    Article  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

    CAS  Google Scholar 

  • Baker D, Senft J (1995) Heavy metals in soils Blackie Academic and Professional, Glasgow

  • Baldi E, Miotto A, Ceretta CA, Quartieri M, Sorrenti G, Brunetto G, Toselli M (2018) Soil-applied phosphorous is an effective tool to mitigate the toxicity of copper excess on grapevine grown in rhizobox. Sci Hortic 227:102–111

    Article  CAS  Google Scholar 

  • Ballabio C et al (2018) Copper distribution in European topsoils: an assessment based on LUCAS soil survey. Sci Total Environ 636:282–298

    Article  CAS  PubMed  Google Scholar 

  • Bankaji I, Caçador I, Sleimi N (2015) Physiological and biochemical responses of Suaeda fruticosa to cadmium and copper stresses: growth, nutrient uptake, antioxidant enzymes, phytochelatin, and glutathione levels. Environ Sci Pollut R 22:13058–13069

    Article  CAS  Google Scholar 

  • Barr R, Crane FL (1976) Organization of electron transport in photosystem II of spinach chloroplasts according to chelator inhibition sites. Plant Physiol 57:450–453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Batool R, Hameed M, Ashraf M, Ahmad MSA, Fatima S (2015) Physio-anatomical responses of plants to heavy metals. Phytoremediation for green energy. Springer, Dordrecht, pp 79–96

    Chapter  Google Scholar 

  • Ben Massoud M, Sakouhi L, Chaoui A (2019) Effect of plant growth regulators, calcium and citric acid on copper toxicity in pea seedlings. J Plant Nutr 42:1230–1242

    Article  CAS  Google Scholar 

  • Bernal M, Ramiro MV, Cases R, Picorel R, Yruela I (2006) Excess copper effect on growth, chloroplast ultrastructure, oxygen-evolution activity and chlorophyll fluorescence in Glycine max cell suspensions. Physiol Plant 127:312–325

    Article  CAS  Google Scholar 

  • Bernal M, Casero D, Singh V, Wilson GT, Grande A, Yang H, Dodani SC, Pellegrini M, Huijser P, Connolly EL, Merchant SS (2012) Transcriptome sequencing identifies SPL7-regulated copper acquisition genes FRO4/FRO5 and the copper dependence of iron homeostasis in Arabidopsis. Plant Cell 24:738–761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bosnić D, Bosnić P, Nikolić D, Nikolić M, Samardžić J (2019) Silicon and iron differently alleviate copper toxicity in cucumber leaves. Plants 8:554

    Article  PubMed Central  CAS  Google Scholar 

  • Brînză M, Chelariu EL, Aiordăchioaiei A, Draghia L (2018) Copper effect on seed germination and plant sprouting of Alyssum murale species. Sci Papers Series B Hortic 571–574

  • Brunetto G et al (2016) Copper accumulation in vineyard soils: rhizosphere processes and agronomic practices to limit its toxicity. Chemosphere 162:293–307

    Article  CAS  PubMed  Google Scholar 

  • Brunetto G et al (2019) Use of phosphorus fertilization and mycorrhization as strategies for reducing copper toxicity in young grapevines. Sci Hortic 248:176–183

    Article  CAS  Google Scholar 

  • Buapet P, Mohammadi NS, Pernice M, Kumar M, Kuzhiumparambil U, Ralph PJ (2019) Excess copper promotes photoinhibition and modulates the expression of antioxidant-related genes in Zostera muelleri. Aquat Toxicol 207:91–100

    Article  CAS  PubMed  Google Scholar 

  • Cambrollé J, García JL, Figueroa ME, Cantos M (2015) Evaluating wild grapevine tolerance to copper toxicity. Chemosphere 120:171–178

    Article  PubMed  CAS  Google Scholar 

  • Cao Y-Y et al (2019) Melatonin alleviates copper toxicity via improving copper sequestration and ROS scavenging in cucumber. Plant Cell Physiol 60:562–574

    Article  CAS  PubMed  Google Scholar 

  • Cervantes-Cervantes MP, Calderón-Salinas JV, Albores A, Muñoz-Sánchez JL (2005) Copper increases the damage to DNA and proteins caused by reactive oxygen species. Biol Trace Elem Res 103:229–248

    Article  CAS  PubMed  Google Scholar 

  • Chamseddine M, Wided BA, Guy H, Marie-Edith C, Fatma J (2009) Cadmium and copper induction of oxidative stress and antioxidative response in tomato (Solanum lycopersicon) leaves. Plant Growth Regul 57:89–99

    Article  CAS  Google Scholar 

  • Chen J et al (2015) Copper induced oxidative stresses, antioxidant responses and phytoremediation potential of Moso bamboo (Phyllostachys pubescens). Sci Rep 5:1–9

    Google Scholar 

  • Chitra K (2017) Effect of copper on germination and seedlings growth of radish (Raphanus sativum L). J Environ Sci 11:1–2

    CAS  Google Scholar 

  • Choi M, Davidson VL (2011) Cupredoxins—a study of how proteins may evolve to use metals for bioenergetic processes. Metallomics 3(2):140–151

    Article  CAS  PubMed  Google Scholar 

  • Chu HH, Conte SS, Chan Rodriguez D, Vasques K, Punshon T, Salt DE, Walker EL (2013) Arabidopsis thaliana Yellow Stripe1-Like4 and Yellow Stripe1-Like6 localize to internal cellular membranes and are involved in metal ion homeostasis. Front Plant Sci 4:283

    PubMed  PubMed Central  Google Scholar 

  • Contreras RA, Pizarro M, Köhler H, Sáez CA, Zúñiga GE (2018) Copper stress induces antioxidant responses and accumulation of sugars and phytochelatins in Antarctic Colobanthus quitensis (Kunth) Bartl. Biol Res 51:1–10

    Article  CAS  Google Scholar 

  • Costa MB, Tavares FV, Martinez CB, Colares IG, Martins CdMG (2018) Accumulation and effects of copper on aquatic macrophytes Potamogeton pectinatus L.: potential application to environmental monitoring and phytoremediation. Ecotox Environ Safe 155:117–124

    Article  CAS  Google Scholar 

  • Cota-Ruiz K et al (2018) Toxicity of copper hydroxide nanoparticles, bulk copper hydroxide, and ionic copper to alfalfa plants: a spectroscopic and gene expression study. Environ Pollut 243:703–712

    Article  CAS  PubMed  Google Scholar 

  • De Conti L et al (2020) Iron fertilization to enhance tolerance mechanisms to copper toxicity of ryegrass plants used as cover crop in vineyards. Chemosphere 243:125298

    Article  PubMed  CAS  Google Scholar 

  • De Oliveira PD, Ambrosini VG, De Melo GWB, Zalamena J, Brunetto G (2015) Uso de calcário na amenização da toxidez de cobre em videiras jovens. Científica 43:427–435

    Article  Google Scholar 

  • De Vos CR, Schat H, Vooijs R, Ernst WH (1989) Copper-induced damage to the permeability barrier in roots of Silene cucubalus. J Plant Physiol 135:164–169

    Article  Google Scholar 

  • Deng F, Yamaji N, Xia J, Ma JF (2013) A member of the heavy metal P-type ATPase OsHMA5 is involved in xylem loading of copper in rice. Plant Physiol 163:1353–1362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9

    Article  CAS  Google Scholar 

  • Djeukam C, Theriault G, Michael P, Nkongolo K (2016) Analysis of gene expression associated with copper toxicity in white birch (Betula papyrifera) populations from a mining region. Biotechnol J Int 15:1–10

    Google Scholar 

  • El-Beltagi HS, Sofy MR, Aldaej MI, Mohamed HI (2020) Silicon alleviates copper toxicity in flax plants by up-regulating antioxidant defense and secondary metabolites and decreasing oxidative damage. Sustainability 12:4732

    Article  CAS  Google Scholar 

  • Farid M, Farooq MA, Fatima A, Abubakar M, Ali S, Raza N, Alhaithloul HA, Soliman MH (2021) Copper-induced responses in different plant species. Approaches to the remediation of inorganic pollutants. Springer, Singapore

    Google Scholar 

  • Fariduddin Q, Yusuf M, Hayat S, Ahmad A (2009) Effect of 28-homobrassinolide on antioxidant capacity and photosynthesis in Brassica juncea plants exposed to different levels of copper. Environ Exp Bot 66:418–424

    Article  CAS  Google Scholar 

  • Fatima A, Farid M, Alharby HF, Bamagoos AA, Rizwan M, Ali S (2020) Efficacy of fenugreek plant for ascorbic acid assisted phytoextraction of copper (Cu); a detailed study of Cu induced morpho-physiological and biochemical alterations. Chemosphere 251:126424

    Article  CAS  PubMed  Google Scholar 

  • Feigl G et al (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

    Article  CAS  PubMed  Google Scholar 

  • Feigl G, Kumar D, Lehotai N, Pető A, Molnár Á, Rácz É, Ördög A, Erdei L, Kolbert Z, 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 Hung 66:205–221

    Article  CAS  PubMed  Google Scholar 

  • Feil SB, Pii Y, Valentinuzzi F, Tiziani R, Mimmo T, Cesco S (2020) Copper toxicity affects phosphorus uptake mechanisms at molecular and physiological levels in Cucumis sativus plants. Plant Physiol Biochem 157:138–147

    Article  CAS  PubMed  Google Scholar 

  • Festa RA, Thiele DJ (2011) Copper: an essential metal in biology. Curr Biol 21(21):R877–R883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fidalgo F, Azenha M, Silva AF, de 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

    Article  Google Scholar 

  • Fifield FW, Haines PJ (2000) Environmental analytical chemistry. Blackwell Science, London

    Google Scholar 

  • Flora C, Khandekar S, Boldt J, Leisner S (2019) Silicon alleviates long-term copper toxicity and influences gene expression in Nicotiana tabacum. J Plant Nutr 42:864–878

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2000) Tansley Review 112. Oxygen processing in photosynthesis: regulation and signaling. New Phytol 146:359–388

    Article  CAS  Google Scholar 

  • Ganesh S, Sundaramoorthy P (2018) Copper and zinc induced changes in soybean (Glycine max (L.) Merr.). Innov Agric 1:9–12

    Google Scholar 

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

    CAS  Google Scholar 

  • Garcia JS, Dalmolin ÂC, Cortez PA, Barbeira PS, Mangabeira PA, França MG (2018) Short-term cadmium exposure induces gas exchanges, morphological and ultrastructural disturbances in mangrove Avicennia schaueriana young plants. Mar Pollut Bull 131:122–129

    Article  CAS  PubMed  Google Scholar 

  • Gong Q et al (2019a) Effects of copper on the growth, antioxidant enzymes and photosynthesis of spinach seedlings. Ecotox Environ Safe 171:771–780

    Article  CAS  Google Scholar 

  • Gong Q, Wang L, Dai TW, Kang Q, Zhou JY, Li ZH (2019b) Effects of copper treatment on mineral nutrient absorption and cell ultrastructure of spinach seedlings Ying yong sheng tai xue bao. J Appl Ecol 30:941–950

    Google Scholar 

  • Hamed SM, Selim S, Klöck G, AbdElgawad H (2017) Sensitivity of two green microalgae to copper stress: growth, oxidative and antioxidants analyses. Ecotox Environ Safe 144:19–25

    Article  CAS  Google Scholar 

  • Hasanuzzaman M, Bhuyan MHM, Anee TI, Parvin K, Nahar K, Mahmud JA, Fujita M (2019) Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress. Antioxidants 8:384

    Article  CAS  PubMed Central  Google Scholar 

  • Hema C, Subramani A (2013) Phytotoxic effect of copper and chromium on seed germination percentage of Vigna radiate L. Int J Cur Res Rev 5:95–100

    CAS  Google Scholar 

  • Hernández JA, Ferrer MA, Jiménez A, Barceló AR, Sevilla F (2001) Antioxidant systems and O2/H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins. Plant Physiol 127:817–831

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoegger PJ, Kilaru S, James TY, Thacker JR, Kües U (2006) Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences. FEBS J 273:2308–2326

    Article  CAS  PubMed  Google Scholar 

  • Hoppen C, Müller L, Hänsch S, Uzun B, Milić D, Meyer AJ, Weidtkamp-Peters S, Groth G (2019) Soluble and membrane-bound protein carrier mediate direct copper transport to the ethylene receptor family. Sci Rep 9:1–11

    Article  Google Scholar 

  • Hossain MS, Abdelrahman M, Tran CD, Nguyen KH, Chu HD, Watanabe Y, Hasanuzzaman M, Mohsin SM, Fujita M, Tran LSP (2020) Insights into acetate-mediated copper homeostasis and antioxidant defense in lentil under excessive copper stress. Environ Pollut 258:113544

    Article  CAS  PubMed  Google Scholar 

  • Hu C, Liu L, Li X, Xu Y, Ge Z, Zhao Y (2018) Effect of graphene oxide on copper stress in Lemna minor L.: evaluating growth, biochemical responses, and nutrient uptake. J Hazard Mater 341:168–176

    Article  PubMed  CAS  Google Scholar 

  • Husak VV (2015) Copper and copper-containing pesticides: metabolism, toxicity and oxidative stress. J Vasyl Stefanyk Precarpathian National Univ 2:39–51

    Google Scholar 

  • Iqbal MZ, Nayab S, Shafiq M (2018) Effects of copper on seed germination and seedling growth performance of Lens culinaris medik. J Plant Dev Sci 25:85

    Article  Google Scholar 

  • İşeri ÖD, Körpe 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

    Article  PubMed  CAS  Google Scholar 

  • Islam F et al (2016) Copper-resistant bacteria reduces oxidative stress and uptake of copper in lentil plants: potential for bacterial bioremediation. Environ Sci Pollut R 23:220–233

    Article  CAS  Google Scholar 

  • Islam S, Zaid A, Mohammad F (2020) Role of triacontanol in counteracting the ill effects of salinity in plants: a review. J Plant Growth Regul 28:1

    Google Scholar 

  • Jalali K, Nouairi I, Kallala N, M’Sehli W, Zribi K, Mhadhbi H (2018) Germination, seedling growth, and antioxidant activity in four legume (Fabaceae) species under copper sulphate fungicide treatment. Pak J Bot 50:1599–1606

    CAS  Google Scholar 

  • Jung HI, Gayomba SR, Rutzke MA, Craft E, Kochian LV, Vatamaniuk OK (2012) COPT6 is a plasma membrane transporter that functions in copper homeostasis in Arabidopsis and is a novel target of SQUAMOSA promoter-binding protein-like 7. J Biol Chem 287:33252–33267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kopsell D, Kopsell D (2007) Handbook of plant nutrition

  • Korshunova YO, Eide D, Clark WG, Guerinot ML, Pakrasi HB (1999) The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol Biol 40:37–44

    Article  CAS  PubMed  Google Scholar 

  • Kumar V, Pandita S, Sidhu GPS, Sharma A, Khanna K, Kaur P, Bali AS, Setia R (2020) Copper bioavailability, uptake, toxicity and tolerance in plants: a comprehensive review. Chemosphere 127810.

  • Kumbhakar DV, Datta AK, Das D, Ghosh B, Pramanik A, Gupta S (2019) Assessment of oxidative stress, antioxidant enzyme activity and cellular apoptosis in a plant based system (Nigella sativa L.; black cumin) induced by copper and cadmium sulphide nanomaterials. Environ Nanotechnol Monit Manag 11:100196

    Google Scholar 

  • Li M, Hu C, Zhu Q, Chen L, Kong Z, Liu Z (2006) Copper and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in the microalga Pavlova viridis (Prymnesiophyceae). Chemosphere 62:565–572

    Article  CAS  PubMed  Google Scholar 

  • Li J, Liang H, Yan M, Chen L, Zhang H, Liu J, Wang S, Jin Z (2017) Arbuscular mycorrhiza fungi facilitate rapid adaptation of Elsholtzia splendens to copper. Sci Total Environ 599:1462–1468

    Article  PubMed  CAS  Google Scholar 

  • Li Q, Chen HH, Qi YP, Ye X, Yang LT, Huang ZR, Chen LS (2019) Excess copper effects on growth, uptake of water and nutrients, carbohydrates, and PSII photochemistry revealed by OJIP transients in Citrus seedlings. Environ Sci Pollut Res 26:30188–30205

    Article  CAS  Google Scholar 

  • Lightbody JJ, Krogmann DW (1967) Isolation and properties of plastocyanin from Anabaenavariabilis. Biochim Biophys Acta 131:508–515

    Article  CAS  PubMed  Google Scholar 

  • Lin CL, Kao CH (2002) Osmotic stress-induced changes in cell wall peroxidase activity and hydrogen peroxide level in roots of rice seedlings. Plant Growth Regul 37:177–184

    Article  CAS  Google Scholar 

  • Lin H, Zhang X-H, Chen J, Liang L, Liu L-H (2019) Phytoremediation potential of Leersia hexandra Swartz of copper contaminated soil and its enhancement by using agronomic management practices. Ecol Eng 127:561–566

    Article  Google Scholar 

  • Liu Q, Zheng L, He F, Zhao FJ, Shen Z, Zheng L (2015) Transcriptional and physiological analyses identify a regulatory role for hydrogen peroxide in the lignin biosynthesis of copper-stressed rice roots. Plant soil 387:323–336

    Article  CAS  Google Scholar 

  • Liu H, Mo Y, Kong X, Liu Y, Liu H (2016) Effects of copper on germination of watermelon seeds and growth of watermelon seedlings. In: Application of materials science and environmental materials (AMSEM2015) proceedings of the 3rd international conference, World Scientific, pp 108–113

  • Liu J, Dhungana B, Cobb GP (2018a) Copper oxide nanoparticles and arsenic interact to alter seedling growth of rice (Oryza sativa japonica). Chemosphere 206:330–337

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Wang J, Lee S, Wen R (2018b) Copper-caused oxidative stress triggers the activation of antioxidant enzymes via ZmMPK3 in maize leaves. PLoS ONE 13:0203612

    Google Scholar 

  • Liu Q, Luo L, Zheng L (2018c) Lignins: biosynthesis and biological functions in plants. Int J Mol Sci 19(2):335

    Article  PubMed Central  CAS  Google Scholar 

  • Liu J, Wolfe K, Cobb GP (2019a) Exposure to copper oxide nanoparticles and arsenic causes intergenerational effects on rice (Oryza sativa japonica Koshihikari) seed germination and seedling growth. Environ Toxicol Chem 38:1978–1987

    Article  CAS  PubMed  Google Scholar 

  • Liu N, Zhong G, Zhou J, Liu Y, Pang Y, Cai H, Wu Z (2019b) Separate and combined effects of glyphosate and copper on growth and antioxidative enzymes in Salvinia natans (L.). Sci Total Environ 655:1448–1456

    Article  CAS  PubMed  Google Scholar 

  • Liu Q et al (2019c) Potassium lignosulfonate as a washing agent for remediating lead and copper co-contaminated soils. Sci Total Environ 658:836–842

    Article  CAS  PubMed  Google Scholar 

  • Liu XS, Feng SJ, Zhang BQ, Wang MQ, Cao HW, Rono JK, Chen X, Yang ZM (2019d) OsZIP1 functions as a metal efflux transporter limiting excess zinc, copper and cadmium accumulation in rice. BMC Plant Biol 19:283

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Maathuis FJ (2013) Plant mineral nutrients: methods and protocols. Springer

    Book  Google Scholar 

  • Mahmood S, Hussain A, Saeed Z, Athar M (2005) Germination and seedling growth of corn (Zea mays L.) under varying levels of copper and zinc. Int J Sci Environ Technol 2:269–274

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Maksymiec W, Russa R, Urbanik-Sypniewska T, Baszyński T (1994) Effect of excess Cu on the photosynthetic apparatus of runner bean leaves treated at two different growth stages. Physiol Plant 91:715–721

    Article  CAS  Google Scholar 

  • Marastoni L, Sandri M, Pii Y, Valentinuzzi F, Brunetto G, Cesco S, Mimmo T (2019) Synergism and antagonisms between nutrients induced by copper toxicity in grapevine rootstocks: monocropping vs. intercropping. Chemosphere 214:563–578

    Article  CAS  PubMed  Google Scholar 

  • 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 229:1–14

    Article  CAS  Google Scholar 

  • Marques D, da Silva A, Mantovani J, Magalhães P, de Souza T (2019) Root morphology and leaf gas exchange in Peltophorum dubium (Spreng.) Taub. (Caesalpinioideae) exposed to copper-induced toxicity. S Afr J Bot 121:186–192

    Article  CAS  Google Scholar 

  • Marschner H (2011) Marschner’s mineral nutrition of higher plants. Academic Press, Cambridge

    Google Scholar 

  • Martins LL, Mourato MP (2006) Effect of excess copper on tomato plants: growth parameters, enzyme activities, chlorophyll, and mineral content. J Plant Nutr 29:2179–2198

    Article  CAS  Google Scholar 

  • 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 22:9922–9931

    Article  CAS  Google Scholar 

  • Melania-Nicoleta B, Micle V (2015) Effects of copper-induced stress on seed germination of maize (Zea mays L.). JASP 3:95–96

    Google Scholar 

  • Migocka M, Posyniak E, Maciaszczyk-Dziubinska E, Papierniak A, Kosieradzaka A (2015) Functional and biochemical characterization of cucumber genes encoding two copper ATPases CsHMA5. 1 and CsHMA5. 2. Elsevier

  • Milner MJ, Seamon J, Craft E, Kochian LV (2013) Transport properties of members of the ZIP family in plants and their role in Zn and Mn homeostasis. J Exp Bot 64:369–381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minkina T et al (2020) Anatomical and ultrastructural responses of Hordeum sativum to the soil spiked by copper. Environ Geochem Health 42:45–58

    Article  CAS  PubMed  Google Scholar 

  • Mishra A, Shukla D, Vaghela K, Saraf M (2019) Copper: Its biologicalrole and toxicity. J Indian Bot Soc 98:26–35

    Article  Google Scholar 

  • Møller SG, McPherson MJ (1998) Developmental expression and biochemical analysis of the Arabidopsis atao1 gene encoding an H2O2-generating diamine oxidase. Plant J 13:781–791

    Article  PubMed  Google Scholar 

  • Monferrán MV, Agudo JAS, Pignata ML, Wunderlin DA (2009) Copper-induced response of physiological parameters and antioxidant enzymes in the aquatic macrophyte Potamogeton pusillus. Environ Pollut 157:2570–2576

    Article  PubMed  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(3):193

    Article  CAS  Google Scholar 

  • Moravcová Š et al (2018a) Influence of salicylic acid pretreatment on seeds germination and some defence mechanisms of Zea mays plants under copper stress. Plant Physiol Biochem 122:19–30

    Article  PubMed  CAS  Google Scholar 

  • Moravcová Š, Tůma J, Dučaiová ZK, Waligórski P, Kula M, Saja D, Słomka A, Bąba W, Libik-Konieczny M (2018b) Influence of salicylic acid pretreatment on seeds germination and some defence mechanisms of Zea mays plants under copper stress. Plant Physiol Biochem 122:19–30

    Article  PubMed  CAS  Google Scholar 

  • Mostofa MG, Fujita M (2013) Salicylic acid alleviates copper toxicity in rice (Oryza sativa L.) seedlings by up-regulating antioxidative and glyoxalase systems. Ecotoxicol 22:959–973

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Nagalakshmi N, Prasad MNV (2001) Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci 160:291–299

    Article  CAS  PubMed  Google Scholar 

  • Nanda R, Agrawal V (2016) Elucidation of zinc and copper induced oxidative stress, DNA damage and activation of defence system during seed germination in Cassia angustifolia Vahl. Environ Exp Bot 125:31–41

    Article  CAS  Google Scholar 

  • Nanda R, Agrawal V (2018) Piriformospora indica, an excellent system for heavy metal sequestration and amelioration of oxidative stress and DNA damage in Cassia angustifolia Vahl under copper stress. Ecotox Environ Safe 156:409–419

    Article  CAS  Google Scholar 

  • Napoli M, Cecchi S, Grassi C, Baldi A, Zanchi CA, Orlandini S (2019) Phytoextraction of copper from a contaminated soil using arable and vegetable crops. Chemosphere 219:122–129

    Article  CAS  PubMed  Google Scholar 

  • Nazir F, Hussain A, Fariduddin Q (2019) Hydrogen peroxide modulate photosynthesis and antioxidant systems in tomato (Solanum lycopersicum L.) plants under copper stress. Chemosphere 230:544–558

    Article  CAS  PubMed  Google Scholar 

  • Nazir F, Fariduddin Q, Hussain A, Khan TA (2021) Brassinosteroid and hydrogen peroxide improve photosynthetic machinery, stomatal movement, root morphology and cell viability and reduce Cu-triggered oxidative burst in tomato. Ecotox Environ Safe 207:111081

    Article  CAS  Google Scholar 

  • Nicholls AM, Mal TK (2003) Effects of lead and copper exposure on growth of an invasive weed, Lythrum salicaria L. (Purple Loosestrife)

  • 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 

  • Orrego F, Ortiz-Calderón C, Lutts S, Ginocchio R (2020) Growth and physiological effects of single and combined Cu, NaCl, and water stresses on Atriplex atacamensis and A. halimus. Environ Exp Bot 169:103919

    Article  CAS  Google Scholar 

  • Osmolovskaya N, Dung VV, Kuchaeva L (2018) The role of organic acids in heavy metal tolerance in plants. Biol Commun 63(1):9

    Article  Google Scholar 

  • Panou-Filotheou H, Bosabalidis AM, Karataglis S (2001) Effects of copper toxicity on leaves of oregano (Origanum vulgare subsp. hirtum). Ann Bot 88:207–214

    Article  CAS  Google Scholar 

  • Parveen A et al (2020) Effect of citric acid on growth, ecophysiology, chloroplast ultrastructure, and phytoremediation potential of jute (Corchorus capsularis L.) seedlings exposed to copper stress. Biomolecules 10:592

    Article  CAS  PubMed Central  Google Scholar 

  • Printz B, Lutts S, Hausman JF, Sergeant K (2016) Copper trafficking in plants and its implication on cell wall dynamics. Front Plant Sci 7:601

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 4:2878–2891

    Article  CAS  Google Scholar 

  • Rather BA, Masood A, Sehar Z, Majid A, Anjum NA, Khan NA (2020) Mechanisms and role of nitric oxide in phytotoxicity-mitigation of copper. Front Plant Sci 11

  • Rebecca RC (2011) Copper: inorganic and coordination chemistry. Encyclopedia of inorganic and bioinorganic chemistry. Wiley, Weinheim

    Google Scholar 

  • Reckova S, Tuma J, Dobrev P, Vankova R (2019) Influence of copper on hormone content and selected morphological, physiological and biochemical parameters of hydroponically grown Zea mays plants. Plant Growth Regul 89:191–201

    Article  CAS  Google Scholar 

  • Rehman M, Liu L, Wang Q, Saleem MH, Bashir S, Ullah S, Peng D (2019a) Copper environmental toxicology, recent advances, and future outlook: a review. Environ Sci Pollut R 26:18003–18016

    Article  CAS  Google Scholar 

  • Rehman M, Maqbool Z, Peng D, Liu L (2019b) 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 26:5851–5861

    Article  CAS  Google Scholar 

  • Rehman M, Liu L, Bashir S, Saleem MH, Chen C, Peng D, Siddique KH (2019c) 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 138:121–129

    Article  CAS  PubMed  Google Scholar 

  • Rodrıguez FI, Esch JJ, Hall AE, Binder BM, Schaller GE, Bleecker AB (1999a) A copper cofactor for the ethylene receptor ETR1 from Arabidopsis. Science 283:996–998

    Article  PubMed  Google Scholar 

  • Rodrıguez FI, Esch JJ, Hall AE, Binder BM, Schaller GE, Bleecker AB (1999b) A copper cofactor for the ethylene receptor ETR1 from Arabidopsis. Science 283(5404):996–998

    Article  PubMed  Google Scholar 

  • Romić M, Matijević L, Bakić H, Romić D (2014) Copper accumulation in vineyard soils: distribution, fractionation and bioavailability assessment. In: Environmental risk assessment of soil contamination. IntechOpen

  • Rout JR, Sahoo SL (2013) Antioxidant enzyme gene expression in response to copper stress in Withania somnifera L. Plant Growth Regul 71:95–99

    Article  CAS  Google Scholar 

  • Roy SK, Cho SW, Kwon SJ, Kamal AHM, Lee DG, Sarker K, Lee MS, Xin Z, Woo SH (2017) Proteome characterization of copper stress responses in the roots of sorghum. Biometals 30:765–785

    Article  CAS  PubMed  Google Scholar 

  • Rozentsvet OA, Nesterov VN, Sinyutina NF (2012) The effect of copper ions on the lipid composition of subcellular membranes in Hydrilla verticillata. Chemosphere 89:108–113

    Article  CAS  PubMed  Google Scholar 

  • Ruyters S, Salaets P, Oorts K, Smolders E (2013) Copper toxicity in soils under established vineyards in Europe: a survey. Sci Total Environ 443:470–477

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Saha D, Mandal S, Saha A (2012) Copper induced oxidative stress in tea (Camellia sinensis) leaves. J Environ Biol 33:861

    CAS  PubMed  Google Scholar 

  • Saleem MH, Fahad S, Rehman M, Saud S, Jamal Y, Khan S, Liu L (2020a) Morpho-physiological traits, biochemical response and phytoextraction potential of short-term copper stress on kenaf (Hibiscus cannabinus L.) seedlings. PeerJ 8:e8321

    Article  PubMed  PubMed Central  Google Scholar 

  • Saleem MH, Rehman M, Kamran M, Afzal J, Noushahi HA, Liu L (2020b) Investigating the potential of different jute varieties for phytoremediation of copper-contaminated soil. Environ Sci Pollut R 27:30367–30377

    Article  CAS  Google Scholar 

  • Saleem MH et al (2020c) Morpho-physiological traits, gaseous exchange attributes, and phytoremediation potential of jute (Corchorus capsularis L.) grown in different concentrations of copper-contaminated soil. Ecotox Environ Safe 189:109915

    Article  CAS  Google Scholar 

  • Saleem MH et al (2020d) Copper-induced oxidative stress, initiation of antioxidants and phytoremediation potential of flax (Linum usitatissimum L.) seedlings grown under the mixing of two different soils of China. Environ Sci Pollut R 27:5211–5221

    Article  CAS  Google Scholar 

  • Sancenón V, Puig S, Mira H, Thiele DJ, Peñarrubia L (2003) Identification of a copper transporter family in Arabidopsis thaliana. Plant Mol Biol 51:577–587

    Article  PubMed  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 soybeanplants grown under conditions of copper excess. Environ Exp Bot 84:52–60. https://doi.org/10.1016/j.envexpbot.2012.04.017

    Article  CAS  Google Scholar 

  • Sánchez-Pardo B, Fernández-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

    Article  PubMed  CAS  Google Scholar 

  • Sedbrook JC, Carroll KL, Hung KF, Masson PH, Somerville CR (2002) The Arabidopsis SKU5 gene encodes an extracellular glycosyl phosphatidylinositol-anchored glycoprotein involved in directional root growth. Plant Cell 14:1635–1648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sethy SK, Ghosh S (2013) Effect of heavy metals on germination of seeds. J Nat Sci Biol Med 4:272

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shabbir Z et al (2020) Copper uptake, essentiality, toxicity, detoxification and risk assessment in soil-plant environment. Chemosphere 127436

  • Shams M, Yildirim E, Guleray A, Ercisli S, Dursun A, Ekinci M, Raziye K (2018) Nitric oxide alleviates copper toxicity in germinating seed and seedling growth of Lactuca sativa L. Not Bot Horti Agrobo 46:167–172

    Article  CAS  Google Scholar 

  • Shams M, Ekinci M, Turan M, Dursun A, Kul R, Yildirim E (2019) Growth, nutrient uptake and enzyme activity response of Lettuce (Lactuca sativa L.) to excess copper. Environ Sustain 2:67–73

    Article  CAS  Google Scholar 

  • Sheldon A, Menzies N (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

    Article  CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Singh H, Kumar D, Soni V (2020) Copper and mercury induced oxidative stresses and antioxidant responses of Spirodela polyrhiza L. Biochem Biophys Rep 23:100781

    PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Souza VL, Almeida AAF, Souza JDS, Mangabeira PA, Jesus RM, Pirovani CP, Ahnert D, Baligar VC, Loguercio LL (2014) Altered physiology, cell structure, and gene expression of Theobroma cacao seedlings subjected to Cu toxicity. Environ Sci Pollut Res 21:1217–1230

    Article  CAS  Google Scholar 

  • Srivastava S, Mishra S, Tripathi RD, Dwivedi S, Gupta DK (2006) Copper-induced oxidative stress and responses of antioxidants and phytochelatins in Hydrilla verticillata (Lf) Royle. Aquat Toxicol 80:405–415

    Article  CAS  PubMed  Google Scholar 

  • Sunkar R, Zhu J-K (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor AA, Tsuji JS, Garry MR, McArdle ME, Goodfellow WL, Adams WJ, Menzie CA (2020) Critical review of exposure and effects: implications for setting regulatory health criteria for ingested copper. Environ Manage 65:131–159

    Article  PubMed  Google Scholar 

  • Theriault G, Nkongolo K (2016) Nickel and copper toxicity and plant response mechanisms in white birch (Betula papyrifera). B Environ Contam Toxicol 97:171–176

    Article  CAS  Google Scholar 

  • Tie SG, Tang ZJ, Zhao YM, Li W (2012) Oxidative damage and antioxidant response caused by excess copper in leaves of maize. Afr J Biotechnol 11:4378–4384

    CAS  Google Scholar 

  • Trentin E et al (2019) Potential of vermicompost and limestone in reducing copper toxicity in young grapevines grown in Cu-contaminated vineyard soil. Chemosphere 226:421–430

    Article  CAS  PubMed  Google Scholar 

  • Van Tichelen KK, Colpaert JV, Vangronsveld J (2001) Ectomycorrhizal protection of Pinus sylvestris against copper toxicity. New Phytol 150(1):203–213

    Article  Google Scholar 

  • Wang SH et al (2011) Copper-induced oxidative stress and responses of the antioxidant system in roots of Medicago sativa. J Agron Crop Sci 197:418–429

    Article  CAS  Google Scholar 

  • Wang R, Huang J, Liang A, Wang Y, Mur LAJ, Wang M, Guo S (2020) Zinc and copper enhance cucumber tolerance to fusaric acid by mediating its distribution and toxicity and modifying the antioxidant system. Int J Mol Sci 21:3370

    Article  CAS  PubMed Central  Google Scholar 

  • Wintz H et al (2003) Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. J Biol Chem 278:47644–47653

    Article  CAS  PubMed  Google Scholar 

  • Xu Q, Qiu H, Chu W, Fu Y, Cai S, Min H, Sha S (2013) Copper ultrastructural localization, subcellular distribution, and phytotoxicity in Hydrilla verticillata (Lf) Royle. Environ Sci Pollut Res 20:8672–8679

    Article  CAS  Google Scholar 

  • Xu Y, Yu W, Ma Q, Zhou H, Jiang C (2017) Toxicity of sulfadiazine and copper and their interaction to wheat (Triticum aestivum L.) seedlings. Ecotox Environ Safe 142:250–256

    Article  CAS  Google Scholar 

  • Xu L, Xing X, Liang J, Peng J, Zhou J (2019) In situ phytoremediation of copper and cadmium in a co-contaminated soil and its biological and physical effects. RSC Adv 9:993–1003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yadav P, Kaur R, Kohli SK, Sirhindi G, Bhardwaj R (2016) Castasterone assisted accumulation of polyphenols and antioxidant to increase tolerance of B. juncea plants towards copper toxicity. Cogent Food Agric 2:1276821

    Google Scholar 

  • Yadav P, Kaur R, Kanwar MK, Sharma A, Verma V, Sirhindi G, Bhardwaj R (2018) Castasterone confers copper stress tolerance by regulating antioxidant enzyme responses, antioxidants, and amino acid balance in B. juncea seedlings. Ecotox Environ Safe 147:725–734

    Article  CAS  Google Scholar 

  • Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Shikanai T (2009) SQUAMOSA promoter binding protein-like7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 21:347–361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang J, Chen Z, Wu S, Cui Y, Zhang L, Dong H, Yang C, Li C (2015) Overexpression of the Tamarix hispida ThMT3 gene increases copper tolerance and adventitious root induction in Salix matsudana Koidz. Plant Cell Tissue Organ Cult 121:469–479

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Younis M, Tourky S, Elsharkawy S (2018) Symptomatic parameters of oxidative stress and antioxidant defense system in Phaseolus vulgaris L. in response to copper or cadmium stress. S Afr J Bot 117:207–214

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Yuan M, Li X, Xiao J, Wang S (2011) Molecular and functional analyses of COPT/Ctr-type copper transporter-like gene family in rice. BMC Plant Biol 11:69

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zehra A, Choudhary S, Mukarram M, Naeem M, Khan MMA, Aftab T (2020) Impact of long-term copper exposure on growth, photosynthesis, antioxidant defence system and artemisinin biosynthesis in soil-grown Artemisia annua genotypes. B Environ Contam Toxicol 104:609–618

    Article  CAS  Google Scholar 

  • Zhang Z et al (2018a) Impact of copper nanoparticles and ionic copper exposure on wheat (Triticum aestivum L.) root morphology and antioxidant response. Environ Pollut 239:689–697

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Chen K, Zhao FJ, Sun C, Jin C, Shi Y, Sun Y, Li Y, Yang M, Jing X, Luo J (2018b) OsATX1 interacts with heavy metal P1B-type ATPases and affects copper transport and distribution. Plant physiol 178:329–344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The first author is thankful to the University Grant Commission, New Delhi for awarding non-net fellowship (Grant Number 17 PHD BT 025).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shamsul Hayat.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mir, A.R., Pichtel, J. & Hayat, S. Copper: uptake, toxicity and tolerance in plants and management of Cu-contaminated soil. Biometals 34, 737–759 (2021). https://doi.org/10.1007/s10534-021-00306-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10534-021-00306-z

Keywords

Navigation