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.
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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
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
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
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
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
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
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
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
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
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
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
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
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
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
Ballabio C et al (2018) Copper distribution in European topsoils: an assessment based on LUCAS soil survey. Sci Total Environ 636:282–298
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
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
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
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
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
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
Bosnić D, Bosnić P, Nikolić D, Nikolić M, Samardžić J (2019) Silicon and iron differently alleviate copper toxicity in cucumber leaves. Plants 8:554
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
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
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
Cambrollé J, García JL, Figueroa ME, Cantos M (2015) Evaluating wild grapevine tolerance to copper toxicity. Chemosphere 120:171–178
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
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
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
Chen J et al (2015) Copper induced oxidative stresses, antioxidant responses and phytoremediation potential of Moso bamboo (Phyllostachys pubescens). Sci Rep 5:1–9
Chitra K (2017) Effect of copper on germination and seedlings growth of radish (Raphanus sativum L). J Environ Sci 11:1–2
Choi M, Davidson VL (2011) Cupredoxins—a study of how proteins may evolve to use metals for bioenergetic processes. Metallomics 3(2):140–151
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
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
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
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
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
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
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
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
Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9
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
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
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
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
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
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
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
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
Festa RA, Thiele DJ (2011) Copper: an essential metal in biology. Curr Biol 21(21):R877–R883
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
Fifield FW, Haines PJ (2000) Environmental analytical chemistry. Blackwell Science, London
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
Foyer CH, Noctor G (2000) Tansley Review 112. Oxygen processing in photosynthesis: regulation and signaling. New Phytol 146:359–388
Ganesh S, Sundaramoorthy P (2018) Copper and zinc induced changes in soybean (Glycine max (L.) Merr.). Innov Agric 1:9–12
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
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
Gong Q et al (2019a) Effects of copper on the growth, antioxidant enzymes and photosynthesis of spinach seedlings. Ecotox Environ Safe 171:771–780
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
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
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
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
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
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
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
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
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
Husak VV (2015) Copper and copper-containing pesticides: metabolism, toxicity and oxidative stress. J Vasyl Stefanyk Precarpathian National Univ 2:39–51
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
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
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
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
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
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
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
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
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
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
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
Lightbody JJ, Krogmann DW (1967) Isolation and properties of plastocyanin from Anabaenavariabilis. Biochim Biophys Acta 131:508–515
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
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
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
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
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
Liu Q, Luo L, Zheng L (2018c) Lignins: biosynthesis and biological functions in plants. Int J Mol Sci 19(2):335
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
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
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
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
Maathuis FJ (2013) Plant mineral nutrients: methods and protocols. Springer
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
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
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
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
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
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
Marschner H (2011) Marschner’s mineral nutrition of higher plants. Academic Press, Cambridge
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
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
Melania-Nicoleta B, Micle V (2015) Effects of copper-induced stress on seed germination of maize (Zea mays L.). JASP 3:95–96
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
Minkina T et al (2020) Anatomical and ultrastructural responses of Hordeum sativum to the soil spiked by copper. Environ Geochem Health 42:45–58
Mishra A, Shukla D, Vaghela K, Saraf M (2019) Copper: Its biologicalrole and toxicity. J Indian Bot Soc 98:26–35
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
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
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
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
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
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
Muccifora S, Bellani LM (2013) Effects of copper on germination and reserve mobilization in Vicia sativa L. seeds. Environ poll 179:68–74
Nagalakshmi N, Prasad MNV (2001) Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci 160:291–299
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
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
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
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
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
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
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
Osmolovskaya N, Dung VV, Kuchaeva L (2018) The role of organic acids in heavy metal tolerance in plants. Biol Commun 63(1):9
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Saha D, Mandal S, Saha A (2012) Copper induced oxidative stress in tea (Camellia sinensis) leaves. J Environ Biol 33:861
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
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
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
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
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
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
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
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
Sethy SK, Ghosh S (2013) Effect of heavy metals on germination of seeds. J Nat Sci Biol Med 4:272
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
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
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
Singh D, Nath K, Sharma YK (2007) Response of wheat seed germination and seedling growth under copper. J Environ Biol 28:409
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
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
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
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
Sunkar R, Zhu J-K (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019
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
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
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
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
Van Tichelen KK, Colpaert JV, Vangronsveld J (2001) Ectomycorrhizal protection of Pinus sylvestris against copper toxicity. New Phytol 150(1):203–213
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
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
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
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
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
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
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
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
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
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
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
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
Yruela I (2009) Copper in plants: acquisition, transport and interactions. Funct Plant Biol 36:409–430
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
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
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
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
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The first author is thankful to the University Grant Commission, New Delhi for awarding non-net fellowship (Grant Number 17 PHD BT 025).
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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
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DOI: https://doi.org/10.1007/s10534-021-00306-z