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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Copper exposure leads to changes in chlorophyll content and secondary metabolite profile in Lantana fucata leaves

Carlise Patrícia Pivetta https://orcid.org/0000-0003-4792-5011 A B # , Samuel Francisco Chitolina https://orcid.org/0000-0001-8532-3973 A # , Nessana Dartora https://orcid.org/0000-0001-7700-0904 A * , Carla Maria Garlet de Pelegrin https://orcid.org/0000-0001-7795-8821 A B , Marlei Veiga dos Santos https://orcid.org/0000-0001-9692-001X A B , Fabiano Cassol https://orcid.org/0000-0001-9633-2955 A and Laura Spohr Batista https://orcid.org/0000-0002-6250-6248 A B
+ Author Affiliations
- Author Affiliations

A Universidade Federal da Fronteira Sul (UFFS), Cerro Largo, Brazil.

B Programa de Pós-Graduação em Ambientes e Tecnologias Sustentáveis (UFFS), Cerro Largo, Brazil.

* Correspondence to: nessana.dartora@uffs.edu.br
# These authors contributed equally to this paper

Handling Editor: Jian Feng Ma

Functional Plant Biology 50(7) 571-584 https://doi.org/10.1071/FP23047
Submitted: 19 October 2022  Accepted: 20 April 2023   Published: 16 May 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Cultivation of plants in environments polluted by metals at toxic levels can affect the biosynthesis of secondary metabolites. Here, we analysed the effect caused by excess copper on the concentration of chlorophylls a and b and the profile of secondary metabolites of Lantana fucata leaves. Five copper (Cu) treatments (mg Cu kg−1 soil) were tested: T0, 0; T1, 210; T2, 420; T3, 630; and T4, 840. We found that the concentrations of chlorophylls in the plants decreased when compared to the control. However, this did not lead to a significant reduction in its growth, possibly due to the low translocation of the metal to shoots and the activation of plant defence systems to tolerate the environment in which they are exposed, increasing the emission of lateral roots and activating pathways for the production of secondary metabolites. Therefore, we found a decrease in the concentration of two key compounds in secondary metabolism, p-coumaric and cinnamic acids in treatments with higher copper concentrations. We also found an increase in phenolics. Decreases in p-coumaric and cinnamic acids may have occurred because these are precursors in the synthesis of phenolic compounds, which are increased in the high Cu treatments. Six secondary metabolites were characterised, described for the first time for this plant species. Thus, the presence of excess Cu in the soil may have triggered an increase in the amount of reactive oxygen species in the plants, which that led to the synthesis of antioxidant compounds, as a defence strategy.

Keywords: chlorophylls, flavonoids, heavy metals, Lantana fucata, lateral roots, medicinal plants, metal stress, phenolics.


References

Ali MB, Singh N, Shohael AM, Hahn EJ, Paek K-Y (2006) Phenolics metabolism and lignin synthesis in root suspension cultures of Panax ginseng in response to copper stress. Plant Science 171, 147–154.
Phenolics metabolism and lignin synthesis in root suspension cultures of Panax ginseng in response to copper stress.Crossref | GoogleScholarGoogle Scholar |

Amin H, Arain BA, Jahangir TM, Abbasi AR, Mangi J, Abbasi MS, Amin F (2021) Copper (Cu) tolerance and accumulation potential in four native plant species: a comparative study for effective phytoextraction technique. Geology, Ecology, and Landscapes 5, 53–64.
Copper (Cu) tolerance and accumulation potential in four native plant species: a comparative study for effective phytoextraction technique.Crossref | GoogleScholarGoogle Scholar |

Appenroth K-J (2010) Definition of “heavy metals” and their role in biological systems. In ‘Soil heavy metals. Soil Biology’. (Eds I Sherameti, A Varma) pp. 19–29. (Springer: Heidelberg, Germany)

Baker AJM, Walker PL (1990) Ecophysiology of metal uptake by tolerant plants. In ‘Heavy metal tolerance in plants: evolutionary aspects’. (Ed. AJ Shaw) pp. 155–157. (CRC Press: Boca Raton, FL, USA)

Batista LS, Marques ERM, Pivetta CP, Dartora N, Pelegrin CMG, Cassol F, Veiga M (2020) Fitorremediação de solo contaminado por cobre: experimento piloto. In ‘Anais da SIEF – Semana Internacional de Engenharia e Economia FAHOR, 7–9 October 2020’. (FAOR, Horizontina, Brazil)

Berni R, Luyckx M, Xu X, Legay S, Sergeant K, Hausman J-F, Lutts S, Cai G, Guerriero G (2019) Reactive oxygen species and heavy metal stress in plants: impact on the cell wall and secondary metabolism. Environmental and Experimental Botany 161, 98–106.
Reactive oxygen species and heavy metal stress in plants: impact on the cell wall and secondary metabolism.Crossref | GoogleScholarGoogle Scholar |

Borghi M, Tognetti R, Monteforti G, Sebastiani L (2007) Responses of Populus x euramericana (P. deltoides x P. nigra) clone Adda to increasing copper concentrations. Environmental and Experimental Botany 61, 66–73.
Responses of Populus x euramericana (P. deltoides x P. nigra) clone Adda to increasing copper concentrations.Crossref | GoogleScholarGoogle Scholar |

Bremm EH, Pivetta CP, Machado FK, Dartora N, Pelegrin CMGd (2020) Morfoanatomia e fitomassa seca de Lantana fucata Lindl. (Verbenaceae) submetida a solo com excesso de cobre. In ‘Anais da X Jornada de Iniciação Científica e Tecnológica, 23–26 November 2020’. (UFFS, Chapecó, Brazil). Available at https://portaleventos.uffs.edu.br/index.php/JORNADA/article/view/14048 [In Portuguese]

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

Carrillo JT, Borthakur D (2021) Methods for metal chelation in plant homeostasis: review. Plant Physiology and Biochemistry 163, 95–107.
Methods for metal chelation in plant homeostasis: review.Crossref | GoogleScholarGoogle Scholar |

Chandran H, Meena M, Barupal T, Sharma K (2020) Plant tissue culture as a perpetual source for production of industrially important bioactive compounds. Biotechnology Reports 26, e00450
Plant tissue culture as a perpetual source for production of industrially important bioactive compounds.Crossref | GoogleScholarGoogle Scholar |

Dar TA, Uddin M, Khan MMA, Hakeem KR, Jaleel H (2015) Jasmonates counter plant stress: a review. Environmental and Experimental Botany 115, 49–57.
Jasmonates counter plant stress: a review.Crossref | GoogleScholarGoogle Scholar |

de la Rosa LA, Moreno-Escamilla JO, Rodrigo-Garcia J, Alvarez-Parrilla E (2019) Phenolic compounds. In ‘Postharvest physiology and biochemistry of fruits and vegetables’. (Ed. EM Yahia) pp. 253–271. (Woodhead Publishing: Cambridge, UK)

de Santana Julião L, Piccinelli AL, Marzocco S, Leitão SG, Lotti C, Autore G, Rastrelli L (2009) Phenylethanoid glycosides from Lantana fucata with in vitro anti-inflammatory activity. Journal of Natural Products 72, 1424–1428.
Phenylethanoid glycosides from Lantana fucata with in vitro anti-inflammatory activity.Crossref | GoogleScholarGoogle Scholar |

de Santana Julião L, Leitão SG, Lotti C, Picinelli AL, Rastrelli L, Fernandes PD, Noël F, Thibaut J-PB, Leitão GG (2010) Flavones and phenylpropanoids from a sedative extract of Lantana trifolia L. Phytochemistry 71, 294–300.
Flavones and phenylpropanoids from a sedative extract of Lantana trifolia L.Crossref | GoogleScholarGoogle Scholar |

Eckert GL, Smaniotto TA, Dartora N, Pelegrin CMGd, Baroni S (2022) The chemical composition of different leaf extracts of Lantana fucata Lindl. influences its cytotoxic potential: a study using the Allium cepa model. Journal of Ethnopharmacology 289, 115003
The chemical composition of different leaf extracts of Lantana fucata Lindl. influences its cytotoxic potential: a study using the Allium cepa model.Crossref | GoogleScholarGoogle Scholar |

Elzaawely AA, Xuan TD, Tawata S (2007) Changes in essential oil, kava pyrones and total phenolics of Alpinia zerumbet (Pers.) B.L. Burtt. & R.M. Sm. leaves exposed to copper sulphate. Environmental and Experimental Botany 59, 347–353.
Changes in essential oil, kava pyrones and total phenolics of Alpinia zerumbet (Pers.) B.L. Burtt. & R.M. Sm. leaves exposed to copper sulphate.Crossref | GoogleScholarGoogle Scholar |

Farah A, Donangelo CM (2006) Phenolic compounds in coffee. Brazilian Journal of Plant Physiology 18, 23–36.
Phenolic compounds in coffee.Crossref | GoogleScholarGoogle Scholar |

Ferreira EL, Sampaio GR, Torres EAFdS, Bastos DHM (2011) Natural antioxidant from Yerba Maté (Ilex paraguariensis St. Hil.) prevents hamburger peroxidation. Brazilian Archives of Biology and Technology 54, 803–809.
Natural antioxidant from Yerba Maté (Ilex paraguariensis St. Hil.) prevents hamburger peroxidation.Crossref | GoogleScholarGoogle Scholar |

Filho AG, Morel AF, Adolpho L, Ilha V, Giralt E, Tarrago T, Dalcol II (2012) Inhibitory effect of verbascoside isolated from Buddleja brasiliensis Jacq. ex Spreng on prolyl oligopeptidase activity. Phytotherapy Research 26, 1472–1475.
Inhibitory effect of verbascoside isolated from Buddleja brasiliensis Jacq. ex Spreng on prolyl oligopeptidase activity.Crossref | GoogleScholarGoogle Scholar |

Garlet TMB, Santos OS, Apel MA, Flores R (2007) Teor e qualidade do óleo essencial de Mentha x gracilis Sole (Lamiaceae) cultivada em hidroponia. Brazilian Journal of Biosciences 51, 14–116.

Goix S, Leveque T, Xiong T-T, Schreck E, Baeza-Squiban A, Geret F, Uzu G, Austruy A, Dumat C (2014) Environmental and health impacts of fine and ultrafine metallic particles: assessment of threat scores. Environmental Research 133, 185–194.
Environmental and health impacts of fine and ultrafine metallic particles: assessment of threat scores.Crossref | GoogleScholarGoogle Scholar |

Hemmerlin A, Harwood JL, Bach TJ (2012) A raison d’être for two distinct pathways in the early steps of plant isoprenoid biosynthesis? Progress in Lipid Research 51, 95–148.
A raison d’être for two distinct pathways in the early steps of plant isoprenoid biosynthesis?Crossref | GoogleScholarGoogle Scholar |

Huang W-L, Wu F-L, Huang H-Y, Huang W-T, Deng C-L, Yang L-T, Huang Z-R, Chen L-S (2020) Excess copper-induced alterations of protein profiles and related physiological parameters in citrus leaves. Plants 9, 291
Excess copper-induced alterations of protein profiles and related physiological parameters in citrus leaves.Crossref | GoogleScholarGoogle Scholar |

Hussain H, Hussain J, Al-Harrasi A, Shinwari ZK (2011) Chemistry of some species genus Lantana. Pakistan Journal of Botany 43, 51–62.

Ibrahim MH, Chee Kong Y, Mohd Zain NA (2017) Effect of cadmium and copper exposure on growth, secondary metabolites and antioxidant activity in the medicinal plant Sambung Nyawa (Gynura procumbens (Lour.) Merr). Molecules 22, 1623
Effect of cadmium and copper exposure on growth, secondary metabolites and antioxidant activity in the medicinal plant Sambung Nyawa (Gynura procumbens (Lour.) Merr).Crossref | GoogleScholarGoogle Scholar |

Iwasaki Y, Hirasawa T, Maruyama Y, Ishii Y, Ito R, Saito K, Umemura T, Nishikawa A, Nakazawa H (2011) Effect of interaction between phenolic compounds and copper ion on antioxidant and pro-oxidant activities. Toxicology in Vitro 25, 1320–1327.
Effect of interaction between phenolic compounds and copper ion on antioxidant and pro-oxidant activities.Crossref | GoogleScholarGoogle Scholar |

Izbianska K, Arasimowicz-Jelonek M, Deckert J (2014) Phenylpropanoid pathway metabolites promote tolerance response of lupine roots to lead stress. Ecotoxicology and Environmental Safety 110, 61–67.
Phenylpropanoid pathway metabolites promote tolerance response of lupine roots to lead stress.Crossref | GoogleScholarGoogle Scholar |

Jesus DdSd, Azevedo BOd, Pinelli MS, Korn MdGA, Azevedo Neto ADd, Lucchese AM, Oliveira LMd (2016) Growth and volatile compounds of Martianthus leucocephalus exposed to heavy metal stress. Ciência Rural 46, 2110–2117.
Growth and volatile compounds of Martianthus leucocephalus exposed to heavy metal stress.Crossref | GoogleScholarGoogle Scholar |

Kandil FE, Grace MH, Seigler DS, Cheeseman JM (2004) Polyphenolics in Rhizophora mangle L. leaves and their changes during leaf development and senescence. Trees 18, 518–528.
Polyphenolics in Rhizophora mangle L. leaves and their changes during leaf development and senescence.Crossref | GoogleScholarGoogle Scholar |

Kováčik J, Klejdus B, Backor M (2009a) Phenolic metabolism of Matricaria chamomilla plants exposed to nickel. Journal of Plant Physiology 166, 1460–1464.
Phenolic metabolism of Matricaria chamomilla plants exposed to nickel.Crossref | GoogleScholarGoogle Scholar |

Kováčik J, Klejdus B, Hedbavny J, Štork F, Backor M (2009b) Comparison of cadmium and copper effect on phenolic metabolism, mineral nutrients and stress-related parameters in Matricaria chamomilla plants. Plant and Soil 320, 231–242.
Comparison of cadmium and copper effect on phenolic metabolism, mineral nutrients and stress-related parameters in Matricaria chamomilla plants.Crossref | GoogleScholarGoogle Scholar |

Kroh GE, Pilon M (2020) Regulation of iron homeostasis and use in chloroplasts. International Journal of Molecular Sciences 21, 3395
Regulation of iron homeostasis and use in chloroplasts.Crossref | GoogleScholarGoogle Scholar |

Kumar S, Narula A, Sharma MP, Srivastava PS (2004) In vitro propagation of Pluchea lanceolata, a medicinal plant, and effect of heavy metals and different aminopurines on quercetin content. In Vitro Cellular & Developmental Biology – Plant 40, 171–176.
In vitro propagation of Pluchea lanceolata, a medicinal plant, and effect of heavy metals and different aminopurines on quercetin content.Crossref | GoogleScholarGoogle Scholar |

Küpper H, Andresen E (2016) Mechanisms of metal toxicity in plants. Metallomics 8, 269–285.
Mechanisms of metal toxicity in plants.Crossref | GoogleScholarGoogle Scholar |

Lajayer BA, Ghorbanpour M, Nikabadi S (2017a) Heavy metals in contaminated environment: destiny of secondary metabolite biosynthesis, oxidative status and phytoextraction in medicinal plants. Ecotoxicology and Environmental Safety 145, 377–390.
Heavy metals in contaminated environment: destiny of secondary metabolite biosynthesis, oxidative status and phytoextraction in medicinal plants.Crossref | GoogleScholarGoogle Scholar |

Lajayer HA, Savaghebi G, Hadian J, Hatami M, Pezhmanmehr M (2017b) Comparison of copper and zinc effects on growth, micro- and macronutrients status and essential oil constituents in pennyroyal (Mentha pulegium L.). Brazilian Journal of Botany 40, 379–388.
Comparison of copper and zinc effects on growth, micro- and macronutrients status and essential oil constituents in pennyroyal (Mentha pulegium L.).Crossref | GoogleScholarGoogle Scholar |

Li Y, Kong D, Fu Y, Sussman MR, Wu H (2020) The effect of developmental and environmental factors on secondary metabolites in medicinal plants. Plant Physiology and Biochemistry 148, 80–89.
The effect of developmental and environmental factors on secondary metabolites in medicinal plants.Crossref | GoogleScholarGoogle Scholar |

Liu S, Ali S, Yang R, Tao J, Ren B (2019) A newly discovered Cd-hyperaccumulator Lantana camara L. Journal of Hazardous Materials 371, 233–242.
A newly discovered Cd-hyperaccumulator Lantana camara L.Crossref | GoogleScholarGoogle Scholar |

Lucini L, Bernardo L (2015) Comparison of proteome response to saline and zinc stress in lettuce. Frontiers in Plant Science 6, 240
Comparison of proteome response to saline and zinc stress in lettuce.Crossref | GoogleScholarGoogle Scholar |

Maestri E, Marmiroli M, Visioli G, Marmiroli N (2010) Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environmental and Experimental Botany 68, 1–13.
Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment.Crossref | GoogleScholarGoogle Scholar |

Mahato SB, Sahu NP, Roy SK, Sharma OP (1994) Potential antitumor agents from Lantana camara: structures of flavonoid- and phenylpropanoid glycosides. Tetrahedron 50, 9439–9446.
Potential antitumor agents from Lantana camara: structures of flavonoid- and phenylpropanoid glycosides.Crossref | GoogleScholarGoogle Scholar |

Maldonado EM, Salamanca E, Gimenez A, Sterner O (2016) Antileishmanial metabolites from Lantana balansae. Brazilian Journal of Pharmacognosy 26, 180–183.
Antileishmanial metabolites from Lantana balansae.Crossref | GoogleScholarGoogle Scholar |

Marques DM, da Silva AB, Mantovani JR, Magalhães PC, de Souza TC (2019) Root morphology and leaf gas exchange in Peltophorum dubium (Spreng.) Taub. (Caesalpinioideae) exposed to copper-induced toxicity. South African Journal of Botany 121, 186–192.
Root morphology and leaf gas exchange in Peltophorum dubium (Spreng.) Taub. (Caesalpinioideae) exposed to copper-induced toxicity.Crossref | GoogleScholarGoogle Scholar |

Megateli S, Semsari S, Couderchet M (2009) Toxicity and removal of heavy metals (cadmium, copper, and zinc) by Lemna gibba. Ecotoxicology and Environmental Safety 72, 1774–1780.
Toxicity and removal of heavy metals (cadmium, copper, and zinc) by Lemna gibba.Crossref | GoogleScholarGoogle Scholar |

Nasim SA, Dhir B (2010) Heavy metals alter the potency of medicinal plants. In ‘Reviews of environmental contamination and toxicology’. (Ed. D Whitacre) pp. 139–149. (Springer: New York, NY, USA)

Rosa DJ, Ambrosini VG, Basso A, Borghezan M, Bruneto G, Pescador R (2014) Photosynthesis and growth of young “Niágara Branca” vines (Vitis labrusca L.) cultivated in soil with high levels of copper and liming. BIO Web of Conferences 3, 01005
Photosynthesis and growth of young “Niágara Branca” vines (Vitis labrusca L.) cultivated in soil with high levels of copper and liming.Crossref | GoogleScholarGoogle Scholar |

Ross CW (1974) ‘Plant physiology laboratory manual.’ (Wadsworth Publishing Company: Belmont, CA, USA)

Samborska IA, Kalaji HM, Sieczko L, Goltsev V, Borucki W, Jajoo A (2018) Structural and functional disorder in the photosynthetic apparatus of radish plants under magnesium deficiency. Functional Plant Biology 45, 668–679.
Structural and functional disorder in the photosynthetic apparatus of radish plants under magnesium deficiency.Crossref | GoogleScholarGoogle Scholar |

Santos ACB, Nunes TS, Coutinho TS, Silva MAP (2015) Uso popular de espécies medicinais da família Verbenaceae no Brasil. Revista Brasileira de Plantas Medicinais 17, 980–991.
Uso popular de espécies medicinais da família Verbenaceae no Brasil.Crossref | GoogleScholarGoogle Scholar |

Schettini AT, Leite MGP, Messias MCTB, Gauthier A, Li H, Kozovits AR (2018) Exploring Al, Mn and Fe phytoextraction in 27 ferruginous rocky outcrops plant species. Flora 238, 175–182.
Exploring Al, Mn and Fe phytoextraction in 27 ferruginous rocky outcrops plant species.Crossref | GoogleScholarGoogle Scholar |

Selmar D, Kleinwächter M (2013) Stress enhances the synthesis of secondary plant products: the impact of stress-related over-reduction on the accumulation of natural products. Plant and Cell Physiology 54, 817–826.
Stress enhances the synthesis of secondary plant products: the impact of stress-related over-reduction on the accumulation of natural products.Crossref | GoogleScholarGoogle Scholar |

Shabbir Z, Sardar A, Shabbir A, Abbas G, Shamshad S, Khalid S, Shahid M (2020) Copper uptake, essentiality, toxicity, detoxification and risk assessment in soil-plant environment. Chemosphere 259, 127436
Copper uptake, essentiality, toxicity, detoxification and risk assessment in soil-plant environment.Crossref | GoogleScholarGoogle Scholar |

Shahid M, Khalid S, Abbas G, Shahid N, Nadeem M, Sabir M, Aslam M, Dumat C (2015) Heavy metal stress and crop productivity. In ‘Crop production and global environmental issues’. (Ed. KR Hakeem) pp. 1–25. (Springer: Cham, Switzerland)

Shahid M, Dumat C, Khalid S, Schreck E, Xiong T, Niazi NK (2017) Foliar heavy metal uptake, toxicity and detoxification in plants: a comparison of foliar and root metal uptake. Journal of Hazardous Materials 325, 36–58.
Foliar heavy metal uptake, toxicity and detoxification in plants: a comparison of foliar and root metal uptake.Crossref | GoogleScholarGoogle Scholar |

Sharma SS, Dietz K-J (2009) The relationship between metal toxicity and cellular redox imbalance. Trends in Plant Science 14, 43–50.
The relationship between metal toxicity and cellular redox imbalance.Crossref | GoogleScholarGoogle Scholar |

Sousa EO, Miranda CMBA, Nobre CB, Boligon AA, Athayde ML, Costa JGM (2015) Phytochemical analysis and antioxidant activities of Lantana camara and Lantana montevidensis extracts. Industrial Crops and Products 70, 7–15.
Phytochemical analysis and antioxidant activities of Lantana camara and Lantana montevidensis extracts.Crossref | GoogleScholarGoogle Scholar |

Stanova A, Ďurisova E, Banasova V, Gurinova E, Nadubinska M, Kenderesova L, Ovecka M, Čiamporova M (2012) Root system morphology and primary root anatomy in natural non-metallicolous and metallicolous populations of three Arabidopsis species differing in heavy metal tolerance. Biologia 67, 505–516.
Root system morphology and primary root anatomy in natural non-metallicolous and metallicolous populations of three Arabidopsis species differing in heavy metal tolerance.Crossref | GoogleScholarGoogle Scholar |

Takeda Y, Takechi A, Masuda T, Otsuka H (1998) An acyclic monoterpene glucosyl ester from Lantana lilacia. Planta Medica 64, 78–79.
An acyclic monoterpene glucosyl ester from Lantana lilacia.Crossref | GoogleScholarGoogle Scholar |

Tarahovsky YS, Kim YA, Yagolnik EA, Muzafarov EN (2014) Flavonoid–membrane interactions: involvement of flavonoid–metal complexes in raft signaling. Biochimica et Biophysica Acta (BBA) – Biomembranes 1838, 1235–1246.
Flavonoid–membrane interactions: involvement of flavonoid–metal complexes in raft signaling.Crossref | GoogleScholarGoogle Scholar |

Tavares SRdL, Oliveira SAd, Salgado CM (2013) Avaliação de espécies vegetais na fitorremediação de solos contaminados por metais pesados. Holos 5, 80–97.
Avaliação de espécies vegetais na fitorremediação de solos contaminados por metais pesados.Crossref | GoogleScholarGoogle Scholar |

Tiecher TL, Tiecher T, Ceretta CA, Ferreira PAA, Nicoloso FT, Soriani HH, Tassinari A, Paranhos JT, De Conti L, Brunetto G (2016) Physiological and nutritional status of black oat (Avena strigosa Schreb.) grown in soil with interaction of high doses of copper and zinc. Plant Physiology and Biochemistry 106, 253–263.
Physiological and nutritional status of black oat (Avena strigosa Schreb.) grown in soil with interaction of high doses of copper and zinc.Crossref | GoogleScholarGoogle Scholar |

Yruela I (2005) Copper in plants. Brazilian Journal of Plant Physiology 17, 145–156.
Copper in plants.Crossref | GoogleScholarGoogle Scholar |

Yruela I (2009) Copper in plants: acquisition, transport and interactions. Functional Plant Biology 36, 409–430.
Copper in plants: acquisition, transport and interactions.Crossref | GoogleScholarGoogle Scholar |

Zeeshan M, Ahmad W, Hussain F, Ahamd W, Numan M, Shah M, Ahmad I (2020) Phytostabalization of the heavy metals in the soil with biochar applications, the impact on chlorophyll, carotene, soil fertility and tomato crop yield. Journal of Cleaner Production 255, 120318
Phytostabalization of the heavy metals in the soil with biochar applications, the impact on chlorophyll, carotene, soil fertility and tomato crop yield.Crossref | GoogleScholarGoogle Scholar |

Zhang H, Xia Y, Wang G, Shen Z (2008) Excess copper induces accumulation of hydrogen peroxide and increases lipid peroxidation and total activity of copper–zinc superoxide dismutase in roots of Elsholtzia haichowensis. Planta 227, 465–475.
Excess copper induces accumulation of hydrogen peroxide and increases lipid peroxidation and total activity of copper–zinc superoxide dismutase in roots of Elsholtzia haichowensis.Crossref | GoogleScholarGoogle Scholar |

Zhang H, Xu Z, Guo K, Huo Y, He G, Sun H, Guan Y, Xu N, Yang W, Sun G (2020) Toxic effects of heavy metal Cd and Zn on chlorophyll, carotenoid metabolism and photosynthetic function in tobacco leaves revealed by physiological and proteomics analysis. Ecotoxicology and Environmental Safety 202, 110856
Toxic effects of heavy metal Cd and Zn on chlorophyll, carotenoid metabolism and photosynthetic function in tobacco leaves revealed by physiological and proteomics analysis.Crossref | GoogleScholarGoogle Scholar |