Elsevier

Chemosphere

Volume 259, November 2020, 127436
Chemosphere

Review
Copper uptake, essentiality, toxicity, detoxification and risk assessment in soil-plant environment

https://doi.org/10.1016/j.chemosphere.2020.127436Get rights and content

Highlights

  • A narrow line exists between beneficial and toxic levels of Cu to plants.

  • Soil properties controls Cu bioavailability, toxicity and detoxification to plants.

  • Copper uptake by plants and transfer to shoot is mediated by different transporters.

  • Copper can induce serious health disorders due to consumption of Cu-rich foods. .

  • Optimum levels of Cu essentiality/toxicity for plants needs more research.

Abstract

Copper (Cu) is an essential metal for human, animals and plants, although it is also potentially toxic above supra-optimal levels. In plants, Cu is an essential cofactor of numerous metalloproteins and is involved in several biochemical and physiological processes. However, excess of Cu induces oxidative stress inside plants via enhanced production of reactive oxygen species (ROS). Owing to its dual nature (essential and a potential toxicity), this metal involves a complex network of uptake, sequestration and transport, essentiality, toxicity and detoxification inside the plants. Therefore, it is vital to monitor the biogeo-physiochemical behavior of Cu in soil-plant-human systems keeping in view its possible essential and toxic roles.

This review critically highlights the latest understanding of (i) Cu adsorption/desorption in soil (ii) accumulation in plants, (iii) phytotoxicity, (iv) tolerance mechanisms inside plants and (v) health risk assessment. The Cu-mediated oxidative stress and resulting up-regulation of several enzymatic and non-enzymatic antioxidants have been deliberated at molecular and cellular levels. Moreover, the role of various transporter proteins in Cu uptake and its proper transportation to target metalloproteins is critically discussed. The review also delineates Cu build-up in plant food and accompanying health disorders.

Finally, this review proposes some future perspectives regarding Cu biochemistry inside plants. The review, to a large extent, presents a complete picture of the biogeo-physiochemical behavior of Cu in soil-plant-human systems supported with up-to-date 10 tables and 5 figures. It can be of great interest for post-graduate level students, scientists, industrialists, policymakers and regulatory authorities.

Introduction

In this era of intense, rapid and uneven industrial development, different kinds of potentially toxic elements (PTE) are released into the environment in large quantities (Antoniadis et al., 2019). Consequently, the environmental contamination by PTE such as heavy metals is becoming progressively more common and serious with the impacts of human activities on the ecosystem (Khalid et al., 2019; Amen et al., 2020). Almost all the compartments of the environment (air, water, sediments and soil) have been reported, in different studies, to be contaminated with different kinds of heavy metal (loid)s (Shahid et al., 2018, 2020b).

Among heavy metals, copper (Cu) is a reddish-brown transition metal having atomic number 29, atomic mass 63.5 g mol−1 and density 8.96 g/cm3. Copper is the 25th most abundant component of the Earth’s crust and 3rd most used metal in the world (Karlin and Tyeklár, 2012). This metal has gained considerable attention because of its dual nature to plants: essential at an optimum level while toxic at high levels (Ameh and Sayes, 2019a).

Copper is among the 8 essential micronutrients necessary for plant growth (Nazir et al., 2019) and is associated with numerous physiological and biochemical processes (Garcia et al., 2014). Copper is a structural constituent of numerous regulatory proteins and impart key roles by participating in mitochondrial respiration, cell wall metabolism, photosynthetic electron transport, responses to oxidative stress, protein synthesis, hormone signaling and ethylene sensing (Nazir et al., 2019; Zhang and Li, 2019). Copper is also incorporated in electron carrier proteins, e.g. plastocyanin, which constitute about 50% of the Cu in the plastids (Pilon et al., 2006; Zhang and Li, 2019).

Owing its capacity to easily lose and gain electrons, Cu acts as a cofactors in numerous enzymes such as laccase, cytochrome c oxidase, polyphenol oxidase, Cu/Zn superoxide dismutase, amino oxidase and plastocyanin (Nazir et al., 2019; Zhang and Li, 2019). In this way, Cu plays a key role in the proper functioning of these important enzymes. Some of these enzymes, having Cu as a cofactor, play a key role (antioxidation) under stress conditions (Zhang and Li, 2019). Copper has also been associated with oxidative phosphorylation, protein trafficking and signal-regulated transcription, and lipid and Fe metabolisms (Ameh and Sayes, 2019b). Hence, Cu is an essential nutrient for the regular functioning of plant metabolism. Under Cu deficient conditions, plants may experience and endure Cu deficiency symptoms.

On the contrary, Cu becomes highly toxic to plants, impairing the normal metabolic system, when its concentration surpasses a certain optimum level. At excess levels, Cu has been characterized to induce a number of toxic effect on various biophysiochemical processes (Cao et al., 2018; Ameh and Sayes, 2019a; Jaime-Pérez et al., 2019; Marastoni et al., 2019b; Ryszka et al., 2019). Excess Cu can greatly interfere with plant growth and development, uptake of essential nutrients, photosynthesis by reducing pigment contents, root development and leaf expansion (Lillo et al., 2019; Zhang and Li, 2019). Excess Cu also disturbs the functioning of key cellular components such as proteins, lipids, DNA, RNA etc. Copper toxicity to cellular macro-molecules can be indirect via the enhanced generation of reactive oxygen species (ROS) (Ameh and Sayes, 2019a; Jaime-Pérez et al., 2019).

In fact, the redox characteristics that make Cu an essential plant nutrient also plays role towards its toxic nature. The interconversion of this element between Cu+ and Cu2+ can result in the enhanced generation of highly toxic ROS and other hydroxyl radicals. These free radicles are capable to oxidize and damage several key biomolecules such as DNA, proteins, RNA, lipids and other essential biomolecules (Shahid et al., 2017c). The oxidation of protein in plants is generally mediated by ROS or other byproducts of oxidative damage (Farooq et al., 2019; Kapoor et al., 2019; Savelli et al., 2019). In most of the cases, the oxidation of proteins is irreversible, except for some sulfur containing amino acids (Ahmad et al., 2017; Kapoor et al., 2019). Therefore, these oxidative damages to plant biomolecules are commonly used as biomarkers for oxidative stress and ROS (Pisoschi and Pop, 2015; Kapoor et al., 2019).

In addition to oxidative damage, exposure to high levels of Cu may endure several visual toxicity symptoms such as impaired root and shoot growth, chlorosis, deficiency of nutrient, necrosis and even plant death under severe toxicity (Zhang and Li, 2019). Under Cu stress conditions, plants regulate their defense mechanisms to control Cu homeostasis. Plants are generally well-equipped with antioxidants to tolerate Cu toxicity (Yadav et al., 2018; Liu et al., 2019; Nazir et al., 2019).

However, the issue of Cu essentiality and/or toxicity, as well as detoxification inside plants, becomes more complex when taken into account its applied/prevailing levels along with different soil conditions and plant species. Therefore, it is highly important from the environmental and crop productivity point of view to elucidate the biochemical behavior of this metal in soil-plant-human systems. Consequently, considering the essential and toxic nature of Cu, this review critically presents its adsorption and phytoavailability in soil, its possible transfer from soil to plant, accumulation in different organs/tissues, essentiality, root-shoot transfer, toxicity, tolerance inside plants and the potential human health risks.

Section snippets

Copper chemistry and minerals

It is proposed that around 2/3rd of Cu in Earth occurs in igneous/volcanic rocks, while approximately 1/4th of Cu is found in sedimentary rocks (USGS, 2019). Copper is a chalcophile element found in sulfide ores (Karlin and Tyeklár, 2012). Copper is mainly found in following minerals which serve as Cu ores during its mining process: 78% in Digenite (Cu9S5), 66% in Covellite (CuS), 63% in Bornite (2Cu2S·CuS·FeS), 58% in Malachite (CuCO3·Cu(OH)2), 55% in Azurite (2CuCO3·Cu(OH)2), 52% in

Global uses and sources of copper in the environment

Copper is a major heavy metal pollutant that occurs both naturally and anthropogenically. Naturally, it is found in rocks, water and air, while its major anthropogenic sources include industries such as refining, metallurgical, fertilizer, printed circuit board production, fungicides, chemical manufacturing, paints, mining drainage, agricultural and municipal wastes and storm water runoff, as well as traffic emissions (Ameh and Sayes, 2019a; Leygraf et al., 2019; USGS, 2019).

Copper possesses

Copper occurrence and maximum allowable levels in the environment

Copper is emitted into different environmental compartments mainly due to human activities. Copper is frequently found in water resources and is considered a priority pollutant by the US-EPA (Sruthi et al., 2018). According to WHO (2004), Cu levels in surface water varied from 0.0005 to 1 mg/L in the USA with 0.01 mg/L of median value. Storm water also contains about 1–100 μg Cu/L (G. Georgopoulos et al., 2001). The natural level of Cu in an upper catchment control site was 0.001 mg/L (WHO, 2004

Bioavailability of copper in soil

Plants are not able to fully access the total metal pool present in the soil. Copper phytoavailability is highly plant-specific and it is dependent on soil properties which govern its mobility and bioavailability in the soil solid/solution phases (Violante et al., 2010). Similar to other metal ions, Cu is also taken up by the plants from soil solution via roots (Sayen et al., 2019). Copper is less mobile in soil (due to high density), so, it mainly tends to accumulate in the topsoil (Araújo

Copper uptake and speciation inside the plant roots

Plants absorb Cu from soil generally in the form of Cu2+ because it has high affinity for binding to OM as compared to other Cu species (Ogunkunle et al., 2019). Copper primarily accumulates in plant roots with low transfer to the aerial parts (Zlobin et al., 2017; Ghazaryan et al., 2019; Ogunkunle et al., 2019). Some studies reported that majority of the Cu2+ absorbed by the plants is accumulated as a layer nearby the root rhizodermis of Elsholtzia splendens (Xu et al., 2014) and Bambusoideae (

Role of copper in plant biology

Copper is involved in a number of biophysiological processes inside the plants such as participation in iron mobilization, protein trafficking, cell-wall metabolism, mitochondrial respiration, photosynthetic electron transport and hormone signaling (Ameh and Sayes, 2019a). In this way, Cu can significantly enhance plant growth and development (Fig. 3). A number of previous studies have reported the essential roles of Cu in plant biochemistry (Table 5). Recently, Gong et al. (2019) reported that

Effect of copper on plant growth

Excessive Cu accumulation affects plant growth and metabolism (Raldugina et al., 2016; Baldi et al., 2018a; Gong et al., 2019; Jaime-Pérez et al., 2019; Marques et al., 2019) (Table 5). Copper stress has significant interference with plant growth directly as well as indirectly. Some previous studies have reported inhibition in plant growth under Cu stress (Jaime-Pérez et al., 2019; Marques et al., 2019). Copper mediated decrease in growth is well-known for different plant species: Brassica napus

Copper homeostasis

Copper plays a key role in the biochemistry of all living organisms. All the living organisms including plants are equipped with an intrinsic cellular defense to combat and tolerate oxidative stress. Copper homeostasis which elucidates the ability of plants to mediate deficient and toxic levels is mainly exhibited by induction of specific genes as well as enzymatic and non-enzymatic antioxidants (Buapet et al., 2019; Kapoor et al., 2019; Navarrete et al., 2019).

When plants are exposed to toxic

Human health risk assessment of copper build-up in edible plant tissues

Depending on its redox status, Cu can accumulate differently in different plant parts (leaf or roots) for different plant species and applied conditions. The soil-plant transfer of Cu and sequestration in different plant organs (edible and non-edible) determines potential health risk associated with the ingestion of Cu-contaminated food. The potential soil-plant transfer and sequestration in different plant organs are mostly presented using different transfer factors (such as soil-plant root

Conclusions

Using the latest published data, this review summarized the biogeophysiochemical behavior of Cu in soil-plant system with respect to its redox-active nature and production of ROS. Generally, Cu induces hermetic effect and there exists a thin line between its essentiality and toxicity to plants. This metal can most likely affect all the major biochemical reactions in plants either by its excess or deficiency. The issue of Cu essentiality and/or toxicity, as well as detoxification inside plants,

Future standpoints

This review proposes the following scientific queries and research gaps based on the latest data of Cu summarized in this article:

  • The essential and toxic levels of Cu have been well-established for soils and plants. However, these essential and toxic levels of Cu may vary for its different redox status, various soil conditions and plant species. For example, biotransformation between Cu+ and Cu2+ and associated toxicity greatly vary among different plant species. Similarly, the acidic and

Declaration of competing interest

Authors declare no conflict of interest.

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