The expansion of industries and urbanization across many parts of the world has led to increased contamination of surface waters, ground waters and soil by heavy metals [1] . Metal distribution in the environment results from the influence of environmental factors and the properties of the metals [2] . Heavy metals exist in the environment and are constantly increasing due to the environment through various anthropogenic activities such as mining, effluent discharge, and farming practices. The increased utilization of synthetic pesticides may lead to water pollution and harm to non-target organisms, thereby affecting the environment [3] . Heavy metals represent a group of dangerous environmental pollutants that, due to their toxic effects on human health in concentrations above the permissible limits, cause widespread concerns [4] . The term “heavy metal” refers to any element possessing metallic properties, has an atomic number greater than 20, a relatively high density greater than 5 g/cm³, and has a toxic or poisonous effect even at a deficient concentration [5] [6] . Also, metals that are five times as heavy as compared to water have been termed “heavy metals”, inclusive of metalloids such as arsenic, which can cause a toxic effect even at a low level of concentration [7] . It is common knowledge that heavy metals are naturally occurring elements on the earth’s crust. However, environmental contamination and subsequent exposure to humans result from several anthropogenic activities such as tanning, mining, electroplating, smelting, and domestic and agricultural uses of compounds containing these metals [8] . Many of these heavy metals are toxic at deficient concentrations; arsenic (As), cadmium (Cd), chromium (Cr), copper (Cu), lead (Pb), mercury (Hg), nickel (Ni), selenium (Se), silver (Ag) and zinc (Zn) are cytotoxic, carcinogenic, and mutagenic [9] .

Heavy metals comprise an essential group of toxic substances encountered in everyday living, from mild to acute, impacting human health [10] . Heavy metals may enter the human body via different routes, including ingestion from contaminated food sources, drinking contaminated water, inhaling the atmosphere, and dermatological contact [11] . These metals may possess beneficial functions due to their oxidative and reductive properties when coordinated with biological macromolecules. They may act as competitive ions binding to active sites of proteins and inactivating them or leading to malfunctions [10] . The binding of heavy metals to cellular components such as proteins, enzymes and nucleic acids may result in oxidative deterioration, eventually interfering with biological functions [12] . Also, electrostatic interaction between Cr (III) and negatively charged phosphate groups of DNA can result in the formation of Cr (III)-DNA complexes, which are toxic and mutagenic. Inorganic forms of arsenic are testified to be toxic to the environment and lethal to living organisms [13] .

Humans, now equipped with knowledge of the downside and long-term effects of these contaminants’ health and the environment at large, have turned to various removal strategies to preserve the integrity of our ecosystem. Various in- situ and ex-situ techniques address soil and waterbody pollution, with some recorded successes and drawbacks. Some conventional methods include ion exchange, membrane filtration, precipitation, electrocoagulation, and adsorption. Specific issues have risen concerning their efficiency, some of which include the incomplete removal of the sludge, their high energy requirement and the possibility of secondary contamination due to the disposal of these materials, not to mention the high operational cost associated with these methods [4] [14] [15] .

Over the past few years, in an attempt to turn towards safer options for removing contaminants from the environment, phytoremediation has become a viable option. As an environmentally safe method, phytoremediation utilizes plants to extract, accumulate and depollute contaminants through various mechanisms [16] . Phytoremediation is one of the most sought-after techniques for environmental clean-up due to its non-hazard approach to eliminating contaminants from the environment. Hyperaccumulator plants with enhanced metal binding abilities were genetically modified to improve their metal accumulation capacity. Sustainability methods ensure the removal of contaminants without creating any adverse effect that may affect agricultural processes [16] . This treatment may remove many contaminants beyond metals, such as antibiotics, petroleum hydrocarbons, pesticides, polychlorinated hydrocarbons, and many others. However, making this process toxicity-free requires a careful implementation process to dispose of contaminated biomass. One such way is to find usefulness for these materials post-harvest [17] . Agromining and phytomining describe processes that recover metals from plant biomass after cultivation on contaminated soil or water. Several studies successfully used this method to recover heavy metals such as nickel [18] , precious metals such as gold [19] and rare earth metals such as cerium, samarium, and yttrium [20] .

The phytoremediation method has been mainly composed of six strategies which are: Phytoextraction, Phytostabilization, Phytovolatilization, Phytodegradation, Rhizofiltration, and Rhizodegradation.

a) Phytoextraction: This process is also known as phytoaccumulation, phytoabsorption, or phytosequestration [21] and involves both the phyllosphere and rhizosphere of plants used [22] . The roots of the plants absorb the contaminants from the soil or water and accumulate the contaminants in the above-ground parts, that is the shoots and leaves. The type of plants used for phytoextraction are hyperaccumulator species because they can accumulate contaminants [23] . Also, they are plants with high biomass production, high pollutants’ translocation factor into the surface biomass, high detoxification and contaminants’ tolerance, and are easy to harvest [22] [24] .

b) Phytostabilization: This method is called phytoimmobilization [25] . Here, the uptake of heavy metals is done in the rhizosphere, limiting the migration of the contaminants into the soil [26] . In this strategy, the plant that is being used alters the soil chemistry but facilitates the absorption and precipitation processes of heavy metals in soil by precipitating them into insoluble compounds [27] [28] . Moreover, this technology is an effective application when the preservation of groundwater and surface waters is needed [25] .

c) Phytovolatilization: Phytovolatilization is also called phytopumping, and highly depends on the physical properties of the pollutants [29] . In this process, plants absorb contaminants from soil, transport the contaminants through the xylem, convert the contaminants into less toxic and volatile components, and release them into the atmosphere via the stomata [26] [30] . Thus, the mode of remediation is in the phyllosphere of the plants. Although phytovolatilization has the advantage of lowering the toxicity of the pollutants, however, it could lead to air pollution [31] . Phytovolatilization can be used for heavy metals such as As, Se, Hg, vinyl chloride, carbon tetrachloride, and 1,4-dioxane [32] .

d) Phytodegradation: In this method, plant enzymes are required to first break down complex organic contaminants, then are incorporated into plant tissues in the phyllosphere [21] . Hence, this process is called phytotransformation because the plants transform the contaminants before releasing them into the atmosphere [25] ; Enzymes usually involved are; laccases, dehalogenases, nitroreductases which break down anilines, pesticides, and chlorinated solvents, and nitroaromatic molecules respectively [21] .

e) Rhizofiltration: This process is mostly used in a contaminated aqueous environment such as; contaminated wastewater, groundwater, and surface water. Here, plants adsorb and precipitate the organic and inorganic contaminants through the rhizosphere. Thus, rhizofiltration is primarily used to remediate an aquatic system with low levels of contaminants and is usually used for heavy metals including Cd, Cr, Cu, Ni, Pb, and Zn which are retained within roots and do not translocate to the shoots [29] . Research work done by [33] made use of Phaseolus vulgaris and Helianthus annuus for rhizofiltration to remove uranium from contaminated groundwater. The uranium removal result by the plants through rhizofiltration has an efficiency of more than 90%, and the uranium is accumulated at the root [26] [33] . The criteria for selecting a plant to use for this method include plants with a high surface area for adsorption, high root biomass, high accumulation capacity, and contaminants’ tolerance [21] .

f) Rhizodegradation: This process is also called phytostimulation because plant roots stimulate soil microbial communities in plant root zones to break down contaminants [29] . Thus, Rhizodegradation is performed by microorganisms such as fungi, bacteria, and yeasts found present in the rhizosphere of plants. Plant-microbial interaction plays a critical role in the efficiency of this treatment method and is normally applied in terrestrial contamination media [34] . These microorganisms in the plant rhizosphere can break down hazardous organic contaminants, such as herbicides, perchlorate, crude oil, Polyhydroxy aromatic compounds, and diesel [35] into harmless and/or nontoxic products. Sugar, amino acids, and alcohols are released by plant roots and microbial communities use these energy and food sources for consuming and digesting organic pollutants. This method is a highly rapid treatment system in comparison with phytodegradation because of microbial community association [34] .

Phytoremediation of Polycyclic aromatic hydrocarbons (PAHs) in the soil can be done either by direct uptake by plants, leading to transformation under enzyme activities, sequestration inside the plant, or transpiration via leaf stomata [36] or through the release of rhizosphere exudates and enzymes by plant roots to stimulate rhizosphere microbial degradation of PAHs [37] . The rhizosphere of plants harbors a diverse range of microorganisms that are involved in plant interaction with contaminated soils [29] . According to [38] , microbes support plants in enduring abiotic and biotic stresses, absorbing nutrients and water, producing plant hormones, and inhibitory allelochemicals [25] . They also boost the growth of plants and induce an increase of biomass in plants which elevates the remediation capacity of plants with the increased surface area for pollutant adsorption [25] . Moreover, the success of phytoremediation is a function of the plant’s ability to resist and accumulate high concentrations of pollutants while producing a large amount of plant biomass [39] . Efficient phytoremediation processes therefore depend on the complex interactions among soil, contaminants, microbes, and plants [40] . Although several plant species are capable of hyperaccumulating pollutants in their tissues. However, phytoremediation in practice has numerous challenges as there are a variety of contaminants [41] . Thus, the combined phytoremediation with microorganisms has been encouraged widely [29] [42] . Among these microbes are Rhizobacteria, Azotobacter, Bacillus, Pseudomonas, Arthrobacter, Achromobacter, and Enterobacter [43] , and Streptomyces spp., which have been reported to have an advantageous influence on various plants growing in contaminated soils [25] [44] [45] . The heavy metal-resistant bacteria strain, Burkholderia sp. significantly increases the biomass of maize and tomato plants and increases between 38% - 192% the Pb and Cd contents in tissue [46] . [47] have also reported that Pseudomonas fluorescens G9 and Bacillus subtilis Tp8 are biosurfactant-producing bacteria that have the potential to remediate Cd-contaminated soils. [48] also reported that Rhodococcus sp., Variovorax paradoxus, Pseudomonas fluorescens Pf 27, and Flavobacterium sp. enhance exchangeable and water-soluble Cd concentration in polluted soil. This in turn increased the Cd uptake and plant biomass of Brassica juncea. Interestingly, arbuscular mycorrhizal fungi (AMF) belonging to Glomeromycota, a monophyletic functional group that forms mutualistic associations with the roots of 80% of vascular plant species [49] , can promote the absorption of nutrients and improve plant biomass, as well as act as a bridge between soil, plant roots, and rhizosphere microorganisms [50] . Salix viminalis is considered a potential woody plant for soil remediation of heavy metals by phytoextraction [51] . However, the inoculation of Funneliformis mosseae (PM), Laroideoglomus etunicatum (PE), and Rhizophagus intraradices (PI) for a combined remediation, showed an increased phytoremediation of up to 62.32% in PM after 90 days in comparison to remediation with Salix viminalis only [51] . Review papers by [25] , [29] and [52] have also made mention of a diverse list of microorganisms reported to augment the phytoremediation of contaminated soils.

Chelation refers to attaching a specific organic molecule with mineral or metal ions to form a metal complex [53] . In the phytoremediation of potentially toxic elements (PTEs), such as Cu, Pb, Cd and others, a chelating agent is a chemical reagent used to enhance the bioavailability of various PTEs in the soil for metal translocation into a plant [54] [55] . Due to the limitations in the standard phytoremediation procedure, such as low decontamination rate, low bioavailability of targeted metals, and reduction of plant growth due to metal toxicity, scientific studies have been made to enhance phytoremediation for PTEs clean-up in the soil using chelating agents [56] [57] . The chelating agents act as a chemical bond to form metal chelate complexes, which enhances the bioavailability and solubilization of PTEs in the soil, for easy translocation into the roots and aboveground part of the plants [34] [54] [58] . Several chelating agents such as ethylene-diamine-tetraacetic acid (EDTA), N, N-dicarboxymethyl glutamic acid tetrasodium salt (GLDA), and ethylene-diamine-N,N’-disuccinic acid (EDDS), diethylene-triamine pentaacetate (DTPA) have been explored to examine their potential to enhance phytoremediation of PTEs in soil [53] [59] [60] . EDTA is the most widely used chelator and extensively studied in field experiments [52] . This may be due to the reason that such chelates are very costly in widespread application, though a limited number of in situ studies have been exploited for other chelating agents. [61] suggested that the addition of GLDA could enhance Cd and As’s bioavailability effectively. EDDS was found to improve the phytoextraction of Ni by Coronopus didymus L. from polluted soils [62] . In addition, [63] utilized citric acid for phytoextraction of metals from multi-metal contaminated soil by soybean plants aided by Kocuria rhizophila (Glycine max L.) [34] . The addition of EDTA enhanced the phytoextraction of Cd and Pb by Pelargonium hortorum [64] . The enhancement of metal accumulation and extraction by Brassica juncea plants in the presence of EDTA significantly enhanced Pb extraction by solubilizing soil-bound Pb [65] . Chelating agents in combination with plants can enhance the phytoremediation efficiency in various types of plants and contaminated sites [54] [58] [66] . However, it has conclusively been shown that plants may experience some phytotoxicity as a result of the high concentration of added chelating agents and the formed metal complex in the soil, which can consequently affect the performance of the plants to uptake toxic metals and contaminants in the soil [67] . Also, the application of chelating agents can reduce the chlorophyll content and plant biomass by suppressing the chlorophyll synthesizing enzyme (α-aminolevulinic acid dehydratase) activity [67] . The inhibition of this enzyme activity might limit the water absorption surface and photosynthetic activity thus reducing the overall plant growth [34] [56] .

Phytoremediation, a promising, eco-friendly, and cost-effective strategy for the remediation of contaminated environments, has been widely investigated for its effectiveness and the variety of pollutants it can remediate [68] . This method capitalizes on the inherent ability of plants and their associated microbiota to degrade, absorb, or stabilize contaminants. The science of phytoremediation has been lauded for its potential to harness natural processes in the treatment of contaminated environments. However, the efficiency of phytoremediation depends on several interconnected factors that influence the overall remediation performance.

Selection of plant species:

Different plant species have varying abilities to uptake and translocate pollutants, and their tolerance to different types and levels of contaminants can greatly differ (Marchiol et al., 2014). High biomass producing species with rapid growth, wide distribution roots, and tolerance to pollutants are often preferred. For instance, sunflowers and Indian Mustard have been identified as hyperaccumulators for heavy metals, including lead and cadmium [69] . Certain plant species are known for their higher metal uptake and tolerance, such as sunflower for lead, Indian mustard for chromium, and willows for cadmium and zinc [70] . The inherent physiological and biochemical characteristics of these plants, including high biomass production, rapid growth rates, and deep root systems, facilitate effective phytoremediation [71] . Phytoremediation efficiency is primarily governed by the type of plant species utilized [72] . Different plant species possess varying capabilities in terms of uptake, translocation, and detoxification of pollutants. For example, hyperaccumulator plants are more effective in extracting heavy metals from soil than non-hyperaccumulators [73] . The use of hyperaccumulators, plants that can take up and concentrate high levels of certain contaminants in their tissues, has been a focal point in phytoremediation research [74] . Moreover, the use of genetically modified plants, with enhanced tolerance and accumulation characteristics, has shown promising results but also raises ethical and environmental concerns [75] . Certain species exhibit higher capacities to uptake, accumulate, or degrade pollutants due to variations in their genetic makeup [75] . Selecting an appropriate plant species is therefore crucial to the success of a phytoremediation initiative.

The role of plant-microbe interactions:

Microorganisms can influence plant health and productivity, increase bioavailability of pollutants, and directly or indirectly contribute to pollutant degradation [76] . In rhizoremediation, a subcategory of phytoremediation, plant root exudates stimulate microbial activity, enhancing the degradation of pollutants [77] . Plant-microbe interactions also significantly influence phytoremediation efficiency. These interactions can enhance the availability of pollutants in the rhizosphere and increase the tolerance of plants to pollutants [78] . Certain bacteria can produce siderophores that mobilize heavy metals, facilitating their uptake by plants [79] .

Impact of soil properties:

Soil properties, such as pH, texture, organic matter content, and pollutant concentration, are other crucial factors influencing the efficiency of phytoremediation. Soil pH affects the solubility of metals, with lower pH generally increasing metal solubility and thus availability for plant uptake [80] . Organic matter content can influence pollutant bioavailability and plant-microbe interactions [81] . Moreover, the physicochemical properties of the contaminated site, including pH, temperature, humidity, nutrient availability, and the presence of other pollutants, significantly influence the phytoremediation process [82] . For example, low pH levels can increase the availability of heavy metals, promoting their uptake by plants [83] . Soil properties, such as pH, organic matter content, and microbial population, can significantly influence phytoremediation efficiency [84] . A favorable pH can enhance the bioavailability of contaminants, while a high organic matter content can inhibit the plant uptake of heavy metals [85] . The role of soil microorganisms should not be understated, as they can aid in contaminant degradation and influence plant health [86] . Soil properties, including its physical, chemical, and biological characteristics, can substantially affect phytoremediation. Factors such as soil pH, texture, organic matter content, and microbial population play crucial roles in determining the bioavailability and mobility of contaminants, subsequently affecting plant uptake and degradation of pollutants [87] . Therefore, manipulating these factors, through soil amendments, for instance, can enhance phytoremediation efficiency.

Contaminants concentration:

The type of contaminant plays a pivotal role in the efficiency of phytoremediation. Some contaminants, such as heavy metals, are more readily absorbed and accumulated by plants, while organic pollutants, like petroleum hydrocarbons, may require specific plant-microbe interactions to enhance degradation [78] . Furthermore, the presence of multiple contaminants can influence the overall phytoremediation process, as certain compounds may antagonize or synergize the plant’s ability to remediate others [88] . Contaminant characteristics also play a pivotal role in phytoremediation outcomes [71] . Variations in contaminant solubility, form, concentration, and depth of penetration in soil can significantly affect the bioavailability of pollutants for plant uptake [89] . Thus, a detailed characterization of the contaminant is necessary to accurately predict phytoremediation efficiency.

Environmental conditions:

The influence of environmental conditions, such as temperature, rainfall, and light intensity on phytoremediation is not fully understood. They can alter plant physiology and growth, potentially affecting their capacity to uptake and metabolize pollutants [90] . However, more research is needed to elucidate the precise impacts of these environmental factors on phytoremediation efficiency. These factors influence microbial activity in the rhizosphere, affecting the overall remediation process [71] . Environmental conditions such as temperature, precipitation, and sunlight influence plant growth and metabolism, thus impacting the phytoremediation process. The optimal temperature and sufficient sunlight are necessary for photosynthesis, which directly impacts plant growth and pollutant uptake [91] .

In conclusion, while phytoremediation is a promising strategy for environmental remediation, its success relies on a complex interplay of several factors, and a comprehensive understanding of these factors, along with the development of techniques to optimize them, could greatly enhance phytoremediation efficiency, offering a viable and promising pathway towards a cleaner and healthier environment.

The application of traditional Phytoremediation techniques to reclaim contaminated sites has been publicly accepted [92] . But in recent times research has unveiled its limitations to the field and large-scale applications. This is because naturally occurring hyper accumulators are slow growing with low above-the-ground biomass production and also their poor ability to tolerate heavy metals toxicity effect [93] . The advent of new technological advancement in the field of phytoremediation strategies has resulted in significant improvements in the increased above the ground biomass production of the hyper accumulator plant species and their enhanced heavy metals tolerance ability [94] . The new technological advancements are discussed below:

Biotechnology paves a way for researchers to understand the intricate relationships that exist between plants and their microbiome, and this had led to enhanced phytoremediation strategies [123] . In this scenario, omics technologies such as proteomics, genomics, transcriptomics, and metabolomics have been used to gain a comprehensive understanding of the molecular mechanisms underlying plants-microbes interaction during phytoremediation. The key approaches used in achieving enhanced phytoremediation are as follows;

While phytoremediation is promising and environmentally friendly technology to reclaim a contaminated environment, it faces several challenges and limitations which include:

The field of phytoremediation is rapidly growing and drawing the attention of the scientific community to elucidate new strategies to deal with toxic environmental contaminants. Hence, investigations in various areas of research are ongoing that could improve the existing phytoremediation strategies. The major areas of ongoing research in phytoremediation include;

Phytoremediation, an eco-friendly method of using plants for removing pollutants should be prioritized for environmental safety. In essence, as scientists continue to explore, phytoremediation will be more efficient, cost-effective, and widely applicable. However, it might be difficult to balance these with the safety of our environment, regulatory concerns, and public acceptability to ensure sustainable implementation. Nevertheless, the potential prospects for the improvement of phytoremediation can be achieved by collaborative efforts between researchers, governments, and stakeholders to address the aforementioned challenges. Despite its challenges, phytoremediation remains crucial for environmental sustainability. Also, extensive research for improved phytoremediation strategies is crucial in areas such as the development of engineered plant species for efficient phytoremediation, the development of new methods such as bioaugmentation for enhanced phytoremediation, and the development of new technologies to monitor and optimize phytoremediation.

The authors declare no conflicts of interest regarding the publication of this paper.

Salifu, M., John, M.A., Abubakar, M., Bankole, I.A., Ajayi, N.D. and Amusan, O. (2024) Phytoremediation Strategies for Heavy Metal Contamination: A Review on Sustainable Approach for Environmental Restoration. Journal of Environmental Protection, 15, 450-474. https://doi.org/10.4236/jep.2024.154026