Advanced phytoremediation strategies: Tackling heavy metal contamination in agricultural soils

Introduction

Soil pollution caused by human activities has led to significant levels of heavy metal contamination, which is now a global concern. The application of agrochemicals and contaminated irrigation water has resulted in elevated levels of heavy metals, such as chromium (Cr), copper (Cu), cobalt (Co), cadmium (Cd), and lead (Pb), in arable soils. This has led to a decline in soil health, as reported by Kaur et al. in 2023. The imprudent utilization of these compounds leads to contamination (Ruba et al., 2023) [78] . Heavy metals present in fertilizers have a non-biodegradable characteristic, which means they can persist in soil for extended periods of time. Eventually, these metals reach the food chain through the soil (Thakur et al., 2022) [97] . Heavy metals are derived from both natural and manmade sources. Heavy metals are commonly linked to volcanic eruptions, wind erosion, forest fires, and the overall use of fossil fuels. Metals derived from natural sources generally have a lesser impact on the environment, while metals originating from human activities such as smelters, thermal power plants, mines, and foundries offer a significant risk to humanity (Angon et al., 2024) [7] . Eliminating heavy metals from the environment is exceptionally challenging due to their resistance to degradation, which renders them impervious to both biological and chemical processes. Different technologies are used for the removal of heavy metals from contaminated soil, both on-site and off-site. Several prevalent technologies include chemical elimination, electrophoresis, excavating, mechanical breaking down, soil cleaning, soil flushing, solidifying, and Nitrification (Wu et al., 2024) [101] . Over time, the gradual accumulation and interactions of heavy metals (HMs) in the soil can have detrimental effects on the ecosystem, presenting significant risks to living organisms. Vegetables could absorb heavy metals (HMs) and store them in sections that are safe for consumption (Madhav et al., 2024) [57] . Heavy metals are a significant source of pollution that has a widespread impact on plants and animals worldwide (Angon et al., 2024) [7] . Crops cultivated in soils contaminated with metals have a propensity to accumulate high levels of heavy metals, which poses a significant threat to the health of humans and animals (Ene et al., 2024; Hamoud et al., 2024) [25,37] . Cropping practices and soil parameters have an impact on the heavy metal concentrations in agricultural soil (Xu et al., 2022; Srinivasarao et al., 2014) [102,93] . Excessive amounts of heavy metals such as Cobalt (Co), Chromium (Cr), and Copper (Cu) might interfere with the regular functioning of organisms, despite their importance in plant and animal metabolism (Noor et al., 2024: Javed and Usmani 2013) [64,43] . It is well-established that Cd and Pb exhibit considerable toxicity and carcinogenicity in both animals and humans (Cirovic and Satarug 2024) [19] . Prolonged exposure to heavy metals by inhalation, ingestion, or contact with air, water, soil, and food can lead to a range of health conditions including cancer, neurological disorders, heart attacks, hypertension, skin abnormalities, damage to internal organs, and dysfunction of the urinary, reproductive, and respiratory systems (Nucera et al., 2024) [65] . Lead (Pb) can endure in soil for a duration of 150-5,000 years and maintains elevated levels for as long as 150 years after sludge is applied to the soil (Beiyuan et al., 2020) [11] . On the other hand, the biologically active half-life of cadmium (Cd) is around 10-30 years (Azhar et al., 2022) [9] .

Remediation of polluted soil

The remediation of soils contaminated with heavy metals is of paramount importance to mitigate their adverse effects on ecosystems (Saxena et al., 2020) [81] . This job is difficult in terms of both expense and technological complexity (Selvi et al., 2019) [83] . Thus far, various physical, chemical, and biological methods have been utilized for this objective. The usual procedures for remediating contaminated soil include in situ vitrification, soil incineration, excavation and landfill, soil washing, soil flushing, solidification, and stabilization using electro-kinetic devices (Razzak et al., 2022; Vardhan et al., 2019) [77,99] . In general, physical and chemical treatments have drawbacks such as being expensive, labor-intensive, causing permanent changes in soil parameters, and disrupting the natural soil microbiota (Osman 2018) [68] . Chemical processes might potentially give rise to other pollution issues. Hence, it is imperative to conduct research in order to devise economical, highly efficient, and environmentally sustainable techniques for purifying heavy metal-contaminated soils (Azhar et al., 2022) [9] . Phytoremediation is a revolutionary method that is seen as an environmentally friendly answer to the issue of heavy metal contamination (Padbhushan and Kumar 2024) [69] .

Phytoremediation Techniques

Phytoremediation is a specialized approach that effectively reduces environmental contamination. Hyperaccumulators, which are plants capable of absorbing heavy metals from both above and below ground, play a crucial role in this process. Microorganisms possess a high level of proficiency in the process of sequestering hazardous metals (Padbhushan and Kumar 2024) [69] .

Bioremediation

Micro-organism-based cleanup approaches, including bioremediation procedures have the capacity to breakdown and detoxify certain pollutants. While these biological systems may be less adaptable to adverse environmental conditions compared to other conventional approaches, they are less expensive. Bioremediation encompasses a range of methods that utilize plants, microbes, and animals to address and mitigate the presence of pollutants. The technology described is a novel and effective method for remediation of heavy metal-contaminated environments. Importantly, it does not have any negative impacts on the surrounding environment (Gomes et al., 2016) [51] .

Advantages and disadvantages of bioremediation

The advantages of bioremediation are numerous when compared to other technologies, which are: • Feasible and widely accepted (Muhammad et al., 2024) [60] .

• Reasonably cheap (Padma et al., 2024) [70] .

• Eradicate secondary atmospheric or aquatic contaminants (Bustamante-Torres et al., 2024) [13,14] . • Even if polluted and unusable plant, the resulting ash is approximately 20-30 tons per 5000 tons soil (Adepoju et al., 2024) [1] . • Growing plants in an area also lessens erosion from wind and water. • Operate with water-replant substances like organic material (Patel and Kulwant 2024) [73] . • Solar-operated.

• Generates recyclable metal-rich plant residue (Hu et al., 2024) [38,39]

Phyto-remediation

The process is rooted in plants and encompasses the activities of translocation, accumulation, transport, transformation, and volatilization (Lavanya et al., 2024) [52] . In addition, the ability of certain plant species (more than 400) to remediate has been verified (Wang et al., 2024) [100] . The technology is highly promising and efficient, with no adverse effects. Nevertheless, the limited ability of heavy metals to be absorbed by plants in soil and the low amount of plant biomass have hindered the effectiveness of this technique. Nonetheless, several diverse approaches have been employed to improve its efficiency. The methods encompass microbiological, physical and chemical, agronomic, and genetic engineering techniques (Hu et al., 2024) [38, 39] . Phytoremediation of soil contaminated with heavy metals involves the use of one or more mechanisms of phytoremediation. The primary methods of phytoremediation are phytoextraction, it Phyto-stabilization, phytovolatilization, and rhizo-filtration, as described by Madhav et al. (2024) [57] .

Fig 1: Different Phyto-remediation techniques

Phytoextraction

Plants absorb contaminants from the soil, water, or sediments through their roots and transport them to the aboveground biomass, where they collect in shoots or other sections of the plant that can be harvested. The technique is referred to as phytoextraction, as documented by Singh et al. (2024) [89] and Madhav et al. (2024) [57] . The transfer of metals to the shoot is an important biochemical process that is necessary for efficient phytoextraction, as it is usually not possible to harvest the root biomass (Yin et al., 2024; Deng et al., 2024) [106,23] . Phytoextraction is regarded as a low impact technology, which means it has environmental advantages. In addition, the Phytoextraction technique involves the use of plants to provide soil cover, which effectively reduces erosion and leaching. By using a process of repeated cultivation and gathering, it is possible to diminish the concentration of pollutants in the soil (Lavanya et al., 2024) [52] . The effectiveness of phytoextraction as an environmental remediation method depends on several factors, such as the accessibility of heavy metals, soil properties, the chemical form of heavy metals, and the plant's ability to absorb metals and accumulate them in aboveground parts. Around 450-500 distinct plant species have been identified as hyperaccumulators (Das et al., 2024) [21] . To be acceptable for phytoextraction, plant species must possess the following characteristics: (I) the ability to tolerate hazardous metals, (II) the capacity to produce a large amount of biomass, and (III) the capability to actively accumulate heavy metals in sections that may be easily harvested (Pajevic et al., 2016) [71] . The fundamental concept underlying phytoextraction in contaminated environments involves cultivating appropriate plant species on-site, harvesting the biomass containing heavy metals, and subjecting it to various treatments such as composting, compressing, dehydrating, and thermal breakdown to reduce its mass and size. The resulting biomass, which is enriched with heavy metals, contains significant amounts of metal pollutants. If it is economically viable, this biomass can be used to recover trace elements again or disposed of as hazardous waste with great care (Patra et al., 2020) [75] . (Evangelou et al., 2007) found that maize (Z. mays L.) has a notable ability to collect and accumulate phytochemicals from the soil. The potential was further enhanced by the inclusion of the metal chelating agent EDTA, resulting in a greater than thirteen times increase in the amount extracted of Lead and a greater than three times rise in the recovery of Cd. (Shiyab 2018) [88] conducted a study to explore the ability of three types of lettuce (Romaine lettuce, Redina lettuce, and iceberg lettuce) to accumulate copper (Cu) contamination. The study found that Redina lettuce has a high capacity for accumulating Cu. The root tissue exhibited an accumulation of 1.89 mg kg -1 , whereas the shoot tissue showed an accumulation of 0.71 mg kg -1 , which is comparatively high in relation to these three types of lettuces (Shiyab 2018) [88] .

Phyto stabilization

Phyto stabilization, also known as Phyto immobilization, refers to the utilization of specific plants to stabilize pollutants present in polluted soils (Alkorta, 2010) [5] . The purpose of this strategy is to decrease the movement and accessibility of contaminants in the environment, hence preventing their movement into groundwater or their introduction into the food chain (Yaqoob et al., 2024) [105] . Plants can trap heavy metals in soils by absorbing them through their roots, causing them to precipitate, forming complexes, or reducing the metal's valence in the rhizosphere (Shackira et al., 2019) [84] . Utilizing metal-tolerant rhizobacteria that produce organic acids, either independently or in conjunction with biogas residues, effectively mitigates soil contamination by Cd through the stabilization of maize roots and the restriction of translocation to shoots (Tahir et al., 2021) [95,96] . Additionally, it aids in enhancing the yield, quality, and physiological characteristics of maize biomass. In addition, the use of chicken manure alone or in conjunction with biogas wastes increases the movement of Cd to the shoot. The production of organic acids in the exudates of maize roots has a crucial role in stabilizing cadmium (Cd) in both the roots and shoots of the plant (Sohail et al., 2019) [91] . The generated amount of organic acid was increased as a consequence of to metal-tolerant rhizobacteria that benefit plants and biogas residues. However, the production was not as effective when poultry waste was used, resulting in a decrease in the Cd level in the root (Tahir et al., 2021) [95,96] . Phyto stabilization halts the movement of pollutants in the root zones of plants, preventing them from entering the vegetative sections (Ogundola et al., 2022) [67] . This strategy can facilitate the restoration of flora in polluted areas with elevated metal levels, where the growth of natural vegetation is not feasible. Metal-tolerant plant species can be used as phyto stabilizers to restrict the movement of different pollutants through wind, rain, and leaching into groundwater sources (Adki et al., 2014) [2] .

Phyto volatilization

Phytovolatilization is the process in which plants absorb heavy metal pollution and convert them into less harmful chemical species that may easily evaporate by transpiration. Certain heavy metals, such as Hg and Se, can be present in the environment in the form of gaseous species (Nwogwu et al., 2024) [66] . Several plants, including musk grass (Chara canescens), Indian mustard (Brassica juncea), and Arabidopsis thaliana, whether naturally occurring or genetically modified, have the ability to take in toxic substances and convert them to gaseous state before distributing these individuals into the surrounding atmosphere (Jabeen et al., 2009) [41] . Phytovolatilization can be regarded as a long-term solution for site remediation, as the gaseous products that are released are highly improbable to re-deposit at or near the site. While the understanding that microbes contribute significantly to the release of selenium from soils has been established for a considerable period, a subsequent study by Ogundola et al., (2022) [67] demonstrated that plants are also capable of performing this function. Alternatively, the items that have undergone remediation might be utilized for a multitude of applications in different remediation methods. Phytovolatilization should be avoided in densely populated cities and areas with atypical weather patterns since these locations can accelerate the release of volatile chemicals (Nissim et al., 2021) [63] . This method is applicable for the removal of organic contaminants as well as some heavy metals such as mercury (Hg) and selenium (Se). Nevertheless, its effectiveness is constrained by the fact that it does not eliminate the pollutant; rather, it only transfers it from one medium (soil) to a different medium (atmosphere), where it can potentially be redeposited. Phytovolatilization is the most contentious among the several phytoremediation processes, (Aithani and Kushwaha 2024) [3] .

Phytodegradation

Phytodegradation refers to the process of breaking down organic pollutants using enzymes like dehalogenase and oxygenase, which are found in plants. This process does not rely on microorganisms in the rhizosphere (Maurya et al., 2023) [58] . Plants have the ability to gather organic contaminants from contaminated surroundings and eliminate them via the process of metabolism (Khan et al., 2023) [49] . From this perspective, green plants might be seen as the "Green Liver" of the biosphere. Phytodegradation exclusively targets the elimination of organic contaminants, while heavy metals are nonbiodegradable (Corami 2023) [20] . In recent times, researchers have displayed their fascination with investigating the process of phytodegradation of diverse organic pollutants, which encompasses synthetic herbicides and insecticides (Dehghani et al., 2024) [22] . Phytodegradation involves the uptake of pollutants by plants, which subsequently break them down into less hazardous and simpler forms. Breakdown in plants can occur in two ways: firstly, through metabolic processes that take place within the plant itself, and secondly, through the action of enzymes that are generated by the plant. The plant utilizes the pollutants that are decomposed into simpler substances to promote accelerated development (Pathak et al., 2024) [74] . Phytodegradation is a process that can break down solvents with chlorination, pesticides, and various other organic molecules, as well as other inorganic compounds (Gupta et al., 2024) [36] . Nitro reductase, laccase, dehalogenase, peroxidase, and nitrilase are catalysts that facilitate the mechanism of photo-degradation (Rani and Kumar 2024) [76] .

Rhizo-degradation

Rhizo-degradation is the process by which microbes in the rhizosphere decompose up organic contaminants in the soil. The rhizosphere, which is approximately 1 mm in size, encompasses the area around the root and is subject to the plant's effect (Bansal et al., 2024) [10] . The primary factor contributing to the accelerated breakdown of contaminants in the rhizosphere is most likely the augmentation of microbial populations and their metabolic functions. Plants can enhance microbial activity in the rhizosphere by secreting exudates that contain sugars, amino acids, and flavonoids. This stimulation can increase microbiological activity by a factor of 10 to 100 (Eze and Amuji 2024) [28,29] . Plant roots emit exudates that contain nutrients, which serve as carbon and nitrogen sources for soil microorganisms. This process creates a nutrient-rich environment that promotes microbial activity. Plants not only secrete organic substances to support the growth and functions of microorganisms in the rhizosphere, but they also produce specific enzymes that can break down organic pollutants in soils (Boujelben et al., 2024) [12] . Rhizo-degradation, also known as Phyto stimulation or improved rhizosphere biodegradation, is the process of soil pollutants being broken down by microorganisms in the soil, which is facilitated by the unique properties of the rhizosphere. Soil microorganisms play a crucial function in enhancing the accessibility of nutrients and the production of plant growth regulators (Gatla et al., 2024) [32] . Simultaneously, they engage in several processes that alter organic materials in the soil and contribute to the breakdown of foreign substances. Another role is to engage in the adsorption and desorption of different substances and the detoxification of both organic and inorganic contaminants (Ethiraj et al., 2024) [26] . Plants secrete chemicals that facilitate the establishment of microbes in the root area through advancement, adsorption, and the presence of polymers. This mutualistic relationship aids the plant in overcoming both living and non-living challenges (Shashirekha et al., 2024) [86] .

Phyto desalination: This approach has been recently published and is currently emerging. Plant-based desalination is the process of using halophytic vegetation to extract ions from saltaffected soils, making them suitable for normal plant growth (John et al., 2024) [46] . According to Chen and Wang (2024) [100] , halophytic crops are believed to possess inherent advantages in dealing with pollutants as opposed to glycophytic vegetation.

Rhizo-filtration

Rhizo-filtration, also known as hydraulic control, is a technique that relies on the ability of plant roots to collect and isolate metal contaminants from water. The process of phytoremediation can effectively remove metals including Cd, Cr, Cu, Ni, Pb, and V, as well as radionuclides like U, Cs, and Sr (Gatla et al., 2024; Jan et al., 2024) [32,42] . Trees with extensive root systems can take in a significant amount of water, which was used as a main ingredient in this process. Long-rooted trees function as hydraulic pumps, extracting substantial quantities of water from the underground water table (Umid et al., 2024) [98] . Hence, impurities present in the water column are assimilated together with the water during this process. Root exudates, such as citric acid and malic acid, could either remove or increase the uptake, attachment, or settling of contaminants (Zou et al., 2024) [108] . [104] 2 Duckweed Pb, Cd, Cu, Zn, Ni, and Cr Kaur and Kanwar (2021) [48] 3 Tobacco Cd and Zn Kozak and Antosiewicz (2022) [50] 4 Sunflower Cu, Cd Cr, Ni, Pb, Zn, and Fe Nikolic and Stevovic (2015) [62] 5 Spinach Pb, Cd, Cu, Ni, Zn, and Cr, Sharma et al., (2020) [85] 6 Rye Cd, Pb, Cu, Mo, Ni, and Zn Nepal et al., (2024) [61]

7

Indian Mustard Metallophytes: Metallophytes are vegetation that possess specialized adaptations enabling them to flourish in soils that contain high concentrations of heavy metals (Smriti et al., 2024) [90] . Plants that are resistant to heavy metals are typically found in soils where ores are exposed, known as metalliferous or orogenic lands (Amils et al., 2024) [6] . The prolonged exposure of metallophytes to an excess of different metals for thousands of years has led to the development of metal resistance in these plants, adapting to the specific environmental circumstances of their local habitat. Mining operations have caused considerable damage to metal-rich habitats, resulting in a reduction in suitable environments for metallophytes, as documented by Saad et al. (2024) [79] . The plants are found within the plant family Brassicaceae. The utilization of these substances, either alone or in conjunction with microorganisms, for the process of phytoremediation in soils that are polluted with heavy metals, is a highly appealing concept. Metallophytes can be classified into three distinct.

Categories: Metal excluders, metallic indications, and metals hyperaccumulators of nutrients (Zhakypbek et al., 2024) [107] .

Enhancement of plant-based remediation strategies

Plant-based remediation might be improved through the utilization of chemical or biological techniques (Madhav et al., 2024) [57] . There are multiple methods to improve phytoremediation procedures.

Augmented contaminants phytoextraction using chemical agents.

Compounds or surfactants as well including CDTA (Xu et al., 2024) [103] , EDTA (Alam et al., 2024) [4] , DTPA (Lindsay and Norvell 1969) [55] , EGTA & CA (Su et al., 2024) [94] , can enhance the movement of metals in soil. By utilizing these compounds, the rate at which metals are absorbed into the plants is further improved (Shen et al., 2024) [87] . Nevertheless, there exist specific risk factors, such as the process of metals leaching into the groundwater. In addition, these soil amendments can potentially endure in the environment, leading to the emergence of unforeseen complications (Selvam et al., 2024) [82] .

Methods of agricultural work:

The incorporation of chemical fertilizers, sources of carbon, and various other methods of agriculture can enhance the development of plants and microbial reproduction (Samantaray et al., 2024) [80] . One example is a multi-process structure that includes land farming (aeration and light exposure), microbial inoculation (introduction of contaminant degrading bacteria), and the phytoremediation (plant development) to increase the rate of uptake for organic pollutants from soil, thereby promoting the overall health and vitality of the ecosystem. The outcome obtained from this procedure indicated that the remedial impact was augmented by 50% (Aransiola et al., 2024) [8] .

Techniques involving the interaction of plants and microbes

Microbes can be introduced into the root zone of soil to improve the phytoremediation mechanism. This approach is highly efficient in removing the pollutant from the soil. An instance of this phenomenon is the documented enhancement of absorbance and assimilation in plants when mycorrhizae are introduced to their roots (Liu et al., 2024) [56] .

Wetland environment

There are two broad types of wetland plants that exhibit significant diversity and can be utilized for the purpose of restoration. Emergent plants, as described, are characterized by having the majority of their components situated above the surface of the water, with their stems anchored in shallow water. Submerged plants, as noted by Cahoon (2024) [15] , yield a greater amount of biomass compared to other plants. This biomass is crucial for the absorption of decontaminants, as highlighted by Gaballah et al. (2024) [31] . A built wetland is employed to decelerate the flow of water in polluted areas and effectively capture toxins such as heavy metals. Additionally, it serves as a means of enhancing the aesthetic appeal of the wetland through landscaping efforts (Lim 2024) [54] .

genetically developed plants

Plants that have undergone genetically modified can help during the phytoremediation operation. By changing the genes of hyper-accumulator plants, it is possible to get more biomass and metals out of the ground. But because of safety and legal issues, these plants can't be used for business. The MT-I trait from Mus Musculus was added to tobacco plants, which made them more resistant to cd from 10 to 200‫ﵼ‬µM (Jia et al., 2024) [44,45] . Also, the MT-II trait from S. cerevisiae was added to Brassica oleracea, which made it more resistant to cadmium from 25 to 400 μM in aquatic solution (Chunduri et al., 2024) [18] .

Energy crops

Annual crops that include Ricinus, the Miscanthus, Jatropha, or, and Populous have been found to be highly beneficial for both bioenergy generation and phytoremediation at the same time (Devi et al., 2024) [24] . Short-rotation woody plants were grown in polluted areas to aid in the cleanup process and also to meet fuel requirements.

Conclusion

The widespread problem of contamination by heavy metals in soils, primarily caused by human activities such as the excessive use of agrochemicals and the use of dirty irrigation water, presents a substantial risk to both the environment and human well-being. Conventional methods of cleanup, although successful, can incur substantial expenses and might result in long-term harm to soil ecosystems. Consequently, there is an increasing focus on implementing more sustainable and economically efficient approaches, such as phytoremediation. This novel strategy harnesses the inherent capabilities of plants and their accompanying microorganisms to assimilate, stabilize, release as gas, or break down pollutants. Phytoextraction, Phyto stabilization, phytovolatilization, phytodegradation, and rhizodegradation are diverse techniques that employ various processes to decrease pollutant levels in the soil. Phytoextraction is the process by which plants absorb metals and are later collected, while Phyto stabilization restricts the movement of pollutants. Phyto-desalination and the utilization of metallophytes are additional techniques that boost the potential of phytoremediation. The incorporation of chemical agents, sophisticated agricultural practices, and microbial interactions can greatly enhance the effectiveness of these plant-based techniques. Wetland habitats and genetically modified plants offer additional options for remediation, although the use of genetically modified plants is currently limited due to regulatory and safety issues. The simultaneous utilization of specific crops for both bioenergy production and phytoremediation presents a synergistic strategy for effectively handling polluted areas. Although there have been promising breakthroughs, additional study is required to optimize these procedures, overcome the limits associated with biomass production and metal uptake, and guarantee the safe disposal or reuse of contaminated plant material. Future study should prioritize the improvement of genetic features in hyperaccumulator plants, investigate the combined effects of plant-microbe interactions, and create scalable models for implementing these strategies on a broad scale. The implementation of this interdisciplinary approach has the capacity to revolutionize soil remediation methods, enhancing their efficiency and sustainability, while also fulfilling the urgent requirements for environmental preservation and safeguarding public health.

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