Heavy Metal Contamination in Soil: Implications for Crop Resilience and Abiotic Stress Management

Abstract

This chapter rigorously examines soil toxic metal/metalloid contamination and its profound implications on crop resilience, focusing on abiotic stress conditions. It begins by elucidating the natural and anthropogenic origins of soil contamination, illustrating how plants absorb these toxicants, and elaborating on their physio-molecular responses. The chapter accentuates the detrimental manifestations of impaired photosynthesis, nutrient uptake, and oxidative stress management, underscoring the urgent need for effective mitigation strategies. Phytoremediation and genetic engineering advancements are explored as promising strategies to optimize plant resilience in contaminated environments. Novel methodologies, including phytochelatins and the strategic application of genetic engineering, demonstrate potential in improving plant growth and resilience, showcasing significant advancements toward sustainable agricultural practices. Moreover, the interaction between plants and soil microbes is dissected, revealing a symbiotic relationship that influences the bioavailability of toxic metals/metalloids and optimizes plant health under stress conditions. This insight into microbial assistance opens new avenues for research and application in crop management and soil remediation. This chapter contributes essential knowledge toward bolstering crop resilience against toxic metal/metalloid contamination by presenting cutting-edge research findings and sophisticated mitigation techniques. It emphasizes the critical role of innovative research in overcoming the challenges posed by soil contamination, paving the way for achieving sustainable agricultural productivity and food security in the face of environmental stressors.

1. Introduction to soil toxic metals/metalloids

Soil toxic metal/metalloid contamination is a paramount global issue that presents considerable challenges to food security, sustainable agriculture, and human health. Principal factors contributing to the contamination of soils with toxic metals/metalloids encompass mining operations, industrial processes, sewage sludge application, and agricultural practices involving fertilizers and pesticides [1]. Lead (Pb), cadmium (Cd), arsenic (As), mercury (Hg), and chromium (Cr) are among the prevalent toxic metals/metalloids frequently encountered in soils that have undergone contamination [2].

Toxic metal/metalloid contamination in soils is globally widespread, with hotspots often found in regions with high industrial and mining activities. In the context of China, it is observed that the levels of soil toxic metal/metalloid pollution surpass the established standard rate of 16.1%. Notably, the Yunnan-Guizhou area, the Pearl River Delta, and southeast Fujian exhibit a significant prevalence of Pb pollution [3]. In the United States, an estimated 600,000 hectares of land are affected by toxic metal/metalloid contamination, while in Europe, countries such as Germany, the United Kingdom, Italy, and Spain, collectively account for approximately 400,000 contaminated sites [3]. A study conducted in southern Tibet, China, found that soil Cu, Zn, and Cd contents near national and nonnational highways were significantly higher than the corresponding background values in the region [3].

Similarly, a study in an industrial agglomeration area in China revealed high-resolution risk mapping of toxic metals/metalloids in soil, identifying high-risk hotspots [4]. These global hotspots of toxic metal/metalloid contamination in soils pose significant risks to agricultural productivity, food safety, and public health. Therefore, developing effective strategies for mitigating toxic metal/metalloid stress in soils and ensuring a safe and sustainable agricultural future is crucial.

Understanding the intricate ways toxic metals/metalloids exacerbate abiotic stress in crops is crucial as it directly impacts agricultural resilience, necessitating innovative approaches for effective management and remediation of contaminated soils.

The term “heavy metals” has been used in environmental and pollution studies for decades, yet its ambiguous nature and the absence of a standardized definition have ignited debates. It frequently amalgamates metals, metalloids, and nonmetals, absent a clear delineation, and is used as a group name for metals associated with contamination and potential toxicity [5]. The controversy over the definition of “heavy metals” complicates scientific discourse and influences public perception and policymaking by obscuring the distinctions between truly hazardous elements and those that are essential or benign at specific concentrations. Consequently, toxic metals/metalloids, rather than merely metal/metalloids, are traditionally delineated as metallic elements with a greater density than water. They are naturally occurring elements with a considerable atomic weight and at least five times the density of water. These elements are often associated with contamination, potential toxicity on living organisms and plants, and their negative impact on human health [6].

Metals can be classified as essential to a living organism and nonessential metals. Essential toxic metals/metalloids are required by living organisms, often functioning as protein cofactors in various biological processes. They are nontoxic when present in trace amounts in an organism but can become toxic if concentrations exceed a certain threshold. Examples of essential metals include copper (Cu), Fe, and zinc [7]. On the other hand, nonessential toxic metals/metalloids have no biological function and are toxic to the organism, even in trace amounts. Nonessential metal ions are chemically like their essential metal counterparts. They can interact similarly with the proteins and pathways that regulate necessary metal ions, although generally disrupting, rather than enabling, these [7]. For instance, essential metals, such as Fe, Cobalt (Co), Cu, Mn, Zn, and molybdenum (Mo), play crucial roles in plant development by participating in metabolic reactions and acting as micronutrients. However, when they exceed their threshold concentrations, their actions are considered toxic to plant development [8].

The toxicity thresholds for toxic metals/metalloids in plants encompass the critical concentration levels beyond which these elements transition from benign or beneficial to detrimental for plant growth and development. This delineation is vital as it underscores the narrow margin within which the biochemical balance of metal ions is maintained in plant systems. Elements, such as As, Ca, Pb, and Cr, among others, exemplify the broad spectrum of metals that, upon surpassing their respective threshold concentrations, initiate adverse effects on plant physiology and development [8].

Central to the detrimental impact of exceeding these toxicity thresholds is generating reactive oxygen species (ROS), a suite of highly reactive molecules derived from molecular oxygen. While integral to normal cellular processes, ROS can inflict significant damage when their production overwhelms the plant’s antioxidative defense mechanisms. Some toxic metals/metalloids, such as Hg and As, can directly alter protein/enzyme activities by targeting their -SH group, further impeding cellular metabolism [9].

A prominent manifestation of toxic metal/metalloid-induced stress is the inhibition of photosynthesis, a process foundational to plant growth and energy production. The mechanism underlying this inhibition is twofold: firstly, toxic metals/metalloids can optimize the activity of chlorophyllase, an enzyme responsible for the degradation of chlorophyll molecules, and secondly, they can replace the central magnesium (Mg) ion in the chlorophyll molecule’s porphyrin ring. Such replacements affect the molecule’s structural integrity and functional capability, culminating in reduced photosynthetic capacity, and, by extension, diminished plant growth and yield [9].

The threshold concentrations of toxic metals/metalloids in plants vary depending on the specific metal. For instance, the World Health Organization (WHO) has set the permissible limits/MRL of their concentrations (mg·Kg⁻¹) in plants: Cu (10), Pb (2), Zn (0.6), and Cd (0.02). Metals with high permissible limits are assumed to be safe. In plants, the permissible limits of Cu are the highest, followed by Pb and Zn, while the permissible limits of Cd are the lowest. These limited values mean that the accumulation of Cd in the plants, even at a lower concentration, is more toxic than the others [10].

Comparative analysis with existing literature reveals a consensus on the mechanism of ROS generation as a pivotal factor in metal/metalloid-induced toxicity. Studies across various plant species and metal/metalloid stressors consistently report oxidative stress, characterized by an overproduction of ROS, as an expected outcome of exposure to toxic metal concentrations beyond the threshold levels. This oxidative stress parallels findings in related studies, which underscore the universal challenge of managing metal/metalloid toxicity across diverse plant systems. However, variations in species-specific responses, metal uptake efficiencies, and antioxidative defense capacities highlight the complexity of metal/metalloid-plant interactions and underscore the significance of tailored research and mitigation strategies for managing metal/metalloid stress in plants.

In the broader context of toxic metal/metalloid research, the intricate balance between metals’ beneficial and harmful effects underscores the complexity of plant responses to abiotic stress. Future research directions could include elucidating the molecular and genetic mechanisms underpinning these responses and focusing on identifying essential genes and pathways involved in metal uptake, sequestration, and detoxification. Furthermore, exploring the potential for genetic engineering and biotechnological interventions to optimize plant resilience against metal/metalloid toxicity presents a promising avenue for sustainable agricultural practices in contaminated environments.

The escalation of soil toxic metal/metalloid contamination is a critical environmental concern attributable to a complex interplay between natural phenomena and human activities (Figure 1). This bifurcation of sources, each with its unique contribution to soil metal levels, underscores the complex dynamics of environmental contamination. An in-depth examination of these sources reveals the inherent variability in contamination mechanisms and the exacerbating influence of human activities on the dispersal and concentration of these toxicants beyond natural background levels.

Figure 1.

Sources of soil toxic metal/metalloid contamination. This diagram depicts the main natural and anthropogenic sources contributing to soil contamination.

Intrinsic to the Earth’s biogeochemical cycles, natural sources such as volcanic emissions, ocean salt sprays, eolian dispersion of soil particles, forest fires, and rock weathering constitute primary pathways through which toxic metals/metalloids infiltrate the soil matrix [11]. While fundamental to ecological balances, these phenomena introduce metals such as As, Hg, and Cd into terrestrial environments, albeit at concentrations typically within natural baseline levels. For instance, volcanic eruptions and rock weathering are pivotal in cycling essential and nonessential metals through the environment, subtly influencing soil composition over geological timescales [11, 12].

Contrastingly, anthropogenic activities amplify the presence and impact of toxic metals/metalloids in soil, often elevating concentrations well above natural background levels. Industrial processes, mining operations, and agricultural practices emerge as dominant anthropogenic vectors, introducing hazardous elements, such as As, Cd, Cr, Cu, Hg, and Pb, into the soil. These elements, deriving from sewage discharge, paints, alloys, electronic waste, and mining effluents, not only elevate soil metal concentrations but also pose considerable environmental and health hazards due to their persistence and bioaccumulative nature [11].

A comparative analysis underscores the disproportionate impact of human activities on soil contamination levels. For example, a notable study by Ma et al. [13] conducted in Tianjin, China, illuminates the extensive contribution of industrial and traffic-related factors to elevated soil concentrations such as Cd, Pb, and zinc (Zn). Such findings, indicative of widespread anthropogenic influence, resonate with observations in Saudi Arabia and Mayabeque, Cuba, where mining and agricultural practices significantly exacerbate soil metal concentrations. These examples, drawn from diverse geographical contexts, elucidate the global scope of anthropogenic soil contamination, highlighting regional variations in sources and impacts [13].

Mining operations also play a critical role in soil contamination with toxic metals/metalloids. Research by Al-Swadi et al. [14] examined the influence of industrial and mining activities on soil and dust in urban and suburban locales in Saudi Arabia. The findings revealed that toxic metals/metalloids, such as Cd, Cu, Zn, and Pb, in mining areas were largely anthropogenic in origin. Contamination levels were markedly higher near mining sites, highlighting the substantial impact of mining activities on the escalation of soil toxic metal/metalloid concentrations [14].

Agricultural practices, especially fertilizers and pesticides, are another significant source of soil toxic metal/metalloid contamination. An investigation by Sosa et al. [15] into the soil composition in Mayabeque, Cuba, revealed the presence of toxic metals/metalloids such as Cu, Pb, Zn, and Hg, which are significantly influenced by agricultural activities. The study indicated that agricultural runoff, laden with these metals, considerably contributes to their accumulation in soil [15].

The advent of industrialization and the relentless pace of urbanization have precipitated a marked escalation in soil toxic metal/metalloid contamination, engendering significant environmental and public health challenges. This phenomenon, characterized by the rapid expansion of industrial operations and urban sprawls, has catalyzed the pervasive dissemination of pollutants, notably toxic metals/metalloids such as Cu, Zn, As, and Hg, into terrestrial ecosystems. The activities central to this dissemination—ranging from the combustion of fossil fuels to the smelting and diverse manufacturing processes—distort the biosphere’s equilibrium, leading to the pronounced accumulation of toxic metals/metalloids in soil matrixes [8].

Urbanization, characterized by extensive anthropogenic activity, contributes to soil toxic metal/metalloid pollution. The conversion of rural land for urban development and population growth leads to environmental degradation and diverse pollution [16]. Discharging wastewater, which often contains toxic metals/metalloids, is a significant source of soil contamination in urban areas [16].

Urbanization further amplifies this contamination through substantial anthropogenic activities. The transformation of rural landscapes into urban and industrial zones contributes to environmental degradation and facilitates the introduction of varied pollutants into the soil [16]. A significant vector of this contamination is the discharge of wastewater enriched with toxic metals/metalloids from urban and industrial sources. This effluent, often a byproduct of myriad industrial processes, including plating, electroplating, battery manufacturing, pesticide production, and more, embodies a composite of harmful substances that, when released untreated into the environment, jeopardizes ecological integrity and human health [16, 17].

The ramifications of these activities extend beyond immediate environmental degradation, heralding long-term ecological and health consequences. Wastewater discharge, in particular, serves as a conduit for toxic metals/metalloids to infiltrate terrestrial and aquatic ecosystems, disrupting the ecological balance and posing bioaccumulation risks to flora and fauna. This bioaccumulation, in turn, facilitates the entry of toxic metals/metalloids into the human food chain, manifesting in a spectrum of adverse health outcomes ranging from acute poisoning to chronic conditions such as neurological disorders, cardiovascular diseases, and cancer.

Current research in environmental pollution and public health directly correlates soil contamination with toxic metals/metalloids and various health issues. Studies highlight the insidious nature of these contaminants, underscoring the necessity for vigilant monitoring and remediation strategies. The role of industrialization and urbanization in exacerbating soil contamination necessitates reevaluating waste management practices and industrial processes, advocating for sustainable development paradigms prioritizing environmental health and safety.

In light of these considerations, the impact of industrialization and urbanization on soil toxic metal/metalloid contamination embodies a multifaceted challenge. It necessitates a concerted effort among policymakers, industry stakeholders, and the scientific community to devise and implement comprehensive strategies to mitigate contamination levels and safeguard public health and ecological systems for future generations.

Other anthropogenic activities contribute to soil toxic metal/metalloid contamination besides industrialization and urbanization. These include farming practices, mining, and the use of domestic effluents [8].

The inadvertent release of toxic metals/metalloids through accidental spills or leaks during industrial operations or transportation constitutes a significant source of environmental contamination [11]. Such incidents, often precipitated by deficiencies in infrastructure integrity or lapses in waste management protocols, underscore the vulnerability of natural ecosystems to anthropogenic disturbances. Due to aging infrastructure or oversight in management practices, releasing toxicants in these contexts compromises soil health and poses broader ecological risks [18].

A critical concern within agriculture is using inorganic fertilizers derived from raw materials, such as phosphate rock [19]. While essential for enhancing crop yield and soil fertility, these fertilizers can also serve as conduits for introducing toxic metals/metalloids into agricultural soils. Phosphate rock, for instance, contains trace amounts of cadmium (Cd) and other potentially harmful elements that, when processed into fertilizers and applied to fields, can accumulate in the soil and subsequently be overtaken by crops [19]. This pathway threatens the integrity of soil ecosystems and raises significant concerns for food safety and human health as the bioaccumulation of toxic metals/metalloids in edible plant parts can lead to their entry into the food chain.

The ramifications of such contamination extend beyond immediate health risks to encompass broader challenges for agricultural sustainability. The persistent nature of toxic metals/metalloids in soils can impair soil biodiversity and fertility over time, undermining efforts to achieve sustainable agricultural practices. Furthermore, the accumulation of toxic metals/metalloids in agricultural produce can compromise food safety, necessitating rigorous monitoring and management measures to protect consumer health.

Recent studies have sought to quantify the impacts of inorganic fertilizer use on soil metal concentrations and the resultant implications for crop safety. For example, research has highlighted the potential for significant increases in soil Cd levels following prolonged phosphate fertilizer application, with consequent risks to crop quality and food safety [19]. These findings underscore the need for a balanced approach to fertilizer use that considers both nutritional efficacy and environmental safety to ensure the long-term viability of agricultural systems and the health of the consuming public.

In light of these considerations, addressing the contributions of various anthropogenic sources to soil toxic metal/metalloid contamination requires a multifaceted strategy. This strategy should encompass enhanced regulatory oversight of industrial and agricultural practices, investment in infrastructure maintenance and waste management technologies, and the promotion of sustainable agricultural inputs. Only through such a comprehensive approach can the dual objectives of environmental protection and food safety be effectively realized.

2. Mechanisms of toxic metals/metalloids uptake in plants

2.1 Root absorption and translocation

Plant roots assimilate toxic metals/metalloids via two primary pathways: passive diffusion (apoplastic pathway) and active transport (symplastic pathway) [20]. Passive absorption entails transporting metals along a concentration gradient without energy input. This process is primarily influenced by the concentration of toxic metals/metalloids in the soil solution [20].

On the other hand, active assimilation necessitates energy and entails specific protein translocation. This process allows plants to absorb toxic metals/metalloids even when their concentrations in the soil solution are low. Active transport is essential to uptake critical toxic metals/metalloids, which plants require in trace amounts for various physiological functions [8, 21].

It is worth noting that the balance between passive and active uptake can be influenced by various factors, including the plant species, the type of toxic metals/metalloids, and the environmental conditions [8, 21]. For instance, some plants have developed mechanisms to limit the passive uptake of nonessential and potentially toxic metals/metalloids while enhancing the active uptake of essential ones [8].

The Casparian strip (CS) and endodermis constitute pivotal elements in the plant root system that act as barriers to metal uptake. The CS is a band-like structure of lignin impregnation in the primary cell wall between endodermal cells, preventing the apoplastic flow of substances from the soil solution to the vascular cylinder [22]. This barrier ensures that minerals, including toxic metals/metalloids, must pass through the selective symplastic pathway to enter the plant’s vascular system, allowing for the selective uptake of essential mineral elements and restricting the movement of potentially harmful substances [22, 23].

The endodermis, the innermost cortex layer, surrounds the vascular cylinder and plays a pivotal role in controlling the radial movement of minerals from the soil solution to the stele [22]. The presence of suberin and lignin in the cell walls of the endodermis further contributes to the barrier function, limiting the radial transport of metals and other solutes [24]. This selective permeability is crucial for the plant’s ability to regulate the internal concentrations of toxic metals/metalloids and other elements, thereby protecting the plant from potential toxicity [23, 24].

Moreover, the CS and suberin lamellae in the endodermis can adapt in response to toxic metal/metalloid stress, potentially modifying their structure and composition to fortify the plant’s defense mechanisms against the toxicity of toxic metals/metalloids [23, 24]. These adaptations may include changes in the thickness and permeability of the endodermal cell walls, which can affect the plant’s ability to absorb and translocate toxic metals/metalloids [23, 24].

2.2 Bioavailability of toxic metals/metalloids in soil

The bioavailability of toxic metals/metalloids in soil, which refers to the portion of toxic metals/metalloids that plants can absorb, is strongly influenced by various soil properties, including redox potential, pH, and organic matter content [19].

The pH of soil plays a vital role in determining the solubility of toxic metals/metalloids. Generally, toxic metals/metalloids are more soluble and, hence, more bioavailable in acidic soils than in neutral or alkaline soils. The increased hydrogen ion concentration in acidic soils can displace toxic metals/metalloids from soil particles, making them more available for plant uptake [20, 25].

Redox potential, often denoted as Eh, also affects the solubility of toxic metals/metalloids. Under reducing conditions (low Eh), some toxic metals/metalloids can be transformed into more soluble forms, increasing their bioavailability. Conversely, under oxidizing conditions (high Eh), toxic metals/metalloids may precipitate or adsorb onto soil particles, reducing their bioavailability [26, 27].

Organic matter in soil can influence toxic metal/metalloid bioavailability in several ways. It can bind toxic metals/metalloids, reducing their solubility and bioavailability. However, specific components of organic matter, known as chelating agents, can form soluble complexes with toxic metals/metalloids, enhancing their bioavailability. Moreover, organic matter can affect soil pH and redox potential, indirectly influencing toxic metal/metalloid bioavailability [19, 20, 28, 29].

A comprehensive elucidation of the determinants influencing the bioavailability of toxic metals/metalloids in the soil matrix and their subsequent implications for phytoaccumulation is paramount for the nuanced understanding of plant-soil interaction dynamics under contamination stress. Table 1 delineates these determinants, their mechanisms of action, and the resultant implications for plant uptake of toxic metals/metalloids.

Determinant	Influence on Bioavailability	Implications for Phytoaccumulation
Soil pH	Acidic conditions facilitate the solubilization of metals, thereby augmenting their bioavailability due to proton-induced desorption from soil particulates.	Enhanced phytoaccumulation in acidic environments, potentially escalating toxicity risks
Redox Potential (Eh)	Reductive states increase the solubility and availability of certain metals/metalloids by promoting their transformation into more soluble forms. Oxidative states, conversely, may precipitate metals, thus diminishing their bioavailability.	Reduction conditions may amplify the uptake of more bioavailable metal/metalloid species, while oxidation could inhibit uptake due to the precipitation of metals.
Organic Matter Content	Organic matter modulates metal solubility and bioavailability through complexation. Chelating agents enhance bioavailability by forming soluble complexes, whereas other organic compounds may immobilize metals.	The impact on metal uptake is contingent upon the composition of organic matter, potentially either facilitating or impeding phytoaccumulation.
Metal Interactions	The phenomenon of competitive adsorption among metals at soil sorption sites and plant root interfaces alters each metal’s bioavailability.	The presence of competing metals may reduce or enhance the uptake of specific metals, affecting the equilibrium of nutrient and metal assimilation.

Table 1.

Determinants of metals bioavailability in soil and implications for phytoaccumulation.

Other metals can significantly influence plants’ bioavailability and soil uptake of toxic metals/metalloids. This phenomenon is known as competitive adsorption, where multiple toxic metals/metalloids may compete for the same sorption sites within the soil matrix [30, 31]. The outcome of this competition can affect the strength and magnitude of metal retention by the soil, potentially increasing the mobility and availability of certain toxic metals/metalloids [30].

For example, a high concentration of one metal can reduce the adsorption of another metal as they compete for binding sites on soil particles or within the root system of plants [30, 31]. This can increase the concentration of the less strongly adsorbed metal in the soil solution, making it more available for plant uptake.

The specific interactions between metals can vary depending on several factors, including the types of metals involved, their relative concentrations, and the soil properties, such as pH and organic matter content [30, 31]. Some metals may have a higher affinity for adsorption sites, thereby out-competing others and influencing their bioavailability.

Understanding the competitive interactions between toxic metals/metalloids is crucial for predicting their soil behavior and potential plant uptake, particularly in areas with multi-metal contamination [32, 33]. This knowledge can inform management practices to reduce the risk of toxic metal/metalloid uptake by crops, thereby protecting food safety and human health.

The bioavailability of toxic metals/metalloids in soil and their plant uptake can be influenced by other metals, leading to synergistic or antagonistic effects. These interactions can either inhibit or optimize the uptake and toxicity of different metals, affecting plant growth and development of metals [34, 35].

Synergistic effects occur when one metal’s presence optimizes another’s uptake or toxicity. For instance, in a study on a plant, Conocarpus lancifolius, it was found that Pb) facilitated the accumulation of Cd without affecting the accumulation of nickel (Ni) [35]. On the other hand, antagonistic effects occur when one metal’s presence inhibits the uptake or toxicity of another. For instance, applying Zn fertilizers reduced the values of all toxic metals/metalloids in groundnut seeds except Zn, indicating an antagonistic effect [36]. Similarly, it was found that phosphorus interferes with Zn uptake as Zn uptake by plants is reduced by increasing phosphorus in soil [36].

The toxicity of toxic metals/metalloids in plants can lead to several physiological and morphological changes responsible for the decline in growth. For instance, plants exposed to Cd demonstrated reduced water and nutrient uptake and a decrease in the rate of photosynthesis, leading to inhibition of growth and browning of root tips that ultimately lead to cell death [37].

The bioavailability and uptake of toxic metals/metalloids are also influenced by pollution level, soil pH, and exposure time [38]. Furthermore, plants’ uptake of toxic metals/metalloids is concentration dependent and depends on whether the plant is exposed to single or multiple toxic metals/metalloids [35].

2.3 Role of transporters and chelators

Transport proteins are crucial in the uptake and movement of toxic metals/metalloids in plants. Critical families of transport proteins include toxic metal/metalloid ATPase transporter proteins (toxic metal/metalloid As), natural resistance-associated macrophage proteins (NRAMPs), cation diffusion facilitator (CDF) family, and ZRT, IRT-like Protein (ZIP) family. These proteins transport various toxic metals/metalloids, including Zn, Fe, Cd, and Co, and are essential for plants’ uptake and detoxification processes [39]).

The regulation and expression of these transport proteins can be particular to the type of metal, the plant species, and the environmental conditions. Understanding the functional mechanisms of these transporters and their regulation is vital for developing strategies to enhance plant tolerance to toxic metal/metalloid stress and for phytoremediation applications [40].

Plants have developed various strategies to cope with toxic metal/metalloid toxicity, including metal sequestration. This process involves compartmentalizing or detoxifying toxic metals/metalloids, restricting them from interfering with vital metabolic pathways [41].

Toxic metals/metalloids can be transported out of the cell or restricted to the vacuole, a process known as sequestration or detoxification. This process allows plants to survive in metal-contaminated areas without experiencing toxic effects [41]. The toxic metal/metalloid transporters are critical in plant resistance to metal toxicity, managing uptake, and cellular regulation of metals. Critical transporter families include CPx-type ATPases, ZIP, and NRAMP, which handle essential metals such as Fe, Cu, Zn, and Cd. Intracellular transporters, especially from the HMA, ABC, and CDF families, are sequestering toxic metals/metalloids into vacuoles, aiding in detoxification and homeostasis [41].

In addition to compartmentalization, plants also employ chelation to cope with toxic metal/metalloid toxicity. Nonprotein thiol compounds, such as glutathione and phytochelatins (PCs), are directly involved in the fight against toxic metal/metalloid stress. Under exposure to toxic metals/metalloids, these compounds can chelate toxic metals/metalloids and then transport them into vacuoles via ABC-like transporters, transport proteins found in all kingdoms of life, including plants, thereby leading to a reduction in the number of metals present in the cytoplasm, which, in turn, shields the plants from the harmful consequences associated with these metals [42].

Another crucial defense mechanism in enhancing plant resistance to toxic metals/metalloids is the compartmentalization of toxic metals/metalloids in cell walls. This mechanism protects cellular organelles and components, such as cell membranes, mitochondria, endoplasmic reticulum, and nuclei, from the harmful effects of toxic metals/metalloids [43].

2.4 Influence of soil pH on metal uptake

The pH of the soil is a critical factor that influences the solubility and bioavailability of toxic metals/metalloids, affecting plant uptake. Lower pH increases toxic metal/metalloid solubility, facilitating plants’ uptake of Mn, Cu, and Zn [44]. For example, Mn solubility is prompted by acidic soils, while Cu exists as hydrolysis products in soil with pH below 7, making it more bioavailable; Zn, being amphoteric, is highly mobile and bioavailable in acidic conditions; toxic metals/metalloids tend to form barely soluble phosphates and carbonates at higher pH levels, reducing their bioavailability [44].

The relationship between soil pH and toxic metal/metalloid solubility is complex and can be influenced by other soil properties and environmental conditions. However, the consensus is that acidic conditions increase the solubility and mobility of toxic metals/metalloids, making them more available for plant uptake, while alkaline conditions immobilize them [29, 44, 45, 46]. Comprehending these interactions is vital for effectively managing soil pollution and ensuring crop safety in impacted regions.

Acidic soil conditions enhance root expansion and growth in Rhododendron, potentially increasing the plant’s uptake of toxic metals/metalloids, as evidenced by the more substantial root systems observed at a pH of 5.5 compared to 6.5 [47]. Likewise, Lupinus angustifolius demonstrates increased specific root length and a predominance of thinner roots in low pH environments, suggesting a possible alteration in toxic metal/metalloid absorption. At the same time, alkaline conditions notably suppress lateral root formation and favor thicker root development, influencing plant-metal interactions [48]. Furthermore, soil pH fluctuations, particularly at higher pH levels, induce changes in root surface traits, such as iron plaque formation, which correlates with the uptake of metals such as cadmium and zinc, indicating a pH-dependent modulation of toxic metal/metalloid sequestration [49].

Soil’s buffering capacity and resistance to pH fluctuations are critical in controlling toxic metal/metalloid bioavailability and plant uptake. Calcareous soils, known for their higher buffering capacity, tend to immobilize toxic metals/metalloids more than acidic soils, even under similar contamination levels [45, 50]; such immobilization, characteristic of high pH environments, limit toxic metal/metalloids mobility [46]. Conversely, bioavailable toxic metals/metalloids increase with soil acidity due to their lower buffering capacity, enhancing mobility [45]. Enhancing soil buffering can mitigate acidification and reduce available toxic metal/metalloid content [51].

2.5 Influence of organic matter on metal uptake

Recent studies have highlighted the complex interplay between soil organic matter (SOM) decomposition and the release and availability of toxic metals/metalloids to plants. A variety of soil properties and environmental factors influence these interactions.

Soil pH is a pivotal factor affecting toxic metal/metalloid solubility and plant uptake, with lower pH increasing Mn, Cu, and Zn availability [44]. Mn solubility rises in acidic soils, Cu becomes more available as hydrolysis products below pH 7, and Zn′s mobility and bioavailability are heightened in acidic conditions. In alkaline soils, toxic metal/metalloids are immobilized, forming insoluble phosphates and carbonates [29, 45, 46], with soil pH’s influence on toxic metal/metalloid bioavailability being further complexified by other soil properties and environmental conditions.

Organic matter, especially dissolved organic matter (DOM), has intricate structures and interactions that can significantly impact environmental processes. One such process is the complexation and interface reactions of toxic metals/metalloids, which can be affected by the formation of complex molecules between organic matter and toxic metals/metalloids. This, in turn, can alter the metals’ bioavailability [52].

Organic functional groups within soil organics play a pivotal role in the adsorption dynamics of metals, with carboxylate groups being notably influential, as demonstrated by Engel et al. [53]. Stefanowicz et al. [54] highlight that organic matter contributes to the vitality of soil microbiota, which indirectly impacts metal bioavailability. Yu et al. provide insights into how humic substances’ diverse binding properties can sequester or mobilize metals, significantly affecting plant uptake. This collective research underscores the complexity of soil metal interactions and their significance in plant-metal assimilation.

In addition to other factors, organic matter can affect the bioavailability of toxic metals/metalloids through chelation. Chelation is a binding process in which a single metal ion is bound to two or more atoms of organic matter. This process can increase the solubility and mobility of toxic metals/metalloids, enhancing their bioavailability to plants [55].

However, the effect of organic matter on metal bioavailability can be more complex. For instance, some studies have found that applying organic amendments, such as compost, can sometimes increase the accumulation of certain toxic metals/metalloids in plants [56].

Humic and fulvic acids, significant components of soil organic matter, can significantly influence plants’ uptake of toxic metals/metalloids. They can form complexes with metals, affecting their solubility and bioavailability [57, 58, 59, 60, 61, 62, 63, 64].

Humic substances, including humic and fulvic acids, can significantly affect the environmental behavior of metal pollutants through processes, such as ion exchange and physical adsorption [60]. They can form complexes with toxic metals/metalloids, altering their mobility and bioavailability [57, 58, 61]. For instance, forming metal-humic complexes can decrease mobility and bioavailability [61]. However, in some cases, the formation of humic and fulvic acid complexes increased toxic metal/metalloid toxicity [58].

The binding of toxic metals/metalloids by humic and fulvic acids can be influenced by the number and identity of organic functional groups within these acids Steinberg & Hodge [58]. This binding can either immobilize metals, reducing their bioavailability, or keep them soluble, increasing their bioavailability [60].

Humic and fulvic acids can impact the bioavailability of toxic metals/metalloids by chelation. Chelation is a process where a single metal ion is bound to dual or more atoms of organic matter; this process can enhance the solubility and mobility of toxic metals/metalloids, which may increase their bioavailability to plants [62].

However, the effect of humic and fulvic acids on metal bioavailability can be more complex. For instance, some studies have found that humic acids can interrelate with metals to form metal-humate complexes, enhancing metal adsorption capacity and influencing plant growth and metal availability [57]. On the other hand, fulvic acids have been reported to inhibit metal availability and might be employed to decrease metal bioavailability [62].

The decomposition of organic matter is a vital process in the global carbon cycle and climate feedback as it redistributes energy and nutrients in ecosystems and determines the amount of soil organic carbon (SOC); this process involves the physical breakdown of substrate and biochemical transformation of complex organic compounds [65].

The relationship between the decomposition of organic matter and the release of toxic metals/metalloids is complex. The decomposition process can influence the environment’s mobility and bioavailability of toxic metals/metalloids. Moreover, the decomposition of organic matter can lead to the release of toxic metals/metalloids, with the release rate increasing with increases in organic carbon mineralization [66].

Microbial activity related to organic matter breakdown can also transform toxic metals/metalloids into more bioavailable forms. For instance, some bacteria can convert less bioavailable forms of toxic metals/metalloids into more soluble forms that plants can take up [11]. Additionally, producing organic acids during decomposition can lead to the dissolution of metal complexes and increase the concentration of free metal ions in the soil solution [67].

However, releasing toxic metals/metalloids during organic matter decomposition can also pose risks, such as increased metal leaching to groundwater or uptake by nontarget organisms, which can have ecological and health implications [11, 31, 67, 68].

Microbial activity in organic-rich soils plays a pivotal role in influencing the bioavailability of toxic metals/metalloids [69, 70, 71] through various processes, including mineralization and immobilization [54, 72, 73, 74, 75].

Microorganisms can initiate metal mobilization or immobilization by redox reactions, impacting bioremediation processes [76]. For example, certain bacteria can convert less bioavailable forms of toxic metals/metalloids into more soluble forms that plants can take up [54, 72]. Additionally, microbial-induced biomineralization can transform free v ions into less bioavailable forms, such as carbonates or phosphates, thus reducing their mobility and uptake by plants [77].

Microbial interventions in the bioremediation of toxic metal/metalloid contaminants in agroecosystems are crucial to prevent the leaching of toxic metals/metalloids or their mobilization and simplify toxic metal/metalloid extraction [69, 72]. Using genetically modified microbes and immobilized microbial cells for toxic metal/metalloid remediation is promising [72].

Furthermore, microbial communities can influence the bioavailability of soil pollutants, facilitating their entry into terrestrial food webs [78]. The application of nitrogen and sulfur fertilizers can regulate microbial communities to affect toxic metal/metalloid absorption, as seen in studies with Salix integra Thunb., where the bioavailability of toxic metals/metalloids was increased, and the microbial community was altered [71].

3. Physiological responses of plants to stress of toxic metals/metalloids

3.1 Perturbation of cellular mechanisms

Toxic metals/metalloids s can disrupt cellular membranes, leading to a cascade of detrimental effects on plant cells. The coherence of cellular membranes is paramount for maintaining homeostasis and controlling the movement of substances into and out of the cell. When toxic metals/metalloids, such as Cd and Pb, accumulate in plant tissues, they can interact with membrane lipids and proteins, causing lipid peroxidation, a critical oxidative process damaging cell membranes and modifying membrane viscosity and permeability [79, 80, 81, 82].

Lipid peroxidation is when ROS, often induced by toxic metal/metalloid stress, attacks the unsaturated fatty acids in the lipid bilayer, forming malondialdehyde (MDA) and other toxic by-products. This oxidative damage to membranes can disrupt normal cellular functions, including nutrient transport, signal transduction, and energy transduction [80, 81].

Toxic metals/metalloids can also bind to membrane proteins, affecting their structure and function. This can inhibit the activity of membrane-bound enzymes, disrupt ion channels and transporters, and interfere with membrane receptors, leading to impaired cellular signaling and metabolic dysregulation [79, 80, 83, 84].

The disruption of membrane integrity by toxic metals/metalloids can have various physiological consequences, including decreased photosynthetic efficiency, altered water relations, and reduced nutrient uptake, ultimately leading to stunted plant growth and development [79, 80, 81, 82].

Toxic metals/metalloids can inhibit various plant enzymes, leading to various detrimental effects on plant physiology and soil health. Understanding these interactions is critical for managing toxic metal/metalloid contamination and protecting plant and soil health [80, 85, 86, 87, 88].

Toxic metals/metalloids can inhibit essential enzymatic reactions within plant cells, disrupting normal physiological processes. Enzymes are crucial for a wide range of metabolic activities, and their inhibition can lead to reduced plant growth, compromised pigment production, hormonal and nutrient imbalance, and even cell death [80].

The cytotoxic and genotoxic effects of toxic metals/metalloids are partly due to their interaction with enzymes, which can bind to the active sites or alter the enzyme’s conformation, rendering them inactive [80]. For example, toxic metals/metalloids, such as Cd and Pb, have been shown to inhibit enzymes involved in photosynthesis and respiration, affecting the plant’s ability to produce energy and synthesize important biomolecules [86, 88].

Toxic metals/metalloids can also affect soil enzymatic activity, which is crucial for nutrient cycling and availability. For instance, Zn and Cu have been reported to inhibit dehydrogenase and urease activities in soil, which are essential for organic matter decomposition and nitrogen cycling [85]. This inhibition can lead to changes in soil properties, productivity limitations, and altered ecosystem function [87].

The inhibition of enzymes by toxic metals/metalloids is not limited to those directly involved in metabolic pathways. Still, it can also extend to those responsible for DNA replication, gene expression, and cell division, leading to genome instability and affecting plant health and development [80].

3.2 Impact on photosynthesis and respiration

Toxic metals/metalloids can significantly impact the synthesis and function of chlorophyll, a crucial component of the photosynthesis process, in plants, leading to adverse effects on plant growth and productivity.

Cd stress has been observed to hinder the expression of crucial enzymes responsible for chlorophyll synthesis in tobacco leaves, reducing chlorophyll concentration. This inhibition of chlorophyll synthesis can significantly downregulate the expressions of photosynthesis-related proteins or subunits, suppress both the xanthophyll cycle and NDH-CEF process, and block the photosynthetic electron transport, resulting in severe photoinhibition of both photosystem II (PSII) and photosystem I (PSI) [89].

In contrast, Zn stress has little effect on tobacco leaves’ photosynthetic function [89]. However, both Cd and Zn can disturb the energy migration from the antenna complexes to the chlorophyll of the reaction centers, leading to an increased inhibition of photosynthetic electron transport [88].

Another study found that chlorophyll synthesis products increased with increasing concentrations of Pb and Cd while the degradation products decreased. These findings indicate that toxic metals/metalloids indirectly impact photosynthesis by regulating the functions of enzymes involved in the manufacture and breakdown of chlorophyll [90].

Toxic metals/metalloids can significantly impact plants’ stomatal conductance and gas exchange, reducing photosynthesis rates and other physiological changes. These influences can vary depending on the type and concentration of the toxic metals/metalloids and the specific plant species involved [79, 91, 92].

The impact of toxic metals/metalloids on stomatal conductance and gas exchange in plants is a well-documented area of research. Stomatal conductance refers to the degree of stomatal opening, which directly affects plant transpiration. Exposure to toxic metals/metalloids primarily induces a reduction in plant stomatal conductance, although there are also opposing findings [91]; for instance, Cd has been shown to cause a significant decrease in the stomatal conductance of various plant species [91].

Toxic metals/metalloids can also affect the hydraulic conductivity of plants. For example, high Zn concentrations significantly reduced the root hydraulic conductivity of Quercus suber L., while As contamination reduces root water absorption in soybean (Glycine max L.) [79]. The photosynthetic metrics, including net photosynthesis (Pn), transpiration rate (E), and stomatal conductance (Gs), exhibited a notable decrease in response to toxic metal/metalloid stress [79].

Different toxic metal/metalloid elements, including Cu, Cr, Cd, and Zn, have been found to lower the Pn rates, water-use efficiency (WUE), and stomatal conductance [92]. Toxic metals/metalloids cause the rate of CO₂ production to decrease and subsequently diminish, thus reducing the leaf’s internal CO₂ concentration, which eventually affects the gaseous exchange process, especially the photosynthetic rate [92].

Understanding the mechanisms of toxic metal/metalloid-induced mitochondrial dysfunction is crucial for developing strategies to mitigate the harmful effects of toxic metals/metalloids on plants. Toxic metals/metalloids can significantly impact a plant’s mitochondrial functions, altering ATP production. They can disrupt the normal functioning of mitochondria, the powerhouses of the cell, leading to ATP depletion and increased ROS production. This can result in oxidative stress, further damaging the mitochondria and other cellular components, ultimately leading to cell death [93, 94, 95].

Toxic metals/metalloids can significantly impact plants’ mitochondrial functions, leading to ATP production alterations. Mitochondria, the primary sites of ATP generation, play a vital role in generating cellular energy. However, exposure to toxic metals/metalloids can disrupt their function, leading to ATP depletion and increased production of ROS, ultimately resulting in cell death [95].

Toxic metals/metalloids can impair mitochondrial function by increasing ROS production and decreasing antioxidant activity [93]. The overproduction of ROS can lead to oxidative stress, which can damage cellular components, including mitochondria; this damage can disrupt the mitochondrial respiratory chain, decouple oxidative phosphorylation, and lead to mitochondrial death [94].

For instance, Cd has been shown to interact directly or indirectly with different macromolecules, accumulating environmental pollutants and oxidative stress in plants; this interaction can affect pathological processes such as excess ROS production, ATP depletion, mitochondrial death, and mitochondrial respiratory chain damage [94].

Moreover, toxic metals/metalloids can also affect the efficiency of water flow in plants by reducing transpiration, which can further impact the plant’s ability to produce ATP [79]. Reducing ATP production can decrease plant growth and development, as ATP is essential for various plant metabolic processes [82].

3.3 Oxidative stress and antioxidant responses

The production of ROS is a critical physiological response of plants to toxic metal/metalloid stress. This process can lead to oxidative stress, significantly destroying plant cells and disrupting their normal functioning [94, 96, 97].

Exposure of plants to toxic metals/metalloids leads to the overproduction of ROS, chemically reactive molecules containing oxygen. This overproduction is a part of the normal metabolism of plant cells. However, when plants are exposed to toxic concentrations of toxic metals/metalloids, the production of ROS can overwhelm the systems protecting the plants, resulting in oxidative stress [97].

One of the immediate effects when plant cells are exposed to toxic concentrations of toxic metals/metalloids is the production of ROS, such as superoxide (O−− 2) and hydroxyl radicals (-OH), as well as non-radicals, such as hydrogen peroxide (H₂O₂) and singlet oxygen (1O2) [97]; ROS can be produced either directly by ROS-active metals through the Haber-Weiss/Fenton reactions or indirectly through the disruption of cellular functions [97].

Toxic metals/metalloids can induce ROS production in two ways. First, they can interact directly or indirectly with different macromolecules and signaling pathways, leading to the accumulation of environmental contaminants and oxidative stress in plants [94]; second, toxic metals/metalloids can lead to the depletion of ATP, excessive formation of reactive oxygen species (ROS), damage to the mitochondrial respiratory chain, disruption of oxidative phosphorylation, and ultimately, mitochondrial death [94].

The overproduction of ROS can affect the redox status of cells, causing dramatic physiological changes leading to oxidative stress [96]. Toxic metal/metalloid-induced ROS can cause damage to plants, such as enzymatic activity suppression, protein oxidation, and lipid peroxidation. At the same time, previous studies demonstrated that ROS production is more toxic to plant macromolecules than toxic metals/metalloids themselves [96].

Activating plant antioxidant systems is a crucial physiological response to toxic metal/metalloid stress. These systems, composed of both enzymatic and nonenzymatic components, work together to neutralize ROS, mitigate oxidative damage, and help the plant manage the toxic effects of toxic metals/metalloids [80, 94, 98, 99].

When exposed to toxic metals/metalloids, plants experience oxidative stress due to the overproduction of ROS. This overproduction results from toxic metals/metalloids interacting directly or indirectly with different macromolecules and signaling pathways, accumulating environmental pollutants, and oxidative stress in plants [94].

To counteract this oxidative stress, plants activate their antioxidant systems. These systems are composed of various antioxidant enzymes, for instance, superoxide dismutase (SOD), catalase (CAT), and peroxidases, which work together to neutralize ROS and mitigate the damaging effects of toxic metals/metalloids [80].

For instance, Brassica juncea, a plant species known for its hyperaccumulation of toxic metals/metalloids, has been observed to activate efficient detoxification mechanisms, such as glutamylcysteine-γ synthetase (γECS) and glutathione reductase (GR1), to avoid metal toxicity. These mechanisms help the plant manage oxidative stress, manifested by excessive ROS production, lipid peroxidation increases, and oxidized protein levels [98].

In addition to these enzymatic defenses, plants also activate nonenzymatic antioxidant defenses. These include the production of antioxidant compounds, such as phenolic antioxidants, which play a crucial role in mitigating toxic metal/metalloid-induced oxidative stress [99].

Moreover, plants have developed strategies to regulate the activation of their antioxidant systems in response to toxic metal/metalloid stress. Various signaling molecules can activate the mitogen-activated protein kinase (MAPK) cascade, leading to the differential expression of genes and the subsequent activation of the antioxidant system [99].

3.4 Effects on nutrient uptake and metabolism

Toxic metals/metalloids can compete with essential nutrients for plant uptake, leading to deficiencies and disrupting plant growth and metabolism. For instance, Cd can interfere with the uptake of Zn and calcium (Ca), while Pb can inhibit the uptake of potassium (K) [100, 101, 102]. This competition occurs because toxic metals/metalloids can mimic essential nutrients, leading to their uptake by the same transporters or interfering with the transport process [100].

Cd is known to have a chemical similarity to Zn, which leads to competitive uptake and can affect the translocation of essential metals, such as Zn and Mn, within the plant [100]. The presence of Cd can also influence the uptake of Fe and Mg, which are critical for chlorophyll synthesis and photosynthesis [101].

The competition between toxic metals/metalloids and essential nutrients can significantly impact plant nutrient metabolism. For example, toxic metal/metalloid stress can decrease the concentration of vital nutrients in plant tissues, affecting photosynthesis, respiration, and enzymatic activities [100, 101]. This can result in stunted plant growth and reduced productivity and ultimately affect the nutritional quality of the plants [100, 101, 102].

The physiological responses of plants to toxic metal/metalloid stress can be diverse, affecting various aspects of plant function and metabolism. One such response is the disruption of nutrient transporters, which can lead to reduced nutrient uptake in plants.

This can significantly impact plant growth and development and make plants more susceptible to other forms of stress. Therefore, understanding the mechanisms of toxic metal/metalloid uptake and its effects on nutrient transporters is crucial for developing strategies to mitigate the impacts of toxic metal/metalloid contamination in soils [8, 39, 80, 101, 102, 103].

For instance, it has been suggested that no specific transporters exist for toxic metals/metalloids, such as Cd and Pb, since these elements do not have any direct biological function. Instead, these toxic metals/metalloids are often cotransported along with other soil nutrients across the root cell membrane, which can disrupt the normal nutrient uptake process [80].

Moreover, toxic metals/metalloids can also interfere with the molecular networks that maintain the homeostasis of essential elements in plants. This can further disrupt nutrient uptake and translocation, leading to nutrient lack and reduced plant growth [102, 103].

Furthermore, toxic metals/metalloids can generate ROS within plants, leading to oxidative harm and additional disruption of nutrient transporters [80, 102]. To counteract this, plants may bolster their defenses by activating antioxidant systems [102].

Furthermore, toxic metals/metalloids can inhibit the expression of auxin biosynthetic and catabolic genes, affecting root growth and further impacting nutrient uptake [8].

The physiological responses of plants to toxic metal/metalloid stress, particularly the inhibition of enzymes involved in nutrient metabolism, is a complex process that can significantly impact plant health and productivity. Toxic metals/metalloids, such as Cr, can inhibit enzymes crucial for nutrient metabolism, affecting ATP production and overall plant health [10, 80, 104].

Cr, for instance, has been found to negatively impact plant growth by impairing essential metabolic processes. This includes inhibiting enzymes involved in nutrient metabolism, such as phosphorus metabolism, which is crucial for ATP production [104]. Cr toxicity can lead to the generation of ROS, causing oxidative stress in plants and further disrupting metabolic processes [104, 105].

Furthermore, toxic metals/metalloids can impede the activity of vital enzymes involved in the metabolism and assimilation of nitrate and ammonia, such as nitrate reductase and nitrite reductase; this can decrease photosynthetic rate and CO₂ assimilation, further impacting plant health and productivity [80].

In addition to Cr, other toxic metals/metalloids, such as Cd and Pb, can also inhibit enzymes involved in nutrient metabolism. For example, Cd can significantly reduce the activity of glucose-6-phosphate dehydrogenase, an enzyme part of the oxidative pentose phosphate pathway. This pathway has essential functions, including the production of building blocks for nucleic acids and fatty acids and the generation of NADPH, which is crucial for basic metabolic processes and combating oxidative stress [106].

Toxic metals/metalloids can lead to significant alterations in root morphology, which can further impact the plant’s ability to absorb nutrients from the soil. This can have important implications for plant health and productivity, particularly in areas with high soil toxic metal/metalloid contamination levels [24, 37, 79, 107].

Toxic metals/metalloids can significantly alter the root morphology of plants, which can further impact the plant’s ability to absorb nutrients from the soil. The absorption efficiency of toxic metals/metalloids by plant roots directly affects their metal enrichment ability [107].

Exposure to toxic metals/metalloids can reduce root diameter due to decreased cell division and size. This is often due to reduced growth and lower elasticity of cell walls, along with a reduction in vessel size, contributing to a reduced vascular cylinder area [24]. For instance, plants exposed to Cd have demonstrated reduced water and nutrient uptake, inhibition of growth, and browning of root tips, which ultimately lead to cell death [37].

Toxic metals/metalloids can also cause significant damage to the root and shoot cells and internal organelles, such as chloroplasts and mitochondria, reducing energy production, imposing oxidative stress, and ultimately affecting plant morphology and survival rate [24].

Moreover, toxic metals/metalloids can cause changes in plant physiology and hydraulics and induce anatomical changes; for instance, toxic metals/metalloids in tailings have been demonstrated to cause a decrease in plant growth, which may be related to plant physiological changes [79].

Toxic metals/metalloids can disrupt the internal balance of nutrients within plant cells, leading to deficiencies or toxicities. This disruption can significantly impact plant health and productivity, affecting various physiological and biochemical processes within the plant [79, 91, 94, 108].

Toxic metals/metalloids, including Cu, can induce toxicity in biological systems by interacting with sulfhydryl groups, generating reactive oxygen species (ROS), inactivating enzymes, and causing oxidative stress. While these mechanisms broadly impact cellular functions and can lead to nutrient imbalances, the specific interaction between Cu and Fe in plants, such as competition for transport mechanisms leading to Fe deficiency, underscores the complex dynamics of toxic metals/metalloids uptake and its potential to disrupt plant nutrient homeostasis [108].

Furthermore, toxic metals/metalloids have the potential to disrupt plant metabolism, leading to the suppression of plant development and reduced crop productivity. Plant productivity is contingent upon their growth and development, which toxic metal/metalloid-induced phytotoxicity can negatively impact. This toxin hinders the operation and effectiveness of the photosynthetic system, stomatal function, and cambium activity [91].

Furthermore, toxic metals/metalloids can cause damage to the stomatal morphology and structure and ultimately interfere with several physiological metabolic processes in plants. For example, Cd can inhibit photosynthesis in plants by decreasing stomatal conductance and initiating a reduction in the availability of intracellular CO₂, leading to a decrease in the photosynthetic rate [91].

Furthermore, toxic metals/metalloids can induce poisoning and turn off enzyme systems, significantly impacting vital physiological and biochemical activities such as photosynthesis, respiration, protein synthesis, and the creation of cellular organic matter. This may result in impaired information transfer, thereby causing changes in structural and physiological aspects of the plant such as leaf area, stomatal density, and stomatal conductance [91].

While mycorrhizal fungi and nitrogen-fixing bacteria can mitigate the effects of toxic metals/metalloids on plants, high concentrations of these metals can disrupt the symbiotic relationships, reducing plant growth and nutrient uptake [24, 109, 110, 111].

Toxic metals and metalloids can significantly affect plants’ symbiotic relationships with mycorrhizal fungi and nitrogen-fixing bacteria, which are crucial for nutrient acquisition and plant growth. However, these symbiotic microorganisms can also enhance plant tolerance to toxic metals and metalloids and improve plant growth under metal stress conditions [109, 111].

Mycorrhizal fungi, for example, can sequester large quantities of toxic metals/metalloids, reducing their bioavailability in the soil and, thus, their plant uptake. They can detoxify metal ions by chelating metallothioneins (MTs) or conjugating toxic metals/metalloids with organic molecules, such as glutathione or organic acids [109]. This reduces the toxicity of toxic metals/metalloids to the plant and improves the plant’s nutrient uptake and growth [109, 111].

Furthermore, the diversity, nitrogen-fixing capacity, and toxic metal/metalloid tolerance of culturable rhizobia associated with leguminous plants, such as Pongamia pinnata, have been studied, demonstrating that these bacteria can survive in toxic metal/metalloid-contaminated environments and continue to provide the essential service of nitrogen fixation to their host plants [110]. Figure 2 summarizes the strategies of these microorganisms for enhancing plant resilience and mitigating the effects of toxic metals/metalloids.

Figure 2.

Strategies of mycorrhizal fungi and rhizobia in enhancing plant resilience.

However, toxic metal/metalloid stress can negatively impact these beneficial plant-microbe interactions. For instance, increased bioaccumulation of toxic metals/metalloids beyond the threshold level can damage the root and shoot cells and internal organelles, such as chloroplasts and mitochondria, and affect symbiotic relationships. This can reduce plant growth and productivity due to impaired nutrient acquisition and metabolism [24].

4. Molecular and genetic responses

4.1 Alterations in gene expression owing to toxic metal/metalloid stress

Plants’ responses to toxic metal/metalloid stress involve significant changes in gene expression, with specific genes being upregulated (turned on) or downregulated (turned off) depending on the particular stress conditions. These changes in gene expression are part of the plant’s adaptive response to mitigate the harmful effects of toxic metals/metalloids [80, 112, 113].

Upregulated genes are those whose expression is increased in response to toxic metal/metalloid stress. Toxic metal/metalloid ATPase (HMA) gene expression in rice was upregulated under toxic metal/metalloid stress [112]. These genes transport toxic metals/metalloids across cell membranes, which is crucial in metal detoxification. Similarly, genes that regulate antioxidant activity and stress responses are upregulated when plants are exposed to toxic metals/metalloids, as observed in Lolium perenne L. exposed to Cd²⁺ and Hg²⁺ [113]. This upregulation enhances the plant’s defense mechanisms against the oxidative stress of toxic metals/metalloids.

Conversely, downregulated genes are those whose expression is reduced under toxic metal/metalloid stress. While specific examples of downregulated genes were not provided in the search results, toxic metal/metalloid stress can lead to the downregulation of genes involved in average plant growth and the development of stress response mechanisms [80].

It is important to note that the specific genes that are upregulated or downregulated can vary depending on the type of toxic metals/metalloids, the plant species, and the specific environmental conditions. Furthermore, these changes in gene expression can be heritable, indicating they can be passed on to subsequent generations, allowing plants to “remember” and respond more effectively to toxic metal/metalloid stress [112].

Under toxic metal/metalloid stress, plants change gene expression, particularly those involving metal-responsive elements. These changes are crucial for the plant’s adaptive response to stress and can affect various processes, such as the transport of metals and the overall tolerance to toxic metal/metalloid stress. Alterations in gene expression can result in the increased or decreased activity of particular genes. These changes are part of the plant’s adaptive response to coping with stress and can even be passed down to subsequent generations, making them heritable [112].

One of the critical components of this response involves metal-responsive elements, which are specific DNA sequences that can bind to metals, thereby influencing gene expression. For instance, research on the Cd-tolerant cultivar of Chinese flowing cabbage and Sedum plumbizincicola revealed elevated expression of specific genes in response to Cd stress [112]. Similarly, in Lycopersicum esculentum, the toxic metal/metalloid transporters COPT1 and COPT2 could be prompted to express under Cu stress [112].

A study investigated the expression patterns of genes in the metal tolerance protein family in Eucalyptus grandis exposed to metal stress conditions. These proteins, which are membrane-bound transporters, play a crucial role in the selective transport of various metals. Variations in their transcript levels may reflect the plant’s adaptive response to metal-induced stress [114].

Moreover, plants respond to toxic metal/metalloid stress-induced oxidative and genotoxic damage via rapid gene expression changes. Various families of transcription factors play a crucial role in triggering such responses [80].

4.2 Function of noncoding RNAs

MicroRNAs (miRNAs) are essential in the plant’s reaction to toxic metal/metalloid stress, regulating a wide array of physiological processes to mitigate the harmful effects of these metals. As our understanding of these small but powerful molecules continues to grow, they may offer promising avenues for enhancing plant tolerance to toxic metals/metalloids and improving phytoremediation strategies [115, 116, 117].

The miRNAs are small, noncoding RNAs that play a fundamental role in controlling gene expression in response to toxic metal/metalloid stress in plants. These miRNAs, usually 20-24 nucleotides long, regulate gene expression following transcription. They mainly achieve this by inhibiting translation or cleaving their target [116, 117].

Rapid industrialization and large-scale chemical fertilizers and pesticides have increased toxic metals/metalloids and soil contamination. This has necessitated the evolution of complex plant mechanisms to cope with toxic metal/metalloid stress. One such mechanism involves using miRNAs to combat metal-induced toxicity [115, 117].

miRNAs regulate plant responses to metal stress through several mechanisms, including antioxidant functions, root growth, hormone signals, transcription factors (TF), and metal transporters [115]. For instance, they can specifically target and reduce the activation of genes responsible for accumulating toxic metals/metalloids in plants, thus reducing the level of metal present and mitigating its detrimental effects on the plant [117].

Next-generation sequencing (NGS) has significantly enhanced our understanding of the population and function of miRNAs in the context of metal stress [115, 116]. These technologies have enabled the discovery of several known and unknown miRNAs that respond to metal stress, revealing their diverse roles in several plants [115].

For example, miRNAs regulate antioxidant systems, which help mitigate the oxidative stress caused by toxic metals/metalloids [115]. They also regulate root growth, which can be adversely affected by toxic metal/metalloid toxicity [116].

Furthermore, miRNAs can regulate hormone signals and transcription factors, which are critical components of the plant’s response to stress; they can also influence the activity of metal transporters, which are responsible for the uptake and distribution of metals within the plant [115].

Noncoding RNAs (lncRNAs) are RNA molecules that do not code for proteins; however, they play a vital role in regulating gene expression in response to toxic metal/metalloid stress in plants [118, 119]. They are “biological regulators” for various developmental processes and plant stress responses [120]. These lncRNAs can modify gene expression at the posttranscriptional and epigenetic levels by targeting various stress-responsive mRNAs, regulatory genes encoding transcription factors, and numerous miRNAs controlling gene expression [120].

In the context of toxic metal/metalloid stress, lncRNAs have been found to respond to toxic metals/metalloids such as Pb, Fe, Cu, Mn, and aluminum (Al) [118]. For instance, a genome-wide analysis of lncRNAs in rice under Cd stress revealed differentially expressed lncRNAs between Cd stress and normal conditions. A total of 69 lncRNAs were found to be upregulated, while 75 lncRNAs were downregulated in the Cd stress group [119]. This suggests that lncRNAs play a role in the plant’s response to toxic metal/metalloid stress, potentially by modulating the expression of genes in stress response pathways.

Nevertheless, the precise mechanisms via which lncRNAs control gene expression in the existence of toxic metal/metalloid stress remain incompletely comprehended. Some studies suggest that lncRNAs may act as a nucleator, a scaffold for numerous complexes, a template, a decoy, or a signal [118]. For example, lncRNAs may bind to specific DNA sequences (metal-responsive elements), influencing gene expression [118]. They may also interact with other noncoding RNAs, such as miRNAs, to regulate gene expression [121].

Despite these advances, our understanding of the role of lncRNAs in toxic metal/metalloid stress responses is still in its infancy. Many lncRNAs have been detected in plants, but their specific functions and the target genes they regulate remain primarily unknown [120]. Further research is needed to elucidate the complex molecular mechanisms by which lncRNAs contribute to plant adaptation to toxic metal/metalloid stress [118, 120]. This could lead to developing new strategies for enhancing plant tolerance to toxic metals/metalloids, such as manipulating the expression of specific lncRNAs [121].

Small interfering RNAs (siRNAs) play a crucial role in plants by mediating epigenetic modifications, particularly DNA methylation, under toxic metal/metalloid stress. These modifications can affect gene expression and potentially enhance the plant’s tolerance to toxic metals/metalloids, leading to transgenerational stress memory [112, 122, 123].

The siRNAs significantly impact the plant’s response to toxic metal/metalloid stress, especially their influence on DNA methylation, a crucial epigenetic modification. DNA methylation is the process of introducing a methyl group to the DNA molecule, resulting in the modification of gene expression without any changes to the underlying DNA sequence. This process is essential for plant adaptation to various environmental stresses, including toxic metal/metalloid toxicity [122, 123].

siRNAs are known to mediate DNA methylation in plants. This process, known as RNA-directed DNA methylation (RdDM), involves the generation of 24-nucleotide siRNAs that guide the de novo DNA methyltransferase to specific genomic regions, leading to methylation [123]. This methylation can suppress the transcription of specific genes, thereby influencing the plant’s response to stress [122, 123].

Several plant species have observed changes in DNA methylation patterns in toxic metal/metalloid stress. For instance, exposure to toxic metals/metalloids, such as Cd and Zn, has been demonstrated to alter global DNA methylation patterns in wheat, potentially conferring tolerance to these metals. Similarly, a study on rice revealed that changes in DNA methylation potentially mediate toxic metal/metalloid stress-induced locus-specific changes in gene expression [112].

Noncoding RNAs (ncRNAs) could engineer plants that are more resistant to toxic metals/metalloids. However, more research is needed to understand how these ncRNAs control gene expression at a molecular level in response to toxic metal/metalloid stress. As research progresses, engineering ncRNAs, particularly miRNAs and lncRNAs, could become an effective tool to develop crop varieties that can tolerate toxic metals/metalloids. These ncRNAs have emerged as critical regulators in plant responses to toxic metal/metalloid stress [115, 118, 120, 121, 124].

miRNAs are tiny, noncoding RNA molecules that regulate gene expression posttranscriptionally, often by silencing genes through mRNA degradation or translational repression. They have been implicated in various plant processes, including development, nutrient homeostasis, and stress responses. In toxic metal/metalloid stress, miRNAs can target metal uptake, transport, and sequestration genes, thereby modulating the plant’s tolerance to toxic metals/metalloids [115, 124].

lncRNAs, exceeding 200 nucleotides in length, can regulate gene expression by many mechanisms such as modifying chromatin, controlling transcription, and influencing posttranscriptional processing. They have been demonstrated to respond to toxic metals/metalloids such as Pb, Fe, Cu, and Mn, suggesting their involvement in toxic metal/metalloid stress responses [118, 120].

The engineering of ncRNAs offers a novel approach to developing plants with enhanced tolerance to toxic metals/metalloids. For example, overexpressing specific miRNAs that confer stress tolerance or silencing miRNAs that negatively regulate stress response genes could be strategies to improve plant resilience to toxic metals/metalloids [115, 121]. Also, manipulating lncRNAs involved in the stress response could be a viable strategy for enhancing tolerance [118, 120].

4.3 Role of metallothioneins and PCs

The MTs act as metal detectors in toxic metal/metalloid stress, binding to excess metal ions and reducing their toxicity. This makes them essential to the plant’s defense against toxic metal/metalloid stress [125]. MTs are small proteins with a molecular weight of 6-7 kilodaltons (kDa) crucial in mitigating the effects caused by excess metal ions. They are rich in cysteine, a sulfur-containing amino acid, which allows them to bind with metals and detoxify them by reducing their presence [59, 125].

MTs involve cellular processes such as cell growth regulation, ROS management, and DNA repair. The structure of MTs consists of two domains, each containing a cluster of metal atoms. These proteins have several isoforms coded by different alleles on chromosome 16 [125].

The induction of MTs is constant with metals such as Cd, Cu, and Zn. The cysteine residues in MTs are essential for their function and are required for life. The architectural integrity, evolutionary conservation, pervasive presence, gene duplication, and regulated expression of MTs during living organisms’ development, regeneration, and reproduction present compelling evidence for their essential functions within biological systems [125, 126].

PCs are essential for detoxifying toxic metals and metalloids in plants, and their synthesis is regulated in response to metal exposure.

PCs are small, cysteine-rich peptides crucial in detoxifying metal/metalloids in plants. Their synthesis is mediated by the enzyme phytochelatins synthase (PCs), which is activated in response to metal exposure. This activation leads to the chelation of toxic metal ions, such as Cd, Cu, and Zn, thus mitigating their toxicity to plants [127, 128, 129].

PCs are synthesized from glutathione, a tripeptide composed of glutamate, cysteine, and glycine, through an enzymatic reaction catalyzed by PCs. The reaction involves the gamma-glutamylcysteine moiety of glutathione being polymerized to form PCs, which can bind to and detoxify metals/metalloids within the plant cells. This process not only plays a significant role in the detoxification and tolerance of metal/metalloids but also highlights the potential for phytoremediation applications, where plants are used to remove pollutants from the environment [127, 129].

Gene regulation of PCS plays a pivotal role in this process. The presence of metal/metalloids highly regulates the expression of PCS genes, and the activation of these genes leads to the synthesis of PCs, which chelate and sequester metals/metalloids in the vacuoles of plant cells. This mechanism ensures the detoxification of metals/metalloids and the protection of cellular functions from metal toxicity [127].

Furthermore, glutathione’s implications in synthesizing PCs highlight the interconnectedness of plant detoxification pathways. Glutathione is a substrate for PCS and acts as an antioxidant, reducing oxidative stress induced by heavy metal exposure. The synthesis of PCs and their role in heavy metal chelation exemplify the plant’s comprehensive strategy to cope with environmental stressors, ensuring survival and maintaining homeostasis in the presence of toxic metals [127, 128].

To encapsulate, the enzyme PCs, regulated by metal/metalloids, catalyzes the formation of PCs from glutathione. These PCs then bind to toxic metals, facilitating their detoxification and sequestration within the plant. This intricate mechanism underlines plants’ adaptive responses to environmental stresses and has significant implications for enhancing phytoremediation strategies and understanding plant resilience to heavy metal toxicity.

5. Conclusions

In summary, as presented in this chapter, the comprehensive examination of toxic metal/metalloid contamination in soil and its implications for crop resilience and abiotic stress management underscores the multifaceted challenges and innovative strategies in sustainable agriculture. The detailed exploration of the sources of natural and anthropogenic soil contamination, alongside the mechanisms of plant absorption and response to these toxicants, provides a foundational understanding of the complexities involved in plant-soil interactions under stress conditions. The physiological and molecular responses of plants to toxic metal/metalloid stress, particularly the impact on photosynthesis, nutrient uptake, and oxidative stress management, highlight the critical areas where plant resilience needs bolstering.

The discussion on phytoremediation and genetic engineering as strategies to alleviate toxic metal/metalloid stress showcases the potential of biotechnological advancements in enhancing plant growth and resilience in contaminated soils. The role of PCs in detoxifying plants and the promising results from the overexpression of PCs genes in Arabidopsis thaliana for improved tolerance and accumulation of toxic metals/metalloids point toward a genetic manipulation approach in developing crops with enhanced resistance to environmental stressors.

Furthermore, the interaction between plants and soil microbes offers an intriguing insight into the bioavailability of toxic metals/metalloids and the support of plant health under adverse conditions. This symbiotic relationship underscores the importance of microbial communities in the soil ecosystem and their potential to support plant resilience and health.

The chapter contributes significantly to the current body of knowledge by presenting advanced mitigation strategies and research findings that can inform and guide sustainable agricultural practices. The insights gained from this chapter are invaluable for researchers, agronomists, and policymakers, aiming to enhance crop resilience against toxic metal/metalloid contamination and to ensure food security in the face of increasing environmental challenges. The innovative approaches discussed herein, including phytoremediation, genetic engineering, and the exploitation of plant-microbe interactions, offer promising pathways toward achieving sustainable agricultural systems resilient to abiotic stresses.

Conflict of interest

The authors declare no conflict of interest.

Disclaimer

The views expressed in this paper are those of the author(s) and do not necessarily reflect those of the SFDA or its stakeholders. Guaranteeing the accuracy and validity of the data is the sole responsibility of the research author(s).