Recent advances in phyto-combined remediation of heavy metal pollution in soil

Heavy metals (HMs) are typically characterized as metals with a density exceeding 5 g/cm3. While trace elements like manganese (Mn), copper (Cu), and zinc (Zn) are essential for various life activities, the majority of HMs, such as mercury (Hg), lead (Pb), cadmium (Cd), cobalt (Co), chromium (Cr), arsenic (As), and nickel (Ni), are non-essential and do not play vital roles in biological processes. Although trace amounts of HMs naturally occur in soils, their excessive accumulation can deteriorate soil quality and harm surface plants. Among HMs, Cr, As, Ni, Cd, Pb, Cu, and Zn are considered as priority toxic pollutants by the United States Environmental Protection Agency (USEPA) (Cheng et al., 2023). Globally, over 10 million sites have been reported with soil contamination, of which a significant majority, exceeding 50%, exhibit alarming concentrations of HMs and/or metalloids (Sánchez-Castro et al., 2023). In Europe, the issue of HM-contaminated soils is also significant. The study found that in Slovakia, even in the second decade after the end of mining and metallurgical activities, the levels of Zn, Cd, Cu, Pb and Hg in the soil exceeded the permissible limits (Musilova et al., 2016). In South Africa, a study conducted by Zerizghi et al. also indicated pronounced levels of soil HMs, underscoring substantial ecological and human health risks (Zerizghi et al., 2022). Similarly, in China, HMs are responsible for >80% of land contamination cases(Cui et al., 2021). The presence of HMs in soils and plants can lead to their transfer and accumulation in the food chain, eventually accumulating in humans and causing significant harm even at low concentrations(Chai et al., 2021; Qasem et al., 2021). For example, Cr is an essential trace element in the human body, which involved in various metabolic activities(Vincent, 2019), but its bio-enrichment in the human body can cause lesions and even cancer in organs such as bone, pharynx, lung, thyroid and bladder(Fang et al., 2014). Similarly, Cd, which is barely detectable in newborn humans, can accumulate through skin contact and respiratory tract exposure, with 85% of it concentrating in the liver or kidneys, posing a threat to human health(Renugadevi and Prabu, 2010; Yan et al., 2020). Consequently, addressing HM contamination in soils has become a crucial concern. A study conducted by Kan et al. examined the HM contamination status in the Pb and Zn mine tailings of China, based on the published literature from 2015 to 2020 screened from the main literature databases including Web of Science, China Knowledge Full–text Literature Database, and China Wanfang Literature Database. The results revealed that the average concentrations of Cd, Hg, As, Zn, Pb, Cu, and Ni in the soil samples greatly exceeded the Chinese Grade II environmental quality standards for soils, approximately 81.2, 57.1, 28.1, 18.0, 13.8, 1.7, and 1.4 times the standards, respectively(Kan et al., 2021). Soil quality and food safety are intimately interconnected. For example, the “Itai Itai Disease” that emerged in Japan in the last century was caused by the consumption of “Cd-contaminated rice” by local residents and the contamination of drinking water with Cd. Given the critical nature of HM contamination in soils, it is imperative to explore efficient, economical, and safe solutions to mitigate ecological damage caused by HMs and minimize associated risks to human health during the remediation process.

Various treatment methods have been developed for the remediation of environmental pollutants, which can be categorized into physical, chemical, and biological methods(Chen et al., 2022; Chen et al., 2023; Zhuo and Fan, 2021). Physical and chemical methods, such as soil replacement, isolation, stabilization, electroremediation, and leaching, are commonly employed(Gong et al., 2018b; Ma et al., 2014; Zhai et al., 2018; Zhao et al., 2019). However, these methods have disadvantages such as extensive construction requirements, high expenses, potential secondary pollution risks, and considerable alteration of soil's physical and chemical properties, affecting the growth of plant(Ali et al., 2013a; Yaashikaa et al., 2022). For example, Ma et al. harnessed the potential of FeCl3 in the process of soil HMs stabilization, coupled with limestone for immobilization. While this approach effectively mitigated the bioavailability of Cd, Cu, Pb, and Zn in the soil, it also exhibited discernible repercussions on soil enzymatic activity(Ma et al., 2014). Meanwhile, The large-scale use of chelating agents with low biodegradability in soil leaching also creates new environmental risks(Manas et al., 2022). A swifter leaching rate in soil leaching often leads to a greater agent consumption and an escalation in leachate volume, which may case secondary pollution(Zheng et al., 2022). Hence, there is a pressing need to investigate an environmentally and ecologically sound, resource-efficient, and economically viable approach. In this regard, phytoremediation, utilizing plants for remediating HM-contaminated soil, emerges as a green and economically feasible solution.

Phytoremediation, a solar-powered in-situ remediation technique, utilizes plants as the foundation to remove HMs from the soil through processes such as absorption, transportation, transformation, accumulation, or volatilization, thereby achieving the goal of remediation. As a result, phytoremediation is considered an environmentally friendly technique capable of effectively removing HMs from the environment. Compared to physical and chemical remediation methods, phytoremediation is more cost-effective, environmentally friendly, and possesses certain landscape value. Additionally, the physicochemical properties of the soil are not significantly altered after phytoremediation, and the plant biomass obtained after remediation can be further processed and transformed into valuable green products(Cui et al., 2021). These advantages make phytoremediation less likely to cause secondary pollution and more readily accepted by the public. However, despite these benefits, phytoremediation faces challenges due to its susceptibility to internal and external environmental factors. Researchers have employed various approaches to enhance the effectiveness of HM phytoremediation and have achieved some progress. For example, the application of ethylenediaminetetraacetic acid (EDTA) has been employed to enhance the bioavailability of heavy metals in soil, thereby facilitating their uptake by plants (Jiang et al., 2019). Through the utilization of genetic engineering techniques, the expression of the HM resistance gene ScYCF1 in plants enables them to accumulate a greater amount of HMs while attenuating associated damages(Shim et al., 2013). Introducing relevant microorganisms into the plant-associated microbiome not only activates HMs in the soil(Rajkumar et al., 2010), but also promotes plant growth(Manoj et al., 2019), thereby enhancing the plant's ability to withstand HM stress. Most of these approaches combined phytoremediation with other technologies. However, limited knowledge of the phyto-combined remediation strategies required to harness the HM phytoremediation for complex in-situ condition is still a challenge.

In addressing these challenges, this review initially presents the principal strategies utilized in the phytoremediation of HMs, followed by an in-depth discourse on the mechanisms pertaining to plant absorption, translocation, accumulation, and detoxification of HMs. Subsequently, an introduction is provided to the phyto-combined remediation strategies that have been demonstrated to significantly enhance the efficiency of HM removal from soils. Despite the abundant literature on this subject, the present work distinguishes itself by providing a thorough examination of the synergistic effects of integrating phytoremediation with innovative approaches, including genetic modification, microbial assistance, the addition of exogenous substances, agronomic techniques, and other strategies such as electroremediation. The crucial significance of these combined strategies in surmounting the inherent limitations of conventional phytoremediation—namely, the impediments of slow plant growth and restricted biomass production, often aggravated by the toxic effects of HMs—is elucidated in this paper. Practical recommendations for the effective implementation of these strategies are offered, thus contributing a valuable perspective to the field that aligns ecological safety with economic feasibility. Finally, a concise summary of the entire text is provided, and potential future research directions for the phyto-combined remediation of HM pollution in soil are explored at the end of this review.

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