Next Article in Journal
Anti-Leptospira Seroprevalence and Associated Risk Factors among Forestry Workers in Lower Saxony, North-West Germany
Next Article in Special Issue
Characteristics of the Perianthic Endophytic Fungal Communities of the Rare Horticultural Plant Lirianthe delavayi and Their Changes under Artificial Cultivation
Previous Article in Journal
A Single Base Change in the csgD Promoter Resulted in Enhanced Biofilm in Swine-Derived Salmonella Typhimurium
Previous Article in Special Issue
Endophytic Fungi Inoculation Reduces Ramulosis Severity in Gossypium hirsutum Plants
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Microorganisms
Volume 12
Issue 7
10.3390/microorganisms12071255
microorganisms-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Sustainable Remediation of Soil and Water Utilizing Arbuscular Mycorrhizal Fungi: A Review

by
Xueqi Zhang
1,
Zongcheng Wang
1,
Yebin Lu
2,
Jun Wei
2,
Shiying Qi
2,
Boran Wu
1,3 and
Shuiping Cheng
1,3,*
1
Key Laboratory of Yangtze River Water Environment, Ministry of Education, College of Environmental Science and Engineering, Tongji University, Shanghai 200092, China
2
Power China Huadong Engineering Corporation Limited, Hangzhou 311122, China
3
Shanghai Institute of Pollution Control and Ecological Security, Shanghai 200092, China
*
Author to whom correspondence should be addressed.
Microorganisms 2024, 12(7), 1255; https://doi.org/10.3390/microorganisms12071255
Submission received: 4 June 2024 / Revised: 18 June 2024 / Accepted: 19 June 2024 / Published: 21 June 2024
(This article belongs to the Special Issue Effect of Microbial Communities for Environmental Protection and Development of Agriculture)
Browse Figures
Review Reports Versions Notes

Abstract

:
Phytoremediation is recognized as an environmentally friendly technique. However, the low biomass production, high time consumption, and exposure to combined toxic stress from contaminated media weaken the potential of phytoremediation. As a class of plant-beneficial microorganisms, arbuscular mycorrhizal fungi (AMF) can promote plant nutrient uptake, improve plant habitats, and regulate abiotic stresses, and the utilization of AMF to enhance phytoremediation is considered to be an effective way to enhance the remediation efficiency. In this paper, we searched 520 papers published during the period 2000–2023 on the topic of AMF-assisted phytoremediation from the Web of Science core collection database. We analyzed the author co-authorship, country, and keyword co-occurrence clustering by VOSviewer. We summarized the advances in research and proposed prospective studies on AMF-assisted phytoremediation. The bibliometric analyses showed that heavy metal, soil, stress tolerance, and growth promotion were the research hotspots. AMF–plant symbiosis has been used in water and soil in different scenarios for the remediation of heavy metal pollution and organic pollution, among others. The potential mechanisms of pollutant removal in which AMF are directly involved through hyphal exudate binding and stabilization, accumulation in their structures, and nutrient exchange with the host plant are highlighted. In addition, the tolerance strategies of AMF through influencing the subcellular distribution of contaminants as well as chemical form shifts, activation of plant defenses, and induction of differential gene expression in plants are presented. We proposed that future research should screen anaerobic-tolerant AMF strains, examine bacterial interactions with AMF, and utilize AMF for combined pollutant removal to accelerate practical applications.

1. Introduction

Soil and water are often the final destinations for chemical waste, and long-term pollution can threaten organisms in the food chain [1]. Human activity is a significant source of soil contamination, with waste from household, industry, and agriculture contributing to the problem [2]. When domestic or industrial wastewater is not properly treated, it can indirectly lead to soil pollution through activities such as irrigation [3]. Unfortunately, wastewater discharges from these activities and farming are common causes of water pollution [4]. Inadequate wastewater treatment in water treatment plants leads to the pollution of drinking water sources [5].
Phytoremediation is a sustainable approach that can be applied in situ, thereby avoiding secondary contamination [6]. The various methods of phytoremediation include phytovolatilization, phytoextraction, phytofiltration, phytostabilization, phytodegradation, and rhizodegradation. Among these methods, the rhizosphere of plants plays a crucial role in effective remediation [7]. Soil microorganisms, especially endophytes, contribute significantly to assisting plants in resisting biotic and abiotic stresses [8]. However, traditional phytoremediation methods have limitations such as low biomass production, high time consumption, and stress caused by the combined toxicity of contaminated media, which can diminish the remediation potential of plants [9]. Rational manipulation of the inter-root microbial assemblage is an effective measure to enhance phytoremediation efficiency and maintain sustainability.
Arbuscular mycorrhizal fungi (AMF) are important components of plant inter-root microbial communities [10]. They have shown the ability to improve plant growth in unfavorable environments and colonization of over 90% of angiosperms [11]. The exchange of nutrients between plants and AMF is the cornerstone for stabilizing this relationship [12]. Plants provide AMF with carbohydrates and lipids, while AMF utilize an extensive mycelial network to obtain water and mineral nutrients from the soil and supply them to the host plant through symbiotic interfaces [13]. The symbiosis between AMF and plants is considered to be one of the most effective ways to counteract biotic and abiotic stresses, including remediation of contaminated media and enhancement of plant tolerance [14,15].
AMF are found in various environments and play a crucial role in regulating ecosystem functions in polluted areas [16]. The concentration of pollutants in different environmental media affects the ecological composition of AMF. The discovery of pollutant-tolerant strains is essential for the study of AMF remediation of polluted media [17]. Studies have found that introducing indigenous AMF into contaminated soil promotes soil enzyme activities and antioxidant enzyme systems of host plants [18]. In contaminated areas, the symbiosis between AMF and plants creates favorable habitats for other soil microorganisms by providing a stable supply of organic material and stimulating root growth [19,20]. The increased soil organic matter resulting from the introduction of AMF traps more available toxic and harmful compounds, promoting the overall remediation of the polluted environment [21].
In this paper, we review the remediation ability, remediation strategy, and tolerance mechanism of the AMF–plant symbiosis system for different polluted environmental media. We outline prospective studies on the AMF–plant symbiosis system to provide new ideas and technologies for the reconstruction of vegetation in polluted areas and the management of polluted environments.

2. Bibliometric Analyses

Since the beginning of the 21st century, there has been a rapid increase in published research works on AMF-assisted phytoremediation, with the first article relevant to this topic published in 2000. A bibliometric analysis of the published literature in the last 23 years (2000–2023) was conducted to identify hotspot issues and associated important factors related to AMF-assisted phytoremediation. From the Web of Science (WOS) core collection database using the query TS = (“arbuscular mycorrhizal fungi”) AND TS = (“phytoremediation”), 520 relevant research articles published by researchers and scholars from around the world were retrieved. The number of annual publications and the percentage of annual publications during this period are shown in Figure 1. The number of published articles related to AMF-assisted phytoremediation consistently increased during this period. The year 2021 had the highest number of publications, with 56 articles, accounting for 11% of the total (Figure 1A). The retrieved 520 articles were analyzed using VOSviewer1.6.18. According to the co-author analysis results, there are 35 authors with 5 or more publications. Among them, Guo Wei has the highest number of publications (13) (Figure 1B). In addition, the country with the highest number of publications was China (187), followed by India (35), the United States (34), Brazil (32), Canada (32), and France (32), which indicate that research on AMF-assisted phytoremediation mainly originated from China (Figure 1C).
Co-occurrence clustering of all keywords was also analyzed by VOSviewer. The minimum number of occurrences of terms was defined as 10, and irrelevant and duplicate terms were merged. After these specific selections, keyword co-occurrence network graphs were generated. The keyword co-occurrence network diagram generated based on the above settings is shown in Figure 2, and the keyword co-occurrence network diagram is divided into 6 clusters. The terminology map shows the hotspot issues and important factors related to AMF-assisted phytoremediation. Among them, the three clusters with the highest term frequency are labeled in red, purple, and green. The red group indicates that the contaminated environmental medium in which AMF-assisted phytoremediation is applied is mainly soil. The green group indicates that promotion of plant growth is an important part of the AMF-assisted phytoremediation process. The purple group indicates that heavy metal (HM) is the pollutant species with the highest frequency of AMF-assisted phytoremediation being applied. The dark blue group makes it clear that the rhizosphere is the primary site of AMF action, and it is closely associated with rhizospheric microbial communities. Therefore, we summarized the research advances from these four clusters below.

3. AMF-Assisted Phytoremediation of Contaminated Soil

3.1. Soil Contaminated with Heavy Metal

HMs can negatively impact the morpho-physiological and biological properties of plants [22]. They even extend to the food chain and cause harm to human health [23]. While some HM-hyperaccumulating plants play a crucial role in phytoremediation, this phenomenon is rare in terrestrial higher plants [24]. Therefore, the efficient phytoremediation of soil contaminated with HMs requires the manipulation of microbial and plant combination [25]. HMs are the most widespread soil contaminants for AMF remediation application. It has been reported in 1990 that inoculation of AMF in soil with either too low or too high concentrations of HMs can ameliorate both of these soil problems [26]. Although the spore diversity of AMF in soil contaminated with HMs tends to be lower than those in uncontaminated soil, this does not mean that the beneficial effects of AMF will be limited [27]. Silva-Castro et al. (2023) demonstrated that indigenous AMF-colonized plants exhibited higher levels of HM accumulation compared to non-indigenous AMF-colonized plants [18]. Therefore, some AMF genera screened from contaminated areas may be highly tolerant to HMs.
Among the studies utilizing AMF for the remediation of soil contaminated with HMs, most attention has been on Zn, Cd, Cu, and Pb. A study by Cabral et al. (2010) reported that the retention of several genera of AMF showed the order of Cu > Zn > Cd > Pb and that soil trace elements, such as Cu and Zn, were retained in AMF tissues at a rapid rate [28]. The inoculation of AMF into plants grown in HM-contaminated areas was able to increase the length of the root system of the host plant and significantly improve the contact area of the plant with the contaminated soil [29]. AMF-colonized plants showed higher root HM content and lower HM content in shoots and fruits compared to non-mycorrhizal plants [14]. These findings demonstrate that AMF in soil contaminated with HMs can reduce HM concentrations and protect plants from HM toxicity.

3.2. Soil Contaminated with Organic Pollutants

AMF lack the enzymes to directly break down organic matter, but their colonization in contaminated soil is significantly higher than in uncontaminated soil [30]. In most of the organically contaminated sites where AMF are present, AMF promote the growth and development of host plants to enhance the uptake of organic pollutants while mitigating the hazards of pollution toxicity [31]. Additionally, AMF stimulate the exudation of plant root secretions, enhancing the uptake and degradation of pollutants by microorganisms, such as glomalin [32]. Overall, AMF play an important role in promoting the degradation and removal of organic pollutants from contaminated soil.

3.2.1. Petroleum Hydrocarbons (PHCs) and Polycyclic Aromatic Hydrocarbons (PAHs)

Industrial activities have led to PHCs being a kind of common organic pollutant in soil [32]. PHCs enter the ecosystem through leaking underground storage tanks, oil spills, transportation processes, and industrial activities. The extensive contamination of soil by PHCs makes it extremely hydrophobic and infertile, ultimately resulting in a reduction in plant and microbial biomass [33]. The total petroleum hydrocarbon (TPH) concentration influences the AMF community structure, which, in turn, may impact bacteria and fungi associated with AMF spores [34]. However, AMF could be identified in plant roots or inter-plant root soil even when there was a high level of TPH contamination. The contamination levels were as high as 91,000 µg TPH/kg of soil, equivalent to 9.1% (w/w) of the TPH content in the soil [35]. This suggests that certain AMF species that are tolerant to high concentrations of TPH may exist in areas that are naturally contaminated with TPH. To enhance the efficiency of TPH degradation, Alarcón et al. (2008) inoculated AMF with a blend of petroleum-degrading microorganisms and found that the degradation efficiency increased in the rhizosphere layer significantly [36].
TPH contains aliphatic and aromatic compounds. Among the aromatic compounds, PAHs are considered risky due to their toxicity, mutagenicity, and carcinogenic properties. PAHs are produced from various sources such as transportation emissions, residential gas, and industrial production. These PAHs are widespread due to their diverse sources and semi-volatility, making them ubiquitous [37]. Plant growth and PAH uptake, along with inter-root soil bioactivity induced by the AMF–plant symbiotic system, significantly reduced the residual amount of PAHs in soil [38]. AMF colonization was able to increase the PAH concentration in host plant root and aboveground parts by more than 50% in PAH-contaminated soil [39].

3.2.2. Polychlorinated Biphenyls (PCBs)

In 2004, the Stockholm Convention identified PCBs as one of the 26 persistent organic pollutants (POPs) that needed to be reduced globally [40]. Over 90 countries have since committed to eliminating and disposing of large quantities of PCBs. However, PCBs remain a significant threat to ecosystems due to their persistence in the environment and slow decomposition. Qin et al. (2016) discovered that AMF hyphae could speed up the dissipation of PCB congeners in soil, and there was a significant correlation between the hyphal length of AMF and the rate of PCB dissipation [41]. Before this study, other research studies used AMF in combination with other helpful organisms to treat PCB-contaminated soil. Lu et al. (2014) found that earthworms and AMF colonization not only increased the biomass production of the host plant but also resulted in the accumulation of PCBs in the plant [42]. Combined application of AMF with beneficial bacteria yields more significant results. Alfalfa shoots inoculated with both AMF and rhizobium accumulated higher concentrations of PCBs than those inoculated with only rhizobium [43]. These studies all suggest that the main reason for the reduction in PCB concentration in soil is the microbiota benefiting from the mycorrhizal binding process. This speculation was confirmed by Qin et al. (2014): inoculation with AMF increased the proportion of Alphaproteo bacteria in the rhizosphere and significantly correlated with the dissipation rate of PCBs in soil [44].
In recent years, novel materials have been employed to break down PCBs in soil. Nanoscale zero-valent iron (nZVI) is highly effective in degrading PCBs in soil but may pose a threat to plants when used in conjunction with phytoremediation [45,46,47]. This will undoubtedly limit the efficiency of nZVI for PCB degradation. Fortunately, AMF can alleviate nZVI-induced toxicity in plants [48]. But a high concentration (10 g/kg) of nZVI in soil inhibits AMF diversity. However, this restriction does not work in the medium-concentration (1 g/kg) soil but rather promotes the remediation of PCB-contaminated soil [49]. This suggests that the co-application of AMF with nanomaterials shows great potential for application in PCB-contaminated soil remediation.

3.2.3. Antibiotics

Animal husbandry, agriculture, and aquaculture are the primary sources of antibiotics found in soil [50]. A significant amount of antibiotics cannot be metabolized by animals and are released into nature through animal manure fertilization and wastewater [51]. Antibiotics are present in soil at concentrations ranging from 0.7 µg/kg to 5 g/kg [52]. The adsorption of antibiotics to soil increases their persistence in the environment, which, in turn, can lead to antibiotic resistance [53]. The addition of AMF increased soil enzyme activities and AMF released secretions containing assimilates into the rhizosphere of the host plant, which led to an increase in soil microbial biomass [54]. Glomalin, which is a mycelial secretion produced by AMF, may stimulate the increase in microflora with oxytetracycline (OTC) degradation capacity [55]. Furthermore, AMF have the ability to enhance the removal efficiency of soil OTC by promoting host plant growth and development through improving the soil nitrogen content [56].

4. AMF-Assisted Phytoremediation of Contaminated Water

In both natural wetlands and constructed wetlands, microorganisms play a crucial role in maintaining the ecosystem’s health [57]. However, excess water may negatively affect AMF, as these microorganisms are sensitive to a lack of oxygen [58]. The discovery of AMF in some wetlands has provided new idea for the remediation of polluted waters [59].
Earlier research has demonstrated that there is a high presence of AMF in ecological floating beds (EFBs) that are perpetually flooded despite the absence of any external introduction of these fungi [60]. This indicates that using AMF in water treatment systems that rely on plant-based processes could be highly beneficial. However, the actual advantages of these AMF communities are not yet fully understood. Several studies have applied AMF-assisted phytoremediation in various human-intervened water treatment systems, such as constructed wetland (CW), EFBs, and stormwater filters, confirming earlier speculations (Table 1). In such installations, AMF have been used to increase the pollutant extraction efficiency of plants, resulting in an overall improvement of the system’s pollutant removal capability [61]. To improve AMF colonization in aquatic habitats, researchers have been exploring various inoculation methods. In some studies, AMF–plant symbiosis systems pre-cultivated in pots were transplanted into water treatment systems [62,63]. In most of the remaining studies, the AMF inoculum was either spread on the surface or middle layer of the substrate of the water treatment system or mixed with it [64,65,66,67]. HMs and nutrients are the most commonly treated contaminants using AMF in water treatment systems. Furthermore, AMF have also been utilized in the treatment of emerging contaminants in contaminated water.

5. Direct Influence of AMF on Pollutant Removal

5.1. Binding and Stabilization of Pollutants by Glomalin

Glomalin-related soil protein (GRSP) is a glycoprotein produced by AMF spores and mycelial walls [74]. It can remain in the soil for up to 42 years and has the potential to maintain soil health with long-term sustainability [75]. GRSP is considered one of the key mechanisms for AMF-assisted phytoremediation of contaminated soil. Studies on rhizosphere and non-rhizosphere soil of mycorrhizal plants in Cu-contaminated ecosystems have found that GRSP-Cu is one of the main forms of “immobilized” Cu in contaminated soil [76,77]. In contaminated soil, GRSP binds to HMs mainly through functional groups such as carboxyl (-COO-), hydroxyl (-OH), carbonyl (-C=O), and amide (-CO-NH) to reduce the toxicity and bioavailability of HMs [78]. This binding effect enables GRSP to be released in rhizosphere soil to aggregate HMs in the roots, inhibiting their transfer into the aerial parts and reducing damage [79].
Soil aggregates have a large surface area and many adsorption sites, making them highly enriched for most HMs [80]. GRSP plays an important role in forming soil macroaggregates. Li et al. (2022b) found that in soil contaminated with Pb, the content of GRSP is significantly and positively correlated with the stability of soil aggregates [81]. Soil aggregation and structural stability can affect soil organic carbon (SOC) sequestration. Long-term HM contamination can increase Basidiomycete, which promotes carbon degradation, and decrease Proteobacteria, which promotes carbon fixation. This leads to SOC loss, affecting SOC storage [82]. At a HM-contaminated site, it was found that GRSP carbon contributed 89% of the total SOC, suggesting the potential of GRSP to sequester SOC under extreme stress [83]. In addition, GRSP can also serve as an additional carbon source and catabolic substrate for microorganisms, which improves microbial catabolic function by promoting the release of extracellular enzymes [84] (Figure 3).

5.2. Pollutant Retention inside Fungal Structure

The most significant aspect of AMF is their mycelium network which spreads beyond the root and is present everywhere, increasing the ground contact area between the plant root system and contaminated soil. The AMF mycelium can store HMs at 10–20 times more than the plant root [85]. It overcomes one of the significant limitations of phytoremediation [32]. In mycorrhizal plants, AMF colonization of plant roots is limited to epidermal and cortical tissues [86]. Wu et al. (2016) used synchrotron radiation micro-X-Ray Fluorescence (SR-μXRF) to observe the exposure of dandelion (Taraxacum platypecidum) to Cr and showed that AMF colonization inhibited the transport of Cr from roots to shoots [87]. Moreover, Cr was present in both the cortex and vascular bundles in the main roots, which was not colonized by AMF, while Cr was detected only in the cortex of mycorrhizal main roots [88]. This confirms the ability of AMF colonization to prevent the transfer of HMs to plant transport tissues and avoid damage to the photosynthetic apparatus (Figure 4). HMs are transported through extraradical mycelium, and in mycorrhizal plants, metal ions mainly accumulate in the fungal structures within the root’s cortical cells [89]. Alvarado-López et al. (2019) discovered that Pb treatment was capable of inducing AMF colonization within the roots of carrots (Daucus carota), resulting in a greater percentage increase in the number of vesicles and mycelium [90]. The adsorption and filtration effects within intraradical mycelium can limit the movement of HM ions into plant roots’ cytoplasm [91]. Meanwhile, AMF vesicles can accumulate a large amount of HMs when subjected to HM stress [92]. Salazar et al. (2018) observed AMF spores in Pb-contaminated soil using micro-X-ray Fluorescence (μXRF) and found that AMF spores functioned in a similar way to vesicles and had an accumulative effect on Pb [93].
The process of HM immobilization in AMF fungal structures is accompanied by the occurrence of complexation reactions, which are essential for reducing damage to mycorrhizal plants. Wu et al. (2016) found that fungal structures and fungal cell walls within mycorrhizal roots were able to provide a site for the reduction of Cr (VI) to Cr (III), and complexation via carboxylate (-COOH) ligands or histidine analogues of Cr (III), thereby inhibiting the transfer of Cr to the plant root cytoplasm [87]. Thus, the retention of HMs by mycorrhizal plants increased with increasing concentrations in the soil, and the formation of arbuscules and vesicles increased. HMs are immobilized in fungal hyphae associated with mycorrhizal plants, which retains HM ions in spores, vesicles, and arbuscules through mycelium transport, and prevents the transfer of HMs to the plant cytoplasm through complexation reactions. This is one of the tolerance strategies through which AMF are directly involved in providing a physical barrier to prevent HMs from entering the plant.

5.3. Trophic Interaction between AMF and Host Plant

Previous research has shown that communities of AMF can allocate more nutrients to plant roots than to the surrounding soil and minimize the damage to plants caused by external disturbances [94]. These fungi are specialized symbionts that use host plants as their sole source of carbon, relying on plant fatty acids to complete their asexual life cycle [95]. They are estimated to receive 4–20% of the total carbon fixed through photosynthesis. In return, AMF provide plants with nitrogen (N), phosphorus (P), and other nutrients, which are usually more difficult to obtain in contaminated soil [32]. The study by Huang et al. (2020) has shown that the supply of P is more crucial than that of N in restoring plant communities in soil contaminated with HMs [96]. In the plant cell, P is a key element for several physiological and biochemical functions. Improving P uptake through AMF is an important mechanism that can benefit mycorrhizal plants that are growing in soil with high concentrations of HMs [97]. AMF promote P uptake in plants by increasing P acquisition by the mycelial network, promoting P mobility in soil, and increasing the activities of P and phytase enzymes [98]. The acquisition of inorganic P at the mycorrhizal symbiotic interface accounted for 70–100% of the plant’s total pi acquisition [99,100]. You et al. (2022) found that the efficiency of AMF in assisting plants to remediate soil contaminated with Cd was affected by the concentration of P [101]. The addition of P allowed AMF to induce the entry of Cd through the Fe uptake pathway, which facilitated the uptake of Cd by the plants. Changes in the level of phosphorus led to the diversification of the mechanisms through which AMF regulated Cd uptake.

6. The Role of AMF in Host Plant’s Tolerance Strategy

6.1. The Role of AMF in Host Plant’s Tolerance Strategy

Plants’ tolerance to HMs and their detoxification mechanisms are related to the subcellular distribution of HMs and their chemical forms [102]. A significant portion of cellular HMs are sequestered in the vacuoles of cortical cells, which can be in the form of free ions or bound to specific molecules like phytochelatins (PCs). Upon exposure to HMs, PCs are synthesized in plants using glutathione (GSH) as a precursor. The HM-PC complex is then transported into a vesicle via the ATP-Binding Cassette (ABC) transporter [103]. This process of sequestration is also present in the cell wall. AMF colonization increases the amount of cell wall polysaccharides (e.g., hemicellulose and pectin), which help to bind HMs to the host plant’s cell wall [104]. Han et al. (2021) found that AMF-colonized ryegrass sequesters more Cd in the root cell wall and vesicles under Cd stress compared to other organelles [105]. This sequestration effect is seen more prominently with elevated Cd concentrations. Gao et al. (2021) reported similar findings, showing that Cd is captured by the cell wall and primarily stored in hemicellulose and pectin components [106].
The biological functions of HMs are closely related to their chemical forms [107]. Different chemical forms of Cd have varying degrees of toxicity. Colonization by AMF can convert HMs into forms that are less toxic and inactive to plants. Zhang et al. (2019) confirmed that inoculation with AMF significantly reduced the proportion of inorganic and water-soluble forms of Cd (which cause the greatest Cd stress to plants) in the shoot and root of maize (Zea mays) [108], while it increased the proportion of pectate acid and protein-bound insoluble phosphate forms of Cd. Similar results were reported in [109].

6.2. AMF Response to Host Plant’s Antioxidant Defense

One of the ways pollutants affect plants is by directly or indirectly producing an excess of reactive oxygen species (ROS) [110]. A high level of ROS can impact the redox state of plant cells and cause oxidative damages [111]. Plants develop both enzymatic and non-enzymatic antioxidant defense mechanisms to eliminate excess ROS and ensure their survival [112]. When excess pollutants are transported to the photosynthetic organs of mycorrhizal plants, AMF promote the activities of antioxidant enzymes such as superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), ascorbate peroxidase (APX), glutathione peroxidase (GPX), and glutathione S-transferase (GST), which protect plants from the damage caused by these pollutants [113,114,115]. On the other hand, regulation of the ascorbate–glutathione (ASA-GSH) cycle in the cytoplasm and chloroplasts by AMF enhances plant tolerance to HM stress, which resists oxidative stress and scavenges reactive oxygen radicals to maintain normal photosynthesis [116] (Figure 5).
Plants that are exposed to abiotic stress often produce toxic aldehydes, such as methylglyoxal (MG). The glyoxalase system, which consists of glyoxalase I (Gly I) and glyoxalase II (Gly II) in combination with GSH, is responsible for the detoxification of MG [117]. Li et al. (2022a) found that AMF can alleviate the negative effects of Cd stress on wheat by speeding up the ASA-GSH cycle [118]. AMF increase the activity of APX, which reduces the production of ROS and oxidative damage by promoting the production of GSH and metallothioneins (MTs) and by breaking down MG. The increased production of GSH and MTs helps in trapping and immobilizing Cd, hence reducing its toxicity [119].

6.3. AMF Regulate Gene Expression Resistance to Pollutant Stress

AMF indirectly affect the tolerance strategies of host plants in two ways, as described above. These processes are successful due to changes in the expression of various transcribed genes involved in the host plant’s antioxidant defense system, transporter activity, and cell wall biosynthesis.
Antioxidant enzymes play a crucial role in removing harmful ROS in living organisms [120]. Ban et al. (2023) found that under stress from CuO-NPs, AMF can up-regulate the expression of six genes that encode GST and three genes that encode POD in plants [68]. This suggests that AMF can help plants detoxify ROS and protect them against oxidative damage. Similarly, Wang et al. (2022) reported that AMF colonization increased the expression of genes that encode antioxidant enzymes, including MtSOD, MtPODp7, and MtCAT4, in Medicago truncatula leaves under Cd stress [121]. This led to an increase in ROS scavenging and a decrease in oxidative damage caused by Cd exposure.
ABC transporters are a class of transmembrane transport proteins commonly found in prokaryotes and eukaryotes, which have been shown to transport As, Cd, and Hg [122]. In plants, ABC transporter proteins are present in the membranes of chloroplasts, mitochondria, peroxisomes, and vesicles. They play vital roles in maintaining cellular osmotic homeostasis, toxin enrichment and efflux, and stomatal motility in response to different types of stress [123]. The genes encoding the ABC transporter family were significantly down-regulated when the accumulation of Cd in the root system of AMF-colonized plants reached the triggering threshold of homeostasis [124]. This strategy can help enhance tolerance and establish good growth under Cd stress via the symbiotic relationship between AMF and plants. The extraradical mycelium of AMF can increase the scope for soil foraging and Pi (phosphate) uptake by extending beyond the Pi depletion zone. Molecular analyses have confirmed that specific members of plants’ PHT1 Pi transporter family play a role in this Pi uptake pathway [125]. The P transporter gene MtPT4 of M.truncatula is localized in the periplasm of tufts and is considered to be a marker of symbiotic function. MtPT4 encodes phosphate transporter proteins involved in the transfer of Pi from AMF to the plant as required [126]. Watts-Williams et al. (2017) reported that as the Zn concentration in the soil increased, AMF induced an increase in the expression of the P transporter gene MtPT4 [127]. This allowed the maintenance of AMF colonization while increasing the Zn concentration in plant biomass and decreasing it in tissue. Li et al. (2018) reported similar results for Medicago sativa under As stress. AMF up-regulated the gene MsPT4, thus improving plant phosphorus levels [128].
Maintaining the stability of cell membranes and cell walls is a key strategy used by plants to cope with abiotic stress [129]. Phosphatidylcholine is responsible for maintaining the integrity of cell membranes in higher plants and plays a significant role in helping plants adapt to environmental stresses [130]. Cui et al. (2022) demonstrated that genes encoding phospho-base N-methyltransferase 3 (PMT3) catalyses, which are responsible for synthesizing phosphatidylcholine, were significantly up-regulated in AMF-colonized Suaeda salsa plants when subjected to the combined stress of Cd and salt [131]. Furthermore, the cell wall serves as the first line of defense against various adverse abiotic and biotic environmental influences. AMF colonization significantly enhances the expression of genes involved in the synthesis of cell wall organization when subjected to abiotic stress [132]. Zhang et al. (2021) reported that AMF colonization caused Pb-stressed plants to increase the transcription of MtPrx05 and MtPrx10 in the root system by 65% and 148%, respectively [133]. These two genes were hypothesized to be involved in polysaccharide cross-linking and cell wall hardening.

7. Conclusions and Perspectives

Over the past 23 years, breakthroughs have been made in studies on AMF-associated phytoremediation. Studies showed that AMF could establish symbiotic relationships with a wide range of plant species and effectively remediate contaminated soil and water. When exposed to pollution, AMF secrete GRSP, retain pollutants inside their fungal structure, and enhance the plant biomass for the removal of pollutants. Furthermore, AMF promote the immobilization of pollutants in a non-toxic form in the root subcellular structures, respond to the plant defense system, and regulate several functional protein genes to protect plants from pollutant toxicity. However, the practical applications of AMF still need to overcome some serious challenges. Future research may focus on the following areas:
  • The lack of oxygen in water and sediment is one of the factors that limit the effectiveness of AMF. To overcome this, it is important to study and identify AMF strains that can adapt to anaerobic environments and have a wide range of applications. Additionally, it is essential to optimize the combination of AMF strains with plant species to maximize the efficiency of remediation.
  • Pollution can affect the community structure of AMF applied to contaminated sites. Only a few AMF species with resistance to pollutant stress can survive in highly polluted areas, which can diminish the expected remediation effect. Future studies focusing on screening and isolating bacterial species that closely interact with AMF in highly polluted environments and understanding the interactions between them should be conducted. Developing strategies that utilize AMF and microbial communities, which interact with AMF, rather than inoculation with AMF alone, is essential for the remediation of contaminated soil and water.
  • Existing research has focused on the remediation of a single type of pollution via AMF–plant symbiosis, while the interactions between different types of pollutants have been neglected. Remediation of composite polluted media with HMs and organic compounds should be emphasized in the future. To address the above challenges, medium-scale remediation trials of actual pollution and site construction should be conducted to accelerate the transition of AMF–plant symbiosis system remediation technology from simulation trials to practical applications.

Author Contributions

Conceptualization, X.Z., Y.L. and S.C.; methodology, software, validation, and formal analysis, X.Z., S.Q. and Z.W.; writing—original draft preparation, X.Z., Z.W. and Y.L.; writing—review and editing, J.W., B.W. and S.C.; supervision, S.C.; funding acquisition, J.W., B.W. and S.C. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by grants from the National Key Research and Development Program of China (2023YFC3207503) and the National Natural Science Foundation of China (No. 52170168).

Conflicts of Interest

Authors Y.L., S.Q., and J.W. were employed by the company Power China Huadong Engineering Corporation Limited. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

  1. Chakraborty, S.; Qamruzzaman, M.; Zaman, M.; Alam, M.; Hossain, D.; Pramanik, B.; Nguyen, L.; Nghiem, L.; Zhou, J.; Mondal, I.; et al. Metals in e-waste: Occurrence, fate, impacts and remediation technologies. Process. Saf. Environ. Prot. 2022, 162, 230–252. [Google Scholar] [CrossRef]
  2. Verma, S.; Bhatt, P.; Verma, A.; Mudila, H.; Prasher, P.; Rene, E.R. Microbial technologies for heavy metal remediation: Effect of process conditions and current practices. Clean Technol. Environ. Policy 2021, 25, 1485–1507. [Google Scholar] [CrossRef]
  3. Maurin, N.; Sayen, S.; Guillon, E. Gas chromatography–mass spectrometry analysis of organic pollutants in French soils irrigated with agro-industrial wastewater. Front. Environ. Sci. 2023, 11, 1125487. [Google Scholar] [CrossRef]
  4. Khorasani, H.; Xu, J.; Nguyen, T.; Kralles, Z.; Westerhoff, P.; Dai, N.; Zhu, Z. Contribution of wastewater- versus non-wastewater-derived sources to haloacetonitriles formation potential in a wastewater-impacted river. Sci. Total Environ. 2021, 792, 148355. [Google Scholar] [CrossRef]
  5. He, X.; Song, S.; Huang, Y.; Huang, X.; Huang, H.; Zhang, T.; Sun, H. Contamination of neonicotinoid insecticides in source water and their fate during drinking water treatment in the Dongguan section of the Pearl River. Sci. Total Environ. 2023, 901, 165935. [Google Scholar] [CrossRef]
  6. He, J.; Strezov, V.; Kumar, R.; Weldekidan, H.; Jahan, S.; Dastjerdi, B.H.; Zhou, X.; Kan, T. Pyrolysis of heavy metal contaminated Avicennia marina biomass from phytoremediation: Characterisation of biomass and pyrolysis products. J. Clean. Prod. 2019, 234, 1235–1245. [Google Scholar] [CrossRef]
  7. Tarla, D.N.; Erickson, L.E.; Hettiarachchi, G.M.; Amadi, S.I.; Galkaduwa, M.; Davis, L.C.; Nurzhanova, A.; Pidlisnyuk, V. Phytoremediation and Bioremediation of Pesticide-Contaminated Soil. Appl. Sci. 2020, 10, 1217. [Google Scholar] [CrossRef]
  8. Jamil, F.; Mukhtar, H.; Fouillaud, M.; Dufossé, L. Rhizosphere Signaling: Insights into Plant–Rhizomicrobiome Interactions for Sustainable Agronomy. Microorganisms 2022, 10, 899. [Google Scholar] [CrossRef]
  9. Srivastava, S.; Shukla, A.; Rajput, V.D.; Kumar, K.; Minkina, T.; Mandzhieva, S.; Shmaraeva, A.; Suprasanna, P. Arsenic Remediation through Sustainable Phytoremediation Approaches. Minerals 2021, 11, 936. [Google Scholar] [CrossRef]
  10. Jajoo, A.; Mathur, S. Role of arbuscular mycorrhizal fungi as an underground saviuor for protecting plants from abiotic stresses. Physiol. Mol. Biol. Plants 2021, 27, 2589–2603. [Google Scholar] [CrossRef]
  11. Lanfranco, L.; Bonfante, P.; Genre, A. The Mutualistic Interaction between Plants and Arbuscular Mycorrhizal Fungi. Microbiol. Spectr. 2016, 4, 727–747. [Google Scholar] [CrossRef]
  12. Roth, R.; Paszkowski, U. Plant carbon nourishment of arbuscular mycorrhizal fungi. Curr. Opin. Plant Biol. 2017, 39, 50–56. [Google Scholar] [CrossRef]
  13. Liu, J.; Chen, J.; Xie, K.; Tian, Y.; Yan, A.; Liu, J.; Huang, Y.; Wang, S.; Zhu, Y.; Chen, A.; et al. A mycorrhiza-specific H+-ATPase is essential for arbuscule development and symbiotic phosphate and nitrogen uptake. Plant Cell Environ. 2020, 43, 1069–1083. [Google Scholar] [CrossRef]
  14. Adeyemi, N.O.; Atayese, M.O.; Sakariyawo, O.S.; Azeez, J.O.; Olubode, A.; Ridwan, M.; Adebayo, R.; Adeoye, S. A Growth and Phosphorus Uptake of Soybean (Glycine max L.) in Response to Arbuscular Mycorrhizal Fungus Rhizophagus Intraradices Inoculation in Heavy Metal-contaminated Soils. Soil Sediment Contam. Int. J. 2021, 30, 1–16. [Google Scholar] [CrossRef]
  15. Diagne, N.; Ngom, M.; Djighaly, P.I.; Fall, D.; Hocher, V.; Svistoonoff, S. Roles of Arbuscular Mycorrhizal Fungi on Plant Growth and Performance: Importance in Biotic and Abiotic Stressed Regulation. Diversity 2020, 12, 370. [Google Scholar] [CrossRef]
  16. Tiwari, J.; Ma, Y.; Bauddh, K. Arbuscular mycorrhizal fungi: An ecological accelerator of phytoremediation of metal contaminated soils. Arch. Agron. Soil Sci. 2020, 68, 283–296. [Google Scholar] [CrossRef]
  17. Faggioli, V.; Menoyo, E.; Geml, J.; Kemppainen, M.; Pardo, A.; Salazar, M.J.; Becerra, A.G. Soil lead pollution modifies the structure of arbuscular mycorrhizal fungal communities. Mycorrhiza 2019, 29, 363–373. [Google Scholar] [CrossRef]
  18. Silva-Castro, G.A.; Cano, C.; Moreno-Morillas, S.; Bago, A.; García-Romera, I. Inoculation of Indigenous Arbuscular Mycorrhizal Fungi as a Strategy for the Recovery of Long-Term Heavy Metal-Contaminated Soils in a Mine-Spill Area. J. Fungi 2022, 9, 56. [Google Scholar] [CrossRef]
  19. Cabral, L.; Soares, C.R.F.S.; Giachini, A.J.; Siqueira, J.O. Arbuscular mycorrhizal fungi in phytoremediation of contaminated areas by trace elements: Mechanisms and major benefits of their applications. World J. Microbiol. Biotechnol. 2015, 31, 1655–1664. [Google Scholar] [CrossRef]
  20. Gou, X.; Ni, H.; Sadowsky, M.J.; Chang, X.; Liu, W.; Wei, X. Arbuscular mycorrhizal fungi alleviate erosion-induced soil nutrient losses in experimental agro-ecosystems. CATENA 2023, 220, 106687. [Google Scholar] [CrossRef]
  21. Yin, L.; Dijkstra, F.A.; Phillips, R.P.; Zhu, B.; Wang, P.; Cheng, W. Arbuscular mycorrhizal trees cause a higher carbon to nitrogen ratio of soil organic matter decomposition via rhizosphere priming than ectomycorrhizal trees. Soil Biol. Biochem. 2021, 157, 108246. [Google Scholar] [CrossRef]
  22. Ghuge, S.A.; Nikalje, G.C.; Kadam, U.S.; Suprasanna, P.; Hong, J.C. Comprehensive mechanisms of heavy metal toxicity in plants, detoxification, and remediation. J. Hazard. Mater. 2023, 450, 131039. [Google Scholar] [CrossRef]
  23. Mwelwa, S.; Chungu, D.; Tailoka, F.; Beesigamukama, D.; Tanga, C. Biotransfer of heavy metals along the soil-plant-edible insect-human food chain in Africa. Sci. Total Environ. 2023, 881, 163150. [Google Scholar] [CrossRef]
  24. Wen, J.; Zhou, J.; Zhang, R.; Ren, W.; Zhao, J.; Cai, D. Current advances of the valorization technologies for heavy metal containing hyperaccumulators. Ind. Crop. Prod. 2024, 209, 118051. [Google Scholar] [CrossRef]
  25. Zhang, Y.; Zhao, S.; Liu, S.; Peng, J.; Zhang, H.; Zhao, Q.; Zheng, L.; Chen, Y.; Shen, Z.; Xu, X.; et al. Enhancing the Phytoremediation of Heavy Metals by Combining Hyperaccumulator and Heavy Metal-Resistant Plant Growth-Promoting Bacteria. Front. Plant Sci. 2022, 13, 912350. [Google Scholar] [CrossRef]
  26. Heggo, A.; Angle, J.; Chaney, R. Effects of vesicular-arbuscular mycorrhizal fungi on heavy metal uptake by soybeans. Soil Biol. Biochem. 1990, 22, 865–869. [Google Scholar] [CrossRef]
  27. Khan, A. Relationships between chromium biomagnification ratio, accumulation factor, and mycorrhizae in plants growing on tannery effluent-polluted soil. Environ. Int. 2001, 26, 417–423. [Google Scholar] [CrossRef]
  28. Cabral, L.; Siqueira, J.O.; Soares, C.R.F.S.; Pinto, J.E.B.P. Retenção de metais pesados em micélio de fungos micorrízicos arbusculares. Quim. Nova 2010, 33, 25–29. [Google Scholar] [CrossRef]
  29. Pedroso, D.d.F.; Barbosa, M.V.; dos Santos, J.V.; Pinto, F.A.; Siqueira, J.O.; Carneiro, M.A.C. Arbuscular Mycorrhizal Fungi Favor the Initial Growth of Acacia mangium, Sorghum bicolor, and Urochloa brizantha in Soil Contaminated with Zn, Cu, Pb, and Cd. Bull. Environ. Contam. Toxicol. 2018, 101, 386–391. [Google Scholar] [CrossRef]
  30. Dagher, D.J.; de la Providencia, I.E.; Pitre, F.E.; St-Arnaud, M.; Hijri, M. Arbuscular Mycorrhizal Fungal Assemblages Significantly Shifted upon Bacterial Inoculation in Non-Contaminated and Petroleum-Contaminated Environments. Microorganisms 2020, 8, 602. [Google Scholar] [CrossRef]
  31. Wang, F.; Adams, C.A.; Yang, W.; Sun, Y.; Shi, Z. Benefits of arbuscular mycorrhizal fungi in reducing organic contaminant residues in crops: Implications for cleaner agricultural production. Crit. Rev. Environ. Sci. Technol. 2019, 50, 1580–1612. [Google Scholar] [CrossRef]
  32. Rajtor, M.; Piotrowska-Seget, Z. Prospects for arbuscular mycorrhizal fungi (AMF) to assist in phytoremediation of soil hydrocarbon contaminants. Chemosphere 2016, 162, 105–116. [Google Scholar] [CrossRef] [PubMed]
  33. Hussain, I.; Puschenreiter, M.; Gerhard, S.; Schöftner, P.; Yousaf, S.; Wang, A.; Syed, J.H.; Reichenauer, T.G. Rhizoremediation of petroleum hydrocarbon-contaminated soils: Improvement opportunities and field applications. Environ. Exp. Bot. 2018, 147, 202–219. [Google Scholar] [CrossRef]
  34. Iffis, B.; St-Arnaud, M.; Hijri, M. Petroleum hydrocarbon contamination, plant identity and arbuscular mycorrhizal fungal (AMF) community determine assemblages of the AMF spore-associated microbes. Environ. Microbiol. 2016, 18, 2689–2704. [Google Scholar] [CrossRef] [PubMed]
  35. Lee, S.-J.; Kong, M.; St-Arnaud, M.; Hijri, M. Arbuscular Mycorrhizal Fungal Communities of Native Plant Species under High Petroleum Hydrocarbon Contamination Highlights Rhizophagus as a Key Tolerant Genus. Microorganisms 2020, 8, 872. [Google Scholar] [CrossRef] [PubMed]
  36. Alarcón, A.; Davies, F.T.; Autenrieth, R.L.; Zuberer, D.A. Arbuscular Mycorrhiza and Petroleum-Degrading Microorganisms Enhance Phytoremediation of Petroleum-Contaminated Soil. Int. J. Phytoremediat. 2008, 10, 251–263. [Google Scholar] [CrossRef] [PubMed]
  37. Ren, K.; Wei, Y.; Li, J.; Han, C.; Deng, Y.; Su, G. Polycyclic aromatic hydrocarbons (PAHs) and their derivatives (oxygenated PAHs, azaarenes, and sulfur/oxygen-containing heterocyclic PAHs) in surface soils from a typical city, south China. Chemosphere 2021, 283, 131190. [Google Scholar] [CrossRef] [PubMed]
  38. Gao, Y.; Cheng, Z.; Ling, W.; Huang, J. Arbuscular mycorrhizal fungal hyphae contribute to the uptake of polycyclic aromatic hydrocarbons by plant roots. Bioresource Technol. 2010, 101, 6895–6901. [Google Scholar] [CrossRef] [PubMed]
  39. Shi, Y.; Wang, S.; Guo, J.; Xu, Z.; Wang, S.; Sang, Y. Effects of arbuscular mycorrhizal inoculation on the phytoremediation of PAH-contaminated soil: A meta-analysis. Chemosphere 2022, 307, 136033. [Google Scholar] [CrossRef]
  40. Song, S.; Xue, J.; Lu, Y.; Zhang, H.; Wang, C.; Cao, X.; Li, Q. Are unintentionally produced polychlorinated biphenyls the main source of polychlorinated biphenyl occurrence in soils? Environ. Pollut. 2018, 243, 492–500. [Google Scholar] [CrossRef]
  41. Qin, H.; Brookes, P.C.; Xu, J. Arbuscular Mycorrhizal Fungal Hyphae Alter Soil Bacterial Community and Enhance Polychlorinated Biphenyls Dissipation. Front. Microbiol. 2016, 7, 939. [Google Scholar] [CrossRef]
  42. Lu, Y.-F.; Lu, M.; Peng, F.; Wan, Y.; Liao, M.-H. Remediation of polychlorinated biphenyl-contaminated soil by using a combination of ryegrass, arbuscular mycorrhizal fungi and earthworms. Chemosphere 2014, 106, 44–50. [Google Scholar] [CrossRef]
  43. Teng, Y.; Luo, Y.; Sun, X.; Tu, C.; Xu, L.; Liu, W.; Li, Z.; Christie, P. Influence of Arbuscular Mycorrhiza and Rhizobium on Phytoremediation by Alfalfa of an Agricultural Soil Contaminated with Weathered PCBs: A Field Study. Int. J. Phytoremediat. 2010, 12, 516–533. [Google Scholar] [CrossRef]
  44. Qin, H.; Brookes, P.C.; Xu, J.; Feng, Y. Bacterial degradation of Aroclor 1242 in the mycorrhizosphere soils of zucchini (Cucurbita pepo L.) inoculated with arbuscular mycorrhizal fungi. Environ. Sci. Pollut. Res. 2014, 21, 12790–12799. [Google Scholar] [CrossRef]
  45. Zand, A.D.; Tabrizi, A.M.; Heir, A.V. The influence of association of plant growth-promoting rhizobacteria and zero-valent iron nanoparticles on removal of antimony from soil by Trifolium repens. Environ. Sci. Pollut. Res. 2020, 27, 42815–42829. [Google Scholar] [CrossRef]
  46. Gil-Díaz, M.; Pérez, R.A.; Alonso, J.; Miguel, E.; Diez-Pascual, S.; Lobo, M.C. Iron nanoparticles to recover a co-contaminated soil with Cr and PCBs. Sci. Rep. 2022, 12, 3541. [Google Scholar] [CrossRef]
  47. Lou, Y.; Cai, Y.; Tong, Y.; Hsieh, L.; Li, X.; Xu, W.; Shi, K.; Shen, C.; Xu, X.; Lou, L. Interaction between pollutants during the removal of polychlorinated biphenyl-heavy metal combined pollution by modified nanoscale zero-valent iron. Sci. Total Environ. 2019, 673, 120–127. [Google Scholar] [CrossRef]
  48. Sun, D.; Hu, J.; Bai, J.; Qin, H.; Wang, J.; Wang, J.; Lin, X. Arbuscular mycorrhizal fungus facilitates ryegrass (Lolium perenne L.) growth and polychlorinated biphenyls degradation in a soil applied with nanoscale zero-valent iron. Ecotoxicol. Environ. Saf. 2021, 215, 112170. [Google Scholar] [CrossRef]
  49. Wen, S.; Sun, D.; Qin, H.; Wang, J.; Lin, X.; Bai, J.; Hu, J. Moderate input of nanoscale zero-valent iron accelerated soil polychlorinated biphenyls dissipation with limited inhibition on arbuscular mycorrhizal fungal diversity. J. Soils Sediments 2024, 24, 1139–1147. [Google Scholar] [CrossRef]
  50. Lee, J.H.; Park, K.S.; Jeon, J.H.; Lee, S.H. Antibiotic resistance in soil. Lancet Infect. Dis. 2018, 18, 1306–1307. [Google Scholar] [CrossRef]
  51. Wu, J.; Wang, J.; Li, Z.; Guo, S.; Li, K.; Xu, P.; Ok, Y.S.; Jones, D.L.; Zou, J. Antibiotics and antibiotic resistance genes in agricultural soils: A systematic analysis. Crit. Rev. Environ. Sci. Technol. 2022, 53, 847–864. [Google Scholar] [CrossRef]
  52. Thiele-Bruhn, S. Pharmaceutical antibiotic compounds in soils—A review. J. Plant Nutr. Soil Sci. 2003, 166, 145–167, Erratum in J. Plant Nutr. Soil Sci. 2003, 166, 546. [Google Scholar] [CrossRef]
  53. Wang, J.; Huang, R.; Liang, Y.; Long, X.; Wu, S.; Han, Z.; Liu, H.; Huangfu, X. Prediction of antibiotic sorption in soil with machine learning and analysis of global antibiotic resistance risk. J. Hazard. Mater. 2024, 466, 133563. [Google Scholar] [CrossRef]
  54. Cao, J.; Ji, D.; Wang, C. Interaction between earthworms and arbuscular mycorrhizal fungi on the degradation of oxytetracycline in soils. Soil Biol. Biochem. 2015, 90, 283–292. [Google Scholar] [CrossRef]
  55. Cao, J.; Wang, C.; Dou, Z.; Liu, M.; Ji, D. Hyphospheric impacts of earthworms and arbuscular mycorrhizal fungus on soil bacterial community to promote oxytetracycline degradation. J. Hazard. Mater. 2018, 341, 346–354. [Google Scholar] [CrossRef]
  56. Cao, J.; Wang, C.; Ji, D. Improvement of the soil nitrogen content and maize growth by earthworms and arbuscular mycorrhizal fungi in soils polluted by oxytetracycline. Sci. Total Environ. 2016, 571, 926–934. [Google Scholar] [CrossRef]
  57. Cao, Q.; Wang, H.; Chen, X.; Wang, R.; Liu, J. Composition and distribution of microbial communities in natural river wetlands and corresponding constructed wetlands. Ecol. Eng. 2017, 98, 40–48. [Google Scholar] [CrossRef]
  58. Jamiołkowska, A.; Księżniak, A.; Gałązka, A.; Hetman, B.; Kopacki, M.; Skwaryło-Bednarz, B. Impact of abiotic factors on development of the community of arbuscular mycorrhizal fungi in the soil: A Review. Int. Agrophys. 2018, 32, 133–140. [Google Scholar] [CrossRef]
  59. Fusconi, A.; Mucciarelli, M. How important is arbuscular mycorrhizal colonization in wetland and aquatic habitats? Environ. Exp. Bot. 2018, 155, 128–141. [Google Scholar] [CrossRef]
  60. Xu, Z.; Lv, Y.; Fang, M.; Liu, J.; Zeng, H.; Ban, Y. Diverse and abundant arbuscular mycorrhizal fungi in ecological floating beds used to treat eutrophic water. Appl. Microbiol. Biotechnol. 2021, 105, 6959–6975. [Google Scholar] [CrossRef]
  61. Xu, Z.; Ban, Y.; Jiang, Y.; Zhang, X.; Liu, X. Arbuscular Mycorrhizal Fungi in Wetland Habitats and Their Application in Constructed Wetland: A Review. Pedosphere 2016, 26, 592–617. [Google Scholar] [CrossRef]
  62. Ban, Y.; Xiao, Z.; Wu, C.; Lv, Y.; Meng, F.; Wang, J.; Xu, Z. The positive effects of inoculation using arbuscular mycorrhizal fungi and/or dark septate endophytes on the purification efficiency of CuO-nanoparticles-polluted wastewater in constructed wetland. J. Hazard. Mater. 2021, 416, 126095. [Google Scholar] [CrossRef]
  63. Xu, Z.; Zhao, Y.; Xu, Z.; Chen, X.; Zhang, X.; Chen, Z.; Ban, Y. Arbuscular mycorrhizal fungi enhanced the drinking water treatment residue-based vertical flow constructed wetlands on the purification of arsenic-containing wastewater. J. Hazard. Mater. 2024, 465, 133241. [Google Scholar] [CrossRef]
  64. Hu, B.; Hu, S.; Vymazal, J.; Chen, Z. Application of arbuscular mycorrhizal fungi for pharmaceuticals and personal care productions removal in constructed wetlands with different substrate. J. Clean. Prod. 2022, 339, 130760. [Google Scholar] [CrossRef]
  65. Zhouying, X.; Kaiguo, L.; Wenxuan, L.; Chen, W.; Xi, C.; Jun, H.; Xiangling, Z.; Yihui, B. The positive effects of arbuscular mycorrhizal fungi inoculation and/or additional aeration on the purification efficiency of combined heavy metals in vertical flow constructed wetlands. Environ. Sci. Pollut. Res. 2022, 29, 68950–68964. [Google Scholar]
  66. Xu, Z.; Huang, J.; Chu, Z.; Meng, F.; Liu, J.; Li, K.; Chen, X.; Jiang, Y.; Ban, Y. Plant and microbial communities responded to copper and/or tetracyclines in mycorrhizal enhanced vertical flow constructed wetlands microcosms with Canna indica L. J. Hazard. Mater. 2023, 451, 131114. [Google Scholar] [CrossRef]
  67. Hu, B.; Hu, S.; Chen, Z.; Vymazal, J. Employ of arbuscular mycorrhizal fungi for pharmaceuticals ibuprofen and diclofenac removal in mesocosm-scale constructed wetlands. J. Hazard. Mater. 2020, 409, 124524. [Google Scholar] [CrossRef]
  68. Ban, Y.; Tan, J.; Xiong, Y.; Mo, X.; Jiang, Y.; Xu, Z. Transcriptome analysis reveals the molecular mechanisms of Phragmites australis tolerance to CuO-nanoparticles and/or flood stress induced by arbuscular mycorrhizal fungi. J. Hazard. Mater. 2023, 442, 130118. [Google Scholar] [CrossRef]
  69. Jiang, Y.; Zhao, Y.; Liu, Y.; Ban, Y.; Li, K.; Li, X.; Zhang, X.; Xu, Z. Removal of sulfamethoxazole and Cu, Cd compound pollution by arbuscular mycorrhizal fungi enhanced vertical flow constructed wetlands. Environ. Res. 2024, 245, 117982. [Google Scholar] [CrossRef]
  70. Lv, Y.; Liu, J.; Fan, Z.; Fang, M.; Xu, Z.; Ban, Y. The function and community structure of arbuscular mycorrhizal fungi in ecological floating beds used for remediation of Pb contaminated wastewater. Sci. Total Environ. 2023, 872, 162233. [Google Scholar] [CrossRef]
  71. Gao, P.; Wang, X.; Sang, Y.; Wang, S.; Dai, D. AM fungi enhance the function of ecological floating bed in the treatment of saline industrial wastewater. Environ. Sci. Pollut. Res. 2020, 27, 16656–16667. [Google Scholar] [CrossRef]
  72. Palacios, Y.M.; Gleadow, R.; Davidson, C.; Gan, W.; Winfrey, B. Do mycorrhizae increase plant growth and pollutant removal in stormwater biofilters? Water Res. 2021, 202, 117381. [Google Scholar] [CrossRef]
  73. Calheiros, C.S.C.; Pereira, S.I.A.; Franco, A.R.; Castro, P.M.L. Diverse Arbuscular Mycorrhizal Fungi (AMF) Communities Colonize Plants Inhabiting a Constructed Wetland for Wastewater Treatment. Water 2019, 11, 1535. [Google Scholar] [CrossRef]
  74. Driver, J.D.; Holben, W.E.; Rillig, M.C. Characterization of glomalin as a hyphal wall component of arbuscular mycorrhizal fungi. Soil Biol. Biochem. 2005, 37, 101–106. [Google Scholar] [CrossRef]
  75. Singh, A.K.; Zhu, X.; Chen, C.; Wu, J.; Yang, B.; Zakari, S.; Jiang, X.J.; Singh, N.; Liu, W. The role of glomalin in mitigation of multiple soil degradation problems. Crit. Rev. Environ. Sci. Technol. 2020, 52, 1604–1638. [Google Scholar] [CrossRef]
  76. Cornejo, P.; Meier, S.; Borie, G.; Rillig, M.C.; Borie, F. Glomalin-related soil protein in a Mediterranean ecosystem affected by a copper smelter and its contribution to Cu and Zn sequestration. Sci. Total Environ. 2008, 406, 154–160. [Google Scholar] [CrossRef]
  77. Singh, P.K. In Vitro Cu-Sequestration by Glomalin from Acaulospora spinosa Walker and Trappe. Natl. Acad. Sci. Lett. 2014, 38, 183–185. [Google Scholar] [CrossRef]
  78. Wang, Q.; Lu, H.; Chen, J.; Jiang, Y.; Williams, M.A.; Wu, S.; Li, J.; Liu, J.; Yang, G.; Yan, C. Interactions of soil metals with glomalin-related soil protein as soil pollution bioindicators in mangrove wetland ecosystems. Sci. Total Environ. 2020, 709, 136051. [Google Scholar] [CrossRef]
  79. Jia, X.; Zhao, Y.; Liu, T.; Huang, S.; Chang, Y. Elevated CO2 increases glomalin-related soil protein (GRSP) in the rhizosphere of Robinia pseudoacacia L. seedlings in Pb- and Cd-contaminated soils. Environ. Pollut. 2016, 218, 349–357. [Google Scholar] [CrossRef]
  80. Fang, X.; Zhong, X.; Cui, Z.; Zhang, Y.; Du, L.; Yang, Y.; Lv, J. Distribution and Remediation Techniques of Heavy Metals in Soil Aggregates Perspective: A Review. Water Air Soil Pollut. 2023, 234, 631. [Google Scholar] [CrossRef]
  81. Li, Y.; Xu, J.; Hu, J.; Zhang, T.; Wu, X.; Yang, Y. Arbuscular Mycorrhizal Fungi and Glomalin Play a Crucial Role in Soil Aggregate Stability in Pb-Contaminated Soil. Int. J. Environ. Res. Public Health 2022, 19, 5029. [Google Scholar] [CrossRef]
  82. Xiao, Z.; Duan, C.; Li, S.; Chen, J.; Peng, C.; Che, R.; Liu, C.; Huang, Y.; Mei, R.; Xu, L.; et al. The microbial mechanisms by which long-term heavy metal contamination affects soil organic carbon levels. Chemosphere 2023, 340, 139770. [Google Scholar] [CrossRef]
  83. Gujre, N.; Agnihotri, R.; Rangan, L.; Sharma, M.P.; Mitra, S. Deciphering the dynamics of glomalin and heavy metals in soils contaminated with hazardous municipal solid wastes. J. Hazard. Mater. 2021, 416, 125869. [Google Scholar] [CrossRef]
  84. Singh, G.; Bhattacharyya, R.; Das, T.; Sharma, A.; Ghosh, A.; Das, S.; Jha, P. Crop rotation and residue management effects on soil enzyme activities, glomalin and aggregate stability under zero tillage in the Indo-Gangetic Plains. Soil Tillage Res. 2018, 184, 291–300. [Google Scholar] [CrossRef]
  85. Wang, L.; Wang, G.; Ma, F.; You, Y. Symbiosis between hyperaccumulators and arbuscular mycorrhizal fungi and their synergistic effect on the absorption and accumulation of heavy metals: A review. Sheng Wu Gong Cheng Xue Bao 2021, 37, 3604–3621. [Google Scholar] [CrossRef]
  86. Carotenuto, G.; Volpe, V.; Russo, G.; Politi, M.; Sciascia, I.; de Almeida-Engler, J.; Genre, A. Local endoreduplication as a feature of intracellular fungal accommodation in arbuscular mycorrhizas. New Phytol. 2019, 223, 430–446. [Google Scholar] [CrossRef]
  87. Wu, S.; Zhang, X.; Sun, Y.; Wu, Z.; Li, T.; Hu, Y.; Lv, J.; Li, G.; Zhang, Z.; Zhang, J.; et al. Chromium immobilization by extra- and intraradical fungal structures of arbuscular mycorrhizal symbioses. J. Hazard. Mater. 2016, 316, 34–42. [Google Scholar] [CrossRef]
  88. Wu, S.; Zhang, X.; Chen, B.; Wu, Z.; Li, T.; Hu, Y.; Sun, Y.; Wang, Y. Chromium immobilization by extraradical mycelium of arbuscular mycorrhiza contributes to plant chromium tolerance. Environ. Exp. Bot. 2016, 122, 10–18. [Google Scholar] [CrossRef]
  89. Sujkowska-Rybkowska, M.; Lisek, A.; Sumorok, B.; Derkowska, E.; Szymańska, M.; Sas-Paszt, L. Arbuscular Mycorrhizal Fungi as an Important Factor Enabling the Adaptation of Anthyllis vulneraria L. to Zn-Pb-Polluted Tailings. Plants 2023, 12, 2092. [Google Scholar] [CrossRef]
  90. Alvarado-López, C.J.; Dasgupta-Schubert, N.; Ambriz, J.E.; Arteaga-Velazquez, J.C.; Villegas, J.A. Lead uptake by the symbiotic Daucus carota L.–Glomus intraradices system and its effect on the morphology of extra- and intraradical fungal microstructures. Environ. Sci. Pollut. Res. 2018, 26, 381–391. [Google Scholar] [CrossRef] [PubMed]
  91. Zhou, X.; Fu, L.; Xia, Y.; Zheng, L.; Chen, C.; Shen, Z.; Chen, Y. Correction: Arbuscular mycorrhizal fungi enhance the copper tolerance of Tagetes patula through the sorption and barrier mechanisms of intraradical hyphae. Metallomics 2017, 9, 989. [Google Scholar] [CrossRef]
  92. Dhalaria, R.; Kumar, D.; Kumar, H.; Nepovimova, E.; Kuča, K.; Islam, M.T.; Verma, R. Arbuscular Mycorrhizal Fungi as Potential Agents in Ameliorating Heavy Metal Stress in Plants. Agronomy 2020, 10, 815. [Google Scholar] [CrossRef]
  93. Salazar, M.J.; Menoyo, E.; Faggioli, V.; Geml, J.; Cabello, M.; Rodriguez, J.H.; Marro, N.; Pardo, A.; Pignata, M.L.; Becerra, A.G. Pb accumulation in spores of arbuscular mycorrhizal fungi. Sci. Total Environ. 2018, 643, 238–246. [Google Scholar] [CrossRef]
  94. Chagnon, P.-L.; Bradley, R.L.; Maherali, H.; Klironomos, J.N. A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci. 2013, 18, 484–491. [Google Scholar] [CrossRef]
  95. Rich, M.K.; Nouri, E.; Courty, P.-E.; Reinhardt, D. Diet of Arbuscular Mycorrhizal Fungi: Bread and Butter? Trends Plant Sci. 2017, 22, 652–660. [Google Scholar] [CrossRef]
  96. Huang, J.; Wang, C.; Qi, L.; Zhang, X.; Tang, G.; Li, L.; Guo, J.; Jia, Y.; Dou, X.; Lu, M. Phosphorus is more effective than nitrogen in restoring plant communities of heavy metals polluted soils. Environ. Pollut. 2020, 266, 115259. [Google Scholar] [CrossRef]
  97. Quan, L.; Zhang, J.; Wei, Q.; Wang, Y.; Qin, C.; Hu, F.; Chen, Y.; Shen, Z.; Xia, Y. Promotion of Zinc Tolerance, Acquisition and Translocation of Phosphorus in Mimosa pudica L. Mediated by Arbuscular Mycorrhizal Fungi. Bull. Environ. Contam. Toxicol. 2021, 106, 507–515. [Google Scholar] [CrossRef]
  98. Zhan, F.; Li, B.; Jiang, M.; Yue, X.; He, Y.; Xia, Y.; Wang, Y. Arbuscular mycorrhizal fungi enhance antioxidant defense in the leaves and the retention of heavy metals in the roots of maize. Environ. Sci. Pollut. Res. 2018, 25, 24338–24347. [Google Scholar] [CrossRef]
  99. Ivanov, S.; Austin, J.; Berg, R.H.; Harrison, M.J. Extensive membrane systems at the host–arbuscular mycorrhizal fungus interface. Nat. Plants 2019, 5, 194–203. [Google Scholar] [CrossRef]
  100. Yang, S.-Y.; Grønlund, M.; Jakobsen, I.; Grotemeyer, M.S.; Rentsch, D.; Miyao, A.; Hirochika, H.; Kumar, C.S.; Sundaresan, V.; Salamin, N.; et al. Nonredundant Regulation of Rice Arbuscular Mycorrhizal Symbiosis by Two Members of the PHOSPHATE TRANSPORTER1 Gene Family. Plant Cell 2012, 24, 4236–4251. [Google Scholar] [CrossRef]
  101. You, Y.; Ju, C.; Wang, L.; Wang, X.; Ma, F.; Wang, G.; Wang, Y. The mechanism of arbuscular mycorrhizal enhancing cadmium uptake in Phragmites australis depends on the phosphorus concentration. J. Hazard. Mater. 2022, 440, 129800. [Google Scholar] [CrossRef]
  102. Lam, C.-M.; Lai, H.-Y. Effect of inoculation with arbuscular mycorrhizal fungi and blanching on the bioaccessibility of heavy metals in water spinach (Ipomoea aquatica Forsk.). Ecotoxicol. Environ. Saf. 2018, 162, 563–570. [Google Scholar] [CrossRef]
  103. Sharma, S.S.; Dietz, K.-J.; Mimura, T. Vacuolar compartmentalization as indispensable component of heavy metal detoxification in plants: Vacuolar functions in HM detoxification. Plant Cell Environ. 2016, 39, 1112–1126. [Google Scholar] [CrossRef]
  104. Pan, J.; Cao, S.; Xu, G.; Rehman, M.; Li, X.; Luo, D.; Wang, C.; Fang, W.; Xiao, H.; Liao, C.; et al. Comprehensive analysis reveals the underlying mechanism of arbuscular mycorrhizal fungi in kenaf cadmium stress alleviation. Chemosphere 2023, 314, 137566. [Google Scholar] [CrossRef]
  105. Han, Y.; Zveushe, O.K.; Dong, F.; Ling, Q.; Chen, Y.; Sajid, S.; Zhou, L.; de Dios, V.R. Unraveling the effects of arbuscular mycorrhizal fungi on cadmium uptake and detoxification mechanisms in perennial ryegrass (Lolium perenne). Sci. Total Environ. 2021, 798, 149222. [Google Scholar] [CrossRef]
  106. Gao, M.Y.; Chen, X.W.; Huang, W.X.; Wu, L.; Yu, Z.S.; Xiang, L.; Mo, C.H.; Li, Y.W.; Cai, Q.Y.; Wong, M.H.; et al. Cell wall modification induced by an arbuscular mycorrhizal fungus enhanced cadmium fixation in rice root. J. Hazard. Mater. 2021, 416, 125894. [Google Scholar] [CrossRef]
  107. Park, J.; Chung, H.; Kim, S.H.; An, J.; Nam, K. Effect of neutralizing agents on the type of As co-precipitates formed by in situ Fe oxides synthesis and its impact on the bioaccessibility of As in soil. Sci. Total Environ. 2020, 743, 140686. [Google Scholar] [CrossRef]
  108. Zhang, X.-F.; Hu, Z.-H.; Yan, T.-X.; Lu, R.-R.; Peng, C.-L.; Li, S.-S.; Jing, Y.-X. Arbuscular mycorrhizal fungi alleviate Cd phytotoxicity by altering Cd subcellular distribution and chemical forms in Zea mays. Ecotoxicol. Environ. Saf. 2019, 171, 352–360. [Google Scholar] [CrossRef]
  109. Li, H.; Luo, N.; Zhang, L.J.; Zhao, H.M.; Li, Y.W.; Cai, Q.Y.; Wong, M.H.; Mo, C.H. Do arbuscular mycorrhizal fungi affect cadmium uptake kinetics, subcellular distribution and chemical forms in rice? Sci. Total Environ. 2016, 571, 1183–1190. [Google Scholar] [CrossRef]
  110. Mukherjee, A.; Agrawal, S.B.; Agrawal, M. Responses of tropical tree species to urban air pollutants: ROS/RNS formation and scavenging. Sci. Total Environ. 2019, 710, 136363. [Google Scholar] [CrossRef]
  111. Wu, B.; Qi, F.; Liang, Y. Fuels for ROS signaling in plant immunity. Trends Plant Sci. 2023, 28, 1124–1131. [Google Scholar] [CrossRef]
  112. Ahmad, P.; Jaleel, C.A.; Salem, M.A.; Nabi, G.; Sharma, S. Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Crit. Rev. Biotechnol. 2010, 30, 161–175. [Google Scholar] [CrossRef]
  113. Luo, J.; Li, X.; Jin, Y.; Traore, I.; Dong, L.; Yang, G.; Wang, Y. Effects of Arbuscular Mycorrhizal Fungi Glomus mosseae on the Growth and Medicinal Components of Dysosma versipellis Under Copper Stress. Bull. Environ. Contam. Toxicol. 2020, 107, 924–930. [Google Scholar] [CrossRef]
  114. Hu, S.; Hu, B.; Chen, Z.; Vosátka, M.; Vymazal, J. Antioxidant response in arbuscular mycorrhizal fungi inoculated wetland plant under Cr stress. Environ. Res. 2020, 191, 110203. [Google Scholar] [CrossRef]
  115. Lenoir, I.; Fontaine, J.; Tisserant, B.; Laruelle, F.; Sahraoui, A.L.-H. Beneficial contribution of the arbuscular mycorrhizal fungus, Rhizophagus irregularis, in the protection of Medicago truncatula roots against benzo[a]pyrene toxicity. Mycorrhiza 2017, 27, 465–476. [Google Scholar] [CrossRef]
  116. Tan, Z.; Xuan, Z.; Wu, C.; Cheng, Y.; Xu, C.; Ma, X.; Wang, D. Effects of Selenium on the AsA-GSH System and Photosynthesis of Pakchoi (Brassica chinensis L.) Under Lead Stress. J. Soil Sci. Plant Nutr. 2022, 22, 5111–5122. [Google Scholar] [CrossRef]
  117. Sharma, S.; Anand, G.; Singh, N.; Kapoor, R. Arbuscular Mycorrhiza Augments Arsenic Tolerance in Wheat (Triticum aestivum L.) by Strengthening Antioxidant Defense System and Thiol Metabolism. Front. Plant Sci. 2017, 8, 906. [Google Scholar] [CrossRef]
  118. Li, H.; Wang, H.; Zhao, J.; Zhang, L.; Li, Y.; Wang, H.; Teng, H.; Yuan, Z.; Yuan, Z. Physio-Biochemical and Transcriptomic Features of Arbuscular Mycorrhizal Fungi Relieving Cadmium Stress in Wheat. Antioxidants 2022, 11, 2390. [Google Scholar] [CrossRef]
  119. Aalipour, H.; Nikbakht, A.; Etemadi, N. Co-inoculation of Arizona cypress with arbuscular mycorrhiza fungi and Pseudomonas fluorescens under fuel pollution. Mycorrhiza 2019, 29, 277–289. [Google Scholar] [CrossRef]
  120. Pandey, A.; Wu, L.-B.; Murugaiyan, V.; Schaaf, G.; Ali, J.; Frei, M. Differential effects of arsenite and arsenate on rice (Oryza sativa) plants differing in glutathione S-transferase gene expression. Environ. Sci. Pollut. Res. 2023, 30, 92268–92281. [Google Scholar] [CrossRef]
  121. Wang, H.-R.; Zhao, X.-Y.; Zhang, J.-M.; Lu, C.; Feng, F.-J. Arbuscular mycorrhizal fungus regulates cadmium accumulation, migration, transport, and tolerance in Medicago sativa. J. Hazard. Mater. 2022, 435, 129077. [Google Scholar] [CrossRef] [PubMed]
  122. Yang, Z.; Yang, F.; Liu, J.-L.; Wu, H.-T.; Yang, H.; Shi, Y.; Liu, J.; Zhang, Y.-F.; Luo, Y.-R.; Chen, K.-M. Heavy metal transporters: Functional mechanisms, regulation, and application in phytoremediation. Sci. Total Environ. 2021, 809, 151099. [Google Scholar] [CrossRef] [PubMed]
  123. Guo, Z.; Yuan, X.; Li, L.; Zeng, M.; Yang, J.; Tang, H.; Duan, C. Genome-Wide Analysis of the ATP-Binding Cassette (ABC) Transporter Family in Zea mays L. and Its Response to Heavy Metal Stresses. Int. J. Mol. Sci. 2022, 23, 2109. [Google Scholar] [CrossRef] [PubMed]
  124. Sun, S.; Fan, X.; Feng, Y.; Wang, X.; Gao, H.; Song, F. Arbuscular mycorrhizal fungi influence the uptake of cadmium in industrial hemp (Cannabis sativa L.). Chemosphere 2023, 330, 138728. [Google Scholar] [CrossRef] [PubMed]
  125. Bucher, M. Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytol. 2006, 173, 11–26. [Google Scholar] [CrossRef] [PubMed]
  126. Sawers, R.J.H.; Svane, S.F.; Quan, C.; Grønlund, M.; Wozniak, B.; Gebreselassie, M.; González-Muñoz, E.; Montes, R.A.C.; Baxter, I.; Goudet, J.; et al. Phosphorus acquisition efficiency in arbuscular mycorrhizal maize is correlated with the abundance of root-external hyphae and the accumulation of transcripts encoding PHT1 phosphate transporters. New Phytol. 2017, 214, 632–643. [Google Scholar] [CrossRef] [PubMed]
  127. Watts-Williams, S.J.; Tyerman, S.D.; Cavagnaro, T.R. The dual benefit of arbuscular mycorrhizal fungi under soil zinc deficiency and toxicity: Linking plant physiology and gene expression. Plant Soil 2017, 420, 375–388. [Google Scholar] [CrossRef]
  128. Li, J.; Sun, Y.; Jiang, X.; Chen, B.; Zhang, X. Arbuscular mycorrhizal fungi alleviate arsenic toxicity to Medicago sativa by influencing arsenic speciation and partitioning. Ecotoxicol. Environ. Saf. 2018, 157, 235–243. [Google Scholar] [CrossRef] [PubMed]
  129. Tufail, A.; Li, H.; Naeem, A.; Li, T.X. Leaf cell membrane stability-based mechanisms of zinc nutrition in mitigating salinity stress in rice. Plant Biol. 2018, 20, 338–345. [Google Scholar] [CrossRef]
  130. Botella, C.; Jouhet, J.; A Block, M. Importance of phosphatidylcholine on the chloroplast surface. Prog. Lipid Res. 2016, 65, 12–23. [Google Scholar] [CrossRef]
  131. Cui, X.; Jia, B.; Diao, F.; Li, X.; Xu, J.; Zhang, Z.; Li, F.Y.; Guo, W. Transcriptomic analysis reveals the molecular mechanisms of arbuscular mycorrhizal fungi and nitrilotriacetic acid on Suaeda salsa tolerance to combined stress of cadmium and salt. Process. Saf. Environ. Prot. 2022, 160, 210–220. [Google Scholar] [CrossRef]
  132. Puccio, G.; Ingraffia, R.; Mercati, F.; Amato, G.; Giambalvo, D.; Martinelli, F.; Sunseri, F.; Frenda, A.S. Transcriptome changes induced by Arbuscular mycorrhizal symbiosis in leaves of durum wheat (Triticum durum Desf.) promote higher salt tolerance. Sci. Rep. 2023, 13, 116. [Google Scholar] [CrossRef] [PubMed]
  133. Zhang, X.; Hu, W.; Xie, X.; Wu, Y.; Liang, F.; Tang, M. Arbuscular mycorrhizal fungi promote lead immobilization by increasing the polysaccharide content within pectin and inducing cell wall peroxidase activity. Chemosphere 2021, 267, 128924. [Google Scholar] [CrossRef] [PubMed]
Microorganisms 12 01255 g001
Figure 1. (A) Annual total number and percentage of publications based on the WOS core collection database from 2000 to 2023. (B) Co-authorship analysis of authors with ≥5 publications. (C) Co-authorship clustering analysis of countries.
Figure 1. (A) Annual total number and percentage of publications based on the WOS core collection database from 2000 to 2023. (B) Co-authorship analysis of authors with ≥5 publications. (C) Co-authorship clustering analysis of countries.
Microorganisms 12 01255 g001
Microorganisms 12 01255 g002
Figure 2. Hotspot cluster analysis of keywords. Different colors indicate different clusters.
Figure 2. Hotspot cluster analysis of keywords. Different colors indicate different clusters.
Microorganisms 12 01255 g002
Microorganisms 12 01255 g003
Figure 3. Different beneficial mechanisms of glomalin-mediated remediation of contaminated soil.
Figure 3. Different beneficial mechanisms of glomalin-mediated remediation of contaminated soil.
Microorganisms 12 01255 g003
Microorganisms 12 01255 g004
Figure 4. The mechanism of AMF-induced heavy metal ion retention inside their fungal structures.
Figure 4. The mechanism of AMF-induced heavy metal ion retention inside their fungal structures.
Microorganisms 12 01255 g004
Microorganisms 12 01255 g005
Figure 5. Antioxidant defense mechanisms of AMF-induced host plants to tolerance to HM stress.
Figure 5. Antioxidant defense mechanisms of AMF-induced host plants to tolerance to HM stress.
Microorganisms 12 01255 g005
Table 1. Different AMF–aquatic plant symbiosis systems are utilized in various types of wastewater treatment systems.
Table 1. Different AMF–aquatic plant symbiosis systems are utilized in various types of wastewater treatment systems.
AMF SpeciesWater Treatment SystemsAquatic PlantsPollutantsReference
Funneliformis mosseaeVertical Flow Constructed Wetland (VFCW)Phragmites australisPb, Zn, Cu, and Cd[65]
F. mosseaeVFCWP. australisCopper oxide nanoparticles (CuO-NPs)[68]
F. mosseaeVFCWP. australisCOD, TN, and CuO-NPs[62]
F. mosseaeVFCWCanna indicaTetracycline and Cu[66]
F. mosseaeVFCWC. indicaSulfamethoxazole, Cu, and Cd[69]
F. mosseaeVFCWPteris vittataAs[63]
F. mosseaeEFBZea maysPb[70]
Glomus etunicatumEFBCyperus alternifoliusTDS, COD, TN, TP, and salt ions[71]
Rhizophagus irregularisVFCWGlyceria maximaPPCPs (Ibuprofen and diclofenac)[67]
R. irregularisVFCWG. maximaPPCPs (Hydrochlorothiazide, chloramphenicol, furosemide, gemfibrozil triclosan and triclocarban)[64]
Commercially available mycorrhizal inoculantStormwater biofilterFicinia nodosa
Juncus australis
Carex appressa		TN, TP, phosphate, and Cd[72]
Native AMF communitiesHorizontal Subsurface Flow Constructed Wetland (HFCW)Canna flaccida
C. indica
Watsonia borbonica
Agapanthus africanus
Zantedeschia aethiopica		TSS, BOD5, COD, PO43−, and NH4+[73]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Zhang, X.; Wang, Z.; Lu, Y.; Wei, J.; Qi, S.; Wu, B.; Cheng, S. Sustainable Remediation of Soil and Water Utilizing Arbuscular Mycorrhizal Fungi: A Review. Microorganisms 2024, 12, 1255. https://doi.org/10.3390/microorganisms12071255

AMA Style

Zhang X, Wang Z, Lu Y, Wei J, Qi S, Wu B, Cheng S. Sustainable Remediation of Soil and Water Utilizing Arbuscular Mycorrhizal Fungi: A Review. Microorganisms. 2024; 12(7):1255. https://doi.org/10.3390/microorganisms12071255

Chicago/Turabian Style

Zhang, Xueqi, Zongcheng Wang, Yebin Lu, Jun Wei, Shiying Qi, Boran Wu, and Shuiping Cheng. 2024. "Sustainable Remediation of Soil and Water Utilizing Arbuscular Mycorrhizal Fungi: A Review" Microorganisms 12, no. 7: 1255. https://doi.org/10.3390/microorganisms12071255

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop