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Kikis, C.; Thalassinos, G.; Antoniadis, V. Soil Phytomining. Encyclopedia. Available online: https://encyclopedia.pub/entry/54541 (accessed on 17 May 2024).
Kikis C, Thalassinos G, Antoniadis V. Soil Phytomining. Encyclopedia. Available at: https://encyclopedia.pub/entry/54541. Accessed May 17, 2024.
Kikis, Christos, Georgios Thalassinos, Vasileios Antoniadis. "Soil Phytomining" Encyclopedia, https://encyclopedia.pub/entry/54541 (accessed May 17, 2024).
Kikis, C., Thalassinos, G., & Antoniadis, V. (2024, January 30). Soil Phytomining. In Encyclopedia. https://encyclopedia.pub/entry/54541
Kikis, Christos, et al. "Soil Phytomining." Encyclopedia. Web. 30 January, 2024.
Soil Phytomining
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This entry is adapted from the peer-reviewed paper 10.3390/soilsystems8010008

Phytomining (PM) is defined as the process of using plants capable of bio-extracting metals from soil in order to explore them economically. This relatively new, innovative method has been gathering significant attention in both the academic and commercial domains. Conventional mining methods are often economically unviable when applied to lean ores, and they can lead to secondary pollution in soil—a situation that applies to all excavated metals. On the other hand, PM is an environmentally friendly and economically viable solution that addresses the growing demands for metal resources, while simultaneously contributing to energy production by harnessing biomass energy. 

hyperaccumulators metal-rich soils biomass energy environmental sustainability economics of agromining

1. Introduction

Phytoremediation is the process of remediating (or cleaning up) a soil elevated with pollutants with the use of plants (“phyto”). Many endemic plants, also known as metallophytes, can be found to be naturally grown in soils with elevated metal concentrations [1]. These unique plant species, also called “hyperaccumulators”, have portrayed natural tolerance to the presence of metals in soil or an enhanced ability for their accumulation. These plants might be genotypes that have evolved such tolerant characteristics due to their establishment in metalliferous areas for centuries or millennia [2]. The accumulation of metals in plants occurs in their root system or in the aerial biomass like stems, leaves, and flowers. According to Soleymanifar et al. [3], a plant capable of concentrating a metal significantly higher than a “regular” plant in its tissues when grown in the same area is characterized as a hyperaccumulator. Hyperaccumulators have the potential of absorbing metals from soil via their root system and translocating them into their aerial parts [4]. In this way, a contaminated soil may be phytoextracted. Thus, phytoextraction is the process of using hyperaccumulator plants to absorb potentially toxic elements from soil with the aim of remediating the soil. A variation in phytoextraction is phytomining (PM). Phytomining is the process under which plants are used to extract (“mine”) valuable inorganic elements from soil in a natural or in an induced manner for the specific purpose of financial gain after valorizing the produced biomass. The difference between PM and phytoextraction is the valorization of the plant biomass; in the former case, it is solely dedicated to being used for recovering the metals for use in the metallurgical industry. In the latter, it can have any uses except from that—pharmaceutical, aromatic, energy, biochar, etc. Conventional mining is only performed in ore deposits where metal contents are highly enriched (i.e., soil concentrations are well above the maximum legal regulation limits). Nevertheless, these kinds of deposits are being depleted because of increased population and emerging needs, as well as rapid industrial and economic advancement [5]. Even though traditional mining methods are successful, they cannot recover all of the valuable metals. After the completion of the mining process, there is still about 3% to 10% of metals left in the soil [5]. These areas are characterized as “degraded” due to the fact that they contain lower concentrations of metals and minerals than what would be economically explorable [6]. Usually, such ore bodies are related to soils formed on ultramafic and serpentine parent materials. During the cool-down of ultramafic magma, minerals such as olivine and pyroxene, rich in magnesium (Mg) and iron (Fe), have a higher melting point and therefore crystallize at higher temperatures, leading to their dominance, along with some elements like nickel (Ni) and chromium (Cr), in ultramafic rocks. These types of soils are rich in various metals such as Mg, Fe, Ni, Cr, manganese (Mn), cobalt (Co), and titanium (Ti) [7][8].
In order to facilitate the phytoaccumulation, metals can be dissolved from the ore by applying strong acids or with the technique of electrorefining, in which metal ions gain electrons and form soil metal deposits at the electrode’s surface [9]. In this way, metals in soil may become more phytoavailable, and thus their uptake to hyperaccumulator plants may be increased and, in turn, PM may occur. Hence, instead of going through the usual procedures of soil excavation for mining, the extractions are performed with the use of hyperaccumulator plants.
The concept of metal accumulation in plants and PM was first introduced by Jaffré et al. [10]. To date, scientists also refer to the process as “agromining” [11], in order to encompass the entire agricultural system of ore–soil–plants. The whole process offers the opportunity to extract metals from sites where conventional mining methods are not economically viable. The environmental effect of the method is minimal due to the balance action of the plants opposing soil erosion caused by excavation [12]. This method offers a sustainable way to remediate or restore soil, while simultaneously recovering valuable metals from soil [13]. Conventional methods used to remediate and decontaminate polluted sites often result in secondary pollution, aggravating the environmental challenges. The presence of plants minimizes the spread of metals and reduces the risk of wind and water soil erosion. Moreover, in large-scale PM applications, there is the possibility to harness the energy stored within the harvested plant biomass [3].
The bioaccumulation factor (BAF) and translocation factor (TF) are used to determine the efficiency of metal uptake from soil to plant and metal translocation within the plant, respectively [14]. The BAF is an index obtained by dividing the concentration of a metal in the aerial parts of a plant by its concentration in the surrounding soil. This factor provides insights into the ability of the plant to absorb and accumulate metals from the soil. On the other hand, TF is the ratio of metal concentration in the aerial plant parts to that in the roots. Higher TF values indicate a greater ability to efficiently translocate metals from the roots to the above-ground parts of a plant [14]. To be classified as a hyperaccumulator, a plant must have both BAF and TF values exceeding 1.0, signifying a great ability to absorb metals from soil and translocate them upwards in the aerial parts [15]. These indicators can be influenced by the effect of metal concentration in the plant. Therefore, biomass production and metal availability in the soil or substrate must be taken into consideration.

2. Elements Involved in Phytomining

2.1. Phytomining Elements

The elements of interest in the PM process are Ni, Co, cadmium (Cd), zinc (Zn), selenium (Se), Mn, thallium (Tl), and the noble metals (NMs). However, the majority of research efforts have focused on advancing the PM process of Ni [16]. For each metal, there is an established threshold that needs to be satisfied in order for a plant to be acknowledged as a hyperaccumulator. The selection of the limits is not entirely random but instead an indicator of a unique form of plant response, suggesting the presence of an unusual behavior. For instance, Sheoran et al. [5] suggested a limit of 1000 mg kg−1 of dry plant weight (DW) for Ni, after tests conducted on Homalium and Hybanthus plants in different areas. Similarly, Baker and Brooks [17] set the limit to 10,000 mg kg−1 DW for Mn and Zn after reporting high Zn concentrations in Thlaspi calaminare and Viola calaminaria leaves. Generally, over 700 plant species have been identified for their PM capabilities, most of which are Ni hyperaccumulators. When selecting plants for metal extraction, certain characteristics are important; these include three important features: high biomass yield, high Ni concentration in shoots (>1%), and fast growth [18]. The reason is that the phytoextracted amount of any given metal is equal to the concentration times biomass yield. All discussion is based on results obtained from field experiments, unless otherwise stated per particular case.
The hyperaccumulation threshold was originally established as a metal concentration in plant shoots 10 to 100 times higher when compared to measurements in the shoots of “normal” plants under similar conditions. It was redefined by Van der Ent et al. [18], who suggested that the initial concentrations should be at least 10 times higher than the measurements obtained in plants on metalliferous soils, and 100 to 1000 times higher in plants grown on regular soils (non-metal-enriched). Typically, most of the hyperaccumulating plant species are endemic to metalliferous soils. Since the root system of these plants is not usually collected during harvest, it is also mandatory for hyperaccumulators to exhibit BAF and TF values over 1, indicating that metals can be relocated in the upper part of the plant and recovered through combustion [14].

2.1.1. Nickel

As already mentioned, soils developed on ultramafic materials are expected to contain large amounts of Ni; hence, they are considered prime cases for Ni PM. Even though Ni in soil can be retained by Fe and Mn oxides, Ni hyperaccumulators can still accumulate a sufficient amount of the metal until the depletion of the source. According to Nkrumah et al. [16], 15–50 years are required before all easily accessible Ni is depleted. In addition, the physical properties of the soil are very important when it comes to PM. Well-drained soils are optimum for the cultivation of Ni hyperaccumulators, while soils that do not drain well may lead to decreased amount of plant biomass that is produced and, therefore, to a decreased amount of Ni that is extracted. For successful and economically viable Ni PM, soils should have an optimum content of moisture to maximize the amount of Ni absorbed by hyperaccumulator plants [19]. In the future, plant breeding techniques can make PM operations more profitable. Most of the plants that can hyperaccumulate Ni are species from approximately 40 different families, with the most important representatives being the Brassicaceae, Euphorbiaceae, Phyllanthaceae, Salicaceae, Buxaceae, and Rubiaceae family groups. Most of them are endemic plants found in soils derived from ultramafic rocks. The first report for Ni hyperaccumulation was made by Minguzzi and Vergnano [20], but the work was not widely recognized. Jaffré et al. [10] were the first to establish the term “phytomining” after noticing the accumulation of Ni in Sebertia accuminata, an endemic tree in forests of New Caledonia. Chaney et al. [21] were the first to conduct a field experiment for PM in the US Bureau mines in Reno, Nevada, where a Ni hyperaccumulator Streptanthus polygaloides was found to have bioaccumulated 10,000 mg kg−1 DW in serpentine soils containing 3500 mg kg−1 Ni. The second field trial was a two-year research study conducted by Robinson et al. [22], who extracted up to 8000 mg kg−1 DW Ni and had 110,000 mg kg−1 Ni in ash in Alyssum bertolonii. They also planted Berkheya coddii, which accumulated a total of 5500 mg kg−1 DW. It was also reported that B. coddii was a very good candidate for Ni extraction due to its high biomass yield, perennial life cycle, and tolerance to abiotic stress [22].
Numerous research studies have reported elevated concentrations of Ni in plant tissues when grown in these types of soils. All Ni PM research has focused on plants that can accumulate amounts more than 1% (i.e., 10,000 mg kg−1) in their leaves and the harvested biomass, after collecting small plant samples (1 cm2 or less) from serpentine soils in California. Indeed, Reeves et al. [23] found that Streptanthus polygaloides was able to accumulate Ni up to 1.5%, which led Mohsin et al. [24] to mention this plant as a good option for PM. Cole [25] reported the uptake of 5000 mg kg−1 Ni in the dried leaves of Hybanthus floribundus in lateritic soils in Western Australia, where background levels were approximately 500 mg kg−1 in the surface soil. In another study, Li et al. [7] reported a concentration of up to 22,000 mg kg−1 that was absorbed by Alyssum murale and Alussum corsicum plants (Brassicaceae), grown in Ni-contaminated soils in a 120-day greenhouse experiment. In addition, plants were fertilized and the pH was adjusted. Recently, Alyssum hyperaccumulators have received wide interest regarding their phytoextraction potential [16]. Durand et al. [26] conducted a 7-month pot experiment using Odontarrhena chalcidica (syn. Alyssum murale) spiked with Ni sulfate. They reported increased metal availability as well as BAF and TF values.

2.1.2. Cobalt

The standard for plants to be classified as Co hyperaccumulators was set at 1000 mg kg−1 by Baker and Brooks [17] until Krämer [27] revised it to 300 mg kg−1, reporting that the former accumulation of Co is rare. Normal amounts of Co in plants are well below 0.1 mg kg−1. Even in soils characterized with elevated amounts of Co, such as those deriving from ultramafic rocks, the amount of Co in plants rarely surpasses 20 mg kg−1. It seems that the presence of Ni in such soils interferes with Co accumulation. For instance, as mentioned before, Berkheya coddii is also a Ni hyperaccumulator. The presence of Co can inhibit the absorption of Ni when these metals are both present in the medium, leading to PM limitations. Keeling et al. [28] reported that Co can be absorbed by B. coddii plants with or without the presence of Ni in the growing medium (50% peat and 50% pumice). On the other hand, increased Co concentrations in soil from 125 up to 1000 mg kg−1 significantly decreased the harvested biomass due to plant toxicity, although the plant’s BAF was not affected. In trials where only Ni (at 1000 mg kg−1) or only Co (at 4–1000 mg kg−1) were present in soil, the crop yielded approximately 14.5 kg ha−1 (when for Ni) and 12.6 kg ha−1 (for Co). On the other hand, when Co and Ni were both present in soil (with concentrations of Ni = 500 and Co = 500 mg kg−1), the metal yield significantly dropped to 0.9 kg of Ni ha−1 and 3.9 kg of Co ha−1, and this indicates that PM may be limited due to interference of each other’s absorption by the plant. Similar to this, Rue et al. [29] suggested that B. coddii could be utilized in areas with high concentrations of Co but low Ni after testing the plant in pot experiments. Specifically, they found that the Co concentration reached 1980 mg kg−1 when treated with 10 mg kg−1 Ni (as Ni(NO3)2·6H2O) and 100 mg kg−1 Co (as Co(NO3)2·6H20), while total biomass can reach up to 22 t ha−1, which could yield 16.3 t Co ha−1. Similar findings were reported by Parks [30], who noticed the competitive role between Ni and Co accumulation in Rinorea bengalensis. However, R. bengalensis was found to be tolerant to Ni and managed to accumulate a concentration of 1200 mg Co kg−1 when grown on ultramafic rocks. Both Ni and Co were added as Ni(NO3)2·6H2O and Co(NO3)2·6H20 at 750 mg kg−1, respectively. An exceptional ability for Co PM was shown after collecting leaf samples of Nyssa sylvatica var. biflora and var. sylvatica (Nyssaceae) grown on ultramafic rocks in New Caledonia, which were found to accumulate up to 845 mg Co kg−1 [31]. The same was reported for the well-known Ni hyperaccumulator Alyssum murale, which accumulated 1320 mg Co kg−1 DW when grown in sandy loam soils (<2 mg Co kg−1 dry soil) spiked with 59.8 mg (1 mmol) Co kg−1 dry soil [32].
The addition of elemental zero-valent sulfur in soil can help increase the amount of metal that plants can absorb. According to Robinson et al. [33], sulfur content in soil at a rate of 5000 mg kg−1 increased the amount of Co that was absorbed by Berkheya coddii plants to 299 mg kg−1 DW, 5 times greater than the control treatment (56 mg kg−1 DW). Hence, this is especially beneficial in soils that do contain some amount of metals but not enough for the plants to take up the maximum quantity they need. In addition, sulfur is a cost–benefit additive, compared to EDTA, ethylenediaminetetraacetic acid, a synthetic molecule frequently used to increase metal mobility and soil, for enhancing the growth of metal-rich plants in soils with low metal concentrations. 

2.1.3. Cadmium

Higher concentrations of cadmium (Cd), ranging from 10 to 200 mg kg−1, can be found in soils that have been exposed to waste materials due to Zn mining. In addition, such elevated Cd levels may also arise in soils that have received industrial waste or phosphate fertilizers enriched with Cd [7]. Natural levels of Cd in plants are usually less than 0.1 mg kg−1, but in Cd-contaminated soils these levels can exceed 20 mg kg−1. The cadmium established threshold in plants is defined as having a concentration of higher than 100 mg kg−1, as proposed by Van der Ent et al. [18]. However, in certain Zn-Pb mines, Noccaea species, such as N. caerulescens and N. praecox, have been found to contain Cd concentrations exceeding 100 mg kg−1, or even higher than 1000 mg kg−1. Shoots of N. caerulescens can easily contain over 2000 mg Cd kg−1, even when grown on contaminated soils, and over 20,000 mg kg−1 when tested in nutrient solutions [34]. Other plants like Impatiens walleriana, Pteris vittata, Sedum alfredii, and Thlaspi caerulescens are capable of removing from soil 1168, 6434, 922.6, and 7400 mg kg−1 of Cd, respectively [35]. Specifically, Nedelkoska et al. [36] treated the roots of T. caerulescens with a H+-ATPase inhibitor and measured a concentration of 62,800 mg Cd kg−1 DW (6.3%) in the hair roots of the plant, which was grown in nutrient medium amended with a Cd concentration of 3710 ppm. On the other hand, there are significant variations among sites and within these plants [37]. Similar findings have been reported for Arabidopsis halleri by Bert et al. [38] and Viola baoshanensis by Deng et al. [39]. Specifically, A. halleri has been reported for its great ability to grow in different environments and its capability to store high amounts of Cd, especially when grown in polluted soils. According to Claire-Lise and Nathalie [40], A. halleri was able to accumulate up to 157 mg kg−1 leaf dry weight when treated with 5 μM Cd or more. Also, it has been used as a plant model on metal tolerance and accumulation for identifying the genes involved. However, it has not been further tested due to the fact that it produces low biomass. Nevertheless, it was noted that for a plant to be considered as a Cd hyperaccumulator, it needs to be naturally grown in an area and sustain itself without human intervention [18]. 

2.1.4. Zinc

As for Zn, it was found that Thlaspi alpestre var. calaminare (nowadays classified as Noccaea caerulescens) contained a minimum of 1% Zn in the dry leaf biomass [41]. Rascio [42] observed another Zn hyperaccumulator, Thlaspi rotundifolium ssp. Cepaeifolium, while Reeves and Brooks [43] proved that the Thlaspi genus consists of many Zn hyperaccumulators, with accumulated concentrations surpassing 1000 mg kg−1 after experiments in mine tailings in Northern Italy. Baker et al. [44] showed that T. caerulescens, when grown in nutrient-rich soils, could accumulate high concentrations of Zn, Cd, Co, Mn, and Ni. There were even instances where Zn accumulation reached the threshold of 10,000 mg kg−1 [17] or surpassed it, which was initially considered as the established limit to characterize a plant as a Zn hyperaccumulator. Furthermore, Brown et al. [45] added 10,000 μΜ Zn and 200 μΜ Cd in a nutrient solution and caused an accumulation of 33,600 mg Zn kg−1 in T. caerulescens. Also A. halleri, after being tested in a hydroponics experiment treated with 1 μΜ and 1000 μΜ Zn, managed to accumulate Zn in the shoots 300 mg kg−1 and 32,000 mg kg−1, respectively [46]. Also, in a hydroponics experiment conducted in China using Potentilla griffithii, it was shown that the plant was able to accumulate up to 11,400 mg Zn kg−1 leaf dry weight after being treated with 160 mg Zn L−1 [47]. However, the threshold of 10,000 mg kg−1 was later revised to 3000 mg kg−1 by Van der Ent et al. [18]. Also, Grimm [48] reported an accumulation of up to 11,700 mg kg−1 in stems of Brassica juncea, when the soil concentration of Zn was only 330 mg kg−1. 

2.1.5. Manganese

Manganese is a major trace nutrient with an expected concentration in plants grown in normal soil of ca. 40–50 mg kg−1 and usual soil pseudo-total concentrations ca. 500–600 mg kg−1. However, in Mn-rich soils, Mn hyperaccumulator plants may accumulate 2 or even 3 orders of magnitude higher Mn concentrations. Research conducted by Jaffré [49][50] reported that 98 out of 450 of the plant species growing on soils developed on ultramafic rocks in New Caledonia with background Mn concentrations of 1000–5000 mg kg−1 had average Mn concentrations above 1000 mg kg−1, while six species among them surpassed even 10,000 mg kg−1. Based on these findings, Baker and Brooks [17] decided to establish a threshold of 10,000 mg kg−1 to define Mn hyperaccumulation. In fact, due to exceptionally high levels of Mn, in some cases reaching a concentration of 2–5% of plant DW, the ash of these plants can contain as much as 10–25% Mn.

2.1.6. Selenium

Selenium (Se) levels in soil are often lower than 2 mg kg−1, but they can increase to a few hundreds of mg kg−1. The selenium concentration in plants dry biomass is typically lower than 0.1 mg kg−1 and may even be as low as 0.01 mg kg−1. Nonetheless, it was discovered that legumes belonging to the Astragalus genus were able to accumulate Se to elevated concentrations, locally exceeding 1000 mg kg−1 in the USA in Se-rich soils [51]. Due to the typically low levels of Se in plant tissues, Reeves [52] argued that a limit of 100 mg kg−1 should be considered for identifying Se hyperaccumulators. To date, utilizing Se hyperaccumulators for the economic extraction of Se has not been suggested. However, there are potential uses of these plant species in phytoremediation for cleaning up contaminated soils in crops harvested for stock feed and Se biofortification [53].

2.1.7. Thallium

Thallium is a precious metal high in demand but comparatively rare in nature. Although it is very toxic and difficult to find in the environment, natural, along with anthropogenic, origins can introduce significant amounts of Tl in soil. Several plant species are capable of extracting Tl from soils, making them useful for reclaiming it. Specifically, according to Leblanc et al. [54], there was an unexpected accumulation of Tl in Iberis intermedia and Biscutella laevigata in Pb/Zn mines in France. Moreover, for I. intermedia, an uptake of 4000 mg of Tl kg−1 was reported and over 14,000 mg kg−1 DW for B. laevigata, where the background concentration of Tl was 10 mg kg−1 in mine tailings. The presence of Tl in soil at levels that make Tl PM feasible is a possibility. However, there are only a few sites where this could be realistically implemented due to the limited availability of suitable soil conditions.

2.1.8. Noble Metals

Recently, NMs are being examined for their PM potential. This category constitutes metals such as gold (Au) and silver (Ag), as well as a sub-group of platinum metals including iridium (Ir), osmium (Os), palladium (Pd), platinum (Pt), rhodium (Rh), and ruthenium (Ru) [15]. These metals find extensive use across different industries and are often referred to as precious metals, obtaining significant attention due to their economic value. Interestingly, while the demand for NMs increases, their primary ore sources are gradually depleted. Hence, alternative methods of extraction, like PM, are being explored. Recent research and development on the extraction and accumulation of these metals in plants has shed light on the PM pathway for recovering these metals, although real-time implementation remains limited [55]. It should be noted that NMs can not be absorbed by plants from the metallic state as plants are capable of absorbing only the soluble species of any inorganic element found in the soil solution.

Gold

Across the world, considerable quantities of Au deposits can be found in natural enriched soils and mine tailings. Mohan [56] mentioned that PM of Au is a cost-effective way to extract Au from mine tailings and low-grade ores. Conventional mining removes the most Au from ores, leaving behind a significant portion of Au that cannot be extracted due to economic disadvantages. Since 1988, the hyperaccumulation limit of Au has been set to be higher than 1 mg kg−1 DW, based on the normal concentrations of Au in plants, which are usually around 0.01 mg kg−1. However, Au must be in the soluble form before absorption can take place. This can be achieved by adding several types of lixiviants (e.g., NaCN, SCN−, S2O3−2) depending on the properties of the substrate. In low-pH sulphate containing substrates, thiocyanate can solubilize Au.
It is reported that conifers growing in areas with Au ores in Canada could accumulate up to 0.02 mg of Au kg−1, while the background levels in plants are 100 times lower [57]. Also, in an experiment where Brassica juncea was planted in pots containing 5 mg Au kg−1 in artificial substrate, Anderson et al. [58] concluded that the application of 160 mg of ammonium thyocanate kg−1 of dry substrate weight achieved an accumulation of 57 mg Au kg−1. Wilson et al. [59] also referred to research where B. juncea was able to absorb 63 mg Au kg−1 DW after soil was treated with sodium cyanide. The plants were grown on an oxidized ore pile containing 0.6 mg Au kg−1. They concluded that an economically viable option for Au extraction that could yield 1 kg of Au ha−1 would require a total harvested biomass of 10,000 kg ha−1 containing 100 mg kg−1. Furthermore, Msuya et al. [60] mentioned that carrots (Daucus carota) accumulated 0.779 mg ha−1 of Au when ammonium thiocyanate was added and 1.45 mg ha−1 when thiosulphate was added, while the concentration of Au in the growing substance was 3.8 mg kg−1. Lamb et al. [61] performed a study where they used cyanide and thiocyanate to test the accumulation of Au in Berkheya coddii, Brassica juncea, and Cichorium intybus. They found that the leaves of B. juncea and C. intybus in soils spiked with cyanide had the highest Au accumulation at a rate of 326 mg kg−1 (B. juncea) and 164 mg kg−1 (C. intybus). Another study conducted by Vural and Safari [62] evaluated the potential of Helichrysum arenarium for Au accumulation; they reported TF and BAF values of 2.04 and 0.59, respectively. They concluded that enhancing the availability of Au in soil by adding chelators like NaCN, SCN−, and thiosulfates can lead to the usage of Helichrysum arenarium in the PM process.

Silver

To date, there are no reports about the hyperaccumulation of Ag by plants. Even though the Ag concentration in plants can be up to 1 mg kg−1, some plants such as Lupinus angustifolius can reach up to 126 mg kg−1 by induced accumulation [5]. Harris and Bali [63] were the first to propose the uptake of Ag nanoparticles by plants. They conducted research in which they observed an accumulation of significant amounts of Ag in Brassica juncea and Medicago sativa plants. Specifically, B. juncea absorbed up to 12.4% of its weight in Ag when exposed to 1000 mg L−1 of AgNO3 for 72 h, while M. sativa accumulated up to 13.6% of its weight in Ag when exposed to a solution containing 10,000 mg L−1 AgNO3 for 24 h. Silver nanoparticles that were stored inside the plant’s tissues had a size of 50 nm. In addition, the application of EDTA was not helpful in enhancing the absorption of Ag. EDTA had a rather negative effect as it caused toxicity to plants and this decreased the amount of Ag that would otherwise be capable for extraction. They concluded that plants could be used to produce large quantities of metallic nanoparticles.

Palladium

Out of all the platinum group metals, Pd has gathered significant attention due to its high abundance compared to others. The first report for Pd accumulation in plants was made by Fuchs and Rose [64], who measured a concentration of 285 μg kg−1 in ash from Pinus flexilis. In addition, Kothny [65] reported an accumulation of 400 μg kg−1 of Pd in the ash of Quercus chrysolepsis, while the background level was 140 μg kg−1. The hyperaccumulator Berkeya coddii was investigated for its ability to absorb Pd by Nemutandani et al. [66] from a contaminated site with 70 μg kg−1 Pd. It was found that B. coddii was able to extract 180 μg kg−1 in roots and 710 μg kg−1 in leaves. The plant demonstrated a notable ability to accumulate and translocate Pd, with BAF and TF values reaching 10.1 and 3.9, respectively.
There have been no officially defined Pd hyperaccumulators; it is anticipated that the threshold for all NMs would be approximately 1 mg kg−1, assuming their normal low concentration in plants. On the other hand, Pd, like Au, has limited solubility in soil. Hence, soil amendments are often used in order to increase Pd solubility and improve the accumulation in plants. For instance, KCN has been utilized to increase the absorption of Pd by plants. Walton [67] used KCN at a rate of 10 g L−1 to enhance Pd accumulation in B. coddii when cultivated in mine tailings containing 315 μg kg−1. They reported that plants had accumulated Pd to levels as high as 7677 μg Pd kg−1. In addition, Aquan [68] conducted an experiment utilizing gossan rock as a substrate, containing 205.5 μg Pd kg−1. They assessed the Pd accumulation in Cannabis sativa and found that the average Pd concentration was 30,336 μg kg−1 in the aboveground part of the plant, reaching as high as 62,420 μg kg−1 when KCN was applied. Another study conducted by Harumain et al. [69] managed to trigger the hyperaccumulation of Pd in Salix purpurea and Miscanthus through the use of KCN. They employed a synthetic ore with a Pd concentration of 50–100 mg kg−1 as growth medium. As a result, the leaves of S. purpurea and Miscanthus were found to contain 820 and 505 mg kg−1, respectively. Overall, the idea of phytomining Pd is relatively new. The effectiveness of using plants to extract this valuable element has only been minimally demonstrated so far.

Platinum

While the potential of plants to accumulate Pt in its tissues was mentioned by Fuchs and Rose [64], it is noteworthy that numerous studies on Pt PM have emerged recently. Nemutandani et al. [66] revealed that B. coddii grown in Pt-polluted areas with concentrations of 0.04 mg kg−1 soil achieved an uptake of 0.22 mg kg−1 in leaves and 0.18 mg kg−1 in roots. The plant exhibited BAF (5.5) and TF (1.2) values greater than 1.0, highlighting its ability to accumulate and translocate Pt. A study conducted by Kovacs et al. [70] reported the identification of plants from contaminated brownfield land with a Pt concentration of 3.06 mg kg−1. Also, Diehl and Gagnon [71] found concentrations of 14.6 mg kg−1 in Daucus carota collected from an area near a heavy-traffic motorway. White mustard, Sinapis alba, was also reported to show great ability in accumulating Pt by Kińska and Kowalska [72]. They found an impressive accumulation of 5973 mg kg−1 dry root weight, while the concentration of Pt in the nutrient solution was 1.0 mg L−1. Despite numerous reports on Pt in plants, it is worth mentioning that experiments aimed at Pt PM have not been conducted.

Rhodium

Generally, studies regarding the occurrence of Rh in plant tissues are very limited due to its scarce presence. A study conducted by Diehl and Gagnon [71] reported a Rh concentration of 0.7 mg kg−1 in Daucus carota that was collected from four different areas near heavy-traffic roads. Bonanno [73] found that the Rh concentration in Phragmites australis, collected from an extremely urbanized riverside area, ranged from 1.11 to 1.13 mg kg−1. Generally, it is worth noting that Rh has the highest solubility among the platinum group elements [15]. This suggests that Rh has great potential use in PM applications.

2.2. Factors Influencing Metal Availability and Behavior in Soil

2.2.1. pH

Soil activity plays a crucial role in how easily certain nutrients can dissolve in the soil solution and be taken up by the plants. As a result, soil pH affects the ability of plants to absorb essential nutrients and other elements from soil. For instance, Punjari [74] reported that when the pH of soil drops below 6.5 and 5.3, the amount of soluble Cd and Zn increases. Likewise, the solubility of Cu and Pb increases at pH levels below 4.5 and 3.5, respectively. On the other hand, at this low pH level, the mobility of As ions decreases. This is related to the fact that As is present in the soil solution as oxyanion, either in its trivalent (arsenite; AsIIIO33−) or its pentavalent species (arsenate; AsVO43−). The same is the case with any other contaminant anions (such as hexavalent chromium; CrVIO42−)—their availability is proportional to soil pH. The significance of pH in determining metal solubility and availability can be indicated by the fact that the pH in the root zone of certain plants is often up to 2 units lower than the surrounding soil pH due to the release of organic acids [75]. The amount of metal extraction is directly related to the concentration of the metal in soil and pH of the extracting agent.
There are various ways to reduce soil pH. This can be achieved by using different substances, including fertilizers containing ammonia, acids, and zero-valent sulfur, as amendments. However, there are limitations as to how much the pH can be lowered because most plant species can only thrive within a specific pH range. Usually, the lowest pH that many plants can tolerate is c. 4.5 [5]. Hence, while it is possible to adjust the pH utilizing soil amendments, it is important to carefully consider the range that allows plants to grow without adverse effects. On the other hand, acidic pH values can be corrected with the application of “liming” materials, which are mainly phases with abundant inorganic carbonate phases, i.e., CO32− and HCO3−, such as marble dust (either calcitic or dolomitic), as well as their derivative, caustic calcium oxide. Robinson et al. [33] studied the effects of different substances, namely MgCO3, CaCO3 (both alkalinity-bearing materials), and sulfur (an acidifying material), on the uptake of Ni and Co by Berkeya coddii. When MgCO3 was added to the soil, it increased the soil pH from 6.9 to 8.7 which led to reduced uptake of Ni and Co by B. coddii. On the other hand, the application of sulfur resulted in a decrease in soil pH from 6.9 to 5.5, which increased the plant’s uptake of both metals. In addition, the application of Ca salts made plants tolerant to Ni [8]. The researchers concluded that the addition of acidifying materials, like sulfur, can help extract more metals from soil by making them more available to plants. The shoot Ni concentration increased in Alyssum sp. at pH levels ranging from 5 to 7, with maximum concentrations being obtained at a pH of 6.5 [76]. The same relationship between cationic metal species and soil pH (which is inversely proportional—the former increases when the latter decreases and vice versa) has repeatedly been confirmed in experimental studies [49][77]. This was also found by Zhong et al. [78] in soil samples collected from heavy metal-contaminated soils in China; they reported a significant availability in soil for Ni, Zn, Cu, Cd, and Cr at pH levels lower than 4.5. They also concluded that soil pH is the most important factor concerning metal availability in soil. Specifically, pH was reported to affect all physicochemical and biological processes in soil, which in turn affect the behavior and the way metals interact with other substances. Since acidic pH tends to decrease metal sorption in soil, metal availability increases due to increased metal concentration in soil solution.

2.2.2. Fertilizers

In order to successfully implement the technique of PM, the availability of metals in soil needs to be ensured. Besides optimizing soil pH levels to guarantee metal absorption, adding fertilizers to achieve high-yielding phytoextraction crops is another factor that needs to be mentioned. Fertilizers containing NH4-N can reduce soil pH due to the fact that NH4+ in aerated soils is readily oxidized within weeks to NO3−, a process yielding 2 mols of H+ per mol of nitrified N. This enhances further the availability of metals in soil, as well as providing optimal conditions for the growth of these certain plant species [79]. In fact, hyperaccumulators grown in soils derived from ultramafic rocks exhibit a noticeable positive response to the application of fertilizers. For instance, in Vertisols in Albania, there was a 10-fold increase in the yield of A. murale after applying inorganic fertilizers [21].
Sheoran et al. [5] highlighted that the application of fertilizers significantly increased the maximum annual growth of Alyssum bertolonii compared to the non-fertilized treatment, which resulted in higher biomass yields. Specifically, the application of NPK fertilizers achieved an overall increase of 308%. Thus, fertilization can greatly affect the phytoextraction process, to remove metals from soil, making it more effective. The same work reported that Ni levels were increased in the leaves of Berkeya coddii from 2500 mg kg−1 to 4200 mg kg−1. Similar results were reported by Bennett et al. [80], where the application of NPK fertilizers doubled the annual biomass production of Alyssum bertolonii, Streptanthus polygalonoides, and Thlaspi caerulescens, without reducing the concentration of Ni in their shoots. In another study, the application of 100 kg P ha−1 in serpentine soils led to an improved yield in Alyssum murale plants [7]. Overall, high N fertilization promotes higher accumulation of Ni, Cd, and Zn. Sheoran et al. [81] used Salix on contaminated soil containing low levels of Cd (1.9–2.4 mg kg−1) and showed that the application of (NH4)2SO4 at 100 mg N kg−1 significantly increased the Cd and Zn plant concentrations to 4.5 for Cd and 400 mg kg−1 for Zn. Similar results were reported by Schmidt [82], who noticed a significant increase in Cd in Lolium perenne after adding (NH4)2SO4 as fertilizer. In that same work, in soils with low concentrations of Zn and Ni, the application of this fertilizer also significantly increased the crop metal concentrations without any loss of total yield. The same was agreed by Babau et al. [83], who tested Robinia pseudoacacia for its ability to absorb Pb, Cd, and Cu with and without the presence of NPK fertilizer. The addition of nutrients to soil (mostly N) increases the ability of plants to absorb metals and thus it is likely to increase the phytomining effectiveness of hyperaccumulators; hence, fertilizers are considered a critical factor for the success of commercial PM processes.

2.2.3. Chelates

In hyperaccumulators, the number of metals these plants can remove from soil depends on biomass production and the concentration of the metals within their tissues; thus, often their extraction ability is limited [84]. In order to increase the extraction of metals, chelates can be a possible option for higher growth rates. Chelates are capable of extracting various metals from soil. They have the ability to bind metals and form water-soluble organometallic complexes. Once they are formed, they can introduce metals into the soil solution by removing them from the surfaces they were attached to [85]. Some of the most used chelating agents are EDTA (ethylenediaminetetraacetic acid), CA (citric acid), DTPA (diethylenetriaminepentaacetic acid), NTA (nitrolenetriaceticacid), EDDS (ethylenediaminedisuccinicacid), and thiosolutions like thiocyanates. The former two agents are the most widely utilized [10][86]. Specifically, Robinson et al. [87] used EDTA and CA on B. coddii in order to phytomine Ni. Interestingly, they found that even though soluble Ni increased in the rhizosphere, the Ni concentration in the shoots decreased. They concluded that competition between EDTA, CA, and the plant’s own excretes resulted in trapping Ni in the root system of the plant. However, Meers et al. [88] reported an increase in Ni uptake in sunflowers which was 1.8 to 2.8 times greater by adding 1.6 mmol kg−1 EDTA and EDDS. Another study conducted by Blaylock et al. [89] where EDTA was applied in heavy metal-contaminated soils showed an enhanced accumulation of Pb, Cd, Cu, and Zn in Brassica juncea shoots. Nevertheless, they concluded that chelators like EDTA may pose an environmental risk due to the fact that they can not be easily degradable by soil microbes, resulting in groundwater pollution. Additionally, Wang et al. [90] reported results from a field experiment where soil-applied EDTA and EDTA−ethyl lactate were found to enhance Cd extraction by 20 and 29%, respectively, in Salix. Gold has also been found to accumulate in plants like Brassica juncea, Zea mays, Daucus carota, and Cichorium spp. by adding chelate agents like thiosolutions.

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Subjects: Soil Science
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Christos Kikis
,
Georgios Thalassinos
,
Vasileios Antoniadis
View Times: 72
Revisions: 2 times (View History)
Update Date: 31 Jan 2024
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