Soil is an important resource that produces food and other raw materials for humans. However, soil is often a sink for wastes, including heavy metals  , from a variety of human activities. In a risk based approach, soil can be classified as contaminated if the bioavailable concentrations of heavy metals is high enough to cause harm directly or indirectly to humans, animals, plants, water quality, the wider ecosystem, buildings and or construction materials  .
Some heavy metals are essential for living organisms at lower concentrations e.g. Co, Cu, Cr, Mn and Zn and are known as trace elements or micronutrients  . The term toxic heavy metalloids include those elements that are nonessential and include heavy metals such as Cd, Pb, Ba, Hg, Sb, Tl, As and U   .
Heavy metals are emitted into the soil environment through anthropogenic and geogenic processes . In nature, heavy metals commonly occur in soil parent materials   and the main natural source of metals and metalloids in the soil environment is the weathering of parent material  .
2. Heavy Metals and Metalloids in Soils
Arsenic has a crustal average of 1.5 - 2 ppm . The background concentration range of As in soil is 1 - 40 mg/kg  with an average As concentrations in soils of approximately 5 ppm. In natural soils, high As concentrations are often related to sulfide deposits and their weathering to produce local mineralised soils . Anthropogenic sources of As contamination in soil include sulfide mining, fossil fuels combustion, smelting, use of As containing pesticides and copper chrome arsenate used as a wood preservative  . In addition, groundwater has been found to be contaminated with As in more than 20 countries including the United States of America, China, India and Bangladesh  and using this water to irrigate soils can create As contamination issues such as leaving risks of soil accumulation of the toxic element and possible exposure of As contamination to the food chain through plant uptake and animal consumption . In Australia, a large source of Ascontamination comes from arsenic-based cattle dips. Arsenical dip solutions were used in the past for cattle tick and sheep lice control .
Zinc has a crustal average of 70 mg/kg  and a background concentration range in soil of 10 - 300 mg/kg. Industrial activities such as mining and smelting  and the long-term application of biosolids to agricultural land  are the primary sources of anthropogenic Zn in soils. Pollution of alkaline sandy soils, which are low in organic matter and clay, with Zn is likely to result in soils with high Zn phytoavailability and therefore a high risk of plants developing Zn toxicity at relatively low total Zn concentrations . Zinc toxicity in plants however has been far less wide spread than cases of Zn deficiencies  .
Nickel has a crustal abundance range of 37 - 72 mg/kg  and background concentration of 16.1 - 30.7 mg/kg . Smelting, ore refining, mining, combustion of fossil fuels and the long-time application of biosolids to agricultural land results in excess Ni being present in soil . Among various industrial operations manufacturing of alkaline storage batteries have resulted in an increase in the extent of nickel in the environment . Natural sources of Ni include serpentine areas in Venezuela, Australia and New Caledonia .
3. Bioavailability of Heavy Metals in Soils
The bioavailable fraction of a heavy metal is defined as that proportion of the total pool of heavy metals in a soil that are extractable in a chemical regent and can potentially be absorbed by plants . Heavy metals generally have low solubility and so are mainly in forms that are unavailable for plant uptake . Thus, in natural undisturbed environments, heavy metals are rarely present in high enough bioavailable concentrations to cause significant toxicity to plants.
Heavy metal bioavailability in soil is related to the solubility of contaminant in that soil  . However, there is debate as to which fraction of heavy metals in soil corresponds to the bioavailable pool . Bioavailability has been associated with heavy metal ion activity in the soil solution and the exchangeable heavy metal fraction  . Nevertheless, there is yet no general consensus among researchers on how to measure bioavailability of heavy metals in soil.
Heavy metal bioavailability, rather than total concentration, is important when accurately assessing the risk associated with soil contamination. Heavy metals that are present in soils occur in several fractions such as the soil solution, exchangeable, organically and colloidally bound, residual and within primary phase of minerals . Soil organisms and plants are not able to access the entire heavy metal pool in the soil. Among these heavy metal fractions, the most available heavy metals and potentially phytotoxic are present in soil solution and absorbed to inorganic soil constituents at ion exchange sites, with the other heavy metal fractions being not/less available for plant uptake .
A significant amount is known about the soil factors that affect the bioavailability of heavy metals to plants. Menzies et al concludes on the extractants that most accurately estimate the phytoavailability of metals in soils . Thus, a series of soil properties and processes control bioavailability and mobility of heavy metals in the soils with organic matter, soil pH, redox potential, clay and oxide content  .
3.1. Organic Matter
A fundamental component of soil is the organic matter which has originated from plants and animals and been set down within the earth’s structural components  . Organic materials can affect the solubility, bioavailability and mobility of heavy metals in soil . Organic matter is involved in the release and retention of heavy metals via cation exchange and adsorption to organic compounds . Studies show that adding organic materials to soil can reduce heavy metal bioavailability and mobility . Generally, stable soluble organic heavy metal complexes are not available for plant uptake and heavy metals, especially Cu, may be available in lower amounts as a result of complexing with dissolved organic carbon (DOC) in soil solutions  .
Humic substances are an important component of soil organic matter that can differ in molecular weight, composition, cation exchange capacity and solubility . Humic substances are often divided into three major fractions: humic acid, fulvic acid and humin based upon solubility in water adjusted to different pH states  . Humic and fulvic acids play an important role in the solubility and binding of heavy metals . Fulvic acid is known to increase the ability of soil solutions to complex heavy metals such as Cu   and Ni . Nickel ions make strong coordinating complexes with organic matter due to its high electronegativity which is second to Cu in the soil environment . Studies that show the effects of organic matter on heavy metal solubility and bioavailability revealed that heavy metal availability to plants and mobility in soil increase because of DOC complexation . For example, organic matter affects Zn solubility by the formation of complexes, although Zn competes less strongly than Ca, Cu and Ni for binding sites .
3.2. Soil pH
Soil pH is a fundamental variable that controls dissolution, precipitation, ion exchange adsorption, redox and other complex reactions within the soil . In the soil solution, pH is involved in the equilibrium between metal speciation, solubility, adsorption on colloids and sites available for heavy metal exchange and binding  .
Soil pH has been found to be a major factor that controls Cd and Zn bioavailability . Nickel solubility and toxicity in soils has been positively identified as related to soil pH and total Ni content . Generally as the pH decreases, the solubility and bioavailability of heavy metals increase  . It has been found in some studies where CaCl2 extractable Cu method was used, that there was little relationship between pH and Cu availability . The reason for this lack of response to pH was that Cu has a strong affinity for organic matter, which dominates Cu bioavailability in most soils  . Thus, dissolved organic matter is often a more important determinant of Cu bioavailability and solubility than pH  .
The soil pH has a significant effect on the bioavailability of As. Arsenic bioavailability is mostly controlled by adsorption and desorption reactions in soil . The effect of pH on As adsorption reactions is relatively well understood with acid and alkaline soils having less As adsorption to soil colloids and thus greater As solubility than more neutral soils . With As adsorption the variable pH-dependent charges develop on the soil particle surfaces  and influence As desorption over extended periods of time .
3.3. Redox Conditions
The reduction and oxidation conditions together are referred to as redox conditions. Redox reactions are simultaneous processes involving electron transfer from a reductant (electron donor) to an oxidant (electron acceptor). Redox conditions in a soil have strong effects on the solubility and speciation of heavy metals in solution . However, redox conditions are not uniform in soils as microbial processes, oxygen concentration, organic matter and pH influence redox conditions. In particular, redox conditions are known to have significant impacts on Mn, Fe, Cr, Sb and As speciation as these elements change their redox state depending on the environmental conditions  . Many of these elements are more toxic and mobile in their most reduced form e.g. As(III) and Mn(II) while others are more toxic in their oxidised form e.g. Cr(VI) . Iron and Mn are the most common oxides in soils and they become increasingly soluble under reducing conditions. Zinc, Ni, Cd and Cu however are mostly present in the divalent form in soils; as the monovalent forms are greatly unstable and so these metals are not significantly reduced under low redox conditions . Hence, redox conditions are considered to play a smaller role in the solubility and bioavailability of Zn, Ni, Cd and Cu compared to heavy metals with multiple redox states such as As, Mn and Cr .
3.4. Clays and Oxides
Clays and oxides are accepted as an important mechanism for controlling the solubility of trace metals . Clays and oxides control metal availability by specific adsorption to hydroxyl groups  , non-specific adsorption to a large number of available binding sites  , co-precipitation  and precipitation . The clay fraction is typically the most influential for cation adsorption reactions, due to the high concentrations of clays in many soils, high surface area and hydroxyl groups present on clay surfaces . Adsorption in soil commonly takes place on the surfaces of clays and oxides. Increasing clays and oxides in soil therefore supplies more sites for adsorption of heavy metals and so reduces the bioavailability of heavy metals  .
4. Rhizosphere Processes
The rhizosphere is the volume of soil that is affected by the presence of roots from growing plants and generally extends out 1 - 2 mm from the surface of roots . The rhizosphere has physical, biological and chemical properties that are different to the bulk soil. Due to the microenvironment that the plant root creates, the rhizosphere has a range of different characteristics to the bulk soil for example larger microbial biomass, altered pH, higher dissolved organic carbon from root exudates  . Much of the research on the rhizosphere has focused on the nutrition of plants and macronutrients including N, P and C cycling  . However, there has also been significant recent rhizosphere research on heavy metals and pollution .
Compared to the bulk soil, the rhizosphere is relatively rich in nutrients due to the loss of up to 40% of plant photosynthates from roots into the surrounding soil medium . The importance of rhizosphere microbial populations for maintaining root health, nutrient uptake and tolerating environmental stress is now recognized  . The rhizosphere has many characteristics.
In the rhizosphere, plant roots release a broad range of organic compounds such as phytosiderophores, which are mostly non-protein amino acids  . Siderophores are mainly synthesized by some microorganisms to solubilize iron under iron deficient conditions   also to solubilize other metals (Zn, Cu, Cd)   . By a specific receptor, the bacteria incorporate the iron siderophore complex . Phytosiderophores released into the soil augment the ability of plants to develop under Fe limiting conditions .
Phytohormones are synthesized by both plants and microorganisms in the rhizosphere and result in larger biomass of roots in plants . Phytohormones cover a wide range of chemicals including, auxin, cytokinin, indole-acetic acid, and gibberellin. Among them, auxins are the most common phytohormones that are known to be involved in the stimulation of roots and enhancement of plant growth .
4.1. Rhizosphere pH Changes
The pH of the rhizosphere can vary from the bulk soil by up to 2.5 units depending upon plant species and the buffering capacity of the soil . The pH of the rhizosphere is different to the bulk soil due to the excretion of hydrogen, bicarbonate salts and organic acids by plant roots to balance the internal charge difference in plants from cation and anion uptake by roots and due to CO2 production from microbial activity .
4.2. Role of Rhizobia and Other Microbes
Rhizobia are bacteria that form symbiotic associations with legumes and are responsible for the fixation of N from the atmosphere into forms accessible by plant roots e.g. . Consequently, legumes absorb more cations than anions and, thus, acidify the surrounding rhizosphere . Nitrogen assimilation by rhizobia results in changes of pH and increases heavy metal solubility and bioavailability where the symbionts exist  .
Research was carried out in the rhizosphere of Ni accumulating plants and plants grown on serpentine soils   . The findings were that the rhizosphere bacteria increased plant availability of Ni by increasing Ni accumulation via the production of siderophores. The siderophores induced the dissolution of minerals carrying Ni and thus promoted shoot and root biomass indirectly  .
Among other microbes in the rhizosphere, mycorrhiza is mutualistic associations between certain soil fungi and the roots of most plant species . Research has found that mycorrhiza assist in nutrient uptake at lower concentrations of metals . Also mycorrhiza is able to reduce metal uptake and in some cases increase plant metal tolerance under conditions of metal contamination . For instance, mycorrhizal Trifolium pratense (red clover) plants grown in acid soils with high Mn bioavailability had less Mn in the roots and the shoots than non-mycorrhizal plants . Also mycorrhizae are able to make plants more tolerant of metals when grown in soils containing high heavy metals concentrations (such as Zn, Cu, Mn, Ni, Cr)   . Possible mechanisms by which mycorrhizae deal with excess metals include the immobilisation of metals in the fungal hyphae or in root tissue .
5. Heavy Metal Uptake and Transport
Heavy metals (such as Fe, Cu, Mn, Zn and Ni) are absorbed passively by plant roots via ion channels . The mechanism for uptake is largely defined by the electrochemical gradients that apply to the transport of a specific nutrient  .
A number of selective transport pathways for heavy metals into plants are now being discovered. For instance, iron bound to phytosiderophores can be transported by Yellow stripe1 (YS1) across the plasma membrane . Yellow stripe1 gene synthesizes Fe(III)-Phytosiderophore (Fe-III-PS) transporter in maize (Zea mays). Also YS1-like (YSL) family of transporters can mobilize Zn and Cu from plant leaves and seeds .
Non-selective channels transport Ca2+ across the root membrane, and it is understood that the uptake of other metals at normal soil solution concentrations occur via this pathway . Competition between cations at the surface of the root shows that non-selective channels facilitate the absorption of essential and non-essential metals . As a result, under conditions of elevated heavy metals, competition for the transport sites leads to favouring the absorption of heavy metals over macronutrients, thus inducing or exacerbating deficiencies of nutrient cations .
Plants that have Fe deficiency are sometimes found to have higher Zn and Mn concentrations as well . In Arabidopsis, root membrane protein IRT1, a general cation transporter, enhances Zn and Mn uptake . A number of transporters are responsible for Fe uptake from soil. This involves transporting from the roots to shoots, transporting to generative parts of plant, xylem unloading, mobilization when seed germination occurs and loading-unloading of Fe from vacuoles. The Fe transporters ZmYS1 and OsYSL15 are able to move additional metals other than Fe such as Cu, Zn and Ni .
There are two strategies that plants use for Fe uptake: strategy I and strategy II (Figure 1). Strategy I plants utilize acidification & reduction reactions to improve Fe solubility and most of these plants belong to the non-grasses. Secreting protons into the rhizosphere lowers the soil pH, and thus, increases Fe solubility. The strategy I mechanism also effects co-suspension of As from Fe oxides or hydroxides. This makes As more soluble and available to plants . Strategy II plants excrete phytosiderophores (PS) which solubilise and bind soil Fe . Strategy II, is utilised by grasses to obtain Fe from soil . Strategy II plants utilizes a chelation mechanism that is utilised by several bacteria and fungi . An example of a phytosiderophore is mugineic acid which is secreted by Fe deficient graminaceous plants . In addition to Fe, phytosiderophores have been shown to mobilize and increase uptake of Zn and Cd in the rhizosphere of graminaceous plants . This strategy takes place to adapt to alkaline soils wherever rhizosphere acidification becomes hard to happen. The phytosiderophores are strong Fe chelators. These are amalgamated by the plant and secreted into the rhizosphere and there they bind with Fe .
6. Heavy Metal Toxicity in Plants
The most common evidence of heavy metal toxicity is a decrease in plant growth as metal toxicity increases. However, as various heavy metals have diverse sites of action within plant, the visual toxic response differs among heavy metals and plant species. From Table 1 it can be seen that the critical tissue concentrations for toxicity vary considerably across metal, species, and the plant tissue being measured.
Figure 1. Iron uptake systems of plant roots. Grass and non-grass species acquire iron from the soil through the plasma membrane (PM) of their root by two different strategies (Strategy I and Strategy II, respectively). Strategy I plants reduce Fe(III) to Fe(II), which is then transported across the plasma membrane by the Iron-regulated transporter 1 (IRT1). Strategy II plants release Fe(III) chelating siderophores and then transport Fe(III)-siderophore complexes across the plasma membrane using Yellow stripe 1 (YS1) transporter (partially adapted from  ).
Table 1. Critical concentrations for for As, Zn, Ni toxicity in soybean and sunflower.
6.1. Arsenic Toxicity
Arsenic is not essential for plants and appears not to be involved in specific metabolic reactions when supplied at low concentrations  . Naturally, As may be present in four oxidation states −3, 0, +3 and +5 . The major forms of As in the soils are arsenate (As(V)) and arsenite (As(III))  with the latter having greater toxicity to most species including plants . The symptoms of As toxicity in plants frequently include poor seed germination and reductions in root growth . These effects may relate to rapid disruption of plasma membrane structure, including fluidisation . At higher concentrations As has been reported to interfere with metabolic processes and sometimes lead to plant death . Where plants survive high As exposure, they may show reduced growth, nutrient deficiencies and chlorosis, resulting from reduced chlorophyll biosynthesis   , as well as reduced photosynthetic oxygen evolution . Critical concentrations of As in shoot tissue range from approximately 21 to 325 µg/g depending on the species and cultivar .
6.2. Zinc Toxicity
Symptoms of Zn toxicity include a general chlorosis of younger leaves where Zn is present in toxic concentrations in the soils  and an overall decrease in leaf size compared to the plants which are unaffected . Chlorosis is the first typical symptom of Zn toxicity . Under further exposure to toxic Zn levels plant symptoms develop into reddened leaves and in severe cases Zn toxicity can lead to necrosis of the tip of the leaf . Reduction in the growth of main, lateral roots and yellowing of the root is how Zn toxicity is manifested in roots . Critical toxicity concentrations of Zn in crop leaves are between 100 µg/g to >300 µg/g depending on the species .
6.3. Nickel Toxicity
Moderate concentrations of Ni can severely limit the growth of plants such as Indian mustard (Brassica juncea) and canola (Brassica napus) . Critical toxicity levels of Ni are in range of 10 µg/g to >50 µg/g in crops of moderately tolerant species . In soil, excess Ni affects root growth with severe inhibition in species that are sensitive to Ni at concentrations < 5 µM in solution culture . The most frequent effect of Ni toxicity is foliar chlorosis and in some cases decreased growth of root  .
7. Concluding Remarks
Metal contamination issues in plants and soils are becoming progressively shared throughout the world. Metal toxicities are often accompanying with a range of symptoms and an overall decline in plant growth   . Contextual knowledge of available different strategies and possible risks of heavy metals is required for the selection of appropriate remedial options. The growth promoting properties of rhizobia to an array of heavy metals for the remediation and stabilisation of contaminated land is an area of research that requires to be further explored.
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