Agronomic Management for Cadmium Stress Mitigation

CHAPTER 3

Agronomic Management for Cadmium Stress Mitigation Meng Wang1, Shibao Chen1, Duo Wang2, Li Chen3 1Key

Laboratory of Plant Nutrition and Fertilizer, Ministry of Agriculture/Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, People’s Republic of China; 2College of Energy, Xiamen University, Xiamen, People’s Republic of China; 3Institute of Plant Protection and Environmental Protection, Beijing Academy of Agriculture and Forestry Science, Beijing, People’s Republic of China

Unlike organic contaminants, most metals do not undergo microbial or chemical degradation, and the total concentration of inorganic metals in soils persists for a long time after their introduction (Adriano, 2001). Therefore, with great public awareness of the implications of contaminated soils by metals on human and animal health, there has been increasing interest in the development of technologies to remediate contaminated lands. Cadmium (Cd) contamination of soil and food crops is a ubiquitous environmental problem that has resulted from uncontrolled industrialization, unsustainable urbanization, and intensive agricultural practices. Being a toxic element, Cd poses high threats to soil quality, food safety, and human health. Land is the ultimate source of waste disposal and utilization; therefore, Cd released from different sources (natural and anthropogenic) eventually reaches soils, and then subsequently bioaccumulates in food crops (Khan et al., 2017). Agronomic management has been regarded as one of the most economic and efficient ways to mitigate soil-Cd stress (Bolan et al., 2013).This chapter provides an overview of various applications of agronomic management that can regulate Cd bioavailability to agricultural crops. Specifically, the effectiveness of agronomic measures includes soil amendment application, fertilizer application, irrigation, and tillage management, as well as plant breeding and plant species selection (Fig. 3.1). Because these can influence the phytoavailability of potentially toxic elements like Cd in soils or enhance Cd tolerance in agricultural crops, the data are reviewed in this chapter, and the possible mechanisms for mitigating Cd stress are analyzed.

Cadmium Tolerance in Plants: Agronomic, Molecular, Signaling, and Omic Approaches ISBN 978-0-12-815794-7 © 2019 Elsevier Inc. https://doi.org/10.1016/B978-0-12-815794-7.00003-5 All rights reserved.

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Figure 3.1  A brief summary of agronomic practices for mitigating soil cadmium stress.

1. SOIL AMENDMENTS APPLICATION For diffused distribution of metals such as pesticide-derived Cd input in soils, one of the most efficient remediation options generally is amelioration of soils to minimize the metal bioavailability. Bioavailability can be minimized through chemical and biological immobilization of metals using a range of inorganic compounds including lime, P compounds, clay minerals, etc., as well as organic amendments (Kumpiene, 2010). Reducing metal availability and maximizing plant growth through inactivation may also prove to be an effective method of in situ soil remediation on industrial, urban, smelting, mining sites, and especially agricultural lands. In such remediation, the metal is not necessarily removed from soils when its risks on crop growth or human health are well controlled and managed (Bolan et al., 2003a; Garau et al., 2007). An overview of soil amendments feasibility in the immobilization of Cd in contaminated soils is displayed in Table 3.1. The principal mechanisms of Cd immobilization by soil amendments are adsorption, precipitation, cation exchange, and surface complexation (Guo et al., 2006; Shaheen and Rinklebe, 2015) as summarized in Fig. 3.2. The selection of a suitable soil amendment depends on its local acquisition and financial implications (Mahar et al., 2015). In this section, some of the promising soil amendments are reviewed and the potential value of these soil amendments through the immobilization of Cd is discussed in relation to their remediation mechanisms.

1.1 Inorganic Amendments 1.1.1 Phosphate Compounds Among chemical immobilization techniques, use of P-containing amendments is a good cost-effective alternative to soil excavation, and could

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Table 3.1  Overview of Soil Amendments Feasibility in the Immobilization of Cd in Contaminated Soils Amendments Immobilization Result(s) References Liming Material

Ca(OH)2 Ca(OH)2, CaCO3 Lime Red mud, zeolite, lime Red mud, lime Lime, cyclonic ash Hydrated lime

Transforming to less-mobile fractions, reduced phytoavailablity Phytotoxicity prevented by Ca(OH)2, but not by CaCO3 Reduced uptake of Cd Reduced solubility of Cd, changes in microbial communities Reduced Cd concentration in grass Reduced Cd concentration in plant and soil pore water Reduced concentration of Cd almost 100% in leachate at pH 7–8.5

Bolan et al. (2003a)

Reduced Cd concentration in brown rice by up to 73.6%, reduced soil extractable Cd fractions Inhibited Cd absorption in spinach shoots, decreased soil extractable concentration Progressively reduced leachable Cd content with increasing dosage Inhibited bioavailability of Cd in ryegrass

Liang et al. (2014)

Considerably reduced bioavailability of Cd in wheat and maize Reduced concentrations of Cd in the roots, shoots, and exchangeable fraction of Cd

Argiri et al. (2013)

Chaney et al. (1977) Brallier et al. (1996) Garau et al. (2007) Gray et al. (2006) Ruttens et al. (2010) Hale et al. (2012)

Clay Minerals

Sepiolite

Sepiolite

Sepiolite Attapulgite Bentonite Bentonite

Sun et al. (2013)

Abad-Valle et al. (2016) Lin et al. (2009)

Sun et al. (2015)

Continued

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Table 3.1  Overview of Soil Amendments Feasibility in the Immobilization of Cd in Contaminated Soils—cont’d Phosphate Compound

KH2PO4 Bonemeal (finely ground, poorly crystalline apatite) Phosphate rock, diammonium phosphate Hydroxyapatite, phosphate rock, triple superphosphate, diammonium phosphate

Enhanced Cd immobilization, decreased its plant availability

Bolan et al. (2003b)

Reduced Cd elution

Basta and Gradwohl (2000)

Reduced plant uptake

Chen et al. (2007)

Reduced mobility and ryegrass uptake Reduced exchangeable fractions

Mench et al. (1994)

Reduced exchangeable fraction and Chinese cabbage uptake Reduced uptake by maize and barley

Cheng and Hseu (2002)

Reduced bioavailability Increased uptake

Bolan et al. (2003c) Merrington and Madden (2000) Brown et al. (1998) Weggler-Beaton et al. (2000)

Metal Oxide

Hydrous Mn oxide Fe-rich waste (Fe [hydro]oxides) with redox cycles Mn oxide Fe oxide waste byproduct

Contin et al. (2007)

Chlopecka and Adriano (1996)

Organic Matter

Biosolid Papermill sludge, sewage sludge Biosolid Biosolid Biosolid, wood ash, K2SO4

Reduced plant availability Increased phytoavailability in biosolid-amended soil by chloro-complexation of Cd Alleviated phytotoxicity of Cd

DeVolder et al. (2003)

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Figure 3.2  The principal mechanisms of Cd immobilization in soils by amendments. (Adapted from Nejad, Z.D., Jung, M.C., Kim, K.H., 2017. Remediation of soils contaminated with heavy metals with an emphasis on immobilization technology. Environ. Geochem. Health (1–2), 1–27.)

provide a long-term solution for Cd-contaminated soils (Zia-Ur-Rehman et al., 2015). Various studies have reported convincing evidence of both water-soluble (diammonium phosphate [DAP]) and water-insoluble (apatite from phosphate rock [PR]) phosphate compounds to immobilize Cd in soils, thus decrease its bioavailability for plant and human uptake, mobility, and transport (Bolan et al., 2003b). Generally, phosphate compounds increase the immobilization of Cd in soils by means of two possible processes: (1) phosphate-induced Cd adsorption, and (2) precipitation of Cd as Cd(OH)2 and Cd3(PO4)2. Several mechanisms are involved in phosphateinduced Cd2+ adsorption, including: (1) increase in pH; (2) increase in surface charge; (3) coadsorption of phosphate and Cd as an ion pair; and (4) surface complex formation of Cd on the phosphate compounds. These fairly stable metal–phosphate compounds have been proved to own extremely low solubility over a wide pH range, which makes phosphate application an attractive technology for managing Cd-contaminated soils (Bolan et al., 2003b). In addition, the mechanism of coprecipitation/adsorption appeared more significant for Cd stabilization as compared to Zn or

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other heavy metals owing to competition between their ionic species with similar ionic size (Xu and Schwartz, 1994). Several studies have shown that treatment of contaminated soil with hydroxyapatite, PR, or phosphoric acid could effectively decrease available Cd by making compounds of low solubility (Table 3.1) (Zia-Ur-Rehman et al., 2015). However, it should be noted that when insoluble P-containing amendments like PRs are added into soils, the phosphate mineral apatite needs to be dissolved to release available P for plants. Rock phosphates are not only effective in decreasing Cd solubility, but they could also decrease the Cd bioavailability very efficiently by the reactions of adsorption and precipitation, thus help in reducing plant toxicity and restricting its entry into the food chain (Basta and Gradwohl, 1998). In addition, dissolution of PRs is necessary for the availability of P to plants. In acid soils, PRs are very effective as a nutrient source, because they dissolve more in acidic than alkaline conditions (Zia-Ur-Rehman et al., 2015). It is, however, important to recognize that, depending on the nature of P compounds and the heavy metal species, application of these materials can cause either mobilization or immobilization of the metals. Furthermore, as some of these materials contain high levels of metals, they can act as a transport agent of metals to soils. Accordingly, these materials should be scrutinized before their large-scale use as immobilizing agent in contaminated sites. 1.1.2 Lime Treatment Lime (e.g., CaCO3, CaO, Ca(OH)2) is a calcium-containing inorganic material in which carbonates, oxides, and hydroxides are predominant. Lime stabilization treatment of contaminated soils laden with hazardous waste (e.g., acid mining disposal) is proven as a reliable technology. Both the technology and its acceptance have progressed dramatically over the years, as it is a simple, cost-effective, flexible treatment method for remediation of soils and recycling them back to usable land (USDA, 1999). Liming is increasingly employed as a regular traditional practice for decreasing levels of Cd in edible parts of agricultural crops, because it can decrease the H+ concentration, increase the negative charge in soils, and subsequently precipitate metals as hydroxides or carbonates. In addition, the lime application to acidic soils, through alkalinization, can increase phosphorus availability for plants. In this case, the interaction of Cd with phosphorus can reduce the mobility of Cd and its availability for roots. A further advantage of soil lime application is the increase of Ca and Mg in the soil. Although, at the root level, the increase of Ca limits the anatomical changes caused by metals, especially by Cd, Cu, Pb,

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and Zn, the Ca concentration in soil solution on dissolution is also a wellknown component of signal-transduction pathways in plants. Furthermore, the simultaneously enhanced content of Mg in shoots guarantees the maintenance of photosynthetic activity by limiting the replacement of Mg in chlorophyll molecules by Cd. Moreover, both cations, favoring a site-specific competition for ions, could compete, and inhibit the translocation of Cd from roots to shoots (Brunetto et al., 2016; Nejad et al., 2017). In particular, the ionic radius of Cd2+ is 0.109 nm, which is closer to that of Ca2+ (0.114 nm), as compared to Zn2+ (0.088 nm); therefore, calcium could suppress ion exchange of Cd in soils (Zachara et al., 1993). Tlustos et al. (2006) reported that liming addition in the Cd-contaminated soil, by 3 g CaO and 5.36 g CaCO3 per kg of soil, increased soil pH up to 7.3 compared to 5.7 in the control treatment. Furthermore, liming decreased mobile Cd in the soil and decreased Cd contents in straw and wheat grains. Similarly, lime application decreased Cd concentration in rice by about 25% compared to the control (Cattani et al., 2008). Li et al. (2008) reported that limestone was most effective in reducing Cd uptake and accumulation in rice plants compared to other amendments including calcium magnesium phosphate, calcium silicate, Chinese milk vetch, pig manure, and peat. However, there are limitations associated with lime treatment of contaminated soils. Agricultural limestone has low solubility and can become coated and ineffective at severely acidic soils. In addition, it can be a source of fugitive dust and may increase soil pH as high as not to be appropriate for optimum plant growth if in high ratio added in soil (Mahar et al., 2015; Nejad et al., 2017). Conversely, the effects of such type of materials on soil pH might not be enough because of the buffering capacity of soils. Thus, studies related to liming-material application in real field conditions are required to draw a conclusion for the practical applicability of such materials. In addition, further studies are also required to estimate when to repeat liming material in Cd-contaminated soils to ensure continuous metal immobilization in the soil even after successive crop growth (Rizwan et al., 2016b). 1.1.3 Metal Oxides Oxides of metal (such as Fe, Al, Ti, and Mn) play an important role in metal geochemistry of soil. Amphoteric nature and highly active surface area make them potentially available for immobilization of diverse soil pollutants. Synthesized industrial byproducts and naturally occurring oxides have been documented in their potentiality to be employed for soil remediation objectives (Kumpiene, 2010).

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Coprecipitations, formation of inner–surface complexes, and specific sorption have been regarded as resulting in a strong metal binding by metal oxides (Kumpiene, 2010). The surface charge of a metal (M) oxide is thus the sum of positively and negatively charged sites resulting from its amphoteric character (Dzombak and Morel, 1990):

= MOH2+ → MOH0 + H +



= MOH0 → = MO − + H +

Oxides of Mn (birnessite and phyllomanganate group of minerals), oxyhydroxides (goethite, ferrihydrite, lepidocrocite, feroxyhite, and akaganeite), and oxides of Fe (magnetite, hematite, and maghemite) mostly occur in soils. The distance between the OH–OH groups in the Fe, Mn, Al oxides matches with the coordination polyhedra of many metal(loid) cations and anions, which are adsorbed on different surface sites, the former share edges and the latter double corners with Fe(O,OH)6 octahedra (Manceau et al., 1992). The surfaces of Fe hydrous oxides play a significant role in metal retention; Pb and Cd were immobilized with amalgamation of Fe(II) and (III) sulfates (Hartley et al., 2004). Because elemental iron is environmentally friendly, NFeOs (nanosized iron oxides) can be used directly to contaminated sites with a negligible risk of secondary contamination. The nanosized iron oxides (NFeOs) were intensively studied for heavy-metal removal from water/wastewater due to their high activities and surface areas, including goethite (FeOOH), hematite (Fe2O3) (Chen et al., 1997a,b), amorphous hydrous Fe oxides (Fan et al., 2005), maghemite (Fe2O3) (Hu et al., 2006), magnetite (Fe3O4) (Badruddoza et al., 2011), and iron/iron oxide (Fe/ FexOy) (Macdonald and Veinot, 2008). Similarly, nanosized Mn oxides, titanium oxides, aluminum oxides, cerium oxides, magnesium oxides, etc. are also referred to as potential adsorbents for metal remediation (Hua et al., 2012). 1.1.4 Clay Minerals Clays are hydrous aluminosilicates composed of mixtures of fine-grained clay minerals, crystals of other minerals, metal oxides, and colloid fractions of soils, sediments, rocks, and water. Clay minerals play an important role in the environment by acting as a natural scavenger of pollutants, through the uptake of cations and anions by ion exchange or adsorption (Yuan et al., 2013). Therefore, clay minerals have been utilized as amendments in the disposal and storage of heavy metal in soils owing to their low cost, abundant reserves, and high performance (Yi et al., 2017). In the remediation of

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agricultural soils polluted by Cd, sepiolite, palygorskite, and bentonite have often been utilized as amendments. In recent years, natural clays have been applied for the immobilization of Cd-polluted soils as shown in Table 3.1. Sepiolite alone or in combination with other materials such as limestone has been reported to significantly reduce the Cd content of brown rice, regardless of its use in pot trials or field demonstrations. For example, sepiolite reduced the Cd content of brown rice to 0.18 mg kg−1 in polluted soil, which is below the maximum levels proposed in the Chinese national standard “Maximum Levels of Contaminates in Foods” (GB 2762-2012) and by the Codex Alimentarius Commission (CAC 153-1995) of the World Health Organization (WHO). In addition to rice, sepiolite has also been shown to decrease the Cd contents of vegetables such as spinach, lettuce, rape, and radish (Liang et al., 2011). Sepiolite combined with other materials, such as limestone, phosphate fertilizer, and biochar, has significant effects on the immobilization of Cd in soils, which reveals that sepiolite is compatible with other amendments (Liang et al., 2011). Similarly, palygorskite could increase the soil pH and significantly reduce the soil HCl-, toxicity characteristic leaching procedure (TCLP)-, CaCl2-, and ammonium acetate (NH4OAc)-extractable Cd concentrations, resulting in a notable decrease in the Cd concentration of brown rice by a field demonstration of paddy soil remediation (Liang et al., 2014). Han et al. (2014) found that 2.00 kg m−2, in a paddy, palygorskite significantly decreased Cd accumulation in brown rice by 54.6%. Montmorillonite is also a clay mineral with substantial isomorphic substitution. Si4+ is substituted by Al3+ in the tetrahedral layer, and Al3+ is substituted by Mg2+ in the octahedral layer. The resulting negative net charge is balanced by exchangeable cations adsorbed between the unit layers and around their edges. As mentioned above, clay minerals such as sepiolite, palygorskite, and bentonite have great advantages in the remediation of Cd-polluted soils, including high performance, universal applicability, and simplicity of use. In situ fieldscale remediation studies have confirmed their potential for application. However, remaining problems such as assessment of remediation effects using new methods or tools, microscopic remediation mechanisms, long-term stability, and improvement of clay minerals should be the focus of further research.

1.2 Organic Amendments The use of organic wastes as a beneficial soil amendment for agriculture has been in practice for several decades (Sims and Pierzynski, 2000). The most commonly used organic wastes include biosolids, municipal solid waste

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composts, crop residues, sea weed, humic substances, etc. (Beesley et al., 2014; Khan et al., 2015). Addition of organic amendments to soil improves its chemical, physical, and biological qualities by increasing the contents of organic matter, changing its pH, providing essential nutrients, improving the water-holding capacity, and altering the bioavailability of heavy metals. Soil pH is regarded as the most influential factor affecting the Cd uptake by plants grown on Cd-contaminated soils (Liu et al., 2015). The possible reasons for this increase of pH by the addition of organic amendments may be due to mineralization of carbon, OH ions production by ligand exchange, and the release of basic cations such as Ca2+, K+, and Mg2+ (Mkhabela and Warman, 2005). Besides, the organic constituents in soils have a great affiliation to metal cations due to the existence of functional groups or ligands, which can form chelates with metals as shown in Fig. 3.3. The alcoholic, phenolic, carbonyl, and carboxyl functional groups dissociate due to increasing pH, thus enhancing ligand ion affinity toward metal cations and forming stable complexes. In addition, organic amendments decrease bioavailability of Cd by altering the pore-water concentrations and the metals-blocking capacity of iron oxides (Mahar et al., 2015). The influence of organic amendments is in favor of decreasing Cd accumulation in crops, and has been verified by Xu et al. (2010), who found a remarkable reduction of Cd levels in grains, straws, and roots of rice in the existence of organic acids and ethylenediamine tetraacetic acid (EDTA). Under most soil conditions, organic acids exist as negative anions, and therefore react vigorously with Cd ions and immobilize Cd in soils, hence decrease the bioavailability of Cd to rice (Li et al., 2017). Similarly, rich in nutrients and organic matter, sewage sludge is sometime applied as a soil amendment on agricultural lands, and the organic matter in sewage sludge can help immobilize the Cd in the soils and thus reduce its uptake by plants through lowering the mobility and availability of Cd (Hu et al., 2016). The remediation of Cd-contaminated soils using organic amendments depends on the availability and cost of organic amendments, as well as their effectiveness (Khan et al., 2017).Though in general, we assume that organic amendments decrease Cd bioavailability and plant transfer; however, this is not true in all cases, as different soil types respond differently. A study on spatial variation of heavy metals in soil and rice in Nanxun, China, conducted by Zhao et al. (2015), revealed that high organic matter in soil would enhance the accumulation and availability of Cd in rice. These contrary results may be due to different experimental conditions, for example, varying environmental conditions and plant species. Therefore, it is difficult to

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Figure 3.3 The possible mechanisms of organic amendments affecting Cd in soil. (Adapted from Khan, M.A., Khan, S., Khan, A., Alam, M., 2017. Soil contamination with cadmium, consequences and remediation using organic amendments. Sci. Total Environ. 601– 602, 1591–1605.)

acquire consistent conclusions. Particularly, for long-term immobilization of Cd, the role of organic wastes is still not clear and often questionable. Usually the problem associated with the application of organic amendments is Cd leaching. Application of organic amendments to Cd-polluted soils has shown to increase Cd leaching compared to nonamended soils (Li et al., 2017). However, sewage sludge frequently contains high levels of heavy metals, including Cd, and consequently increases the total contents of heavy metals in the amended soils (e.g., Cd, Pb, Ni, and Cr) and in plant parts (Cheng et al., 2007; Singh and Agrawal, 2010). Besides, sewage sludge also has high contents of soluble salts (including chloride), which can complex with Cd2+ and enhance the uptake of Cd by plants (Cheng et al., 2007; Weggler-Beaton et al., 2000). Therefore, although sewage sludge could be used as an effective organic fertilizer to improve soil fertility and agricultural productivity, its application on paddy fields should be avoided due to the potential problem of elevated accumulation of Cd in the soils and rice grains (Hu et al., 2016). There has been growing interest in the use of biochar, which is a carbonrich material made from pyrolysis of biomass and in particular agricultural waste, as a soil amendment to increase soil fertility and sequester carbon over the past decade. Biochar has porous structure and large surface area

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covered with a range of functional groups, which can immobilize metal cations in soils through adsorption and complexation (Beesley et al., 2011). Meanwhile, biochar also contains alkaline components, including high concentrations of phosphorus, calcium, magnesium, and organic anions, with the biochar being produced at high charring temperatures having great alkalinity (Liu and Zhang, 2012; Mukherjee et al., 2011). As a result, biochar amendment has a well-known “liming effect,” which can significantly reduce the mobility and bioavailability of Cd in soils. A growing body of the literature showed that biochar application decreased heavy-metal toxicity in plants, more information will be provided later. Although research is needed regarding the use of organic amendments for remediation purposes, research should also consider and account for the effect of organics on soil physicochemical properties while applying it to different soil types. In addition, it should address the effect of these organics on available and total Cd concentrations in a variety of soils, as well as the possibility of the decomposition of organic amendments after application to soils to result in the release of the bounded metals (Khan et al., 2017). In conclusion, because most of the Cd-enriched farmland soil is acidic (pH < 7.0), alkaline amendments, such as sepiolite, lime, sewage sludge, biochar, etc., showed excellent remediation of Cd, their additions can greatly reduce the phytoavailable Cd (e.g., exchangeable forms) content in soils and change the percentage of Cd speciation, such as exchangeable, carbonate-bound, Fe–Mn oxide–bound, and OM-bound forms (Li et al., 2014). So far, the assessment of the remediation performance of soil amendments mostly depends on some short-term parameters including the variation in soil phytoavailable metal speciation and cementation during the crop-growth period, crop biomass, and metal-uptake level. Longterm stability of the amendments with Cd in the field soil is the most important factor that impacts on the general restoration performance. A change of the geochemical processes may lead to the reactivation of Cd and its release from amendments in the soil, and subsequently enhance the crop uptake risk. Therefore, both large-scale and long-term field experiments need to be conducted to validate the stability of in situ remediation (Tang et al., 2016).

1.3 Exogenous Application of Soil Organisms Though soil microorganisms cannot degrade or destroy the heavy metals, they can affect the migration and transformation by changing their physical and chemical characteristics. Many soil microorganisms are resistant to

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heavy-metal toxicity and could transform toxic metal forms in the soil into less toxic forms. They could also reduce their availability to plants by different mechanisms, including extracellular complexation, precipitation, oxidation–reduction reaction, intracellular accumulation, etc. Moreover, soil microorganisms could improve plant health and solubilize nutrients for plant growth (Nejad et al., 2017; Rizwan et al., 2017b). It has been widely reported that the application of soil microorganisms can increase growth, biomass of various crops under Cd stress (Table 3.1) (Rizwan et al., 2017a). Cd-tolerant bacteria, isolated from rhizosphere soil, were reported to increase plant growth, biomass, and relative water content, decrease oxidative stress in Cd-stressed wheat seedlings, and decreased Cd uptake in both shoots and roots (Ahmad et al., 2015; Hassan et al., 2015). In another study, Moreira et al. (2014) reported that plant growthpromoting rhizobacteria (PGPR) inoculation increased maize growth and decreased Cd in shoots as compared to the untreated control. Similarly, Cd-resistant Micrococcus sp. TISTR2221 improved growth and Cd accumulation by maize as compared to uninoculated plants, and little Cd was found in maize grains (Sangthong et al., 2016). However, the bacteria response to Cd stress varies among strains in promoting crop growth and lowering Cd uptake. Recently, Suksabye et al. (2016) reported that the addition of 2% (v/v) microorganisms, Pseudomonas aeruginosa, Bacillus subtilis, and Beauveria bassiana, in the soil decreased Cd concentrations in rice grains but the decreasing effect varied among microorganism strains. It has been reported that four Cd-tolerant bacterial isolates, isolated from Cd-contaminated rice fields, decreased Cd accumulation in rice and increased plant growth and biomass in the presence of 200 μM CdCl2 by the formation of nontoxic insoluble cadmium sulfide (CdS) and absorption by Cd-binding proteins. However, the response of bacterial strains toward CdS formations varied among strains being maximum with Cupriavidus taiwanensis application (Siripornadulsil and Siripornadulsil, 2013). These studies showed that microbes could be used for the reduction of Cd toxicity in plants. In conclusion, exogenous application of soil organisms can increase plant growth and stabilize Cd in the contaminated soils. However, the protective response varies with type of organisms and plant species. Further studies are required to isolate local microorganisms from Cd-contaminated soils and focus on their effect on Cd stabilization because these organisms could be more efficient as they are better adapted to local conditions of the area.

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2. FERTILIZERS AND MANURE MANAGEMENT Proper management of fertilization has long been recognized as one of the most efficient but easily achievable means to increase the yields of crops (Ercoli et al., 1999). There has been some evidence that fertilization with a single nutrient (e.g., nitrogen [N], phosphorus [P], potassium [K], and calcium [Ca]), or a combination of several nutrients, can be an effective strategy in reducing Cd uptake and accumulation in plants by changing Cd fractions in soils and bioavailability to crops (Catherine et al., 2006; Sun et al., 2007a). The role of some important mineral elements in reducing Cd accumulation in crops is described shortly.

2.1 Nitrogen Level Nitrogen, a macronutrient for plants, its application does affect crops growing ability and nutritional quality (Gao et al., 2012). In pot experiments, nitrogen fertilization based on ammonium supply has been shown to decrease soil pH in the rhizosphere. In the field, nitrification occurred rapidly, but this would still cause localized acidification (Mench, 1998). Thus, the application of nitrogen fertilizers would further result in the activation of soil Cd and the increase of free Cd availability. Gao et al. (2010) conducted a 3-year field trial to determine the effect of source, timing, and placement of N fertilizer on Cd concentration in durum wheat grains under reduced and conventional tillage practices, and found that N application increased Cd and decreased Zn concentrations in grains and a significant year-to-year variation occurred in grain Cd accumulations. Similarly, urea application increased Cd concentrations in shoots and roots, as well as total Cd extracted by Solanum nigrum compared to the control (Wei et al., 2010). Nitrogen forms of fertilizers affect the Cd uptake by plants. For example, Cd accumulation was greater in S. nigrum with NH4+ than NO3− supply in the growth medium, but no effect on Cd speciation in plants was observed (Cheng et al., 2016). Ammonia fertilization was found to increase wheat grain Cd concentrations as compared to urea and ammonium nitrate, in this study, Cd concentrations were higher in grains grown on sandy loam soil than on clay loam, and reduced tillage decreased grain Cd concentrations as compared to conventional tillage practices (Gao et al., 2010). Similarly, NH4Cl fertilizer increased Cd concentration in wheat grains as compared with (NH4)2SO4 or urea fertilizers in both field and pot experiments. However, NH4Cl application at tillering–jointing and flowering stages having nearly equal effects on Cd concentrations in grains as

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compared to other N fertilizers was reported by Ishikawa et al. (2015), the authors suggested that the increase in Cd concentration with NH4Cl application might be due to the presence of Cl− in the soil, which increased Cd mobility and plant uptake as compared to other fertilizers. Besides, increase in Cd concentration with ammonium fertilizers was believed to be due to decrease in soil pH, nitrification and/or NH4 uptake by plants as compared to other N fertilizers (Gao et al., 2011). It also has been reported that supplying NO3− is more efficient than NH4+ in promoting the phytoextraction of Cd by Thlaspi caerulescens (Schwartz et al., 2003; Xie et al., 2009), whereas the opposite is true for Helianthus annuus (Zaccheo et al., 2007). As to a given N fertilizer, its efficacy for a species is also dependent on the initial fertility of target soils (Catherine et al., 2006; Schwartz et al., 2003). In addition, the response of N toward Cd accumulation in crop grains varied between cultivars, seeding date, year-to-year wheat growth, and across the sites (Wangstrand et al., 2007; Perilli et al., 2010). Overall, above studies showed that N fertilizer types, soil types, tillage practices, application methods, etc. do affect Cd concentrations in crops. Thus, selection of a suitable N source, application timing and placement is very important in minimizing crop grain Cd concentrations.

2.2 Phosphatic Fertilizers Phosphatic fertilizers can alter soil characteristics, such as surface charge, soil pH, and soil-available phosphate, or can react with Cd directly in soils, leading to conversion of the mobile Cd into more-stable forms (Yan et al., 2015). For example, this effect of different phosphate fertilizers, including potassium phosphate monobasic (MPP), diammonium phosphate (DAP), calcium phosphate tribasic (TCP), and calcium superphosphate (SSP), on Cd immobilization was evaluated by Yan et al. (2015).They found that these fertilizers could supply available phosphate, have the advantage in increasing soil pH, which lead to the sorption of Cd in soils as formation of Cd-carbonate precipitates and complexes, and thus cause a decrease in bioavailable Cd in soils (Li et al., 2017). Jiang et al. (2007) reported that P application, as H2PO4, in solution culture decreased Cd uptake by maize, and found that type of P fertilizer and growth medium affected Cd uptake by crops. Besides, though addition of P fertilizers to soils could help to overcome the deficiency of some of the essential trace elements, such as Mo, it may also introduce toxic trace elements, such as Cd and F. In this context, Cd contamination of agricultural soils is of particular concern, because this

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trace element reaches the food chain through regular and frequent use of Cd-containing P-fertilizer materials. Wang et al. (2014) conducted a longterm (over 20 years) field trial with a crop rotation of winter wheat and summer maize with seven fertilizer treatments in different combinations. Results showed that the Cd level increased in soil with long-term P fertilization as compared to other treatments, but Cd uptake by crops decreased, which might be due to the precipitation of Cd with phosphate in the soil. It also has been found that P-fertilizer application in the Cd-contaminated field increased the Cd concentrations in durum wheat grains in a dose- and site-dependent manner (Shi et al., 2015). Similarly, P application increased Cd concentrations in wheat shoots, but decreased in roots (Zhao et al., 2005). Jafarnejadi et al. (2011) reported that overuse of P fertilizers increased the Cd concentrations in the topsoil and wheat grains. Comparison between unfertilized native and fertilized agricultural soils has often been employed to scrutinize the link between soil contamination and agricultural practices. For example, in New Zealand and Australia, most of the Cd accumulation in pasture soils has been attributed to the use of P fertilizers containing the trace elements of CD and F (Loganathan et al., 2008). This showed that P fertilizers must be used with caution in agricultural lands to reduce Cd entry into the food chain through crops.

2.3 Zinc Fertilization Zinc, a micronutrient for plants, has physical and chemical properties almost similar to Cd and can compete for common transport mechanism for uptake and translocation of Cd in crops, thus application of Zn, particularly in Zn-deficient soils, could reduce Cd uptake (Singh and McLaughlin, 1999). Salah and Barrington (2006) reported that application of 5.6 mg kg−1 of Zn into soil decreased Cd uptake by wheat plants, whereas high Zn addition increased Cd uptake causing a synergistic effect in Cd uptake. Saifullah et al. (2014) suggested that foliar application of 0.3% Zn in the form of ZnSO4 effectively ameliorated the adverse effects of Cd and decreased grain-Cd concentration in wheat. Welch et al. (1999) reported a competitive interaction between Cd2+ and Zn2+ at the root-cell plasma membrane of both bread and durum wheat. In addition, Zn concentration (≥1.0 mM) decreased the Cd translocation from one root section to others, thus inhibiting the movement of Cd via phloem in durum wheat (Welch et al., 1999). Köleli et al. (2004) suggested that Zn-mediated alleviation of Cd toxicity in durum wheat might be due to improving in antioxidative defense and/or Zn competing with Cd for binding to critical cell constituents in Cd-stressed

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wheat seedlings. The lower level of Zn increased the activities of catalase (CAT) and ascorbate peroxidase (APX) in Cd-stressed wheat roots, whereas higher Zn decreased enzyme activities (Sanaeiostovar et al., 2012). In addition, foliar applied Zn (6.0 g L−1 as ZnSO4) at booting stage increased nutrients (P, K, and Na), gas-exchange characteristic (photosynthetic rate, transpiration rate, and stomatal conductance), and chlorophyll contents in Cd-stressed wheat seedlings (Sarwar et al., 2015). Hassan et al. (2005) reported that 1.0 μM of Zn concentration in the nutrient solution increased the Cd translocation from roots to shoots. However, Zn supply increased the plant growth and photosynthetic pigments, and reduced the malondialdehyde (MDA) concentration and activities of antioxidant enzyme activities in rice under Cd stress. Note that, in a nutrient solution, addition of Zn was found to reduce short-term uptake of Cd (<24 h), though, under Zn deficiency, losses in membrane integrity can lead to enhanced Cd uptake. However, for this to increase Cd uptake requires a (plant-available) Cd-concentration gradient to exist from the soil to the root, which is unlikely to occur (McLaughlin et al., 1998). However, Zn2+ applied with phosphate fertilizers can cause desorption of Cd2+ sorbed on cation exchange sites of the soil components, increasing the concentration of Cd2+ in soil solutions (Roberts, 2014). In conclusion, Zn supply might be effective in reducing Cd concentrations in crop seedlings and translocation to grains. However, the Zn response toward Cd toxicity varies with genotypes, the dose, and duration of Zn and Cd exposure. Furthermore, high Zn concentration has been itself toxic to plants, thus it is rarely possible to reduce Cd stress in plants. More studies are required to investigate the proper Zn/Cd ratios to reduce Cd toxicity in crops (Rizwan et al., 2016a,b).

2.4 Sulfur Fertilization Sulfur (S) as a fertilizer source is one of the essential nutrients required for protein synthesis; it is also a structural component of several coenzymes and prosthetic groups for normal plant growth and development (Iqbal et al., 2013; Nazar et al., 2014). Different sources of S have been used for the reduction of metal uptake and toxicity in many plant species (Asgher et al., 2014; Zia-Ur-Rehman et al., 2015). For example, application of H2S could decrease Cd concentration in roots, stems, and leaves of rapeseed and cotton under Cd stress. It can be explained by the fact that H2S can reduce the MDA and H2O2 contents by improving antioxidant enzymes activities, e.g., superoxide dismutase (SOD), peroxidase (POD), CAT, and APX, under Cd stress.

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Further, H2S application increases K, Mg, and Ca contents in leaves and roots, increases photosynthesis, and enhances net photosynthesis rate (Pn), stomatal conductance (Gs), and transpiration rate (Tr) in leaves under Cd stress. Except that, H2S could regulate the metal-induced morphophysiological and ultrastructural changes in plants (Bharwana et al., 2014; Qian et al., 2014). In addition, S availability was reported to play a favorable role in alleviating Cd stress in maize at least plasma membrane Sarcoplasmic/ Endoplasmic Reticulum Calcium ATPase (H+-ATPase) level by compensating increased S demand for phytochelatins (PCs) synthesis in roots (Astolfi et al., 2004, 2005). In a similar way, application of S to Cd-treated mustard plants was found to protect against Cd-induced oxidative stress by reducing thiobarbituric acid-reactive substances (TBARS) contents in leaves, and increase plant biomass and photosynthesis through an increase in ascorbate (AsA) and glutathione (GSH) contents (Masood et al., 2012; Asgher et al., 2014).Therefore, an external supply of S is considered an important strategy in reducing heavy-metal toxicity in plants of agricultural importance (Rizwan et al., 2017c). However, elemental sulfur has also been regarded as a good soil-acidification material because sulfur-oxidizing bacteria (Thiobucillus) can oxidize sulfur to sulfate and protons (Zia-Ur-Rehman et al., 2015). This acidification process can increase the solubility of Cd and enhance Cd availability to plants (Kayser et al., 2000). Sulfur application in Cd-spiked soil was found to decrease soil pH and increase biomass and Cd concentrations in maize (Cui et al., 2004). Sulfur application to a Cd (1.4 mg kg−1)-contaminated field increased maize growth and Cd uptake in the leaves and roots, whereas grains contained Cd concentrations below the detection limit (0.03) of the instrument used for analysis (Fässler et al., 2010). The previous literature shows some controversial effects of S-containing fertilizer in Cd-contaminated soils. S response to Cd-stressed crops varies with species, cultivars, growth condition, dose, and duration of Cd exposure, as well as soil types, etc., before application; more investigations are required.

2.5 Silicon Fertilization Silicon (Si) is the second most abundant element present on the Earth’s crust. As a beneficial element for crop plants, it has been shown to alleviate the abiotic stresses to many plant species (Greger et al., 2016; Rizwan et al., 2016b). Silicon application can increase growth, biomass, photosynthetic pigments of crops, decrease Cd uptake and translocation in their seedlings grown under Cd stress, and reduce Cd concentration in grains (Hussain

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et al., 2015a; Naeem et al., 2015). For example, application of 200 mg kg−1 of Si under Cd stress with the concentration of 10 mg kg−1 increased shoot and root biomass of maize, and increased photosynthetic pigments of leaves (da Cunha and Ferreira, 2008;Vaculík et al., 2015). Shi et al. (2005) reported that Si could obstruct the apoplastic bypass flow through the roots, and suppress the apoplastic transport of Cd, and thus decrease rice-shoot Cd by 33%. In contrast to these findings, others show silicon application increased total Cd uptake by crops grown in either the soil (da Cunha and Ferreira, 2008) or solution culture (Vaculík et al., 2015). For example, the Si application was found to increase Cd accumulation in maize in a dose-dependent manner up to 150 mg kg−1 Si of soil, whereas higher Si concentration (200 mg kg−1) decreased Cd uptake by shoots and roots of maize plants (Liang et al., 2005; da Cunha and Ferreira, 2008). Overall, the reaction of a metal (M) with a SiO2 substrate which is existed in some of organic/inorganic fertilizers may result in the formation of both metal silicides and metal oxides,i.e., Mx + SiO2 → My − Si + Mx − y O2 . Silicon dioxide (silica) is one of the most commonly encountered substances in metal stabilization. Metal adsorption ions through SiO2 bond may also involve different silica in fertilizers as shown later (Ricou-Hoeffer et al., 2000). In acid solution, [ ]2 + SiOH ⋯ H − O − H M(OH2 )3 ↔ Si − OM + H3 O + Fertilizers with high CaO contents are thought to have higher adsorption efficiency due to the formation of Ca and Si complexes such as calcium silicates (2CaO∙SiO2). In neutral solutions,

mCaSiO3 HSiO3− + MOH + ↔ mCaSiO3 MSiO3 + H2 O

In alkaline solutions,

mCaSiO3 HSiO3− + M(OH)2 ↔ mCaSiO3 MSiO3 + H2 O + OH −

Generally, the Si-mediated increase in crop biomass and increase and/or decrease in Cd uptake might be due to different mechanisms occurring in soil and in roots and shoots of crops. Vaculík et al. (2009) reported that suberin lamellae formation initiated at a greater distance from the root apex of maize in the Cd + Si than in the Cd treatment alone. In addition, Si application decreased symplasmic and increased apoplasmic Cd concentrations in shoots, whereas it did not affect the Cd distribution in roots of maize

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plants (Vaculík et al., 2012). Recently, Vaculík et al. (2015) reported that Si improved the thylakoid formation in bundle-sheath cell chloroplasts of maize under Cd stress, which may contribute to the enhancement in photosynthetic rate and increase in biomass production. Besides, the Si-mediated decrease in Cd concentrations in wheat seedlings was found to be due to the increase in soil pH (Rizwan et al., 2012). Silicon application at 400 mg kg−1 increased soil pH and decreased available Cd in the soil, whereas soil pH was unaffected at lower Si treatments (Liang et al., 2005). In conclusion, Si could be used in enhancing Cd tolerance or phytoextraction by using plants. However, the alleviating effect of Si on Cd toxicity in crops depends on the Cd and Si concentration, growth conditions, and cultivars. Thus, proper selection of crop species, cultivars, Si application rate, and Cd concentration might be effective in enhancing Cd tolerance in crops grown on Cd-contaminated soils. Long-term field studies are also required to evaluate its feasibility (Rizwan et al., 2016a,c, 2017a).

2.6 Iron Fertilization Among various strategies to ameliorate Cd stress in crops, application of Fe fertilizer could be an effective way. Fe displays the ability to reduce Cd-toxic effects and improve plant growth, photosynthetic pigments, and energetic photosynthesis by reducing Cd uptake, and transportation in plant parts, alleviating complex protein, oxidative stress, retention of chloroplast, and providing a shield to photosynthetic tissues (Nada et al., 2007; Qureshi et al., 2010). Beneficial role of Fe in reducing Cd uptake and translocation has been observed in many crops due to iron plaque (IP) formation on the root surface. It is well documented that rice can form IP under both controlled and field conditions (Wang et al., 2013; Zhou et al., 2015). Cadmium concentrations in rice roots were significantly lower with IP than in roots without IP (Liu et al., 2010; Zhou et al., 2015). Sheng et al. (2008) documented that soil application of Fe fertilizer effectively enhanced rice grain, shoots, and roots by limiting Cd concentration. Liu et al. (2008) investigated that Fe application improved rice production by limiting Cd uptake and accumulation in target species. It was also observed that Fe decreased oxidative stress induced by Cd in rice. Fe improved plant growth, chlorophyll content, and MDA in both leaves and roots of rice by alleviating Cd-toxic effects (Shao et al., 2008). Furthermore, iron is a key cofactor of antioxidant enzymes. It was reported that Fe enhanced antioxidant enzyme activities and secured against oxidative damage by ameliorating the toxic effects of Cd in rice seedlings (Sharma et al., 2004).

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On the other hand, Fe deficiency enhances heavy-metal toxicity. Effects of Cd under Fe shortage were observed on physiological responses of corn and wheat crops. Results showed that Fe shortage improved Cd accumulation in both corn and wheat, and reduced chlorophyll content, phytosiderophores (PSs) release, and root and shoot biomass as compared to Fe-sufficient treatments (Bao et al., 2012). Similar effects of Fe deficiency were observed in Solanum nigrum L under Cd stress, when it was found that Fe deficiency enhanced Cd accumulation in plants by variable soil pH and redox potential (Bao et al., 2009). In addition, Cd also disturbed Fe uptake and accumulation in cucumber plants, increased Cd concentration, decreased Fe content, and vice versa (Kovács et al., 2010).Therefore, a significant correlation identified between Fe and Cd that Fe deficiency improves Cd uptake and translocation in crops might be because the enhanced-Fe nutrition reduces the adverse effect of Cd (Liu et al., 2010).

2.7 Organic Fertilizer (Composts and Manures) Application of animal manures, which are an excellent source of nutrients and organic matter, to fertilize agricultural lands is a traditional practice, especially in China (Yang et al., 2004). Improvement in soil fertility, root growth, nutrient uptake, and yields of crops with incorporation of manures has been well documented (Eneji et al., 2001; Yang et al., 2004). Besides high contents of organic matter, addition of animal manures can also increase the pH of soils due to their calcareous property (Han et al., 2012). The rise in soil pH is believed to be a key factor responsible for decreasing Cd uptake of plants, and the effect is particularly strong for poultry manures, which have much higher calcium carbonate contents compared to those of bovine and swine (Han et al., 2012). As a result, manure application could result in low Cd accumulation in crops, with more pronounced effect at high application rates. Application of cow manure in Cd/Zn-contaminated soil increased maize growth and grain yield, and decreased Cd and Zn uptake by maize (Putwattana et al., 2015). Khurana and Kansal (2014) reported that application of farmyard manure (FYM) (0 and 20 ton ha−1) in a sandy loam soil under greenhouse conditions increased the dry matter yield of maize, whereas it reduced the uptake of Cd, because FYM decreased water-soluble and exchangeable Cd in the soil and bound the Cd to less-mobile fractions. It also was found that the FYM application in soil increased maize biomass in 3 years cropping, whereas decreased Cd uptake occurred in the first year and then increased Cd uptake in the second and third years of the experiment.

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It might be due to soil acidification in the latter years, which increased the mobile form of the Cd in the soil (Gondek, 2010). Zhao et al. (2014) studied the effect of long-term cattle manure application on soil properties and Cd uptake by maize in a field experiment, and found that manure application increased the Cd availability in soil and uptake by maize, but the Cd was mainly accumulated in stems as compared to the grains. However, some studies reported that manure additions had little effect on Cd concentrations in plant parts (Kashem and Singh, 2001). In a similar way, organic fertilizers such as sawdust, peat, and compost can effectively reduce soil Cd solubility and plant uptake in highly contaminated soils (Guo et al., 2006). The addition of 2.5% (dry by weight [w/w]) municipal compost reduced the Cd content in onions, spinach, and lettuce by up to 60% (Mamun et al., 2016). Lignite (added at a rate of 1%) reduced the solubility of Cd and decreased the transfer of Cd from soil to Lolium perenne L. by 30% (Simmler et al., 2013). It can be because organic fertilizers contain humic substances, which are produced during the decomposition process of organic materials, including a large group of amorphous and colloidal organic polymers (Tang et al., 2016). The previous studies showed that compost or manure application increased and/or decreased Cd availability and uptake by plants depending upon the types of the organic fertilizer applied to the soils; its contribution also varies depending on the soil types, because it is much greater on calcareous soil than on acidic soil.

3. IRRIGATION MANAGEMENT Water management is a popular and cost-effective cultural practice for alleviating Cd contamination, especially for rice.Water management can change the reduction/oxidation (redox) potential and pH of soil, and subsequently affect Cd solubility in soils and availability to crops and thus manipulate its accumulation in crops (Honma et al., 2016). Common finding from pot and field experiments showed that flooding prior to and after heading was successful in reducing Cd concentration, whereas aerobic treatment increased Cd concentration in rice (Table 3.2) (Hu et al., 2015). It was broadly reported that flooding was the most effective in reducing Cd concentrations in rice; taking traditional irrigation as control, flooding during the whole growth period significantly reduced the soil acid extractable Cd content and the Cd levels in ip, as well as in brown rice, rice husk, and straw (Arao et al., 2009; Tang et al., 2016). Cadmium concentrations in the rice husk were lower in intermittent and flooding treatments than those aerobic intermittent

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Table 3.2  Effect of Water Management on Cadmium Content in Rice Grains (Sakurai et al., 2005) Water management after heading time Flooded Soila

A B C D

Cd (mg kg−1)

Greenhouse Field test

aEach

Drained

Trace Trace 0.09 0.16

1.10 0.68 0.23 0.33

soil is from different Cd-contaminated areas of Japan.

treatments. In field experiment, Cd concentrations in rice straw decreased from 1.76 to 0.35 mg kg−1 with the irrigation volume increased from aerobic to flooding. Moreover, long-term flooding reduces nearly 70% of the Cd content in brown rice, in contrast to the values obtained under humid irrigation (Hu et al., 2015). Similar findings have been reported elsewhere; e.g., Xu et al. (2007) found that the Cd content of rice was 0.39 mg kg−1, if the paddy soil was submerged during the whole growth period. However, the Cd content in rice was 1.12 mg kg−1 for a traditional field water-managing mode such as alternate dry–wet circulation. Water management during rice growth has been widely practiced in Japan and Taiwan as a means of reducing Cd accumulation in rice grains (Hseu et al., 2010). Besides, water management during the growth period also affects the Cd uptake by vegetables. For example, limited water supply during periods of high water demand increased the Cd concentrations in spinach compared to other watering regimes when the total Cd content in the soil was moderate (0.45 mg kg−1) (Tack, 2017). Seed soaking with hydrogen-rich water was also found to decrease the Cd concentration in Chinese cabbage and increase the plant growth and biomass compared to the control, by enhancing the activities of antioxidant enzymes and decreasing the oxidative stress (Wu et al., 2015). It is most likely that a considerable decrease in Cd absorption by crops under submerged conditions is due to a decrease in the Cd solubility because of the formation of carbonates (Khaokaew et al., 2011) and/or CdS (de Livera et al., 2011) as mentioned in the following equations:

CdCO3 (Otavite) + 2H + = Cd2 + + CO2 (g) + H2 O log K0 = 6.16



CdS (Greenockite) = Cd2 + + S2 − log K0 = − 27.07

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The former, Cd carbonate, is the primary form under alkali conditions (Khaokaew et al., 2011), whereas the latter, CdS, could be a dominant form under slightly acidic conditions. Augmentation of the redox potential is usually accompanied by an increase of soil phytoavailable Cd content and plant biomass accumulation of Cd. Previous research indicated that when the sediment redox potential (Eh) increases from −180 to 430 mV, dissolved Cd increases as well from 0.3 to 4.6 mg L−1, and Cd associated with Fe(III) and Mn(IV) oxides also increases (Guo et al., 1997). Therefore, the control of water content can regulate the redox potential of soil, and then achieve the objective of reducing the activity of Cd in soil. Theoretically, flooding paddy field shifts Eh toward a reduced state (a sharp decrease in Eh), in which the sulfate ion is reduced to the sulfide, and Eh is expressed as: ( ) Eh = 0.301 − 0.0739 pH + 0.00739 log SO24 − /H2 S

In addition, during flooding of paddy soils, soil microbes respire by utilizing oxidized soil components, including NO3− , SO4 2 −, Mn(III/VI), and Fe(III) species that are present in oxide phases, as well as the dissimilation products of organic matter. These species receive electrons during the reduction reactions, which generate NO2 −, S2−, Mn2+, Fe2+, and low molecular weight organic acids, accompanied by a decrease of the redox potential (de Livera et al., 2011). Consequently, Cd solubility could be decreased due to the enhanced adsorption of Cd on Fe and/or Mn oxyhydroxides and precipitation of CdS (Sun et al., 2007b). Oppositely, during drainage periods, the paddy soil is in an oxidative condition with increased Eh. Cadmium could form water-soluble cadmium sulfate (CdSO4), leading to a higher solubility and uptake of Cd by crops (Sebastian and Prasad, 2014a). However, it should be noted that irrigation water with high chloride contents can lead to great Cd mobility and plant uptake due to formation of Cd-chloro complexes (López-Chuken et al., 2010). Note that salinity cannot always be readily or economically manipulated, except by changing the site of production (especially for dryland salinization), or by switching to higher-quality irrigation water (McLaughlin et al., 1999; Hu et al., 2016). Water management along with other amendments might also be effective in reducing Cd concentrations in plants (Li and Xu, 2015). It has been reported that application of sepiolite in combination with phosphate fertilizer decreased exchangeable Cd by 18.2%, 13.7%, and 12.5% and brown

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rice Cd by 52.3%, 46.0%, and 46.8%, under continuous flooding, conventional irrigation, and wetting irrigation, respectively, compared to the control groups. The authors observed gradual increase of Fe2+ in soil and increase in competition between Fe2+ and Cd2+ on adsorption sites in roots with amendments (Li and Xu, 2015).

4. TILLAGE MANAGEMENT Crop rotations, tillage (reduced tillage, conventional tillage, etc.), and residue handling practices affect soil physical and chemical factors (e.g., soil redox and pH conditions, organic matter decomposition, nutrient stratification in the soil profile, soil moisture, temperature, etc.) and thus have been found to influence Cd uptake by field crops (McLaughlin et al., 1999; Hu et al., 2016). For example,Yu et al. (2014) revealed that rotating crops with a high Cd-accumulating oilseed rape could reduce the Cd contents of rice. Gao et al. (2010) reported that compared to conventional tillage, reduced-tillage management decreased grain Cd concentration and accumulation in wheat. It may because high soil organic matter in reduced-tillage soils, caused by residue from previous crops, can enhance the adsorption and complexation of Cd. Moreover, the reduced tillage management may affect microbial activity and the release of Cd from residue (Gao et al., 2010; Li et al., 2017)

4.1 Crop Rotation Crop rotation can markedly influence crop Cd concentration. Studies of crop rotation compared treatments, such as continuous cultivation, and a 2-year rotation cereal/legume, cereal/volunteer pasture, and plant/fallow, and indicated that the Cd concentrations in grain were highest in wheat grown after lupins, and lowest in wheat grown after cereal (Oliver et al., 1993). McLaughlin et al., (1999) found that wheat grown after legume crops had higher Cd concentrations in grain than wheat grown after fallow or other cereals.Wu et al. (2011) found that Cd concentration in rice grains decreased about 46.80% when it was rotated with oilseed rape in a pot experiment under greenhouse conditions. However, opposite results were obtained by Yu et al. (2014), who conducted a field experiment in alluvial loam soil under oilseed rape–rice rotation, and found that Cd concentrations were increased in rice plants as compared to a previous fallow treatment. This happened because oilseed rape cultivation in the soil mobilized the Cd concentrations and increased uptake of Cd by the successive rice crop. In addition, uptake of Cd varies between cultivars of both oilseed rape

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and rice, which showed that plant species should be taken into account during crop rotation to assure food safety (Yu et al., 2014). Precultivation with Cd-hyperaccumulating plants may reduce Cd concentration in postcultivated crops. It was reported that precultivation of Salix significantly decreased the Cd concentration in postgrown wheat grains under field conditions. A high density of Salix plantation decreased Cd in wheat grains faster than a low-density plantation (Greger and Landberg, 2008). In another study, cultivation of indica rice varieties, Chokoukoku and IR8, decreased Cd concentrations in wheat varieties, Chugoku165 and Shir-Oganekomugi, grown after rice cultivation (Ibaraki et al., 2014). These studies showed that precultivation with phytoextraction might be effective in reducing Cd concentrations in crop grains. However, more studies are required to identify other plant species for phytoextraction of Cd before crops cultivation grown in different soils varying in Cd contents and diverse environmental conditions (Rizwan et al., 2016a).

4.2 Intercropping In the practice of agriculture, intercropping offers farmers the opportunity to achieve a greater yield per unit land area by growing two or more crops in proximity, whereby crops can make use of resources that would otherwise not be utilized by a single crop (Karpenstein-Machan and Stuelpnagel, 2000). The cultivation practice of intercropping has also been proved effective in reducing Cd toxicity and promoting plant growth in mild-to-moderate Cd contamination in arable soils Ogbazghi et al., 2015; Xu et al., 2015), generally due to the following advantages. (1) Mixed stands may lose only one or two species to a disease, whereas monocultures may be entirely susceptible so that one event can destroy the entire phytotechnology system; and (2) intercropping supports more-diverse microbial communities that possibly promote an enhancement of the process. Furthermore, (3) synergistic effects such as nutrient cycling can occur in mixed stands; (4) the biodiversity and potential habitat restoration qualities are promoted; and (5) a higher volume of soil is explored by roots, then root metal uptake can contemporary occur at different soil depths (Marchiol and Fellet, 2011). For example, Cd uptake and plant biomass increased in radish genotypes when they were intercropped in different combinations in both pot and field experiments, which might be due to the increase in soil exchangeable Cd with intercropping compared to monoculture (Lin et al., 2014). Wu et al. (2003) reported that wheat/rice intercropping reduced the Cd concentrations in wheat and rice shoots as well as in wheat grains when compared to

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monoculture plants.The selection of a crop for planting patterns also affects the metal uptake by plants. Liu et al. (2012) studied the effect of crops (maize [Zea mays], tomato, cabbage, and pakchoi), and different planting patterns such as monoculture crops companion-planted with a legume, and crop companion planted with another crop on heavy-metal uptake by plants under field conditions. A higher Cd concentration was found in tomato and pakchoi than in cabbage and maize. Companion planting with Japanese clover increased the Cd concentration in crops compared to the monoculture. The increase in Cd uptake by plants with coplanting was believed to be due to the increase in bioavailable Cd concentration in the soil aroused by the release of low molecular weight organic acids from roots of the second crop as suggested by Liu et al. (2012). Tang et al. (2012) further confirmed that cocropping with phytoextraction plants and food crops may reduce Cd concentrations in food crops, thus, might be an option to reduce Cd concentrations in grains (Rizwan et al., 2016a). Conversely, proper cropping pattern might possibly enhance Cd phytoremediation by crops. From the perspective of phytoextraction, however, a major mechanism for enhancing phytoextraction by intercropping is that an intercropped hyperaccumulator can mobilize selected metals for a coplanted high-biomass nonhyperaccumulator (Gove et al., 2002). In recent years, there has been increased interest in the role that intercropping may be helpful in further improving Cd phytoextraction. Intercropping of Cd hyperaccumulator + high-biomass Cd accumulator systems are always more efficient than cropping of high-biomass Cd accumulator as a monoculture in extracting Cd from the soils (Fuksová et al., 2009). Moreover, there is an important lesson from the previous studies that the Cd removed by hyperaccumulators often accounted for the majority (60–90%) of the total extracted by the intercropping systems (Fuksová et al., 2009; Wu et al., 2007). On this basis, it should be proposed that when considering the establishment of a successful intercropping system for enhancing Cd phytoextraction, one should attempt to enable a hyperaccumulator to achieve its maximum possible contribution in the system (Li et al., 2012).

4.3 Other Tillage Practices Tillage practices, i.e., conventional cultivation, reduced till, direct drill, etc., may also play certain roles in affecting Cd concentrations in crop grains, whereas it is generally too inconsistent to allow conclusions to be drawn. Although it has also been reported that the Cd concentration in wheat grains reduced in reduced tillage as compared to conventional tillage (Gao

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and Grant, 2012). Higher Cd concentrations in wheat grain (>30%) were found to grow in a continuous wheat rotation under direct drilling, compared to reduced till or conventional cultivation. This may be due to the restriction of root growth to the upper soil horizons where nutrients and anthropic metals such as Cd are mainly located (Mench, 1998). Selection of proper soil type does influence Cd concentration in crop grains. For example, Cieslinski et al. (1996) reported that wheat cultivars that were grown in Chernozemic soil accumulated more Cd in grains than in the Orthic Gray Luvisol soil. Rojas-Cifuentes et al. (2012) suggested that matching durum wheat with the proper soil series might be the best management practice to produce seed with low Cd concentrations. Aziz et al. (2015) studied the effect of two soils, yellow Periudic Argosols, and calcareous Calcaric Regosols, on Cd availability to rice grains in a greenhouse experiment with increasing Cd concentrations in these soils. Results showed that Cd bioavailability and polished-grain Cd contents were higher in the yellow soil as compared to calcareous soil, which could be explained by the fact that the yellow soil had less organic matter content, CEC, and soil pH than calcareous based on the analysis of soil chemical properties (Aziz et al., 2015). Similar effect of soil type and properties on Cd phytoavailability was also observed in rice and other crops (Rizwan et al., 2012; Sebastian and Prasad, 2014b).The study on the effect of soil properties of 19 representative paddy soils from different parts of China on Cd bioaccumulation in rice grains showed that Cd bioavailability was mainly controlled by soil pH and organic carbon content in soils (Ye et al., 2014). Therefore, selection of proper soil type may help to reduce Cd toxicity and accumulation in crops and ultimately to avoid Cd entry into the food chain (Rizwan et al., 2016b). Overall, the information related to the effects of tillage practices on Cd availability is important to select the suitable management that balances crop yield and Cd concentration in crop grains.

5. PLANT BREEDING AND PLANT SPECIES SELECTION Selection and breeding of low Cd-accumulating cultivars are considered as the most cost-effective and environmentally friendly methods for reducing the risk of Cd contamination in food (Grant et al., 2008). Plant breeding as a means can improve crop quality by increasing crop concentrations of desirable trace elements and reducing those of potentially harmful trace elements such as Cd (Graham et al., 2007). Similarly, cultivar selection is an attractive method for changing the trace-element profile of crops, as its

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benefit could persist in the seed and can reduce the requirement for other management techniques (Grant et al., 2008). Theoretically, the accumulation and distribution of Cd in plants may be influenced by the following physiological processes: (1) size and morphology of the root system, (2) production of root exudates that can mobilize Cd, (3) transfer from roots to shoots via the xylem, (4) transfer from xylem to phloem, and (5) phloem transport into grains (Grant et al., 2008). Therefore, both accumulation and distribution of Cd in the plant differ depending on the species, cultivar, or growing conditions.

5.1 Differences Among Species Based on the concentration of Cd in commercially grown crops destined for international trade, crops such as sunflower, flax, rice, and durum wheat have been identified as accumulators of Cd, frequently containing more than 0.10 mg Cd kg−1 dry matter. The concentration of Cd in peanut, potato, and soybean may also be of concern, particularly when they comprise a large portion of the diet. Conversely, spring wheat, barley, oat, and maize generally contain Cd concentrations below 0.10 mg kg−1 (Grant et al., 2008). The Cd uptake also varies considerably among different vegetables grown in the same Cd-contaminated soils. It was reported that legume vegetables accumulated the lower amount of Cd and other metals, including Cu, Zn, and Pb, than root and leafy vegetables (Alexander et al., 2006). Cd concentration varies considerably (between 0.01 and 0.1 mg kg−1) in six vegetable species including pakchoi (Brassica rapa L.), radish, Chinese leek (Allium tuberosum L.), carrot (Daucus carota L.), cucumber, and tomato grown in field trials containing 2.55 mg Cd kg−1 of soil pots and fields trials (Yang et al., 2009). Similarly, spinach (Spinacia oleracea L.) accumulated the highest amount of Cd, whereas sweet pea accumulated the lowest amount of Cd when grown in same Cd-contaminated soil (Yang et al., 2010). Cd bioavailability depending on plant species can be specifically explained by the following reasons: (1) Specific chelating compounds can be released by some plants called phytosiderophores and/or root exudates (Mench and Martin, 1991). In general, phytosiderophores are produced by graminaceous plants such as barley, wheat, and rice under Fe deficiency, which mobilizes Fe from sparingly soluble forms (Reichard et al., 2005). These phytosiderophores can complex Cd and affect its bioavailability. Similarly, root exudates may influence the Cd bioavailability and toxicity by modifying the rhizosphere pH and redox potential (Eh), chelating/complexing, and depositing with Cd ions. (2) Differences among species in Cd

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concentration of the seeds may be in part related to differences in the abilities of plants to control movement of Cd from the xylem into the phloem and via the phloem to the seeds (Tanaka et al., 2007). It was found that Cd concentration in the phloem sap of rice increased with Cd application in the nutrient solution, providing direct evidence for translocation of Cd via the phloem (Tanaka et al., 2003). In subsequent studies, measurement of distribution ratios of 109Cd between rice grain and glumes indicated that more than 90% of the Cd in the grains had been translocated via the phloem (Tanaka et al., 2007). Cakmak et al. (2000) reported that there were genotypic differences in Cd binding to wheat-cell walls, and Cd transport to sink might be affected by the composition of phloem sap ligands. Such factors may alter Cd behavior and Cd uptake by different species.

5.2 Differences Among Cultivars The Cd concentration varies not only among plant species but also among the genotypes of the same species, as the uptake and translocation of Cd in plants differs significantly among different cultivars (Uraguchi et al., 2009; Xu et al., 2010). For example,Wan Dan 13 maize cultivar was more effective in alleviating Cd-induced oxidative damage as compared to Run Nong 35, which was related to high root-Cd accumulation and antioxidant activities in this cultivar (Anjum et al., 2015). Tanwir et al. (2015) reported that Cd uptake and accumulation were much higher in a Cd-sensitive cultivar (31P41-Pioneer) as compared to tolerant cultivar (3062-Pioneer). It can be seen that Cd concentrations in brown rice ranged from 0.13 to 4.31 mg kg−1 in Fluvisols and 0.79–7.65 mg kg−1 in Andosols. The ranking of rice cultivars was maintained across the soils, suggesting that Cd concentration of rice grains could be controlled by genetic factors rather than environmental conditions. In addition, relative rankings of five cultivars was similar when they were evaluated in pots simulating either upland or paddy conditions. Differences among rice cultivars in Cd concentration in the grain were found much higher than in the roots, stems, and leaves (Liu et al., 2007). In addition, 100 tomato genotypes were tested for their ability to accumulate Cd in different parts. From the results, eight genotypes showed the highest yield with minimum Cd contents in fruits under Cd stress (3 and 6 mg kg−1 soil) compared to the control (Hussain et al., 2015b). Similarly, Cd concentration varied in edible parts of onion cultivars with same amount of Cd applied in the growth medium (Li et al., 2016). These differences might be associated with the root acidifications, root organic acid, and oxidation abilities secretions, etc. (Ye et al., 2012). The previous studies show that proper

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selection of cultivars might play a very important role in remediation of Cd-contaminated soils. Conversely, large differences in Cd accumulation among cultivars enable us to develop phytotechnologies, such as selection and breeding of low Cd-accumulating varieties for reducing the Cd levels in grains and phytoextraction of Cd by using high Cd-accumulating varieties (Shi et al., 2015; Kubo et al., 2016). The physiological detoxification reasons of different cultivars are summarized as follows: (1) low grain–Cd-accumulating cultivar usually has a stronger capacity in restraining Cd transport to soluble or organelle fractions due to the crucial role of cell wall to bind more Cd than high grain– Cd-accumulating cultivar; and (2) low grain–Cd-accumulating cultivar owns a higher transportation rate in stem and higher Cd outflow in the roots, which results in less injury to roots and ultimately lower Cd accumulation in grains (Zhang et al., 2009; Wang et al., 2015). Major-effect Quantitative trait locus (QTL) (named qGCd7) has been broadly reported to control Cd concentration in grains without affecting concentrations of essential trace metals (Cu, Fe, Mn, and Zn), and it is located on the shortarm chromosome 7 (Ishikawa and Li, 2010). Moreover, this QTL has no significant effect on important agronomic traits, such as grain yield, grain weight, and days to heading, etc. It also has been revealed that Oryza sativa heavy metal-transporting P-type ATPase 3 (OsHMA3), a P1B-type ATPase, is a gene that controls root-to-shoot Cd translocation (Miyadate et al., 2011; Ueno et al., 2010). Functional analyses of the OsHMA3 gene in yeast shows that low-Cd cultivars contain a functional version of this gene, which is involved in Cd storage in root vacuoles. The high-Cd cultivars have lost this function; consequently, a much higher amount of Cd could be loaded into the xylem. Overexpression of the functional OsHMA3 gene from the low-Cd cultivar can drastically decrease Cd accumulation, not only in shoots but also grains. Thus, this gene can be used to develop the phytotechnologies for controlling Cd accumulation in crops (Grant et al., 2008). Though cultivar selection could be an important method to limit Cd uptake and accumulation in crops, the process is long and complex. Initially breeders have to: (1) find genetic variation in the Cd concentration in existing germplasm; (2) learn the inheritance of the low-Cd genetic character; (3) develop a breeding strategy to combine low-Cd traits with high yields, disease resistance, and other quality traits in modern cultivars; and (4) develop inexpensive methods to combine the low-Cd characteristic with other desired traits.Therefore, identifying low-Cd phenotypes by analysis of

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the grain is more costly than many other conventional breeding activities, due to the high cost of analysis (Grant et al., 2008).

6. CONCLUSIONS Cadmium is one of the major inorganic contaminants in the environment. Its presence in the soil has been recognized as a serious threat to agriculture, as its presence is potentially toxic to agricultural crops and may decrease plant growth, biomass, photosynthesis, and overall plant quality. Unlike organic contaminants, soil Cd does not undergo microbial or chemical degradation and persists for a long time after its introduction. Bioavailability of Cd plays a vital role in the remediation of contaminated soils. This chapter provides an overview of potential effective applications of agronomic management that regulate Cd bioavailability to agricultural crops.These Cd strategies employed for successful mitigation of Cd uptake and toxicity in crops mainly include proper application of essential nutrients such as N, Zn, Fe, Se, P, and Si in Cd-contaminated soils, inorganic amendments such as liming materials, clays, metal oxides, etc., and organic amendments such as compost, manure, and biochar, or the exogenous application of microorganisms. Efficient water management, cocropping, crop rotation, and soil type have been employed for the alleviation of Cd toxicity in crops. Effectively integration of conventional breeding procedures with molecular markers is a more practical way of selecting for low-Cd cultivars with desirable agronomic traits.Therefore, due importance should be given to test the effect of different rates of such agricultural practices on remediation of Cd-contaminated soils for a safe environment. However, there is still a need to integrate these agronomic measures to detoxify the Cd-enriched soil during the interim period of plant cultivation, and simultaneously guarantee that its edible part is safe during the growth period.

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FURTHER READING Arao, T., Ae, N., Sugiyama, M., Takahashi, M., 2003. Genotypic differences in cadmium uptake and distribution in soybeans. Plant Soil 251 (2), 247–253. Murakami, M., Nakagawa, F., Ae, N., Ito, M., Arao, T., 2009. Phytoextraction by rice capable of accumulating Cd at high levels: reduction of Cd content of rice grain. Environ. Sci. Technol. 43 (15), 5878–5883. Rehman, M.Z., Rizwan, M., Ghafoor, A., Naeem, A., Ali, S., Sabir, M., et al., 2015. Effect of inorganic amendments for in situ stabilization of cadmium in contaminated soils and its phyto-availability to wheat and rice under rotation. Environ. Sci. Pollut. Res. 22 (21), 16897–16906.