1. Introduction
Soil heavy metal contamination has emerged as a major issue worldwide as urbanization and industrialization have intensified, severely endangering environmental safety and subsequent agricultural productivity [1]. Cadmium (Cd), a hazardous and non-essential metal, can enter the human body through the soil–plant–human pathway and cause skeletal, reductive, cardiovascular and urinary diseases [1]. Wheat (Triticum aestivum L.) is regarded as one of the most important crops growing all over the world, providing calories, proteins and essential micronutrients for humans [2]. However, when compared with other crops, wheat more easily accumulates Cd in its edible parts. It is particularly concerning that wheat grain appears to be problematic in meeting the 0.1 mg/kg limit of the Chinese food standard in many of the Chinese major wheat-producing regions [1]. Furthermore, the ongoing need and consumption of wheat may be a possible source of dietary exposure of Cd. Thus, it is critical to develop a feasible strategy to prevent Cd accumulation in wheat grains and lower the risk to human health.
Various technologies have been proposed by researchers to decrease Cd accumulation in plant edible parts, including soil amendment application [1], foliar fertilization [3,4], agricultural practices [5] and water management [6]. Foliar fertilization is widely recommended among them due to its advantages such as simple operation, high efficiency and low effective cost [7]. A number of chemical mediators such as trace elements [8], amino acids [4] and hormones [9] have been applied to mitigate Cd stress and decrease Cd accumulation in crops grown on Cd-contaminated soils. Remarkably, as a divalent element, zinc (Zn) is similar to Cd in structural and geochemical properties and can interact with Cd in terms of uptake and translocation. Furthermore, unlike the application of fertilizers to the soil, where the fertilizer may quickly become unavailable to plants due to soil fixation, foliar-applied Zn can be absorbed quickly by the leaf epidermis and then transferred via the phloem [10]. Previous studies have demonstrated that foliar Zn application could regulate Cd accumulation by modulating Cd uptake by the roots, root-to-shoot translocation and stem/leaf-to-grain remobilization in rice (Oryza sativa L.) [11], maize (Zea mays L.) [12] and wheat [13] through the antagonistic interactions between Zn and Cd. Furthermore, Wu et al. [8] found that foliar application of ZnSO4 efficiently improved wheat growth and simultaneously reduced Cd concentrations in wheat grains by 13–50% in Cd-contaminated soils. Consequently, the foliar application of Zn has a great deal of promise for achieving safe agro-production on Cd-contaminated soils.
Additionally, regardless of crop varieties and soil types, foliar spraying with Zn fertilizer is considered as a promising strategy for agronomic biofortification since it can efficiently increase the amount of Zn and nutritional quality in the edible portion of crops [13]. Through foliar Zn spraying, it has been demonstrated that the Zn concentration in the edible parts of wheat [14], rice [11] and green bean [15] meets the target Zn level. Lian et al. [16] proved that optimal Zn application not only increased grain Zn concentrations but also improved grain nutritional quality by increasing the crude protein level as well as reducing phytic acid content. However, due to the short retention time in leaves and rapid release of Zn2+ from normal Zn sources, such as ZnSO4 [3,8], EDTA–Zn [17] and amino-acid-cheated Zn [4], the uptake efficiency by plants is usually very low. Recently, researchers found that nanomaterials are effective in promoting the penetration of droplets in crops and control the release rate of their active ingredients, thus increasing the persistence of foliar fertilizer [16]. Hussain et al. [18] reported that Cd concentrations in wheat straws and grain were intensely lowered by foliar spraying with ZnONPs.
Our previous research reported that a foliar Zn fertilizer, synthesized with ZnSO4, organic foliage fertilizer and nano emulsion, could effectively inhibit Cd uptake and biofortify Zn translocation in water spinach [19]. To investigate the influence of the foliar Zn fertilizer on wheat, a field experiment with different application rates of the foliar Zn fertilizer was conducted on wheat in the South China Plain over two consecutive years (2017–2018 and 2018–2019). Therefore, the objectives of this study were to assess the effects of the foliar Zn fertilizer on: (i) plant growth and wheat grain yield, (ii) accumulation and translocation of Cd in wheat and the health risks of Cd in human body and (iii) nutritional quality and Zn bioavailability in wheat grain.
2. Materials and Methods
2.1. Preparation and Characterization of the Foliar Zn Fertilizer
The foliar Zn fertilizer used in this study was prepared according to Tang et al. [19] with some modifications: 125 g ZnSO4.7H2O (Sinopharm, Shanghai, China) was dissolved using a 150 mL a commercially available amino acid fertilizer (Kangso 1#, Kangso, Huzhou, China). Then, 100 mL of nano emulsion (Nano Green, Livermore, CA, USA) with a micelle size range of less than 100 nm was added and mixed thoroughly. The elemental composition of the foliar Zn fertilizer was determined via energy dispersive X-ray (EDS, XFlash®6|30, Bruker, Berlin, Germany) analysis. The results showed that the foliar Zn fertilizer consisted of carbon (C), oxygen (O), sulfur (S), magnesium (Mn), potassium (K), silicon (Si), sodium (Na) and Zn, which accounted for 16.84%, 35.93%, 10.33%, 0.19%, 1.49%, 1.74%, 11.36% and 21.81% of the weight, respectively (Figure 1).
2.2. Field Experiments
The field experiments were conducted in 2017–2018 and 2018–2019 in Changxing county (119°84′ E, 31°03′ N), Zhejiang province, China. This site is a subtropical monsoon area with an average temperature of 15.6 °C, mean annual rainfall of 1309 mm, sunshine duration of 1810 h and frostless duration of 240 days. The soil in this site was identified as a stagnic anthrosol type and was dominated by wheat–rice crop rotation. The general soil physiochemical properties were as follows: pH, 5.12 (H2O, w/v, 2.5:1); CEC, 18.4 cmol(+)/kg; organic C, 29.3 g/kg; total N, 0.98%; available P, 38.2 mg/kg; available K, 90.0 mg/kg; total Pb, 32.8 mg/kg; total Zn, 90.3 mg/kg; total Cd, 0.42 mg/kg; DTPA-Pb, 6.78 mg/kg; DTPA-Zn, 2.54 mg/kg; and DTPA-Cd, 0.19 mg/kg (Table S1). According to the soil environmental quality guidance (risk control standard for soil contamination of agricultural land, GB15618-2018) [20], the soil in the tested field was slightly contaminated with Cd. Aikang58 was selected here as the tested wheat cultivar. The field trials were performed in a randomized complete block design with three replicates in an area of 23.37 m2 (5.7 m × 4.1 m). Wheat seeds were sown in early November in both cultivated years. The field management was kept the same, with conventional farming practices. The foliar Zn fertilizer was applied three times at the tillering, booting and filling stages, which are considered to be the best timings for foliar spraying to improve the quality of wheat [16,21]. Five treatments were set as follows: (i) T1: control, application of deionized water; (ii) T2: application of the 1000-fold dilution of the foliar Zn fertilizer; (iii) T3: application of the 750-fold dilution of the foliar Zn fertilizer, (iv) T4: application of the 500-fold dilution of the foliar Zn fertilizer and (v) T5: application of the 250-fold dilution of the foliar Zn fertilizer. Spraying was applied after sunset at a rate of 750 L/ha using a hand-held electric sprayer [19]. No soil Zn fertilizer was applied throughout the entire experiment.
2.3. Plant Sample Collection and Chemical Analysis
At maturity, wheat plant samples were harvested from a 1 m2 area of each plot. A total of 10 representative plants from each treatment were divided into grain, glume, flag leaf, stem and root. A composite sample was generated by mixing each tissue together. Fresh samples after careful washing were dried for milling at 65 °C until a constant weight. The dried grain samples were weighed to determine the grain yield. After that, all dried samples were ground to powder with a pulverizer for chemical analysis.
Dried fine samples (0.200 g) were digested with HNO3/HClO4 at 120 °C for 6 h and then the digested solutions were subjected to inductively coupled plasma mass spectroscopy (ICP-MS, 7500a, Agilent, Santa Clara, CA, USA) to determine the Cd concentrations [22]. The Cd translocation factors (TF) were calculated according to the following formulas: TFm/n = Cm/Cn, where Cm and Cn represent the Cd concentrations of the upper tissues and lower tissues of wheat, respectively. For the analysis of plant Zn, Ca, Fe and Mn concentrations, 0.200 g of the dry plant samples were digested with HNO3/HClO4 (5/1, v/v) at 120 °C for 6 h and then the digested solutions were subjected to inductively coupled plasma optical emission spectroscopy (ICP-OES, ICP6000, Thermo Fisher Scientific, Waltham, MA, USA) [22].
The phytic acid was determined as described by Liu et al. [23]. The total protein content in plants was determined using Coomassie brilliant blue colorimetry at a 595 nm wavelength. A trivariate model based on Zn homeostasis in the human intestine and the molar ratio of phytic acid to mineral elements (PA/Ca, PA/Fe and PA/Mn molar ratios) were employed to calculate the mineral element bioavailability in a quantitative value [24]. The detailed calculation process of Zn bioavailability is described as follows:
where is 0.091, which is the maximum Zn absorption. is 0.680, which is the equilibrium dissociation constant of the Zn–receptor binding reaction. is 0.033, which is the equilibrium dissociation constant of the Zn–PA binding reaction [25]. is the total daily absorbed Zn (mg Zn/day), which is based on reference adults consuming wheat flour (300 g/day) as the only daily source of Zn, and phytate and was termed as “estimated Zn bioavailability”. is the total daily dietary Zn (mmol Zn/day). is the total daily dietary PA (mmol PA/day).2.4. Human Health Risk Assessment
The human health risk index () of Cd was assessed separately by calculating the daily intake of metals () and dividing it with oral reference doses () of Cd.
where the value for Cd is 0.001 mg/kg body weight/day [26], is Cd concentration in wheat grains (mg/kg), is the conversion factor (0.085) and is the daily consumption of wheat grains (an average of 300 g/day for Chinese adults, 150 g/day for Chinese children and 75 g/day for Chinese infants) [27]. is the mean value of body weight, which was considered to be 56.8 kg for adults, 25.6 kg for children and 15.9 kg for infants.2.5. Statistical Analysis
For all data, SPSS 20.0, Origin Pro 8.5 and Excel 2016 were used for statistical analysis based on two-way analysis of variance (ANOVA) at a significant level of p < 0.05. Duncan’s multiple range test (DMRT) at 5% was applied to separate treatment differences. Means of significant differences between the two cultivation years on each Zn treatment were separated at p < 0.05 via a t-test. All results are expressed based on dry weight. Through routine analysis, quality accuracy analysis was performed on the standard reference (GSS-5 for soil and GBW (E) 100360 for plants), and blanks were also included.
3. Results
3.1. Grain Yield of Wheat
Spraying with the foliar Zn fertilizer influenced the grain yield in two consecutive years (Table 1 and Table S2). The effect of the foliar Zn fertilizer application on grain yield varied with the dilution ratio of the stock solution (Table 1). Based on the average of two years’ results, the grain yield under the T4 and T5 treatments, which were 500-fold (T4) and 250-fold (T5) dilutions of the foliar Zn fertilizer, respectively, were 7.66% and 11.8% higher than control (T1), respectively. Unexpectedly, the T2 and T3 treatments (1000- and 750-fold dilution of the stock solution) showed tiny negative effects on the grain yield. In addition, two-way ANOVA also showed that the cultivation year significantly influenced the wheat growth and grain yield (Table S2).
3.2. Cd Accumulation and Translocation in Wheat
The spraying of the foliar Zn fertilizer significantly altered Cd accumulation in wheat plants (Figure 2 and Table S2), which was generally dependent on the dilution ratio of the stock solution. The grain Cd concentration ranged from 0.0907 mg/kg (T4) to 0.146 mg/kg (T1) in the first year and from 0.0891 mg/kg (T2) to 0.188 mg/kg (T1) in the second year. Interestingly, for two consecutive years, the T2 treatment obviously decreased the grain Cd concentrations by 36.3% and 52.7% as compared with the T1 treatment (Figure 2A). Similarly, although the T2 treatment did not show the lowest glume Cd concentrations, it still remarkably reduced the glume Cd concentration by 13.4% on average for the two years when compared with the T1 treatment (Figure 2B). However, the T2 treatment did not lower the leaf and stem Cd concentrations when compared with the T1 treatment for both years (Figure 2C,D). For example, in the second year, compared with T1 treatment, the stem Cd concentration was significantly decreased by 4.16%, 8.31% and 14.7% under the T3, T4 and T5 treatments, respectively, whereas it increased by 5.63% under the T2 treatment (Figure 2D). As for the root Cd concentration, there was no clear patten after the foliar Zn fertilizer application (Figure 2E). Moreover, two-way ANOVA also showed that the cultivation year significantly influenced the Cd accumulation in wheat (Table S2).
In terms of the translocation factor (TF), as shown in Figure 3, spraying with the foliar Zn fertilizer significantly affected the translocation of Cd within wheat plants. Generally, translocation factors in wheat plants were presented in the order of TFLeaf/Root > TFStem/Root > TFGrain/Glume > TFGrain/Stem > TFGrain/Leaf > TFGrain/Root. Specifically, for two years, the T2 treatment showed higher values for TFStem/Root and TFLeaf/Root but the lowest values for TFGrain/Root, TFGrain/Stem, TFGrain/Leaf and TFGrain/Glume. Based on the average of two years’ results, the T2 treatment increased the TFLeaf/Root and TFStem/Root values by 0.438% and 7.21%, respectively (Figure 3B,C), but decreased the TFGrain/Root, TFGrain/Stem, TFGrain/Leaf and TFGrain/Glume values by 4.48%, 4.92%, 4.57% and 3.75%, respectively (Figure 3A,D–F), when compared with the T1 treatment. In addition, two-way ANOVA indicated that there was a significant difference in the Cd translocation in wheat after the foliar Zn fertilizer spraying (Table S2).
3.3. Human Health Risk Assessment of Cd
Spraying with the foliar Zn fertilizer influenced the values of Cd to varying degrees dependent on the dose of Zn fertilization (Table 2). All values of the for Cd under different treatments did not exceed 1.0. The average values of Cd for adults, children and infants under different treatments were in the order of (0.069) > (0.063) > (0.056). Based on the average results for the two years, spraying with the foliar Zn fertilizer reduced the values of Cd compared with the control for all populations except for the T5 treatment. Specifically, the values of Cd were reduced by 45.5%, 15.5% and 41.4% compared with the T1 treatment under the T2, T3 and T4 treatments, respectively, whereas the values increased by 19.0% under the T5 treatment.
3.4. Zn, Ca, Fe, Mn Concentrations of Wheat Grains
Spraying with the foliar Zn fertilizer showed significant positive effects on the concentrations of medium and trace elements in wheat grains (Table S2). Generally, the application of the foliar Zn fertilizer augmented the grain Zn, Ca, Fe and Mn concentrations in two consecutive years (Figure 4), whereas the positive effect was associated with the dilution ratio of the stock solution. Except for the grain Mn concentrations, the grain Zn, Ca and Fe concentrations were in the order of T2 > T3 > T4 > T5 > T1 based on the results for the two years. Specifically, the T2 treatment showed the highest values for grain Zn, Ca, Fe and Mn concentrations, which were on average 37.8%, 48.9%, 37.6% and 14.8% larger than the T1 treatment, respectively. Moreover, the grain Zn concentration ranged from 44.4 mg/kg (T1) to 62.1 mg/kg (T2) in the first year and from 45.3 mg/kg (T5) to 62.5 mg/kg (T2) in the second year. For the two consecutive years, the T2 treatment obviously increased the grain Zn concentration by 39.8% and 35.8%, respectively, as compared with the T1 treatment (Figure 4A). However, two-way ANOVA showed that the cultivation year significantly influenced the grain Ca and Fe concentrations in wheat plants, whereas the grain Zn and Mn concentrations did not differ in terms of the cultivation year (Table S2).
3.5. Nutritional Quality of Wheat Grains
As shown in Figure 5, spraying with the foliar Zn fertilizer exerted an obvious effect on the grain nutritional quality. Different application rates of the foliar Zn fertilizer increased the grain phytic acid content (PAC) for both years. Notably, based on an average of two years’ results, the lowest increase in grain PAC was observed with the T2 treatment (Figure 5A). As for the total protein content (TPC) in the grain, spraying with the foliar Zn fertilizer showed significant positive effects, except for T5 treatment. Indeed, different dose of the foliar Zn fertilizer improved the grain TPC to varying degrees. In the first year, the T2 treatment induced the highest rise, with a 12.2% increase over the T1 treatment. However, the maximum grain TPC was observed for the T3 treatment in the second year (Figure 5B). Generally, there was no significant difference in the estimated Zn bioavailability in wheat grains among T1, T3 and T4 treatments. It is noted that maximum value of the estimated Zn bioavailability was observed in the T2 treatment in the two consecutive years, which were 32.7% and 25.1% larger than for the T1 treatment, respectively. Conversely, in the two cultivation years, the T5 treatment caused the greatest reductions in the estimated Zn bioavailability in grain, by 19.5% and 0.0609%, respectively (Figure 4A). In contrast, the T2 treatment significantly reduced the values of the PA/Ca, PA/Fe and PA/Mn molar ratios by 27.8%, 21.4% and 5.81%, respectively, based on the average of two years’ results (Figure 4B–D).
4. Discussion
Growth inhibition and plant biomass reduction are normally considered to be the initial symptoms of Cd toxicity in plants grown on Cd-contaminated fields [19]. It is widely reported that the application of Zn could alleviate Cd toxicity by mitigating oxidative stress and promoting the photosynthesis process, thereby increasing the biological and grain yields [12]. Similarly, the present study showed that proper application rates of the foliar Zn fertilizer significantly increased grain yield, which might be attributed to the positive role of Zn in various biochemical processes, such as cell division, somatic embryogenesis, seed development and plant growth under Cd stress. The results indicated that the increase in grain yield may not only depend on the supply of water and N, P and K fertilizers but also trace elements such as Zn, especially on soils with Cd contamination [28].
Foliar Zn fertilization is widely regarded as a cost-effective and highly efficiency agronomic practice for Cd minimization in wheat [29]. In the current study, spraying with different rates of the foliar Zn fertilizer significantly affected Cd uptake and accumulation in wheat plants. Generally, the optimum application of the foliar Zn fertilizer (T2 treatment) lowered the Cd content in wheat grains by increasing the Cd contents in wheat stems and leaves, as well as restricting Cd translocation from the stems and leaves to the grains (Figure 2A and Figure 3E,F). Similarly, Zhen et al. [30] also illustrated the same mechanisms, showing that grain Cd contents in rice were decreased by strengthening Cd fixation onto the cell walls of leaves and limiting Cd re-transport from the leaves to the grains after Zn foliar application. There are two main reasons for Cd reduction in plants under exogenous Zn application. On the one hand, the effects of Zn on reducing Cd uptake and translocation mainly depend on the role of Zn in ameliorating Cd toxicity in enzyme reactions and gene expressions, such as the alleviation of oxidative stress by antioxidant production and the restoration of the structure of chlorophyll through balancing mineral elements [31]. For example, Yang et al. [32] speculated that the ameliorating effect of Zn on Cd toxicity might be partly attributed to sulfur metabolic processes, which are highly involved in antioxidant defense mechanism, as evidenced by the significant accumulation of sulfur-based substances (glutathione, phytochelatins and non-protein sulfhydryl compounds). Due to the important roles of Zn and Fe in photosynthetic electron transport, the photorespiratory system, carbohydrate metabolism and nitrogen metabolism [33,34], exogenous Zn could reduce the Cd toxicity in plants by increasing the chlorophyll content and improving photosynthesis through balancing mineral elements (such as Zn and Fe) [19]. On the other hand, previous researchers have suggested that the competitive interaction between Cd and Zn uptake and transport might account for the Cd reduction in plants, where the mutual transport system that is located on plasma membranes and regulated by P1B-type ATPases (HMAs), Zn/Fe regulated transporter-like protein (ZIP) and iron-regulated transporter (IRT) plays a crucial role [3,35,36]. There are many genes encoding these transporters, including ZIP3, LCT1, ZNT1, HMA3 and HMA2, etc., which are very easily influenced by environmental conditions such as foliar spraying [37,38,39,40]. Wang et al. [41] revealed that the application of Zn may cause Cd extrudation from roots due to the special upregulation of the HMAs family and PCR4, which helps to reduce the accumulation of Cd in roots. Tian et al. [40] reported that the co-expression of OsLCT1, OsHMA2 and OsZIP3 could reduce the Cd content in shoots and roots under Zn application conditions, indicating that Zn could regulate the specific genes that determine Cd uptake and accumulation. However, in the present study, we noticed that the influences of the application of the foliar Zn fertilizer on Cd uptake and accumulation varied with the application rate of the foliar Zn fertilizer. Sarwar et al. [42] also suggested a strong relationship between the antagonistic effects of different application rates of Zn and the grain Cd concentration in wheat. This might be attributed to the synergism of Zn to grain Cd when the application rate at some specific level. In addition, our results showed that the proper application of the foliar Zn fertilizer reduced the values of and for Cd more than spraying with deionized water only, indicating that application of the foliar Zn fertilizer could reduce the health risks of Cd from the consumption of food produced from Cd-contaminated soils. Although the value of Cd was lower than 1 under all treatments, the risk of exceeding the safe standard is not eliminated, as contaminated food could be consumed for longer periods. Thus, the application of foliar Zn fertilizer, which could function efficiently in Cd-contaminated areas, should be paid more attention [43].
Due to the wide application of foliar nutrients, especially in the late growth stage of crop plants, it is necessary to study the effect of foliar nutrients on increasing grain quality. In the present study, it is noticeable that the optimum application of Zn fertilizers increased the grain Zn concentration in wheat in both cultivation years (Figure 4A). The target Zn concentration (45 mg/kg) in wheat grains was achieved via the application of all rates of the foliar Zn fertilizer (Figure 4A), meaning biofortification sufficient to prevent Zn deficiency in humans could be achieved [44]. Consistent with our results, Olsen and Palmgren [45] also suggested that the re-translocation of Zn from leaves into developing grains via the phloem could be readily promoted after foliar application of Zn at the late flowering stage. Ca, Fe and Mn are also important minerals in the human body [22]. Our results showed that the grain Zn, Ca, Fe and Mn concentrations varied with the application rates of the foliar Zn fertilizer in Cd-contaminated soil, which could be ascribed to the antagonistic effect of Zn, Ca, Fe and Mn with Cd [29,46] and the synergistic effect of Ca, Fe and Mn with Zn [22]. This might be due to Zn, Ca, Fe, Mn and Cd sharing the same transmembrane transporter mechanisms and competing for the same binding sites in phytochelatins during phloem transport, such as YSL, ZIP, NRAMP, HMA, etc. However, the existing results from previous research are conflicting [46], which might be attributed to the discrepancies in wheat genotype, environmental conditions and/or type, dosage and timing of fertilization [22].
As a structural and catalytic component of protein for normal growth and development, Zn plays a vital role in the processes of protein synthesis [47]. The current study reveals that the external Zn supply increased the TPC on account of the increased Zn concentration, which is similar to previous research [28]. PA functions as a store of P and energy and plays an important role in plant growth and development [48]. The investigation by Erdal et al. [49] showed that Zn biofortification decreased grain PAC in 20 wheat cultivars, which may be ascribed to the dilution effect of increasing grain yield. However, in the current study, the application of different rates of the foliar Zn fertilizer uncharacteristically increased grain PAC in both cultivation years. This discrepancy could be explained by the differences in wheat genotype, environmental conditions and application period [22]. Unfortunately, to a certain extent PA is thought to be an antinutrient that reduces the bioavailability of mineral elements, especially Fe and Zn [24]. Considering the inhibition of PA on the absorption of mineral elements, element bioavailability in the human diet is thought to be an important index for evaluating biofortification [50]. Scientists recently developed a trivariate model of Zn absorption as a function of dietary Zn (accounting for 80% of the variability in the quantity of Zn absorption) [25]. Since Zn and phosphorus/PA share a common transport channel, indicating an inhibition of phosphorus/PA transport to the grains due to the increased Zn concentration, the optimum application of the foliar Zn fertilizer obviously increased the estimated Zn bioavailability because of the increased grain Zn concentration and the subsequent grain PAC decrease.
Accordingly, our results indicated that the optimal application of the foliar Zn fertilizer could achieve the safe production of wheat as well as crop biofortification. Similarly, Lian et al. [29] showed that that foliar spraying with Glyzinc could be an effective supplement to mitigate Cd accumulation in wheat grains during Zn biofortification. Therefore, based on the corresponding standard, the optimum application of the foliar Zn fertilizer in our research is an operative and practical interim measure to alleviate Cd health risks as well as maintain grain nutritional quality that could be applied in soils that are slightly Cd contaminated and where wheat is the main food source.
5. Conclusions
Field trials were performed in two consecutive years to evaluate the influence of foliar Zn fertilizer on Cd minimization and microelement biofortification in wheat. The results indicated that the appropriate application of the foliar Zn fertilizer could decrease the grain Cd concentration. At the same time, the nutritional quality in wheat grains was improved with increased Zn, Ca, Fe and Mn concentrations and total protein contents, as well as Zn, Ca, Fe and Mn bioavailability. Overall, these results highlight the great potential for Cd minimization and “hidden hunger” alleviation of the foliar Zn fertilizer in developing countries. However, little knowledge is available on the absorption and translocation mechanisms in wheat following the application of the foliar Zn fertilizer. Further and more in-depth work through a hydroponic experiment is necessary to advance this issue.
Conceptualization of work and validation by M.L. and X.Y. Methodology and investigation by Y.L. and Z.H. Data curation and formal analysis performed by Y.F. and B.Q. The article was organized and revised by M.L., Y.L., Y.F., B.Q., Z.H., X.Y. and C.Y. Project administration, resources and funding achieved by M.L., X.Y. and C.Y. All authors have read and agreed to the published version of the manuscript.
All data are available within the text or
The authors declare no conflicts of interest.
Footnotes
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Enlarge this image.Figure 1. Element composition analysis and the corresponding energy dispersive X-ray spectra (EDS) graphs of the stock solution of the foliar Zn fertilizer.
Enlarge this image.Figure 2. Cd concentrations in the different tissues of wheat with different treatments in two consecutive years. (A) Cd concentrations in grain, (B) Cd concentrations in glume, (C) Cd concentrations in leaf, (D) Cd concentrations in stem and (E) Cd concentrations in root. Data are the means of three replicates and error bars represent the standard error. Different letters at the top of the bars indicate significant differences among the treatments at the p < 0.05 level. * and ** indicate significant differences between the two cultivation years at the p < 0.05 and p < 0.01 levels, respectively. T1: control, application of deionized water; T2: application of the 1000-fold dilution of the foliar Zn fertilizer; T3: application of the 750-fold dilution of the foliar Zn fertilizer; T4: application of the 500-fold dilution of the foliar Zn fertilizer; and T5: application of the 250-fold dilution of the foliar Zn fertilizer.
Enlarge this image.Figure 3. Cd translocation factors (TFs) of wheat with different treatments in two consecutive years. (A) TFGrain/Root, (B) TFLeaf/Root, (C) TFStem/Root, (D) TFGrain/Glume, (E) TFGrain/Leaf and (F) TFGrain/Stem. Data are the means of three replicates and error bars represent the standard error. Different letters at the top of the bars indicate significant differences among the treatments at the p < 0.05 level. * and ** indicate significant differences between the two cultivation years at the p < 0.05 and p < 0.01 levels, respectively. T1: control, application of deionized water; T2: application of the 1000-fold dilution of the foliar Zn fertilizer; T3: application of the 750-fold dilution of the foliar Zn fertilizer; T4: application of the 500-fold dilution of the foliar Zn fertilizer; and T5: application of the 250-fold dilution of the foliar Zn fertilizer.
Enlarge this image.Figure 4. Mineral element concentrations (histogram) and bioavailability of wheat grains (line graph) with different treatments in two consecutive years. (A) Zn concentrations and the estimated Zn bioavailability, (B) Ca concentrations and PA/Ca molar ratio, (C) Fe concentrations and PA/Fe molar ratio and (D) Mn concentrations and PA/Mn molar ratio. Data are the means of three replicates and error bars represent the standard error. Different letters at the top of the bars indicate significant differences among the treatments at the p < 0.05 level. * and ** indicate significant differences between the two cultivation years at the p < 0.05 and p < 0.01 levels, respectively. T1: control, application of deionized water; T2: application of the 1000-fold dilution of the foliar Zn fertilizer; T3: application of the 750-fold dilution of the foliar Zn fertilizer; T4: application of the 500-fold dilution of the foliar Zn fertilizer; and T5: application of the 250-fold dilution of the foliar Zn fertilizer. PA, phytic acid.
Enlarge this image.Figure 5. Nutritional quality of wheat grains with different treatments in two consecutive years. (A) Phytic acid content. (B) Total protein content. Data are the means of three replicates and error bars represent the standard error. Different letters at the top of the bars indicate significant differences among the treatments at the p < 0.05 level. ** indicate significant differences between the two cultivation years at the p < 0.01 level. T1: control, application of deionized water; T2: application of the 1000-fold dilution of the foliar Zn fertilizer; T3: application of the 750-fold dilution of the foliar Zn fertilizer; T4: application of the 500-fold dilution of the foliar Zn fertilizer; and T5: application of the 250-fold dilution of the foliar Zn fertilizer.
Grain yield (kg/ha) of wheat as affected by different application rates of the foliar Zn fertilizer in two consecutive years.
| T1 | T2 | T3 | T4 | T5 | |
|---|---|---|---|---|---|
| The first year | 3241 ± 76.2 b | 2520 ± 20.2 d | 2878 ± 31.1 c | 3402 ± 16.4 a | 3422 ± 26.6 a |
| The second year | 3283 ± 75.0 bc | 3340 ± 26.0 bc ** | 2960 ± 107 c | 3622 ± 134 ab | 3870 ± 184 a |
Data are means of three replicates and error bars represent standard error. Different letters indicate significant differences among all treatments at p < 0.05 level. ** indicate significant differences between the two cultivation years at the p < 0.01 level. T1: control, application of deionized water; T2: application of the 1000-fold dilution of the foliar Zn fertilizer; T3: application of the 750-fold dilution of the foliar Zn fertilizer; T4: application of the 500-fold dilution of the foliar Zn fertilizer; and T5: application of the 250-fold dilution of the foliar Zn fertilizer.
Daily intake of metals (
| Adults | Children | Infants | |||||
|---|---|---|---|---|---|---|---|
| The First Year | The Second Year | The First Year | The Second Year | The First Year | The Second Year | ||
| | T1 | 6.55 × 10−5 ± 6.98 × 10−7 b | 8.46 × 10−5 ± 3.06 × 10−7 a | 7.26 × 10−5 ± 7.75 × 10−7 b | 9.38 × 10−5 ± 3.39 × 10−7 a | 5.85 × 10−5 ± 6.24 × 10−7 b | 7.55 × 10−5 ± 2.73 × 10−7 a |
| T2 | 4.17 × 10−5 ± 3.39 × 10−7 d | 4.00 × 10−5 ± 9.26 × 10−8 d | 4.62 × 10−5 ± 3.76 × 10−7 d | 4.44 × 10−5 ± 1.03 × 10−7 d | 3.72 × 10−5 ± 3.02 × 10−7 d | 3.57 × 10−5 ± 8.27 × 10−8 d | |
| T3 | 6.22 × 10−5 ± 8.88 × 10−7 c | 6.46 × 10−5 ± 5.71 × 10−7 b | 6.90 × 10−5 ± 9.85 × 10−7 c | 7.17 × 10−5 ± 6.34 × 10−7 b | 5.55 × 10−5 ± 7.93 × 10−7 c | 5.77 × 10−5 ± 5.10 × 10−7 b | |
| T4 | 4.07 × 10−5 ± 5.09 × 10−7 d | 4.72 × 10−5 ± 4.75 × 10−7 c | 4.52 × 10−5 ± 5.64 × 10−7 d | 5.24 × 10−5 ± 5.27 × 10−7 c | 3.64 × 10−5 ± 4.54 × 10−7 d | 4.22 × 10−5 ± 4.24 × 10−7 c | |
| T5 | 9.51 × 10−5 ± 9.76 × 10−7 a | 8.35 × 10−5 ± 1.17 × 10−6 a | 1.05 × 10−4 ± 1.08 × 10−6 a | 9.26 × 10−5 ± 1.30 × 10−6 a | 8.49 × 10−5 ± 8.72 × 10−7 a | 7.45 × 10−5 ± 1.04 × 10−6 a | |
| | T1 | 6.55 × 10−2 ± 6.98 × 10−4 b | 8.46 × 10−2 ± 3.06 × 10−4 a | 7.26 × 10−2 ± 7.75 × 10−4 b | 9.38 × 10−2 ± 3.39 × 10−4 a | 5.85 × 10−2 ± 6.24 × 10−4 b | 7.55 × 10−2 ± 2.73 × 10−4 a |
| T2 | 4.17 × 10−2 ± 3.39 × 10−4 d | 4.00 × 10−2 ± 9.26 × 10−5 d | 4.62 × 10−2 ± 3.76 × 10−4 d | 4.44 × 10−2 ± 1.03 × 10−4 d | 3.72 × 10−2 ± 3.02 × 10−4 d | 3.57 × 10−2 ± 8.27 × 10−5 d | |
| T3 | 6.22 × 10−2 ± 8.88 × 10−4 c | 6.46 × 10−2 ± 5.71 × 10−4 b | 6.90 × 10−2 ± 9.85 × 10−4 c | 7.17 × 10−2 ± 6.34 × 10−4 b | 5.55 × 10−2 ± 7.93 × 10−4 c | 5.77 × 10−2 ± 5.10 × 10−4 b | |
| T4 | 4.07 × 10−2 ± 5.09 × 10−4 d | 4.72 × 10−2 ± 4.75 × 10−4 c | 4.52 × 10−2 ± 5.64 × 10−4 d | 5.24 × 10−2 ± 5.27 × 10−4 c | 3.64 × 10−2 ± 4.54 × 10−4 d | 4.22 × 10−2 ± 4.24 × 10−4 c | |
| T5 | 9.51 × 10−2 ± 9.76 × 10−4 a | 8.35 × 10−2 ± 1.17 × 10−3 a | 10.55 × 10−2 ± 1.08 × 10−3 a | 9.26 × 10−2 ± 1.30 × 10−3 a | 8.49 × 10−2 ± 8.72 × 10−4 a | 7.45 × 10−2 ± 1.04 × 10−3 a | |
Data are the means of three replicates and error bars represent the standard error. Different letters indicate significant differences among all treatments at the p < 0.05 level. T1: control, application of deionized water; T2: application of the 1000-fold dilution of the foliar Zn fertilizer; T3: application of the 750-fold dilution of the foliar Zn fertilizer; T4: application of the 500-fold dilution of the foliar Zn fertilizer; and T5: application of the 250-fold dilution of the foliar Zn fertilizer.
Supplementary Materials
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References
1. Zhao, F.J.; Ma, Y.B.; Zhu, Y.G.; Tang, Z.; McGrath, S.P. Soil contamination in China: Current status and mitigation strategies. Environ. Sci. Technol.; 2015; 49, pp. 750-759. [DOI: https://dx.doi.org/10.1021/es5047099] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/25514502]
2. Cakmak, I. Enrichment of cereal grains with zinc: Agronomic or genetic biofortification?. Plant Soil; 2008; 302, pp. 1-17. [DOI: https://dx.doi.org/10.1007/s11104-007-9466-3]
3. Saifullah,; Sarwar, N.; Bibi, S.; Ahmad, M.; Ok, Y.S. Effectiveness of zinc application to minimize cadmium toxicity and accumulation in wheat (Triticum aestivum L.). Environ. Earth Sci.; 2014; 71, pp. 1663-1672. [DOI: https://dx.doi.org/10.1007/s12665-013-2570-1]
4. Ali, S.; Mfarrej, M.F.B.; Hussain, A.; Akram, N.A.; Rizwan, M.; Wang, X.; Maqbool, A.; Nafees, M.; Ali, B. Zinc fortification and alleviation of cadmium stress by application of lysine chelated zinc on different varieties of wheat and rice in cadmium stressed soil. Chemosphere; 2022; 295, 133829. [DOI: https://dx.doi.org/10.1016/j.chemosphere.2022.133829] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/35120959]
5. Naveed, M.; Saifullah,; Riaz, U.; Murtaza, G.; Bibi, S.; Arooj, A.; Zaman, Q.U. Strategic use of water: A step toward cadmium-free basmati rice (Oryza sativa L.). Paddy Water Environ.; 2018; 16, pp. 867-873. [DOI: https://dx.doi.org/10.1007/s10333-018-0675-6]
6. Seyfferth, A.L.; Amaral, D.; Limmer, M.A.; Guilherme, L.R.G. Combined impacts of Si-rich rice residues and flooding extent on grain As and Cd in rice. Environ. Int.; 2019; 128, pp. 301-309. [DOI: https://dx.doi.org/10.1016/j.envint.2019.04.060] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/31077999]
7. Niu, J.H.; Liu, C.; Huang, M.L.; Liu, K.Z.; Yan, D.Y. Effects of foliar fertilization: A review of current status and future perspectives. J. Soil Sci. Plant Nut.; 2021; 21, pp. 104-118. [DOI: https://dx.doi.org/10.1007/s42729-020-00346-3]
8. Wu, C.; Dun, Y.; Zhang, Z.J.; Li, M.L.; Wu, G.Q. Foliar application of selenium and zinc to alleviate wheat (Triticum aestivum L.) cadmium toxicity and uptake from cadmium-contaminated soil. Ecotoxicol. Environ. Saf.; 2020; 190, 110091. [DOI: https://dx.doi.org/10.1016/j.ecoenv.2019.110091]
9. Wang, F.J.; Tan, H.F.; Huang, L.H.; Cai, C.; Ding, Y.F.; Bao, H.; Chen, Z.X.; Zhu, C. Application of exogenous salicylic acid reduces Cd toxicity and Cd accumulation in rice. Ecotoxicol. Environ. Saf.; 2021; 207, 111198. [DOI: https://dx.doi.org/10.1016/j.ecoenv.2020.111198]
10. Xie, R.H.; Zhao, J.Q.; Lu, L.L.; Ge, J.; Brown, P.H.; Wei, S.; Wang, R.Z.; Qiao, Y.B.; Webb, S.M.; Tian, S.K. Efficient phloem remobilization of Zn protects apple trees during the early stages of Zn deficiency. Plant Cell Environ.; 2019; 42, pp. 3167-3181. [DOI: https://dx.doi.org/10.1111/pce.13621]
11. Hussain, S.; Khan, A.M.; Rengel, Z. Zinc-biofortified wheat accumulates more cadmium in grains than standard wheat when grown on cadmium-contaminated soil regardless of soil and foliar zinc application. Sci. Total Environ.; 2019; 654, pp. 402-408. [DOI: https://dx.doi.org/10.1016/j.scitotenv.2018.11.097] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/30447578]
12. Du, J.; Zeng, J.; Ming, X.Y.; He, Q.L.; Tao, Q.; Jiang, M.Y.; Gao, S.P.; Li, X.; Lei, T.; Pan, Y.Z. et al. The presence of zinc reduced cadmium uptake and translocation in Cosmos bipinnatus seedlings under cadmium/zinc combined stress. Plant Physiol. Biochem.; 2020; 151, pp. 223-232. [DOI: https://dx.doi.org/10.1016/j.plaphy.2020.03.019] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/32234661]
13. Velu, G.; Ortiz-Monasterio, I.; Cakmak, I.; Hao, Y.; Singh, R.P. Biofortification strategies to increase grain zinc and iron concentrations in wheat. J. Cereal Sci.; 2014; 59, pp. 365-372. [DOI: https://dx.doi.org/10.1016/j.jcs.2013.09.001]
14. Dapkekar, A.; Deshpande, P.; Oak, M.D.; Paknikar, K.M.; Rajwade, J.M. Zinc use efficiency is enhanced in wheat through nanofertilization. Sci. Rep.; 2018; 8, 6832. [DOI: https://dx.doi.org/10.1038/s41598-018-25247-5] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/29717180]
15. De Almeida, H.J.; Carmona, V.M.V.; Inocencio, M.F.; Neto, A.E.F.; Mauad, M. Zinc application improves the yield and nutritional quality of three green bean genotypes grown in a Red Latosol. Sci. Hortic.; 2020; 274, 109636. [DOI: https://dx.doi.org/10.1016/j.scienta.2020.109636]
16. Lian, J.P.; Cheng, L.P.; Zhai, X.; Wu, R.F.; Huang, X.W.; Chen, D.; Pan, J.Q.; Shohag, M.J.I.; Xin, X.P.; Ren, X.W. et al. Zinc glycerolate (Glyzinc): A novel foliar fertilizer for zinc biofortification and cadmium reduction in wheat (Triticum aestivum L.). Food Chem.; 2023; 402, 134290. [DOI: https://dx.doi.org/10.1016/j.foodchem.2022.134290]
17. Xu, M.; Liu, M.J.; Si, L.L.; Ma, Q.X.; Sun, T.; Wang, J.; Chen, K.J.; Wang, X.J.; Wu, L.H. Spraying high concentrations of chelated zinc enhances zinc biofortification in wheat grain. J. Sci. Food Agric.; 2022; 102, pp. 3590-3598. [DOI: https://dx.doi.org/10.1002/jsfa.11705]
18. Hussain, A.; Rizwan, M.; Ali, S.; Rehman, M.Z.U.; Qayyum, M.F.; Nawaz, R.; Ahmad, A.; Asrar, M.; Ahmad, S.R.; Alsahli, A.A. et al. Combined use of different nanoparticles effectively decreased cadmium (Cd) concentration in grains of wheat grown in a field contaminated with Cd. Ecotoxicol. Environ. Saf.; 2021; 215, 112139. [DOI: https://dx.doi.org/10.1016/j.ecoenv.2021.112139]
19. Tang, L.; Hamid, Y.; Liu, D.; Shohag, M.J.I.; Zehra, A.; He, Z.L.; Feng, Y.; Yang, X.E. Foliar application of zinc and selenium alleviates cadmium and lead toxicity of water spinach-Bioavailability/cytotoxicity study with human cell lines. Environ. Int.; 2020; 145, 106122. [DOI: https://dx.doi.org/10.1016/j.envint.2020.106122]
20.
21. Ghasemi, S.; Khoshgoftarmanesh, A.H.; Afyuni, M.; Hadadzadeh, H. The effectiveness of foliar applications of synthesized zinc-amino acid chelates in comparison with zinc sulfate to increase yield and grain nutritional quality of wheat. Eur. J. Agron.; 2013; 45, pp. 68-74. [DOI: https://dx.doi.org/10.1016/j.eja.2012.10.012]
22. Lu, M.; Cao, X.R.; Pan, J.Q.; Gurajala, H.K.; He, Z.L.; Yang, X.E.; Khan, M.B. Genotypic variations in zinc accumulation and bioaccessibility among wheat (Triticum aestivum L.) genotypes under two different field conditions. J. Cereal Sci.; 2020; 93, 102953. [DOI: https://dx.doi.org/10.1016/j.jcs.2020.102953]
23. Liu, Z.H.; Cheng, F.M.; Zhang, G.P. Grain phytic acid content in japonica rice as affected by cultivar and environment and its relation to protein content. Food Chem.; 2005; 89, pp. 49-52. [DOI: https://dx.doi.org/10.1016/j.foodchem.2004.01.081]
24. Liu, D.Y.; Liu, Y.M.; Zhang, W.; Chen, X.P.; Zou, C.Q. Agronomic approach of zinc biofortification can increase zinc bioavailability in wheat flour and thereby reduce zinc deficiency in humans. Nutrients; 2017; 9, 465. [DOI: https://dx.doi.org/10.3390/nu9050465] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/28481273]
25. Hambidge, K.M.; Miller, L.V.; Westcott, J.E.; Sheng, X.; Krebs, N.F. Zinc bioavailability and homeostasis. Am. J. Clin. Nutr.; 2010; 91, pp. 1478S-1483S. [DOI: https://dx.doi.org/10.3945/ajcn.2010.28674I] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/20200254]
26. Mahmood, A.; Malik, R.N. Human health risk assessment of heavy metals via consumption of contaminated vegetables collected from different irrigation sources in Lahore, Pakistan. Arab. J. Chem.; 2014; 7, pp. 91-99. [DOI: https://dx.doi.org/10.1016/j.arabjc.2013.07.002]
27. Zhong, J.M.; Yu, M.; Liu, L.Q.; Chen, Y.P.; Hu, R.Y.; Gong, W.W. Study on the dietary nutrition intake level in Zhejiang Province. Dis. Surveill.; 2006; 21, pp. 670-672. (In Chinese)
28. Tang, L.; Hamid, Y.; Zehra, A.; Shohag, M.J.I.; He, Z.L.; Yang, X.E. Endophytic inoculation coupled with soil amendment and foliar inhibitor ensure phytoremediation and argo-production in cadmium contaminated soil under oilseed rape-rice rotation system. Sci. Total Environ.; 2020; 748, 142481. [DOI: https://dx.doi.org/10.1016/j.scitotenv.2020.142481]
29. Lian, J.P.; Cheng, L.P.; Zhai, X.; Wu, R.F.; Liu, W.T.; Pan, J.Q.; Shohag, M.J.I.; Xin, X.P.; He, Z.L.; Yang, X.E. Foliar spray of combined metal-oxide nanoparticles alters the accumulation, translocation and health risk of Cd in wheat (Triticum aestivum L.). J. Hazard. Mater.; 2022; 440, 129857. [DOI: https://dx.doi.org/10.1016/j.jhazmat.2022.129857]
30. Zhen, S.; Shuai, H.; Xu, C.; Lv, G.H.; Zhu, X.D.; Zhang, Q.; Zhu, Q.H.; Núñez-Delgado, A.; Conde-Cid, M.; Zhou, Y.Y. et al. Foliar application of Zn reduces Cd accumulation in grains of late rice by regulating the antioxidant system, enhancing Cd chelation onto cell wall of leaves, and inhibiting Cd translocation in rice. Sci. Total Environ.; 2021; 770, 145302. [DOI: https://dx.doi.org/10.1016/j.scitotenv.2021.145302]
31. Manzoor, N.; Ahmed, T.; Noman, M.; Shahid, M.; Nazir, M.M.; Ali, L.; Alnusaire, T.S.; Li, B.; Schulin, R.; Wang, G. Iron oxide nanoparticles ameliorated the cadmium and salinity stresses in wheat plants, facilitating photosynthetic pigments and restricting cadmium uptake. Sci. Total Environ.; 2021; 769, 145221. [DOI: https://dx.doi.org/10.1016/j.scitotenv.2021.145221]
32. Yang, J.Y.; Chen, X.; Lu, W.C.; Chen, R.C.; Liu, M.N.; Yao, H.L.; Li, J.H.; Hong, J.L.; Mao, X.Y. Reducing Cd accumulation in rice grain with foliar application of glycerol and its mechanisms of Cd transport inhibition. Chemosphere; 2020; 258, 127135. [DOI: https://dx.doi.org/10.1016/j.chemosphere.2020.127135] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/32535432]
33. Ali, W.; Mao, K.; Zhang, H.; Junaid, M.; Xu, N.; Rasool, A.; Feng, X.; Yang, Z. Comprehensive review of the basic chemical behaviours, sources, processes, and endpoints of trace element contamination in paddy soil-rice systems in rice-growing countries. J. Hazard. Mater.; 2020; 397, 122720. [DOI: https://dx.doi.org/10.1016/j.jhazmat.2020.122720] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/32387828]
34. Cao, X.S.; Yue, L.; Wang, C.X.; Luo, X.; Zhang, C.C.; Zhao, X.L.; Wu, F.C.; White, J.C.; Wang, Z.Y.; Xing, B.S. Foliar application with iron oxide nanomaterials stimulate nitrogen fixation, yield, and nutritional quality of soybean. ACS Nano; 2022; 16, pp. 1170-1181. [DOI: https://dx.doi.org/10.1021/acsnano.1c08977] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/35023717]
35. Sarwar, N.; Saifullah,; Malhi, S.S.; Zia, M.H.; Naeem, A.; Bibi, S.; Farid, G. Role of mineral nutrition in minimizing cadmium accumulation by plants. J. Sci. Food Agric.; 2010; 90, pp. 925-937. [DOI: https://dx.doi.org/10.1002/jsfa.3916]
36. Liu, Y.L.; Yu, X.F.; Feng, Y.M.; Zhang, C.; Wang, C.; Zeng, J.; Huang, Z.; Kang, H.Y.; Fan, X.; Sha, L.N. et al. Physiological and transcriptome response to cadmium in cosmos (Cosmos bipinnatus Cav.) seedlings. Sci. Rep.; 2017; 7, 14691. [DOI: https://dx.doi.org/10.1038/s41598-017-14407-8] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/29089633]
37. Takahashi, R.; Ishimaru, Y.; Shimo, H.; Ogo, Y.; Senoura, T.; Nishizawa, N.K.; Nakanishi, H. The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice. Plant Cell Environ.; 2012; 35, pp. 1948-1957. [DOI: https://dx.doi.org/10.1111/j.1365-3040.2012.02527.x] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/22548273]
38. Sasaki, A.; Yamaji, N.; Ma, J.F. Overexpression of OsHMA3 enhances Cd tolerance and expression of Zn transporter genes in rice. J. Exp. Bot.; 2014; 65, pp. 6013-6021. [DOI: https://dx.doi.org/10.1093/jxb/eru340]
39. Tan, L.T.; Zhu, Y.X.; Fan, T.; Peng, C.; Wang, J.R.; Sun, L.; Chen, C.Y. OsZIP7 functions in xylem loading in roots and inter-vascular transfer in nodes to deliver Zn/Cd to grain in rice. Biochem. Biophys. Res. Commun.; 2019; 512, pp. 112-118. [DOI: https://dx.doi.org/10.1016/j.bbrc.2019.03.024]
40. Tian, S.Q.; Liang, S.; Qiao, K.; Wang, F.H.; Zhang, Y.X.; Chai, T.Y. Co-expression of multiple heavy metal transporters changes the translocation, accumulation, and potential oxidative stress of Cd and Zn in rice (Oryza sativa). J. Hazard. Mater.; 2019; 380, 120853. [DOI: https://dx.doi.org/10.1016/j.jhazmat.2019.120853]
41. Wang, Y.; Wang, X.; Wang, C.; Peng, F.; Wang, R.J.; Xiao, X.; Zeng, J.; Kang, H.Y.; Fan, X.; Sha, L.N. et al. Transcriptomic profiles reveal the interactions of Cd/Zn in dwarf polish wheat (Triticum polonicum L.) roots. Front. Physiol.; 2017; 8, 168. [DOI: https://dx.doi.org/10.3389/fphys.2017.00168]
42. Sarwar, N.; Ishaq, W.; Farid, G.; Shaheen, M.R.; Imran, M.; Geng, M.; Hussain, S. Zinc-cadmium interactions: Impact on wheat physiology and mineral acquisition. Ecotoxicol. Environ. Saf.; 2015; 122, pp. 528-536. [DOI: https://dx.doi.org/10.1016/j.ecoenv.2015.09.011] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/26426697]
43. Rizwan, M.; Ali, S.; Hussain, A.; Ali, Q.; Shakoor, M.B.; Zia-ur-Rehman, M.; Farid, M.; Asma, M. Effect of zinc-lysine on growth, yield and cadmium uptake in wheat (Triticum aestivum L.) and health risk assessment. Chemosphere; 2017; 187, pp. 35-42. [DOI: https://dx.doi.org/10.1016/j.chemosphere.2017.08.071] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/28834770]
44. Ortiz-Monasterio, J.I.; Palacios-Rojas, N.; Meng, E.; Pixley, K.; Trethowan, R.; Peña, R.J. Enhancing the mineral and vitamin content of wheat and maize through plant breeding. J. Cereal Sci.; 2007; 46, pp. 293-307. [DOI: https://dx.doi.org/10.1016/j.jcs.2007.06.005]
45. Olsen, L.I.; Palmgren, M.G. Many rivers to cross: The journey of zinc from soil to seed. Front. Plant Sci.; 2014; 5, 30. [DOI: https://dx.doi.org/10.3389/fpls.2014.00030] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/24575104]
46. Li, L.P.; Zhang, Y.Q.; Ippolito, J.A.; Xing, W.Q.; Qiu, K.Y.; Wang, Y.L. Cadmium foliar application affects wheat Cd, Cu, Pb and Zn accumulation. Environ. Pollut.; 2020; 262, 114329. [DOI: https://dx.doi.org/10.1016/j.envpol.2020.114329]
47. Zhang, L.; Yan, M.F.; Li, H.B.; Ren, Y.Y.; Siddique, K.H.M.; Chen, Y.L.; Zhang, S.Q. Effects of zinc fertilizer on maize yield and water-use efficiency under different soil water conditions. Field Crop Res.; 2020; 248, 107718. [DOI: https://dx.doi.org/10.1016/j.fcr.2020.107718]
48. Bohn, L.; Meyer, A.S.; Rasmussen, S.K. Phytate: Impact on environment and human nutrition. A challenge for molecular breeding. J. Zhejiang Univ. Sci. B; 2008; 9, pp. 165-191. [DOI: https://dx.doi.org/10.1631/jzus.B0710640]
49. Erdal, I.; Yilmaz, A.; Taban, S.; Eker, S.; Torun, B.; Cakmak, I. Phytic acid and phosphorus concentrations in seeds of wheat cultivars grown with and without zinc fertilization. J. Plant Nutr.; 2002; 25, pp. 113-127. [DOI: https://dx.doi.org/10.1081/PLN-100108784]
50. Hussain, S.; Maqsood, M.A.; Rengel, Z.; Aziz, T. Biofortification and estimated human bioavailability of zinc in wheat grains as influenced by methods of zinc application. Plant Soil; 2012; 361, pp. 279-290. [DOI: https://dx.doi.org/10.1007/s11104-012-1217-4]
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; Qi, Bin 3 ; He, Zhenli 4
; Yang, Xiaoe 2 1 State Key Laboratory of Nutrient Use and Management, Tea Research Institute, Shandong Academy of Agricultural Sciences, Jinan 250100, China;
2 Key Laboratory of Environmental Remediation and Ecosystem Health, Ministry of Education (MOE), College of Environmental and Resources Sciences, Zhejiang University, Hangzhou 310058, China
3 Shandong Institute of Pomology, Tai’an 271000, China
4 Department of Soil, Water and Ecosystem Sciences, Indian River Research and Education Center, University of Florida—IFAS, Fort Pierce, FL 34945, USA