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Article

Simultaneous Biofortification: Interaction between Zinc and Selenium Regarding Their Accumulation in Wheat

by
Lingxuan Kong
1,
Yanjin Tao
1,
Yang Xu
2,
Xuan Zhou
2,
Guohai Fu
2,
Lijie Zhao
1,
Qi Wang
1,
Huafen Li
1 and
Yanan Wan
1,*
1
Beijing Key Laboratory of Farmland Soil Pollution Prevention and Remediation, Key Laboratory of Plant-Soil Interactions of the Ministry of Education, College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, China
2
National Agro-Tech Extension and Service Center, Ministry of Agriculture and Rural Affairs, Beijing 100026, China
*
Author to whom correspondence should be addressed.
Agronomy 2024, 14(7), 1513; https://doi.org/10.3390/agronomy14071513
Submission received: 7 June 2024 / Revised: 7 July 2024 / Accepted: 10 July 2024 / Published: 12 July 2024
(This article belongs to the Special Issue Importance of Zn Fertilization: Biofortification of Food Crops and Soil Zn Status)
Browse Figures
Versions Notes

Abstract

:
Wheat (Triticum aestivum L.) is a staple food worldwide, and agronomic biofortification with selenium (Se) and zinc (Zn) is a simple and effective way to increase nutrient intake. This study aimed to evaluate the combined effects of Zn and Se on the biofortification of wheat grain. Zinc sulfate (ZnSO4·H2O, 1.74, 2.61 and 3.48 kg Zn hm−2) and sodium selenite (Na2SeO3, 15 and 30 g Se hm−2) were sprayed individually or simultaneously at key stages of wheat growth (the jointing, booting, and filling stage) under field conditions. On the basis of soil Zn application, the foliar application of Zn or Se alone greatly increased grain Zn by 12.07–71.88% (up to 41.66–64.30 mg kg−1), and grain Se content by 131.81–527.21% (up to 0.21–0.50 mg kg−1), while the soil application of Zn had little effect on grain Zn. Compared with the foliar application of Zn or Se alone, the co-application of Se increased the grain Zn content by 1.74–16.15%, while the co-application of Zn significantly reduced grain Se content by 25.43–86.34% and the effect was more pronounced with an increase in Zn dosage. Moreover, positive correlations were found between Zn and copper (Cu) in grains, and wheat grains could provide adequate dietary intakes of manganese (Mn), Cu, and molybdenum (Mo) for humans. In summary, the soil application of 11 kg Zn hm−2 combined with the foliar application of 2.61 kg Zn hm−2 and 30 g Se·hm−2 is a feasible Zn-Se co-enrichment strategy, which would provide the recommended nutrient intake (RNI) of 113.63–124.72% (female) and 68.18–74.84% (male) of Zn and 81.30–95.85% of Se.

1. Introduction

Zinc (Zn) and selenium (Se) are essential and beneficial trace elements for plants, respectively, but both are essential for humans. Zn deficiency may lead to growth retardation, with potential adverse effects on the human immune, nervous and reproductive systems [1]. A lack of Se also causes various diseases, such as Keshan disease and Kashin-beck disease [2]. However, approximately 17% and 15% of the world’s population is Zn- and Se-deficient, respectively [3,4]. Their deficiency is mainly attributed to an inadequate dietary intake of these elements. Wheat (Triticum aestivum L.) is a widely cultivated staple food globally, accounting for 22% of the world’s arable land, and provides nearly half of the daily calorie intake [5,6]. However, the Zn content in non-biofortified wheat grains is generally less than 30 mg kg−1 [7]. Similarly, with the exception of a few Se-rich regions, the Se content in wheat grains is typically low. The average content of Zn and Se in winter wheat grains are 30.3 and 0.06 mg kg−1, respectively, which are lower than the lowest biofortification targets of 40 mg Zn kg−1 and 0.1 mg Se kg−1 [6,8,9,10,11].
The low contents of Zn and Se in wheat grains are mainly caused by the deficiency of Zn and Se in soil. The diethylenetriaminepentaacetic acid extractable Zn (DTPA-Zn) contents in potential Zn-deficient soils range from 0.5 to 1.0 mg kg−1, and <0.5 mg kg−1 and >1.0 mg kg−1 are Zn-deficient and Zn-sufficient soils, respectively [12]. In alkaline soils, particularly those in which pH > 8, the binding capacities of soil iron oxide and calcite with Zn are strengthened, thereby resulting in a lower Zn availability of plants [13]. Most of the Se-deficient regions in China are distributed from northeast to southwest, whereas other such regions are scattered throughout China. In these regions, the soil Se content is typically <0.2 mg kg−1 [14]. Moreover, acidic soil and complexation with iron or aluminum also reduce the uptake of selenium by plants [2].
Crops generally absorb nutrients through roots or leaves, and agronomic biofortification such as soil application or foliar spraying techniques are considered to be effective methods to alleviate the deficiency of trace element in cereals [12]. Zn can be applied to soil to increase soil DTPA-Zn content, ameliorate soil Zn deficiency and increase crop yield, although the impact on increasing grain Zn content is not obvious [6]. However, foliar application can deliver supplemental nutrients directly to the crop leaves and thereby facilitate the efficient transport of Zn and Se to the grains through the xylem and phloem, thus avoiding the long-distance transportation from the roots. Foliar application also has high application efficiency, especially in the grain filling stage, and has a greater effect on grain Zn and Se enrichment [15].
The most economic and effective way to supplement the human daily intake of micronutrients is to consume Zn- and Se-enriched cereals. Many studies have indicated that the foliar application of Zn or Se alone could effectively increase the content of Zn or Se in cereals [16,17]. Furthermore, the combined foliar application of Zn and Se at an appropriate dosage may facilitate simultaneous fortification with Zn and Se. Previous studies have revealed that compared with foliar Se alone, co-supplementation with Zn increased the Se content of wheat grains [18]; this phenomenon was also found in peas (Pisum sativum L.) [19]. Conversely, Fand et al. [20] found that the addition of foliar Zn had no significant effect on the content of grain Se in rice (Oryza sativa L.). Likewise, an antagonistic effect of Se on Zn was discovered in rice [21], whereas no significant effect was found in wheat [18]. Since the interaction between Zn and Se is still unclear, it is meaningful to figure out how Zn and Se interact with each other. The interaction between Zn and Se may differ depending on crop species or cultivars, as well as the types and rates of fertilizer and the soil conditions [22], which deserves further study.
At present, most of the studies on wheat biofortification have focused on the impacts of the sole application of Zn or Se fertilizer, whereas their co-application has received comparatively little attention, and the interaction between Zn and Se remains somewhat controversial. Also, finding the optimal Zn-Se co-enrichment strategy in wheat could also help alleviate the problem of the inadequate intake of both Zn and Se in the population. Therefore, field experiments were set up in this study to explore the effects of the foliar spraying of Zn and Se on (1) the accumulation and transportation of Zn and Se in wheat; (2) the interaction of Zn and Se in their accumulation and transportation; (3) other elements contents (Mn, Cu, and Mo) in wheat grain, as well as to evaluate the efficiency of Zn and Se enrichment in grains, and the contribution of wheat grain to dietary Zn and Se intakes.

2. Materials and Methods

2.1. Site Description of Field Experiment

Field trials were conducted at two experimental sites in order to exclude the effects of chance and geographical differences in two sites (Figure 1). One was located in Quzhou Experimental Station, Hebei Province (36°51′ N, 115°0′ E), another in Shangzhuang Experimental Station, Beijing, China (40°14′ N, 116°19′ E). The average temperature during wheat cultivation in the Quzhou and Shangzhuang areas was 10.9 °C and 9.0 °C, respectively, and the total precipitation was 186.9 and 97.2 mm, respectively. The physical and chemical properties of soil in Quzhou were as follows: pH 8.77; cation exchange capacity (CEC), 9.00 cmol kg−1; total N, 0.58 g kg−1; available phosphorus (P), 21.98 mg kg−1; available potassium (K), 111.38 mg kg−1; organic matter (OM), 11.82 g kg−1; total Zn, 48.74 mg kg−1; DTPA-Zn, 0.53 mg kg−1; and total Se, 141.89 μg kg−1. The physical and chemical properties of soil in Beijing were as follows: pH 8.23; CEC, 12.15 cmol kg−1; total N, 0.53 g kg−1; available P, 18.27 mg kg−1; available K, 60.88 mg kg−1; OM, 12.90 g kg−1; total Zn, 61.94 mg kg−1; DTPA-Zn, 1.61 mg kg−1; and total Se, 73.06 μg kg−1.

2.2. Experimental Design

The wheat varieties in Quzhou and Shangzhuang Experimental Station are Longtang 2 and Zhongmai 175, respectively. The experiment included 27 plots, with an individual plot area of 80 m2 (Quzhou) and 40 m2 (Shangzhuang). The experimental treatments were as follows: (1) CK; (2) B; (3) B + Zn1; (4) B + Zn2; (5) B + Zn3; (6) B + Se1; (7) B + Se2; (8) B + Zn2 + Se2; and (9) B + Zn3 + Se2. Each treatment contained three repetitions. CK represents foliar spraying with water; B represents a soil application of 11 kg Zn hm−2 as ZnSO4·H2O prior to planting and foliar spraying with water; Zn1, Zn2 and Zn3 indicate foliar spraying with 1.74, 2.61, and 3.48 kg Zn hm−2 as ZnSO4·H2O, respectively; and Se1 and Se2 indicate foliar spraying with 15 and 30 g Se·hm−2 as Na2SeO3, respectively. A completely random arrangement was adopted, and protection rows were set around the experimental fields. The plots were plowed to a depth of 20 cm, and wheat was generally sown in early October. The foliar spraying of Zn and Se fertilizer was conducted at the jointing, booting and filling stages using a motorized backpack sprayer. The Zn and Se fertilizer were dissolved in water with a dosage of 800 L hm−2 and added with 0.01% surfactant (Tween 20). Conventional field managements practices, such as weeding, irrigation and pest control, were conducted during the growing stage.

2.3. Sample Collection and Analysis

At maturity, the above-ground wheat plants from an area of 4 m2 per plot were collected, which were then threshed to separate the grain from the straw/husk for determining the yield. Additionally, in each plot, five randomly selected plants per plot were collected, which were then divided into grains, husks, and straw. After rinsing with deionized water, these samples were oven-dried at 75 °C to a constant weight and then ground using a stainless steel grinder for subsequent elemental determinations.
Plant samples (0.2500 g) were digested with 8 mL of HNO3 (GR) using a graphite digester (Digiblock ED54, LabTech, Beijing, China). The digests were then diluted with highly pure water and filtered. For the determination of Se, 1 mL of HCl/H2O (v:v = 1:1) was added to 4 mL of diluted digest and bathed for 2 h at 98 °C water. The concentration of total Se was determined using atomic fluorescence spectrometer (AFS-920, Jitian Instruments, Beijing, China), whereas the concentration of Zn, Mn, Cu, and Mo were determined using inductively coupled plasma mass spectrometry (ICP-MS 7700, Agilent Technologies, Santa Clara, CA, USA). Blank and certified reference material (GBW10049) were included in each batch for quality control and the recoveries was 87–115%.

2.4. Data Analysis

All results are presented on a dry weight basis. The transfer factors (TFs) were used to evaluate the transport capacity of elements between different parts of wheat. Recovery of basal (RB) and foliar (RF) application were used to evaluate soil or leaf fertilizer utilization efficiency in the different parts of wheat. Daily intake (DI) was estimated according to the daily consumption of wheat grains per person and the contents of Zn, Se, Mn, Cu, and Mo in wheat grains. The contribution rate (CR) reflects the degree of the contribution of wheat to the dietary intake of Zn, Se, Mn, Cu, and Mo. The formulae used for calculations were as follows:
TFs = Ci/Cj
where Ci and Cj (mg kg−1) represent the contents Zn or Se in different wheat tissues, and i and j represent the different parts of wheat (grain, husk, and straw).
RBZn (%) = (CB × YB − CC × YC) × 100/BZn
RFZn/Se (%) = (CF × YF − CB × YB) × 100/FZn/Se
where CB, CF, and CC (mg kg−1) are the Zn or Se content in different parts of wheat under soil Zn application, foliar Zn or Se application, and the control, respectively. YB, YF, and YC (t hm−2) are the yield of wheat, with the yield of straw being estimated based on the grain to straw ratio of 1.366 [23]. BZn and FZn/Se (g hm−2) are the fertilizer input of soil Zn and the foliar application of Zn or Se, respectively.
DI (mg day−1 person−1) = C × 172.9/1000
where C represents the contents of Zn, Se, Mn, Cu, and Mo (mg kg−1) in wheat grains; 172.9 (g day−1 person−1) is the consumption of wheat flour per day per person [24].
CR (%) = DI × 100/RNI
where RNI represents the recommended nutrient intake of an adult for Zn (7.5 and 12.5 mg day−1 for females and males, respectively), Se (60 μg day−1), Mn (4.5 mg day−1), Cu (0.8 mg day−1), and Mo (0.1 mg day−1) according to the recommended nutrient intake (Zn, Se, Cu and Mo) of the Chinese dietary reference intakes [25] or the appropriate intake (Mn) of the Dietary Guidelines for Chinese residents [26].

2.5. Statistical Analysis

All data are presented as mean values ± standard error (n = 3). One-way analysis of variance was performed using IBM SPSS Statistics 26 (SPSS, Inc., Chicago, IL, USA). Duncan test (p < 0.05) was used to compare the mean values between different treatments.

3. Results

3.1. Zn and Se Contents in Grain, Husk, and Straw

The yields of wheat grains were not significantly affected by the soil Zn application or combined foliar spraying of Zn and Se in Quzhou and Shangzhuang, which were 7.10–9.82 t hm−2 and 6.54–7.72 t hm−2, respectively (Tables S1 and S5).
Compared with the control, all treatments promoted the accumulation of Zn in different parts of wheat in two sites (Figure 2a–c). Without foliar Zn treatment, the Zn content of the different wheat tissues followed the order grain > husk > straw, and the treatments, including foliar-applied Zn, followed the order husk > grain > straw. Although the soil application of 11 kg Zn hm−2 (B) had no significant effects on the Zn content of grain, it did promote an increase in the Zn content in the husk and straw. On the basis of soil Zn application, regardless of whether it was combined with foliar Se, the foliar application of Zn obviously increased the Zn content in the grain, husk and straw of wheat at two sites, and the Zn content increased with increasing spraying concentration. Under treatment based on the sole foliar application of Zn, the highest grain Zn content was detected in B + Zn3 treatment, with increases of 30.80% and 71.88% compared with the control in Quzhou and Shangzhuang, respectively, up to 44.23 and 64.30 mg kg−1. Compared with the spraying of Zn alone, the combined foliar application of Zn and Se increased the grain Zn content by 12.04–16.15% in Quzhou. In addition, increases in Zn content were also found in the husk and straw, particularly in the treatment of spraying high doses of Zn.
On the basis of soil Zn, the foliar application of Zn, Se, and their combination significantly affected Se content in the different parts of wheat (Figure 2d–f). Compared with the control, foliar Se applied alone or in combination with Zn increased the Se content in wheat grain, husk, and straw, with increases of 5.80–396.17% and 228.12–527.21% for grain Se content in Quzhou and Shangzhuang (except for B + Zn3 + Se2), respectively, up to 0.10–0.45 mg kg−1 and 0.26–0.50 mg kg−1. Furthermore, relative to foliar spraying with Se alone (B + Se2), the combined foliar application of Zn and Se significantly decreased the Se content in wheat grain by 25.43–78.68% and 43.21–86.34% in Quzhou and Shangzhuang, respectively, with the effects becoming more pronounced with an increase in Zn dosage. Contrastingly, compared with foliar application of Se alone, the combined application with Zn increased the Se content of the husk and straw. Except for B + Zn3 + Se2, the treatments containing the foliar application of Se exceeded the recommend value for the grain Se of wheat (0.1–0.5 mg kg−1) [11].
There was a significant positive correlation between the Zn or Se foliar application rates and the Zn or Se content in wheat grain (Figure 3a,b). According to the relational model, the content of Zn in grain increased by 1.45 and 7.56 mg kg−1 in response to the foliar application of 1 kg Zn hm−2 as ZnSO4·H2O in Quzhou and Shangzhuang, respectively, and similarly, the content of Se in grain increased by 0.012 mg kg−1 and 0.014 mg kg−1 in response to the foliar application of 1 g Se hm−2 as Na2SeO3. Moreover, on the basis of soil Zn, wheat cultivated in Quzhou and Shangzhuang should be sprayed with at least 0.68 and 0.45 kg Zn hm−2 to reach the Zn biofortification goal of grain (40 mg kg−1), and 2.50 g Se hm−2 and 2.36 g Se hm−2 should be sprayed to reach the Se biofortification goal of grain (0.1–0.5 mg kg−1), respectively.

3.2. Transfer Factors

All treatments decreased the TFs of Zn from husk to grain, with the effects being more pronounced for foliar-applied Zn than for soil-applied Zn (Table 1 and Table S5). Specifically, the TFs were reduced by 15.92% and 45.43% under soil Zn treatment in Quzhou and Shangzhuang, respectively, whereas corresponding reductions of 44.66–72.33% and 73.88–77.14% were shown under the treatment containing foliar Zn (B + Zn and B + Zn + Se). Contrastingly, the TFs of Zn from straw to husk were greatly improved by different treatments, whereas the TFs of Zn from husk to grain were decreased, and the foliar application of Zn was more effective than the soil application of Zn.
The TFs of Se from husk to grain with the foliar application of Se alone were higher than those sprayed with a combination of Zn and Se (Table 1 and Table S5). Compared to B + Se2, the TFs of Se from husk to grain were markedly inhibited by the foliar application of Zn, especially at the highest concentration of Zn3, which were decreased by 90.00% and 92.86% in Quzhou and Shangzhuang, respectively. Relative to the foliar application of Se alone, the addition of foliar Zn increased the TFs of Se from straw to husk, especially in Shangzhuang.

3.3. Zn or Se Recovery

The results obtained for the recovery of Zn and Se in wheat are shown in Table 2. In general, the values obtained for RBZn were considerably lower than those of RFZn, and RBZn in Quzhou was higher than that in Shangzhuang. In Quzhou, the RFZn was notably influenced by the concentration of foliar-applied Zn and the addition of Se, and the RFZn in grain and straw was 1.14–6.70% and 4.80–8.93%, respectively. The highest RFZn was achieved in the lowest Zn application (Zn1) in both parts. In Shangzhuang, the RFZn in grain and straw was 3.94–6.88% and 6.29–9.64%, respectively. Although there was no significant difference, the RFZn in grain was generally higher when spraying with higher Zn concentrations, whereas the highest RFZn in straw was achieved when the lowest Zn concentration was sprayed. The RFZn in straw was usually higher than those in grain, while the opposite results were observed in the case of RFSe. At both experimental sites, the foliar application of a higher Se concentration increased the RFSe in grain and straw (Table 2). The RFSe in wheat grain was 5.29–10.62% at two sites, and the RFSe in Se2 was the highest in both sites. Moreover, at two sites, the combined application with Zn2 and Zn3 contributed to sharp declines of 49.74–51.63% and 94.06–98.69% in the RFSe in grain, respectively. Conversely, the combined application with Zn increased the RFSe in straw, particularly the application of Zn2.

3.4. Effects of Application of Zn and Se on Other Elements in Wheat Grain

In addition to the element of Zn and Se, different treatments and regions had differing effects on the contents of other essential trace elements (Mn, Cu and Mo) (Table S3 and Figure 4). We found that soil Zn treatment generally had little effect on the contents of Mn, Cu, and Mo. Meanwhile, the contents of Mn, Cu (except for B + Zn1) and Mo increased slightly in Quzhou under the combined application of soil and foliar Zn treatments. Compared with the foliar application of Zn2, the application combined with Se2 contributed to a reduction in the Mo content in Quzhou. Under the treatments containing Se2, the Mo content was reduced by 5.15–14.53% (Quzhou) and 10.42–31.60% (Shangzhuang) compared with the control (Figure 4). Furthermore, in Shangzhuang, the Mn content was obviously decreased by 12.04% under the B + Zn1 treatment and increased by 10.24% under the B + Zn3 + Se2 treatment (Figure 4). Compared with the corresponding application of either Zn or Se alone, the combined application of Zn3 and Se2 resulted in a higher grain content of Mn. Similar results were obtained for the elements of Cu. In response to all treatments, increases and reductions were detected in the contents of Cu and Mo, respectively.
The correlation coefficients between different trace elements in the grains of wheat at the two experimental sites are shown in Table 3. At both sites, the content of Zn in grains were found to be positively correlated with Cu, although they were negatively correlated with Mn at Quzhou. In the case of Mn and Cu, we detected opposite associations at the two sites, with significant negative and positive correlations being detected for grains at Quzhou and Shangzhuang, respectively.

3.5. Estimation of Daily Intake

Results indicated that whereas the foliar application of Zn alone and the combined foliar application of Zn and Se could almost meet the requisite daily Zn intake for adult females, none of the treatments could achieve this goal in the case of adult males (Figure 5 and Table S2). These wheat grain provided 57.62–68.55% and 63.66–90.49% of the dietary Zn intake for adult males in the Quzhou and Shangzhuang regions, respectively, which represented the corresponding daily Zn intake deficits of 3.93–5.29 and 1.18–4.54 mg day−1 person−1. With regard to Se, we found that only spraying with 30 g hm−2 Se could meet the daily Se intake, which provided 128.54% (Quzhou) and 143.16% (Shangzhuang) of the recommended intake. Other treatments containing foliar Se provided 27.41–95.85% (Quzhou) and 19.56–81.30% (Shangzhuang) of the dietary Se intake, which represented the corresponding daily Se intake deficits of 0.002–0.044 and 0.011–0.048 mg day−1 person−1, respectively.
Estimates of daily Mn, Cu and Mo intakes are shown in Table S4. The values of DIMn ranged from 6.44 to 7.58 mg day−1 person−1 (Quzhou) and 6.24 to 7.82 mg day−1 person−1 (Shangzhuang), which provided 143.05–168.52% and 138.71–173.86% of the recommended daily intake (4.5 mg day−1 person−1). The values of DICu ranged from 1.08 to 1.24 mg day−1 person−1 (Quzhou) and 1.14 to 1.67 mg day−1 person−1 (Shangzhuang), which provided 134.94–155.08% and 143.10–209.00% of the recommended daily intake (0.8 mg day−1 person−1). The foliar application of Zn, Se and their combination increased the CRCu, particularly in Shangzhuang. The values of DIMo ranged from 0.12 to 0.15 mg day−1 person−1 (Quzhou) and 0.09 to 0.13 mg day−1 person−1 (Shangzhuang), which provided 119.45–153.00% and 87.77–128.33% of the recommended daily intake (0.1 mg day−1 person−1). In a word, wheat grains could provide the adequate dietary intakes of Mn, Cu, and Mo for humans.

4. Discussion

4.1. Accumulation and Translocation of Zn in Different Parts of Wheat

The content of Zn in different parts of wheat was significantly improved by the application of Zn at two experimental sites, particularly in the wheat receiving a foliar application of Zn (Figure 2a–c). The Zn content in wheat grain was not significantly affected by soil Zn treatment. The soil application of Zn usually had little effect on increasing grain Zn [7]. Nevertheless, in regions with alkaline soils, it is vital to apply the Zn fertilizer to soil to ensure a sufficient source Zn for root uptake, as Zn can bind tightly to minerals in soil with a high pH [27]. Zn is applied to the soil primarily as a source of nutrition in the early vegetative growth stage. During the later reproductive growth stage, the re-mobilization of nutrients from the leaves to the reproductive tissues serves as an important source of nutrients for the grains, so using appropriate and timely foliar applications to ensure adequate nutrition in leaves is important [28].
A series of field experiments conducted in seven countries has revealed increases of 12.3%, 83.5%, and 89.7% in the Zn content of grain in response to treatments with soil-applied Zn, foliar-applied Zn alone, and a combination of soil- and foliar-applied Zn, respectively [7]. Similarly, Yin et al. [29] considered that the contents of grain Zn could be enhanced in the order of soil + foliar Zn > foliar Zn > soil Zn. Zhang et al. [17] found that spraying with 1.1 kg Zn hm−2 as ZnSO4·7H2O had the best effect on improving the Zn content in wheat grains. In the present study, the most effective method to increase the grain Zn content is the treatment of B + Zn3 + Se2. In foliar spraying, Zn is applied directly to the stems and leaves, and thereby enhances the transportation efficiency to grain [13]. Our study found that the treatment containing foliar application of Zn enhanced the TFs from straw to husk but reduced them from husk to grain, thus accounting for the increase in Zn content in the husk (Table 1). Yin et al. [29] demonstrated that it was more important to improve the translocation ability from above-ground tissues to grain rather than the root uptake from the soil. However, our study found that the translocation ability from husk to grain was decreased with the foliar application of Zn. Consequently, further studies should focus on increasing the translocation ability from the husks to grains of wheat.
The recovery of Zn reflects the Zn rich efficiency under the soil and foliar application of Zn. The recovery of Zn in wheat grains depends on the form and dosage of fertilizer, as well as the method, time, and stage of fertilizer application (Table 4). ZnSO4 is the most common form of Zn fertilizer that is widely used. In these studies, the dosage of ZnSO4 used for foliar application was substantially lower than that of the Zn applied to soil, and the Zn content, increasing rate and grain recovery treated by foliar application were all higher than those of soil application. The coefficient of variation (CV) of recovery was 0.02 and 0.77 under the soil and foliar application, respectively. The higher CV of recovery of foliar application could explain why foliar spraying with Zn led to different changes in the grain Zn content of wheat in two regions (Figure 2a). Specifically, it might be due to the fact that the Zhongmai 175 was a Zn-rich variety, so it be might more sensitive to Zn fertilizer and have a high Zn uptake capacity. In addition, it could absorb sufficient Zn from the soil due to high DTPA-Zn during the whole lifespan of the wheat growth [30]. Therefore, the increase in Zn content was more obvious when spraying with Zn in Shangzhuang.
To meet the daily Zn requirement of humans, the Zn content of grains needs to reach 40–60 mg kg−1 [6]. In the present study, all foliar applications of Zn reached 40 mg kg−1, and on the basis of linear regression, we estimated that at least 0.68 and 0.45 kg Zn hm−2 should be sprayed in Quzhou and Shangzhuang, respectively, to attain the requisite levels. Based on the Chinese dietary reference intakes [25], the recommended nutrient intake (RNI) of Zn for adult males and females is 12.5 and 7.5 mg day−1, respectively. Under the treatments containing the foliar application of Zn, adult males still need to obtain additional Zn supplementation in other ways to compensate for the daily Zn intake deficits of 3.93–5.29 and 1.18–4.54 mg day−1 in Quzhou and Shangzhuang, respectively (Figure 5), whereas adult females in the Quzhou region need only minimal Zn supplementation in B + Zn1 (0.30 mg day−1) and B + Zn2 (0.16 mg day−1) treatments.

4.2. Accumulation and Translocation of Se in Different Parts of Wheat

We found that the foliar application of Se had no significant effects on the yield of wheat grains (Table S1), thereby indicating that Se might not play a prominent role in plant growth. The total Se contents of soil in the Quzhou and Shangzhuang region were <0.175 mg kg−1 and <0.125 mg kg−1, respectively, which accordingly identifies these soils as Se-marginal and Se-deficient, respectively, and consequently, the Se contents in the cereals cultivated in these soils is also insufficient [14,31]. Plant roots usually absorb Se from soil in the absence of exogenously added Se. Li et al. [32] found that this process was partially regulated by phosphate transporters. Having been absorbed by plants, selenite could easily convert to organic Se, and is thereafter transported from leaves to other tissues mediated by phosphate transporters [33]. Further study had indicated that higher Se content could be detected when selenium was applied in the form of selenate rather than selenite, which is believed to be attributable to the faster mobility of the former in vessels [34]. In contrast to soil application, foliar spraying has attracted much attention due to its higher bioavailability [35]. The foliar application of Se is an effective method to improve the Se content in edible parts of crops, such as in rice [20], naked oats [36] and maize [37]. The present study confirmed that foliar spraying with Na2SeO3 was an effective way to improve the Se content, and our results showed that foliar application of Se alone improved the grain Se by 131.81–527.21% (Figure 2d). In this process, the overexpression of TaSBP-A increased the transportation from flag leaves to grains, and then promoted the accumulation of Se in grains [38]. As mentioned by Galinha et al. [39], the foliar application of Se could increase the content of organic Se, particularly selenomethionine (SeMet) in grains. However, selenite and selenate have different effects on Se accumulation in cereals. Selenate is absorbed by plants mainly through sulfate transporters with high affinity, while selenite is absorbed through phosphate transporters and aquaporins (OsNIP2) [40]. A study found that the foliar application of selenite was more effective than selenate on Se enrichment, and the accumulation of Se in grains was mainly mediated via transport from node 1 to internode 1, and the main form of organic Se is SeMet [41]. The difference in Se content in different parts of wheat among treatments is also related to the transport of Se. In this study, the foliar application of Se or a higher dose of Se fertilizer promoted the transfer ability of Se from the straw to the husk (Table 1), which was probably due to the dilution effect of the straw.
In order to know the factors affecting the efficiency of Se enrichment, the Se recovery of wheat grains treated with different fertilizer form (Na2SeO3, Na2SeO4, organic Se, nano-Se, etc.), and the dosage of fertilizer, method, times and stage of application were summarized (Table 5). The changes in grain Se content under different treatments were consistent in two regions (Figure 2d), which could be attributed to the lower CV of Se recovery (0.54). However, the CV of the Se increasing rates was higher than the value obtained for Zn, which might due to the fact that the plants were more sensitive to Se, so, hence, this element was more easily regulated by Se fertilizer.
The content of Se in Se-enriched cereals should reach 0.1–0.5 mg kg−1 [11]. In this study, the content of grain Se was 0.08–0.09 mg kg−1 under the treatments without Se applied, which was lower than the standard. However, the content of Se in wheat grains reached the standard under the foliar application of Se alone, up to 0.21–0.50 mg kg−1. According to the relational model, wheat should be sprayed with at least 2.50 and 2.36 g Se hm−2 to reach the requisite 0.1 mg kg−1 level in Quzhou and Shangzhuang, respectively. Considering the necessity of maintaining public health, an appropriate daily Se intake is recommended in some regions. According to WHO and FAO [42], the recommended intake of Se for an adult is 25–34 μg day−1. The daily Se intake recommended by the German Nutrition Society for adult men and women is 70 and 60 μg day−1, respectively [43]. Similarly, on the basis of the Chinese dietary reference intakes [25], the recommended dietary intake of Se for an adult is 60 μg day−1. Notably, we found that the foliar application of 30 g Se hm−2 as Na2SeO3 could provide 128.54% (Quzhou) and 143.16% (Shangzhuang) of the dietary requirement of Se, which met the RNI of Se for a Chinese adult.
Table 4. Summary of Zn content and recovery of wheat grains under application of Zn fertilizer in field conditions.
Table 4. Summary of Zn content and recovery of wheat grains under application of Zn fertilizer in field conditions.
FormDosage
(g Zn hm−2)		MethodApplication Time and StageControl
(mg kg−1)		Grain Content
(mg kg−1)		Increasing Rates
(%)		Grain Recovery
(%)		References
ZnSO4·7H2O2.71FoliarTwo times, at the end of anthesis and 1 week later29.0158.30100.975.93[44]
ZnSO4·7H2O2.71FoliarTwo times, at the end of anthesis and 1 week later24.1077.90223.247.00
ZnSO4·7H2O0.79FoliarOne time, at the end of anthesis 15.9020.5028.934.36[45]
ZnSO4·7H2O0.79FoliarOne time, at the end of anthesis 26.4032.6023.486.76
ZnSO4·7H2O11.30SoilBefore planting27.4030.5011.310.18[7]
ZnSO4·7H2O1.81FoliarTwo times, at heading and milk stages27.4048.0075.185.89
ZnSO4·7H2O1.45FoliarTwo times, at early milk stage, and the second spraying occurred a week later21.8043.1097.719.87[46]
ZnSO4·7H2O1.01FoliarThree times, at tillering, booting and milking stages19.7539.91102.0823.13[47]
ZnSO4·7H2O1.01FoliarThree times, at tillering, booting and milking stages30.6942.5738.7117.47
ZnSO4·7H2O1.01FoliarThree times, at tillering, booting and milking stages28.7545.4157.9521.90
ZnSO4·7H2O1.01FoliarThree times, at tillering, booting and milking stages17.5348.68177.7032.05
ZnSO4·7H2O9.60FoliarFour times, at jointing, booting, flowering and grain filling stages24.1936.8652.380.96[48]
ZnSO4·7H2O11.40SoilBefore planting39.8042.376.460.18[49]
ZnSO4·7H2O0.91FoliarTwo times, at the start of flowering and two weeks later34.4546.8936.116.33
ZnSO4·H2O11.00SoilBefore planting37.1739.034.990.41This study
ZnSO4·H2O11.00SoilBefore planting37.4138.302.380.06
ZnSO4·H2O1.74FoliarThree times, at jointing, booting and filling stages39.0341.666.746.70
ZnSO4·H2O1.74FoliarThree times, at jointing, booting and filling stages38.3046.0220.173.94
ZnSO4·H2O2.61FoliarThree times, at jointing, booting and filling stages39.0342.448.752.13
ZnSO4·H2O2.61FoliarThree times, at jointing, booting and filling stages38.3056.9848.774.49
ZnSO4·H2O3.48FoliarThree times, at jointing, booting and filling stages39.0344.2413.353.78
ZnSO4·H2O3.48FoliarThree times, at jointing, booting and filling stages38.3064.3067.894.71
SoilCoefficient of variation (CV)0.180.160.270.02
FoliarCoefficient of variation (CV)0.210.300.700.77
Note: the calculation of CV is excluded from the results of our study.
Table 5. Summary of Se content and recovery of wheat grains under application of Se fertilizer in field conditions.
Table 5. Summary of Se content and recovery of wheat grains under application of Se fertilizer in field conditions.
FormDosage
(g Se hm−2)		MethodApplication Time and StageControl
(mg kg−1)		Grain Content
(mg kg−1)		Increasing TimesGrain Recovery
(%)		References
Na2SeO327.41FoliarTwo times, at the end of anthesis and 1 week later0.030.7423.712.98[44]
Na2SeO327.41FoliarTwo times, at the end of anthesis and 1 week later0.020.5024.07.89
Nano-Se15FoliarOne time, at flowering stage0.050.243.69.20[50]
Organic-Se15FoliarOne time, at flowering stage0.050.284.411.00
Na2SeO330FoliarOne time, at flowering stage0.050.254.04.90
Na2SeO330FoliarOne time, at flowering stage0.070.384.46.65[51]
Na2SeO430FoliarOne time, at flowering stage0.070.293.14.77
SeMet30FoliarOne time, at flowering stage0.070.364.16.67
Nano-Se30FoliarOne time, at flowering stage0.070.161.32.28
Na2SeO410FoliarOne time, at the start of flowering0.030.102.43.00[49]
Na2SeO310FoliarOne time, at the end of tillering stage0.070.151.31.63[52]
Na2SeO320FoliarOne time, at the end of tillering stage0.070.252.81.69
Na2SeO340FoliarOne time, at the end of tillering stage0.070.435.51.68
Na2SeO410FoliarOne time, at the end of tillering stage0.070.273.03.53
Na2SeO420FoliarOne time, at the end of tillering stage0.070.8211.36.87
Na2SeO440FoliarOne time, at the end of tillering stage0.071.3819.85.90
Na2SeO315FoliarOne time, at filling stage0.050.182.56.20[53]
Na2SeO330FoliarOne time, at filling stage0.050.243.74.80
Na2SeO345FoliarOne time, at filling stage0.050.304.94.50
Na2SeO360FoliarOne time, at filling stage0.050.437.44.70
Na2SeO315FoliarThree times, at jointing, booting and filling stages0.090.211.35.29This study
Na2SeO315FoliarThree times, at jointing, booting and filling stages0.080.262.48.04
Na2SeO330FoliarThree times, at jointing, booting and filling stages0.090.454.010.62
Na2SeO330FoliarThree times, at jointing, booting and filling stages0.080.505.39.13
Coefficient of variation (CV)0.270.751.010.54
Note: the calculation of CV is excluded from the results of our study.

4.3. Interactive Effects between Zn and Se in Wheat

Compared with the foliar application of Zn alone, the combined application with Se slightly increased the Zn content in different parts of wheat (Figure 2a–c). In other plants, such as pea (Pisum sativum L.), a positive interaction between Zn and Se has also been found [54]. Se can alleviate abiotic stress by alleviating oxidative stress, maintaining cellular structural and functional integrity, enhancing photosynthesis, and balancing the uptake of essential nutrients [55]. Zn is a cofactor of SOD, while a moderate amount of Se could increase the activity of SOD [56], so exogenous Se could indirectly increase Zn content in plants by enhancing SOD activity. In addition, the processes of Zn absorption, translocation, and accumulation are regulated by transporter proteins, such as ZIP, which regulates the Zn uptake, and HMA and YSL, which regulate the xylem loading and unloading of Zn [3]; the application of Se may influence the gene expression of these proteins and thus influence the uptake, absorption, and transportation of Zn. However, Fang et al. [20] found that the foliar application of Na2SeO3 and ZnSO4 had no impact on the absorption of Zn and Se in rice, and they considered that the metabolic pathways of Zn and Se were different, which were mainly mediated via ZIP and phosphorus or sulfur transporters, respectively. Consequently, there may be no pronounced competition between Zn and Se for absorption. Germ et al. [18] and Mangueze et al. [21] also found that Se had no apparent effect on increasing Zn content. We accordingly speculate that the observed differences in the effects of Se on Zn might be associated with the differences in application method, spray concentrations, chemical forms, and crop species [57].
In the present study, compared with B + Se2, the addition of foliar Zn significantly reduced the grain Se content but increased the Se content in the husk and the straw, which could be attributed to the lower TF from the husk to the grain. The antagonistic effect of Zn on Se in grains was also confirmed by Mangueze et al. [21] and Ning et al. [44], who found that the application of Zn decreased the grain Se content of rice and wheat. The foliar spraying of Zn may influence the proteins that regulate the phloem loading and unloading, xylem to phloem transition in nodes, xylem unloading, and other processes [58], which might collectively contribute to a reduction in the Se content in grains and increases in the husk and the straw. Zn and other metals could cause the formation of S-containing compounds [59], while Se and S have the similar chemistry properties and metabolic pathway [60], and the movement of Se in plants is mediated by sulfate transporters [61]. In addition, the application of SO42− (ZnSO4·H2O) also brought S. These may accordingly explain why the Se content in wheat apparently changed when more ZnSO4·H2O was applied. Consequently, it is necessary to further study whether the effect of ZnSO4 on Se is caused by Zn2+ or SO42−.

4.4. Accumulation of Other Elements in Wheat Grain

Trace elements are associated with human development and many diseases [62]. Biofortification not only mitigates elemental deficiencies but also can regulate the other elements by influencing the element interactions. Some research demonstrated that the application of Zn and Se could influence the contents of various other elements, including phosphorus, potassium, calcium, magnesium, copper, iron, etc. [37,63,64]. By combining the results obtained at two experimental sites, we found that there were no obvious changes in apparent regularity on Mn, Cu and Mo contents under the foliar-applied Zn and Se treatments (Table S3 and Figure 4), while the estimated intakes of Mn, Cu and Mo in grains were found to exceed their respective RNI (Table S4). However, there was a significant positive correlation between Zn and Cu (Table 3). Germ et al. [18] found that the soil application of Zn only increased Mo content in wheat grains, whereas the foliar application of Se had no significant effects on other elements. Lian et al. [30] considered that Zn and Mn are usually transported through similar transporters or involved in similar metabolic processes, while Zn and Mo might be the different transport mechanisms, so the influence is usually different when spraying Zn fertilizer. Moreover, antagonistic effects between Zn and Fe/Mn/Cu were found [65,66]. Furthermore, the impact of Se on other mineral elements was not obvious [67].

5. Conclusions

In the present study, the contents of Zn or Se in different parts of wheat were increased under the foliar application of ZnSO4·H2O or Na2SeO3 alone under field conditions. For the interaction between Zn and Se, the content of Zn in different parts of wheat was increased by the foliar application of Na2SeO3. However, compared with the foliar application of 30 g Se hm−2 Na2SeO3 alone, the biofortification effect of Se was weakened when adding the foliar application of 2.61 and 3.48 kg Zn hm−2 ZnSO4·H2O, and the transport ability of Se from husk to grain was inhibited. Nevertheless, the wheat grain biofortification target of 40 mg Zn kg−1 and 0.1 mg Se kg−1 could be achieved with the soil application of 11 kg Zn hm−2 combined with the foliar application of 2.61 kg Zn hm−2 and 30 g Se·hm−2. Daily Zn intake in adult females could generally be met when the treatment contains the foliar application of Zn, while adult males would still need to supplement this gap with other foods. Daily Se intake could be met with the foliar application of 30 g Se hm−2 Na2SeO3. The daily Mn, Cu and Mo intake requirements for humans could generally be met by wheat grains. A positive correlation was found between Zn and Cu in grains. Thus, foliar application achieved Zn and Se enrichment in wheat grains at two experimental sites, and the interactive mechanism between Zn and Se needs further study.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy14071513/s1, Table S1: Effects of different Zn and Se fertilizer treatments on grain yields of wheat in two sites (t hm−2); Table S2: Contribution rates (CR) of wheat to dietary Zn or Se intake in residents (%); Table S3: Effects of different Zn, Se fertilizer treatments on trace elements contents in grain of wheat (mg kg−1); Table S4: Estimation of daily Mn, Cu and Mo intake (DI) and contribution rates (CR) of wheat to dietary intake in residents (%); Table S5: Analysis of variance results of treatments.

Author Contributions

Conceptualization, Y.X., X.Z., G.F. and Q.W.; Data curation, L.K. and Y.T.; Formal analysis, L.K. and Y.T.; Funding acquisition, H.L.; Investigation, Y.T., Y.X., X.Z., G.F. and L.Z.; Methodology, Q.W.; Resources, Q.W. and H.L.; Software, L.Z.; Supervision, H.L.; Validation, L.K.; Visualization, L.K.; Writing—original draft, L.K.; Writing—review and editing, L.K. and Y.W. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Key Research and Development Program of China (2023YFD1700104).

Data Availability Statement

The raw data supporting the conclusions of this article will be made available by the authors on request.

Conflicts of Interest

The authors declare they have no conflicts of interest.

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Agronomy 14 01513 g001
Figure 1. Location map of two experimental sites.
Figure 1. Location map of two experimental sites.
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Figure 2. Effects of different Zn and Se treatments on the Zn (a–c) and Se (d–f) contents in the grain, husk and straw of wheat in two sites. Red lines represent the lowest biofortification target value on the Zn or Se contents in a grain of wheat. Different letters indicate significant differences at p < 0.05 level (Duncan test).
Figure 2. Effects of different Zn and Se treatments on the Zn (a–c) and Se (d–f) contents in the grain, husk and straw of wheat in two sites. Red lines represent the lowest biofortification target value on the Zn or Se contents in a grain of wheat. Different letters indicate significant differences at p < 0.05 level (Duncan test).
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Figure 3. Relationship between Zn or Se foliar application rates and Zn (a) or Se (b) content in wheat grain. Red lines represent the lowest biofortification target value on the Zn or Se contents in a grain of wheat. * and ** indicate p < 0.05 and p < 0.01, respectively.
Figure 3. Relationship between Zn or Se foliar application rates and Zn (a) or Se (b) content in wheat grain. Red lines represent the lowest biofortification target value on the Zn or Se contents in a grain of wheat. * and ** indicate p < 0.05 and p < 0.01, respectively.
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Figure 4. Effects of different Zn and Se treatments on trace element content changes in grains of wheat in Quzhou (a) and Shangzhuang (b) compared with the control. Data are means (n = 3). Red and blue colors indicate increase and decrease, respectively. The changes in trace element content are expressed as percentage.
Figure 4. Effects of different Zn and Se treatments on trace element content changes in grains of wheat in Quzhou (a) and Shangzhuang (b) compared with the control. Data are means (n = 3). Red and blue colors indicate increase and decrease, respectively. The changes in trace element content are expressed as percentage.
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Figure 5. Estimation of daily Zn (a) and Se (b) intake per person. Red lines represent the lowest recommended nutrient intake (RNI) of an adult of Zn or Se. Different letters indicate significant differences at p < 0.05 level (Duncan test).
Figure 5. Estimation of daily Zn (a) and Se (b) intake per person. Red lines represent the lowest recommended nutrient intake (RNI) of an adult of Zn or Se. Different letters indicate significant differences at p < 0.05 level (Duncan test).
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Table 1. Effects of different Zn, Se treatments on transfer factors (TFs) of Zn and Se in different tissues of wheat.
Table 1. Effects of different Zn, Se treatments on transfer factors (TFs) of Zn and Se in different tissues of wheat.
TreatmentQuzhouShangzhuang
Grain/HuskHusk/StrawGrain/HuskHusk/Straw
ZnCK2.45 ± 0.3 a1.56 ± 0.03 d4.49 ± 0.10 a1.32 ± 0.03 d
B2.06 ± 0.07 b1.54 ± 0.06 d2.45 ± 0.08 b1.70 ± 0.02 c
B + Zn11.14 ± 0.08 c1.86 ± 0.02 c0.56 ± 0.02 c3.21 ± 0.18 a
B + Zn20.82 ± 0.11 cd2.23 ± 0.03 a0.63 ± 0.01 c3.17 ± 0.08 a
B + Zn30.68 ± 0.03 d1.98 ± 0.04 b0.64 ± 0.01 c3.01 ± 0.03 ab
B + Zn2 + Se20.93 ± 0.00 cd1.83 ± 0.06 c0.60 ± 0.01 c3.13 ± 0.08 ab
B + Zn3 + Se20.57 ± 0.01 d2.31 ± 0.04 a0.59 ± 0.03 c2.87 ± 0.07 b
SeCK--1.86 ± 0.09 a0.98 ± 0.08 d
B--2.12 ± 0.02 a0.58 ± 0.07 e
B + Se18.36 ± 4.49 a0.23 ± 0.05 c1.11 ± 0.05 b3.34 ± 0.04 b
B + Se23.00 ± 0.68 ab1.08 ± 0.18 b1.96 ± 0.19 a2.67 ± 0.03 c
B + Zn2 + Se22.48 ± 0.77 ab0.35 ± 0.08 c0.48 ± 0.01 c3.33 ± 0.12 b
B + Zn3 + Se20.30 ± 0.08 b1.72 ± 0.21 a0.14 ± 0.02 d3.71 ± 0.21 a
Different letters within the same column indicate significant differences among treatments at p < 0.05 level.
Table 2. Recovery (%) of soil Zn, foliar Zn and foliar Se under different treatment in wheat in two sites.
Table 2. Recovery (%) of soil Zn, foliar Zn and foliar Se under different treatment in wheat in two sites.
TreatmentQuzhouShangzhuang
GrainStrawGrainStraw
RBZnB0.41 ± 0.250.40 ± 0.150.06 ± 0.020.21 ± 0.03
RFZnZn16.70 ± 0.57 a8.59 ± 1.39 a3.94 ± 1.44 a9.64 ± 1.53 a
Zn22.13 ± 0.69 bc4.80 ± 1.16 a4.49 ± 0.69 a6.68 ± 0.82 a
Zn33.78 ± 0.95 b8.46 ± 1.93 a4.71 ± 1.44 a6.29 ± 1.04 a
Zn2 + Se21.14 ± 0.20 c5.26 ± 0.53 a5.36 ± 0.07 a6.60 ± 1.28 a
Zn3 + Se24.49 ± 0.96 ab8.93 ± 2.03 a6.88 ± 0.37 a9.30 ± 0.71 a
RFSeSe15.29 ± 4.55 ab3.01 ± 0.99 b8.04 ± 1.90 ab0.61 ± 0.09 b
Se210.62 ± 1.17 a3.47 ± 1.30 b9.13 ± 0.86 a0.82 ± 0.13 b
Zn2 + Se25.34 ± 0.46 ab11.39 ± 0.81 a4.42 ± 0.81 b3.23 ± 0.77 a
Zn3 + Se20.63 ± 0.12 b5.14 ± 1.27 b0.12 ± 0.02 c0.16 ± 0.03 b
Different letters within the same column indicate significant differences among treatments at p < 0.05 level.
Table 3. Correlation coefficient (r) between different trace elements in wheat grain.
Table 3. Correlation coefficient (r) between different trace elements in wheat grain.
Site SeZnMnCuMo
QuzhouSe1nsnsnsns
Zn 1−0.443 *0.407 *ns
Mn 1−0.496 **ns
Cu 1ns
Mo 1
ShangzhuangSe1nsnsnsns
Zn 1ns0.471 *ns
Mn 10.730 **ns
Cu 1ns
Mo 1
*, ** and ns indicate p < 0.05, p < 0.01 and p > 0.05, respectively.
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Kong, L.; Tao, Y.; Xu, Y.; Zhou, X.; Fu, G.; Zhao, L.; Wang, Q.; Li, H.; Wan, Y. Simultaneous Biofortification: Interaction between Zinc and Selenium Regarding Their Accumulation in Wheat. Agronomy 2024, 14, 1513. https://doi.org/10.3390/agronomy14071513

AMA Style

Kong L, Tao Y, Xu Y, Zhou X, Fu G, Zhao L, Wang Q, Li H, Wan Y. Simultaneous Biofortification: Interaction between Zinc and Selenium Regarding Their Accumulation in Wheat. Agronomy. 2024; 14(7):1513. https://doi.org/10.3390/agronomy14071513

Chicago/Turabian Style

Kong, Lingxuan, Yanjin Tao, Yang Xu, Xuan Zhou, Guohai Fu, Lijie Zhao, Qi Wang, Huafen Li, and Yanan Wan. 2024. "Simultaneous Biofortification: Interaction between Zinc and Selenium Regarding Their Accumulation in Wheat" Agronomy 14, no. 7: 1513. https://doi.org/10.3390/agronomy14071513

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