Next Article in Journal
Silicon Improves the Production of High Antioxidant or Structural Phenolic Compounds in Barley Cultivars under Aluminum Stress
Next Article in Special Issue
Pre-Harvest Foliar Application of Mineral Nutrients to Retard Chlorophyll Degradation and Preserve Bio-Active Compounds in Broccoli
Previous Article in Journal
Effects of Nitrogen Fertilization and Seed Piece Applied Fungicides on Establishment, Tiller Dynamics, and Sucrose Yields in Successively Planted Sugarcane
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agronomy
Volume 9
Issue 7
10.3390/agronomy9070386
agronomy-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Foliar Zn Spraying Simultaneously Improved Concentrations and Bioavailability of Zn and Fe in Maize Grains Irrespective of Foliar Sucrose Supply

by
Haiyong Xia
1,2,3,*,†,
Weilin Kong
1,3,†,
Lan Wang
1,2,3,
Yanhui Xue
1,3,
Wenlong Liu
4,
Chunyan Zhang
5,
Shenggang Yang
6 and
Chong Li
6
1
Crop Research Institute, Shandong Provincial Key Laboratory of Crop Genetic Improvement, Ecology and Physiology, Shandong Academy of Agricultural Sciences, Jinan 250100, China
2
College of Life Sciences, Shandong Normal University, Jinan 250014, China
3
National Engineering Laboratory of Wheat and Maize, Shandong Academy of Agricultural Sciences, Jinan 250100, China
4
State Key Laboratory of Efficient Development and Comprehensive Utilization of Nutrient Resources, Kingenta Ecological Engineering Group Co., Ltd., Linyi 276799, China
5
Linyi Academy of Agricultural Sciences, Linyi 276012, China
6
Laoling Ronghai Selenium Enrichment Food Co., Ltd., Laoling 253602, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2019, 9(7), 386; https://doi.org/10.3390/agronomy9070386
Submission received: 8 June 2019 / Revised: 14 July 2019 / Accepted: 15 July 2019 / Published: 16 July 2019
(This article belongs to the Special Issue Foliar Fertilization of Crop Plants: Current State of Knowledge and Perspectives)
Browse Figure
Versions Notes

Abstract

:
Zinc (Zn) deficiency is a global nutritional problem that is reduced through agronomic biofortification. In the current study, the effects of foliar spraying of exogenous ZnSO4·7H2O (0.2% in Quzhou and 0.3% in Licheng, w/v) and/or sucrose (10.0%, w/v) on maize (Zea mays L.) agronomic traits; concentrations of Zn, iron (Fe), calcium (Ca), total phosphorus (P), phytic acid (PA) P, carbon (C), and nitrogen (N); C/N ratios; and Zn and Fe bioavailability (as evaluated by molar ratios of PA/Zn, PA × Ca/Zn, PA/Fe and PA × Ca/Fe) in maize grains were studied under field conditions for two years at two experimental locations. The results confirmed that there were no significant differences in maize agronomic traits following the various foliar treatments. Compared with the control treatment of foliar spraying with deionized water, foliar applications of Zn alone or combined with sucrose significantly increased maize grain Zn concentrations by 29.2–58.3% in Quzhou (from 18.4–19.9 to 25.2–29.6 mg/kg) and by 39.8–47.8% in Licheng (from 24.9 to 34.8–36.8 mg/kg), as well as its bioavailability. No significant differences were found between the foliar spraying of deionized water and sucrose, and between Zn-only and “sucrose + Zn” at each N application rate and across different N application rates and experimental sites. Similar results were observed for maize grain Fe concentrations and bioavailability, but the Fe concentration increased to a smaller extent than Zn. Foliar Zn spraying alone or with sucrose increased maize grain Fe concentrations by 4.7–28.4% in Quzhou (from 13.4–17.1 to 15.2–18.5 mg/kg) and by 15.4–25.0% in Licheng (from 24.0 to 27.7–30.0 mg/kg). Iron concentrations were significantly and positively correlated with Zn at each N application rate and across different N application rates and experimental locations, indicating that foliar Zn spraying facilitated the transport of endogenous Fe to maize grains. Therefore, foliar Zn spraying increased the Zn concentration and bioavailability in maize grains irrespective of foliar sucrose supply while also improving Fe concentrations and bioavailability to some extent. This is a promising agricultural practice for simultaneous Zn and Fe biofortification in maize grains, i.e., “killing two birds with one stone”.

1. Introduction

Maize (Zea mays L.), one of the world’s paramount cereal crops, along with wheat and rice. It is very popular due to its diverse functionality as a food source for both humans and animals [1,2]. Zinc is an essential micronutrient for the survival of plants, animals, and humans [3]. However, maize grains do not inherently contain enough Zn to meet daily human requirements, particularly when grown in Zn-deficient soils [4]. Since the 1990s, crop Zn deficiency has been very common worldwide, with 33% of the world’s total cultivated area containing Zn-deficient soil [5]. In China, more than 40% (60 million hectares) of the soil is Zn-deficient [6,7]. In recent years, an increased crop yield, imbalanced fertilization, large-scale irrigation practices, and changes in climatic and soil conditions (e.g., increases in atmospheric CO2 and soil available phosphorus) have exacerbated deficiencies of micronutrients, especially Zn and Fe, in the soil–plant systems in many countries, thereby threatening human nutrition [8,9,10,11,12,13,14,15,16]. It has been reported that nearly one-third of the world’s population does not have sufficient Zn intake [17], and 1.9% of the total global burden of disease is caused by Zn deficiency [18]. Limited food diversity and insufficient dietary Zn intake affects about 100 million people in China, mostly children under five and pregnant women living in rural areas [19]. It is therefore of great interest to improve Zn nutrition in maize grains through integrated soil–crop system management to improve food security and provide human health benefits [20,21].
Zn deficiency leads to white mosaic disease in maize. In previous studies, Zn application to Zn-deficient soils was shown to correct the visible symptoms of this condition, significantly increase the maize grain yield by more than 20% [22], and enhance the maize grain Zn concentration [23] by up to 40% [24]. In addition, foliar Zn spraying has been used to improve the quality of edible crop parts as well as nearly double the Zn concentration [25], with a significant and positive linear correlation found between the Zn concentration in wheat grains and the foliar Zn application rates [26]. Compared with the soil application of Zn fertilizer, foliar Zn spraying was found to more effectively enrich maize grains with Zn, resulting in higher grain Zn recovery, especially in Zn-sufficient soils [27]. Iron is also an important microelement that needs to be biofortified to correct Fe deficiency in plants and meet human nutritional requirements [17,28]. According to a recent study by Niyigaba et al. (2019) [29], separate application of Zn and Fe fertilizers increased their concentration in wheat grains more than when they were applied as a combined foliar spray. Most studies of soil and/or foliar Zn application have focused on Zn concentrations in edible parts; however, comprehensive studies of these strategies on Fe and other nutritional quality-related traits are currently lacking. In particular, scientists are interested in determining whether agronomic biofortification of Zn is benign for Fe in cereals [30].
Both the carbohydrate status within the plant and any exogenous sucrose supply influence the transport of Zn into developing grains. The depletion of carbohydrate reserves within cultured wheat ears (through maintaining them in darkness prior to labeling) was shown to reduce the transport of radioisotope 65Zn into grains, possibly due to a decrease in the mass flow of carbohydrates within the phloem [31]. Because of the limitation of the grain sink capacity, when supplied at high rates, exogenous sucrose may accumulate in the peduncle and chaff, resulting in stomatal closure, the abatement of transportation by the xylem, and finally decreased micronutrient (including Zn) accumulation in wheat grains [32]. Several investigators found that the wheat grain Zn concentrations were significantly reduced by increasing the sucrose supply to detached ears, due to a dilution effect resulting from the increase in grain weights [33,34]. Our latest study showed that a synergistic foliar spray of “Zn + sucrose” was more effective for the biofortification of Zn than Zn alone in wheat grains/ears grown under real field conditions [3,35]. Most of the studies mentioned investigated the effects of the carbohydrate status within the plant or exogenous sucrose supply on Zn accumulation in wheat grains under controlled environments including detached ear cultures and field experiments; however, it is less known whether the exogenous sucrose supply (with/without Zn) affects Zn and even Fe accumulation in maize under various environmental conditions. In particular, field experiments are lacking.
The bioavailability of a given element (e.g., Zn and Fe) is related not only to its total nutrient concentration but also to the concentrations of anti-nutritional compounds such as phytic acid (PA) and phenolic compounds [4,36]. Maize grains are rich in phytic acid, which binds tightly with Zn or Fe to form spherical crystals with an insoluble protein structure [37]. A deficiency of phytase in humans and animals has been shown to reduce the bioavailability of Zn and Fe in the digestive tract [36,38]. The molar ratio of PA to Zn or Fe has been widely used as an indicator of the bioavailability of Zn or Fe in the human diet [39,40,41]. Under normal circumstances, the critical molar ratio of PA/Zn that causes Zn absorption and utilization inhibition is 15–20; a molar ratio of 5–15 represents about 30–35% Zn availability, and higher than 15 represents about 15% Zn availability [42]. The critical value of the molar ratio of PA/Fe is 10 [43]. Calcium ions (Ca2+) could enhance the binding ability of PA with Zn2+ to form a PA–Ca–Zn complex; therefore, the molar ratio of PA × Ca/Zn has also been suggested to predict the bioavailability of Zn, and a molar ratio higher than the critical value of 200 is not conducive to Zn absorption and utilization [44]. Therefore, in the present study, the molar ratios of PA/Zn, PA/Fe, PA × Ca/Zn, and PA × Ca/Fe were used as predictors of the potential bioavailability of Fe and especially Zn in maize grains treated by different foliar sprays under field conditions.
The objectives of this research were (1) to quantify the effects of foliar applications of sucrose only, Zn only, and a mixed solution of both on maize grain yields and other agronomic traits; (2) to quantify their effects on the nutritional qualities of Zn and Fe including their concentrations and bioavailability for humans in maize grains; (3) to quantify their effects on C, N, total and phytate P, and Ca concentrations, and on the ratios of C/N and phytate P/total P in maize grains; and (4) to elucidate relationships between maize grain Zn and Fe concentrations across different foliar treatments and experimental locations. The results from these experiments will be useful for providing guidance on agronomic practices aimed at improving the Zn and Fe nutritional qualities of maize grains in the field, thereby providing health benefits to humans.

2. Materials and Methods

2.1. Study Site

The field experiments were conducted at two experimental sites/years in China, Quzhou in Hebei province (in 2010) and Licheng in Shandong province (in 2016), separated by a distance of around 200 km. The detailed climatic conditions in these two cities during the experiments were reported previously by Zhang et al. (2013) [45] and Xia et al. (2019) [46], respectively. Quzhou and Licheng have a similar and typical warm, sub-humid, continental monsoon climate, with rain and heat coinciding in the same season, leading to dry and cold winters and rainy and hot summers. The annual cumulative temperatures above 10 °C are 4000–5000 °C. The annual frost-free period is 175–220 days. Annual precipitation is 500–700 mm, with about 70% of rainfall occurring during the corn growing season. Detailed site locations (geographic coordinates) and soil basal properties are presented in Table 1.

2.2. Experimental Design and Crop Management

For the Quzhou experiment, summer maize (Zea mays L., cv. Zhengdan 958) was planted in split-plots (with nitrogen fertilizer in the main plots and foliar spraying treatments in the sub-plots) with three replicates. The main plot treatments included zero N supplement and 105 kg N/ha as urea based on in-season root-zone N management strategies [2,45]. The sub-plot treatments consisted of four foliar treatments (T1–T4), as shown in Table 2. Before tasseling, nine plants were tagged for spraying with each foliar treatment. For the Licheng experiment, summer maize (cv. Zhengdan 958) was grown in fields with uniform fertility and a N application rate of 225 kg/ha as urea. Foliar treatments are shown in Table 2. Each spraying treatment was performed on three replicates, and five plants were tagged before tasseling for each replicate.
The foliar treatments were repeated four times at seven- (in Licheng) or 7–10- (in Quzhou) day intervals after tasseling. It was almost at the flowering stage (BBCH 61–65) when the maize plants were sprayed with solutions for the first time and at the dough or physiological maturity stage (BBCH 85–87) the last time. All solutions contained 0.01% (v/v) TWEEN 20 as a surfactant, and 50 (in Quzhou) or 100 (in Licheng) mL were applied to the maize leaves of each plant each time using a 1.5-L manual pneumatic hand-held sprayer with a rod (DEEPBANG, Guangdong, China).
The two experiments were conducted in a winter wheat–summer maize rotation system. Detailed information about fertilizer applications and crop husbandry was previously described by Zhang et al. (2013) [45] and Xue et al. (2014) [2] for the experiment in Quzhou and by Xia et al. (2019) [46] for the experiment in Licheng. Weeds were well controlled; no obvious water, disease, or pest stress was observed during the maize growing season, and no fungicide or pesticide was used.

2.3. Plant Sampling and Nutrient Analysis

At maturity, all sprayed plants were harvested manually to investigate agronomic traits. After being rapidly washed with deionized water, grain samples were oven-dried at 60–65 °C for 72 h and then ground with a stainless-steel grinder (RT-02B, Rong Tsong, Taizhong, Taiwan). Ground samples were digested with HNO3–H2O2 in a microwave accelerated reaction system (CEM, Matthews, NC, USA). The concentrations of nutrients (Zn, Fe, P, and Ca) in the digested solutions were determined by inductively coupled plasma atomic emission spectroscopy (ICP-AES, OPTIMA 3300 DV, PerkinElmer, Waltham, MA, USA). A reference sample IPE556 (Wageningen University, Wageningen, The Netherlands) in Quzhou or IPE568 (Wageningen University, The Netherlands) in Licheng was included in each batch of digestions to ensure analytical quality. Analysis of IPE556 gave values of 46.7 mg Zn/kg and 36.2 mg Fe/kg, which are in good agreement with the certified values of 46–54 mg Zn/kg and 36–46 mg Fe/kg, respectively. Analysis of IPE568 gave values of 58.26 mg Zn/kg, 40.28 mg Fe/kg, 3.23 g P/kg, and 0.464 g Ca/kg, which are also in good agreement with the certified values of 51.34–60.46 mg Zn/kg, 38.05–54.15 mg Fe/kg, 3.09–3.49 g P/kg, and 0.307–0.501 g Ca/kg, respectively. The phytate P concentration was analyzed according to the method of Haug and Lantzsch (1983) [47]. Phytate P was converted to PA by dividing by 0.282. The C and N concentrations and ratios of C/N were determined using Multi N/C 3100 (Analytik Jena AG, Thuringia, Germany). All nutrient concentrations in maize grains were expressed on a dry weight basis.

2.4. Statistical Analysis

Data from the single-factor completely randomized design and split-plot design experiments were subjected to an analysis of variance (ANOVA) using SAS software (SAS 8.0, SAS Institute, Cary, NC, USA), and mean values were compared by Fisher’s protected least significant difference (LSD) test at the 5% level. SPSS Statistics 17.0 (SPSS Incorporation, Chicago, IL, USA) software was used for calculating Pearson correlation coefficients.

3. Results

3.1. Maize Agronomic Traits and Grain Zn and Fe Accumulation in Quzhou

Split-plot ANOVAs revealed significant impacts of N application rates on maize yield traits, grain Zn contents, and both Fe grain concentrations and contents, as well as significant effects of foliar treatments on grain Zn concentrations and Zn and Fe contents (Table 3). Irrespective of foliar treatments, N supply increased the maize grain dry weight, the total dry weight including grain and straw, the hundred grain dry weight, the grain Zn content, and both the Fe grain concentration and content compared to when no N fertilizer was applied. Across the two N application rates, compared with foliar spraying of deionized water (T1) and sucrose (T2), foliar Zn spraying alone (T3) or in combination with sucrose (T4) generally resulted in significant increases in grain Zn concentrations from the initial 18.4–19.9 mg/kg to 25.2–29.6 mg/kg by 29.2–58.3%, and in grain Zn contents from 1.2–2.1 mg/plant to 1.7–3.2 mg/plant by 30.8–83.3%. No significant differences were observed between foliar spraying of deionized water and sucrose, and between Zn-only and “Sucrose + Zn” treatments. Similarly, T3 and T4 also enhanced Fe concentrations from 13.4–17.1 (in treatments T1 and T2) to 15.2–18.5 mg/kg (4.7–28.4%) and Fe contents from 0.9–1.8 to 1.0–2.0 mg/plant (0–44.4%). There were significant differences between T3 and both T1 and T2 (Table 3).

3.2. Maize Agronomic Traits in Licheng

Compared with the control treatment, there were some numerical differences (an increase or decrease to some extent) in maize grain dry weights, hundred grain dry weights, and other ear traits following foliar spraying of sucrose and/or Zn (Table 4). However, as expected, non-significant differences among various foliar treatments were observed in the statistical analysis.

3.3. Maize Grain Zn and Fe Concentrations, Contents, and Bioavailability in Licheng

Except for significant reductions in the molar ratios of PA × Ca/Zn and PA × Ca/Fe, foliar spraying of sucrose-only (T2) did not significantly affect maize grain Zn and Fe accumulation (concentrations and contents) or molar ratios of PA/Zn and PA/Fe as compared with the foliar spraying of deionized water (Table 5). In comparison with the control (T1), foliar Zn-only spraying (T3) significantly increased the grain Zn concentration from 24.9 to 36.8 mg/kg (47.8%) and the Zn yield from 3.6 to 5.3 mg/plant (47.2%). In contrast, it significantly reduced the molar ratio of PA/Zn from 34.9 to 22.1 (36.7%) and PA × Ca/Zn from 70.1 to 35.8 (48.9%). Similarly, T3 significantly enhanced the grain Fe concentration by 25.0% and the content by 26.5%, and significantly reduced the molar ratio of PA/Fe by 24.5% and PA × Ca/Fe by 39.8%. Similar results were found in the Zn + sucrose treatment (T4). Except for the molar ratios of PA × Ca/Zn and PA × Ca/Fe, the grain Fe concentration in T4 and the molar ratio of PA/Fe in T3, both foliar Zn-biofortified treatments including T3 and T4 had significantly higher grain Zn and Fe accumulation and bioavailability than T2. No significant differences were found between Zn-only and Zn + sucrose (Table 5) foliar treatments.

3.4. Concentrations of Carbon, Nitrogen, Total and Phytate Phosphorus and Calcium, and Ratios of C/N and Phytate P/Total P in Maize Grains in Licheng

Compared with the control, foliar spraying of sucrose, Zn, or sucrose + Zn had no significant effects on carbon concentration or on the ratio of phytate P/total P, whereas the total and phytate P concentrations were significantly reduced by the sucrose + Zn treatment. Also, the Ca concentration was reduced in the sucrose-only treatment (Table 6). Sucrose alone or in combination with Zn significantly decreased the nitrogen concentration, but significantly increased the ratio of C/N as compared to the control and the Zn-only treatment.

3.5. Relationships between Zn and Fe Concentrations in Maize Grains

There were significant and positive linear correlations between Zn and Fe concentrations in maize grains when no N or 105 kg/ha N was applied, and across both N supply levels in the field experiment at Quzhou (Figure 1). Maize grain Fe concentrations were also significantly and positively correlated with Zn concentrations in the field experiment at Licheng and across both experimental sites (Figure 1).

4. Discussion

In a study by Mohsin et al. (2014) [48], the combined application of Zn as seed priming and foliar spray significantly improved the performance of maize hybrids, including the plant height, cob length, cob diameter, 1000 grain weight, biological yield, grain yield, and harvest index. Interestingly, increased Zn concentrations in maize kernels were also positively correlated with the grain yield, 1000 grain weight, cob length, and cob diameter [48]. Zinc fertilization has also been reported to have additional benefits like promoting growth at early stages and improving tolerance/resistance to abiotic/biotic stresses [36,49]. In the current study, foliar Zn and/or sucrose applications did not affect the yield or other agronomic traits of maize in Quzhou and Licheng (Table 3 and Table 4), suggesting that the dry-matter accumulation in maize grains is less dependent on exogenous foliar Zn and/or carbohydrate supply, at least under the conditions used in this study. Similar results were previously reported for maize and wheat under pot or field conditions [3,26,27,35,38,50,51]. For Zn, this finding may be attributed to the high Zn concentration in soil and the suitable soil conditions, and thus the good Zn nutritional status of plants. It could also be due to the very late application of Zn, which failed to promote crop growth during the seedling stage [27]. As an exception, the exogenous foliar spraying of Zn effectively supplemented the demand of wheat plants for Zn, which reduced drought-induced oxidative cell damage due to an improved antioxidative defense ability [52], thus increasing the grain yield under drought conditions, even in soil with a high DTPA–Zn concentration [53]. It has been observed that increasing sucrose concentrations within the optimal level substantially enhance grain yields and single grain weights of wheat and rice under detached-ear culture conditions [33,34,54]. Sasaki et al. (2005) [54] speculated that an increased supply of sucrose during the grain-filling period might improve the activity of enzymes involved in starch synthesis and lead to an increase in single grain weights. Hence, the effects of foliar applications of Zn and/or sucrose on maize yield situations warrant further research under various environmental conditions.
Consistent with other studies, the foliar supply of Zn alone significantly increased maize grain Zn accumulation [27] as well as the estimated Zn bioavailability in this study (Table 3 and Table 5). It has been reported that Zn concentrations in cereal grains are significantly and positively correlated with those in leaves, suggesting the importance of the source strength of physiologically available Zn within vegetative tissues, which can be effectively translocated or remobilized to the grain sink after flowering [50,55,56,57]. Hence, the foliar applied Zn would undoubtedly penetrate across the cuticle into maize leaves and contribute to an increase in grain Zn accumulation, as presented in the current study. Various studies have confirmed that eating Zn-biofortified maize helps individuals to meet their Zn requirements [58]. The current marked increase in the maize grain Zn concentration (9.2 and 11.9 mg/kg on average in Quzhou and Licheng, respectively) caused by Zn-only spraying would have a measurable impact, improving the human dietary intake of Zn to alleviate malnutrition [50,59]. Therefore, foliar Zn spraying should be adopted as an effective way to biofortify maize with Zn. However, to overcome Zn malnutrition, a Zn concentration of more than 37 mg/kg in the whole grain [60] and an increase of 30 mg/kg in the endosperm (www.harvestplus.org) of maize (because the major proportion of the maize grain is comprised of endosperm) are recommended. In terms of Zn bioavailability, the critical molar ratio of PA/Zn is 15–20; a value of 5–15 represents about 30–35% Zn availability, and ≥15 represents about 15% Zn availability [42]. The effectiveness of foliar Zn spraying on grain Zn concentrations is related to the spray timing, location, rates, type of fertilizers (e.g., nano-particles), maize genotypes, and environmental conditions [60]. Based on the low maize grain Zn concentrations (< 37 mg/kg) and high PA/Zn values (> 15) achieved by foliar spraying of 0.2% or 0.3% ZnSO4·7H2O (w/v) in our present study (Table 3 and Table 5), there is still a need to further enhance Zn absorption by maize, its translocation to grains, and its bioavailability, possibly by appropriately increasing the spraying frequency and Zn concentration and spraying with other beneficial fertilizers (e.g., urea) or stimulators [51]. Gomez-Coronado et al. (2016) [61] found that the foliar spraying of 0.5% ZnSO4·7H2O (w/v) on wheat increased grain Zn concentrations effectively with a better bioavailability. It is worth pointing out that the spraying doses of 50 or 100 mL for each maize plant were only applied under our experimental conditions, not for the actual practice. For actual large-scale practices, drone spraying with a higher Zn concentration solution containing some high efficient additives is possible to save a lot of doses, which need to be further studied.
In 1953, it was reported that the addition of sucrose to urea sprays reduced the injury of maize leaves, perhaps by reducing the rate of urea absorption and increasing the rate of urea translocation within the plant [62]. In our previous studies, foliar application of sucrose + Zn was associated with greater improvements in the concentration, content, and bioavailability of Zn in wheat (a C3 plant) than the spraying of Zn only [3,35]. As mentioned by Zhao et al. (2014) [51], the relatively higher effectiveness of sucrose + Zn may be attributed to (1) the longer drying time of the spraying solution; (2) enhanced leaf cuticle penetration; and (3) enhanced translocation of Zn from the absorption site to the grain sink. However, in the current study, this was shown to be totally ineffective for C4 maize (Table 3 and Table 5). Although treatments of foliar applications of Zn alone and combined with sucrose increased maize grain Zn concentrations, contents, and bioavailability, no significant differences were found between these two treatments regardless of the N application rate and experimental locations. It was found that 14C-sucrose was not transported within the grain in the same way as 65Zn [63]. The spraying of only sucrose had no impact on either grain Zn accumulation or bioavailability (as estimated by the molar ratio of PA/Zn) of maize (Table 3 and Table 5). In addition, foliar sucrose supply (with or without Zn) did not affect the maize grain C concentration significantly; rather, the significantly lower N concentrations led to significantly higher ratios of C/N (Table 6). However, higher C/N ratios were not associated with higher Zn accumulation and bioavailability in maize grains (Table 3, Table 5, and Table 6). Therefore, unlike wheat, foliar sucrose spraying played no role in lowering the deliquescent relative humidity of spray solutions [64] or facilitating swelling of the cuticle by the absorption of substantial amounts of water to form “water-filled pores” [65] to enhance the penetration of hydrophilic solutes across the maize cuticle [64] and ultimately increase the rate/amount of foliar Zn absorption. Simultaneously, its effect on the remobilization and translocation of Zn from maize leaves to grains might be negligible. Whether the sprayed sucrose, accompanying Zn or not, entered leaf cells and was translocated from leaves to grains needs to be further investigated. In a study by Myers et al. (2014) [12], in comparison with values under ambient CO2 conditions, the decline of grain Zn concentrations at elevated CO2 levels was notable in C3 crops, but the effect was less pronounced in C4 crops, which is consistent with the differences in their physiological processes. A high concentration of CO2 in C4 crops internally resulted in photosynthesis being CO2-saturated even under ambient CO2 conditions, leading to no stimulation of photosynthetic carbon assimilation at elevated CO2 levels under mesic growing conditions [66]. Similarly, the more prominent impact of foliar spraying “sucrose + Zn” than the foliar spraying Zn alone on improving Zn accumulation and bioavailability in wheat but not in maize grains in our study may also be consistent with the physiology of different types of crops. Maize (as a C4 plant) has a higher photosynthetic capacity to produce more carboxylates than C3 wheat; hence, maize grain mineral accumulation is less dependent on an exogenous foliar sucrose supply.
The relationship between Zn and Fe concentrations in major cereal crops (maize, rice, and wheat) is still uncertain, mostly antagonistic [67], seldom synergistic [68,69,70], and sometimes indifferent [71]. If biofortification of Zn in cereals leads to a loss of Fe, this is unacceptable, because the malnutrition caused by Fe deficiency is no less severe than that of Zn [30]. Saha et al. (2015) [30] reported that Zn application through soil (as basal) in combination with two foliar sprays (at maximum tillering (6–8 leaves) and flowering/silking stages) yielded Zn-dense but Fe-starved grains (including the ultimate processed food products) and straws/stalks of most cultivars (~90%) of maize, rice, and wheat. A significant positive linear correlation was found between the grain Fe and Zn concentrations in maize (but not wheat) in different soils and foliar Zn treatments in the Loess Plateau, China [27]. However, these studies did not clearly distinguish between the effects of soil Zn application and foliar Zn spraying. Soil and foliar applications have been reported to have differential effects on Zn concentrations of maize kernels [60]. Our study revealed that effects of various foliar treatments on maize grain Fe accumulation and bioavailability were similar to those on Zn. Foliar Zn spraying simultaneously improved the concentrations and bioavailability of Zn and Fe in maize grains irrespective of the foliar sucrose supply, but Fe increased to a lesser extent than Zn (Table 3 and Table 5). Significant and positive linear correlations between Zn and Fe concentrations in maize grains were observed at each N concentration and across both N supply levels in the field experiments at both Quzhou and Licheng as well as across these two different experimental locations (Figure 1). In contrast to Saha et al. (2015) [30], this indicates that Zn enrichment by foliar spraying of Zn has a benign effect on Fe in maize grains. This result suggests that this process can successfully achieve simultaneous Zn and Fe biofortification. In case of foliar Zn applications, genetic mechanisms regulating Zn absorption by maize leaves and translocation to grains are still unidentified [60]. It has also been reported that the foliar application of Zn not only increases the transport of shoot Fe to grains but also reduces cadmium toxicity in maize and other cereals [69]. This synergetic effect of Zn and Fe may be attributed to pleiotropic effects or linkage among the genes governing Zn and Fe accumulation in kernels. There are large numbers of genes involving the transport of various metals, some of them encoding proteins that are capable of transporting multiple metals, and the QTLs for these traits are also co-localized in the same chromosomal regions [72].

5. Conclusions

Foliar spraying of Zn and sucrose alone or in combination did not impact the agronomic traits of maize, including yield, indicating that dry-matter accumulation in grains is less dependent on exogenous foliar Zn and/or carbohydrate supply, at least under the conditions used in this study. The foliar applied Zn (with or without sucrose) undoubtedly penetrated the cuticle into maize leaves and contributed to an increase in grain Zn accumulation and bioavailability. The spraying of sucrose alone had no impact on either grain Zn accumulation or bioavailability. The combination of zinc and sucrose did not lead to a further significant increase in maize grain Zn accumulation and bioavailability compared with Zn-only spraying. In addition, the significantly lower N concentrations caused by the spraying of sucrose (with or without Zn) led to significantly higher ratios of C/N in maize grains, rather than higher Zn accumulation and bioavailability. Therefore, unlike the previously reported effects on wheat, foliar spraying of exogenous sucrose did not promote the absorption of Zn by maize leaves and its transport to grains. This may be consistent with the physiology of different types of crops. C4 maize has a higher photosynthetic capacity to produce more carboxylates than C3 wheat, leading to maize grain mineral accumulation that is less dependent on an exogenous foliar sucrose supply. Similar results were obtained for maize grain Fe accumulation and bioavailability, but the Fe concentration increased less than that of Zn. The Fe concentration was significantly and positively correlated with Zn, indicating that foliar Zn spraying facilitated the transport of endogenous Fe to maize grains. Therefore, foliar spraying of Zn achieved biofortification of both Zn and Fe in maize grains simultaneously, i.e., “killing two birds with one stone.”

Author Contributions

Methodology, H.X.; investigation, H.X., W.K., L.W. and Y.X.; resources, W.L., C.Z., S.Y. and C.L.; writing—original draft preparation, H.X. and W.K.; writing—review and editing, H.X.

Funding

This research was financially supported by the National Key Research and Development Program of China (2017YFD0300407, 2016YFD0300202), the Shandong Provincial Innovation Project for Agricultural Key Technology Application: Research and Demonstration of Annual Planting Patterns and Key Technologies for Green Improvement of Grain, Industrial and Forage Crops Production, the Innovation Project of Shandong Academy of Agricultural Sciences (CXGC2016B04), the National Natural Science Foundation of China (31501834), and the Corn Innovation Team of Shandong Provincial Modern Agricultural Industry and Technology System (SDAIT-01-021-11, SDAIT-02-11).

Acknowledgments

We thank the reviewers for valuable comments and suggestions, and the editors for their valuable work. The assistance of Yanfang Xue from Maize Research Institute of Shandong Academy of Agricultural Sciences, China, with the Quzhou field experiment is also gratefully acknowledged.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Nuss, E.T.; Tanumihardjo, S.A. Maize: A paramount staple crop in the context of global nutrition. Compr. Rev. Food Sci. Food Saf. 2010, 9, 417–436. [Google Scholar] [CrossRef]
  2. Xue, Y.; Yue, S.; Zhang, W.; Liu, D.; Cui, Z.; Chen, X.; Ye, Y.; Zou, C. Zinc, iron, manganese and copper uptake requirement in response to nitrogen supply and the increased grain yield of summer maize. PLoS ONE 2014, 9, e93895. [Google Scholar] [CrossRef]
  3. Xia, H.; Xue, Y.; Liu, D.; Kong, W.; Xue, Y.; Tang, Y.; Li, J.; Li, D.; Mei, P. Rational application of fertilizer nitrogen to soil in combination with foliar Zn spraying improved Zn nutritional quality of wheat grains. Front. Plant Sci. 2018, 9, 677. [Google Scholar] [CrossRef] [PubMed]
  4. Cakmak, I. Enrichment of cereal grains with zinc: Agronomic or genetic biofortification? Plant Soil 2008, 302, 1–17. [Google Scholar] [CrossRef]
  5. Takkar, P.N.; Walker, C.D. The distribution and correction of zinc deficiency. In Zinc in Soils and Plants; Robson, A.D., Ed.; Kluwer Academic Publishers: Dordrecht, The Netherlands, 1993; Volume 55, pp. 151–165. [Google Scholar]
  6. Yang, X.; Chen, W.; Feng, Y. Improving human micronutrient nutrition through biofortification in the soil-plant system: China as a case study. Environ. Geochem. Health 2007, 29, 413–428. [Google Scholar] [CrossRef]
  7. Wang, S.; Gao, L.; Liu, Z.; Huang, J.; Chen, L.; Liu, R.; Wang, H. Effect of zinc on maize leaf cell ultra-structure under different soil moistures. Chin. J. Eco-Agric. 2013, 21, 959–965. (In Chinese) [Google Scholar] [CrossRef]
  8. Cakmak, I. Plant nutrition research: Priorities to meet human needs for food in sustainable ways. Plant Soil 2002, 247, 3–24. [Google Scholar] [CrossRef]
  9. Garvin, D.F.; Welch, R.M.; Finley, J.W. Historical shifts in the seed mineral micronutrient concentration of US hard red winter wheat germplasm. J. Sci. Food Agric. 2006, 86, 2213–2220. [Google Scholar] [CrossRef]
  10. Scagel, C.; Bi, G.; Fuchigami, L.; Regan, R. Irrigation frequency alters nutrient uptake in container-grown rhododendron plants grown with different rates of nitrogen. HortScience 2012, 47, 189–197. [Google Scholar] [CrossRef]
  11. Saha, B.; Saha, S.; Poddar, P.; Murmu, S.; Singh, A.K. Uptake of nutrients by wheat as influenced by long-term phosphorus fertilization. Bioscan 2013, 8, 1331–1335. [Google Scholar]
  12. Myers, S.S.; Zanobetti, A.; Kloog, I.; Huybers, P.; Leakey, A.D.B.; Bloom, A.J.; Carlisle, E.; Dietterich, L.H.; Fitzgerald, G.; Hasegawa, T.; et al. Increasing CO2 threatens human nutrition. Nature 2014, 510, 139–142. [Google Scholar] [CrossRef] [PubMed]
  13. Shewry, P.R.; Pellny, T.K.; Lovegrove, A. Is modern wheat bad for health? Nat. Plants 2016, 2, 16097. [Google Scholar] [CrossRef] [PubMed]
  14. Cakmak, I.; Kutman, U.B. Agronomic biofortification of cereals with zinc: A review. Eur. J. Soil Sci. 2018, 69, 172–180. [Google Scholar] [CrossRef]
  15. Li, X.; Ulfat, A.; Lv, Z.; Fang, L.; Jiang, D.; Liu, F. Effect of multigenerational exposure to elevated atmospheric CO2 concentration on grain quality in wheat. Environ. Exp. Bot. 2019, 157, 310–319. [Google Scholar] [CrossRef]
  16. Moreno-Jiménez, E.; Plaza, C.; Saiz, H.; Manzano, R.; Flagmeier, M.; Maestre, F.T. Aridity and reduced soil micronutrient availability in global drylands. Nat. Sustain. 2019, 2, 371–377. [Google Scholar] [CrossRef] [PubMed]
  17. White, P.J.; Broadley, M.R. Biofortification of crops with seven mineral elements often lacking in human diets—Iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol. 2009, 182, 49–84. [Google Scholar] [CrossRef] [PubMed]
  18. Rodgers, A.; Ezzati, M.; Hoorn, S.V.; Lopez, A.D.; Lin, R.-B.; Murray, C.J.L.; Collaborating, G.C.R.A. Distribution of major health risks: Findings from the global burden of disease study. PLoS Med. 2004, 1, e27. [Google Scholar] [CrossRef] [PubMed]
  19. Ma, G.; Jin, Y.; Piao, J.; Kok, F.; Guusje, B.; Jacobsen, E. Phytate, calcium, iron, and zinc contents and their molar ratios in foods commonly consumed in China. J. Agric. Food Chem. 2005, 53, 10285–10290. [Google Scholar] [CrossRef]
  20. Clemens, S. Zn and Fe biofortification: The right chemical environment for human bioavailability. Plant Sci. 2014, 225, 52–57. [Google Scholar] [CrossRef]
  21. Chen, X.; Zhang, Y.; Tong, Y.; Xue, Y.; Liu, D.; Zhang, W.; Deng, Y.; Meng, Q.; Yue, S.; Yan, P.; et al. Harvesting more grain zinc of wheat for human health. Sci. Rep. 2017, 7, 7016. [Google Scholar] [CrossRef]
  22. Orabi, A.A.; Mashadi, H.; Abdallah, A.; Morsy, M. Effect of zinc and phosphorus on the grain yield of corn (Zea mays L.) grown on a calcareous soil. Plant Soil 1981, 63, 291–294. [Google Scholar] [CrossRef]
  23. Hossain, M.A.; Jahiruddin, M.; Islam, M.R.; Mian, M.H. The requirement of zinc for improvement of crop yield and mineral nutrition in the maize–mungbean–rice system. Plant Soil 2008, 306, 13–22. [Google Scholar] [CrossRef]
  24. Kanwal, S.; Rahmatullah, A.R.; Ahmad, R. Zinc partitioning in maize grain after soil fertilization with zinc sulfate. Int. J. Agric. Biol. 2010, 12, 299–302. [Google Scholar]
  25. Peck, A.W.; McDonald, G.K.; Graham, R.D. Zinc nutrition influences the protein composition of flour in bread wheat (Triticum aestivum L.). J. Cereal Sci. 2008, 47, 266–274. [Google Scholar] [CrossRef]
  26. Zhang, Y.-Q.; Sun, Y.-X.; Ye, Y.-L.; Karim, M.R.; Xue, Y.-F.; Yan, P.; Meng, Q.-F.; Cui, Z.-L.; Cakmak, I.; Zhang, F.-S.; et al. Zinc biofortification of wheat through fertilizer applications in different locations of China. Field Crops Res. 2012, 125, 1–7. [Google Scholar] [CrossRef]
  27. Wang, J.; Mao, H.; Zhao, H.; Huang, D.; Wang, Z. Different increases in maize and wheat grain zinc concentrations caused by soil and foliar applications of zinc in Loess Plateau, China. Field Crops Res. 2012, 135, 89–96. [Google Scholar] [CrossRef]
  28. Prasad, R.; Shivay, Y.S.; Kumar, D. Agronomic biofortification of cereal grains with iron and zinc. Adv. Agron. 2014, 125, 55–91. [Google Scholar]
  29. Niyigaba, E.; Twizerimana, A.; Mugenzi, I.; Ngnadong, W.A.; Ye, Y.P.; Wu, B.M.; Hai, J.B. Winter wheat grain quality, zinc and iron concentration affected by a combined foliar spray of zinc and iron fertilizers. Agronomy 2019, 9, 250. [Google Scholar] [CrossRef]
  30. Saha, S.; Mandal, B.; Hazra, G.C.; Dey, A.; Chakraborty, M.; Adhikari, B.; Mukhopadhyay, S.K.; Sadhukhan, R. Can agronomic biofortification of zinc be benign for iron in cereals? J. Cereal Sci. 2015, 65, 186–191. [Google Scholar] [CrossRef]
  31. Pearson, J.N.; Rengel, Z.; Jenner, C.F.; Graham, R.D. Manipulation of xylem transport affects Zn and Mn transport into developing wheat grains of cultured ears. Physiol. Plant. 1996, 98, 229–234. [Google Scholar] [CrossRef]
  32. Ma, Y.Z.; MacKown, C.T.; Van Sanford, D.A. Differential effects of partial spikelet removal and defoliation on kernel growth and assimilate partitioning among wheat cultivars. Field Crops Res. 1996, 47, 201–209. [Google Scholar] [CrossRef]
  33. Zhang, Y.; Zhang, Y.; Liu, N.; Su, D.; Xue, Q.; Stewart, B.; Wang, Z. Effect of source-sink manipulation on accumulation of micronutrients and protein in wheat grains. J. Plant Nutr. Soil Sci. 2012, 175, 622–629. [Google Scholar] [CrossRef]
  34. Liu, N.; Zhang, Y.; Wang, B.; Xue, Y.; Yu, P.; Zhang, Q.; Wang, Z. Is grain zinc concentration in wheat limited by source? Aust. J. Crop Sci. 2014, 8, 1534–1541. [Google Scholar]
  35. Xia, H.; Xue, Y.; Kong, W.; Tang, Y.; Li, J.; Li, D. Effects of source/sink manipulation on grain zinc accumulation by winter wheat genotypes. Chil. J. Agric. Res. 2018, 78, 117–125. [Google Scholar] [CrossRef]
  36. Welch, R.M.; Graham, R.D. Breeding for micronutrients in staple food crops from a human nutrition perspective. J. Exp. Bot. 2004, 55, 353–364. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  37. Brinch-Pedersen, H.; Borg, S.; Tauris, B.; Holm, P.B. Molecular genetic approaches to increasing mineral availability and vitamin content of cereals. J. Cereal Sci. 2007, 46, 308–326. [Google Scholar] [CrossRef]
  38. Cakmak, I.; Pfeiffer, W.H.; McClafferty, B. Biofortification of durum wheat with zinc and iron. Cereal Chem. 2010, 87, 10–20. [Google Scholar] [CrossRef]
  39. Morris, E.R.; Ellis, R. Phytate, wheat bran, and bioavailability of dietary iron. ACS Symp. Ser. 1982, 203, 121–141. [Google Scholar]
  40. Ryan, M.H.; McInerney, J.K.; Record, I.R.; Angus, J.F. Zinc bioavailability in wheat grain in relation to phosphorus fertiliser, crop sequence and mycorrhizal fungi. J. Sci. Food Agric. 2008, 88, 1208–1216. [Google Scholar] [CrossRef]
  41. Liu, D.; Liu, Y.; Zhang, W.; Chen, X.; Zou, C. Agronomic approach of zinc biofortification can increase zinc bioavailability in wheat flour and thereby reduce zinc deficiency in humans. Nutrients 2017, 9, 465. [Google Scholar]
  42. World Health Organization (WHO). Trace Elements in Human Nutrition and Health; WHO: Geneva, Switzerland, 1996. [Google Scholar]
  43. Glahn, R.P.; Wortley, G.M.; South, P.K.; Miller, D.D. Inhibition of iron uptake by phytic acid, tannic acid, and ZnCl2: Studies using an in vitro digestion/Caco-2 cell model. J. Agric. Food Chem. 2002, 50, 390–395. [Google Scholar] [CrossRef] [PubMed]
  44. Ellis, R.; Kelsay, J.L.; Reynolds, R.D.; Morris, E.R.; Moser, P.B.; Frazier, C.W. Phytate: zinc and phytate × calcium:zinc millimolar ratios in self-selected diets of Americans, Asian Indians, and Nepalese. J. Am. Diet. Assoc. 1987, 87, 1043–1047. [Google Scholar] [PubMed]
  45. Zhang, S.; Yue, S.; Yan, P.; Qiu, M.; Chen, X.; Cui, Z. Testing the suitability of the end-of-season stalk nitrate test for summer corn (Zea mays L.) production in China. Field Crops Res. 2013, 154, 153–157. [Google Scholar] [CrossRef]
  46. Xia, H.; Wang, L.; Xue, Y.; Kong, W.; Xue, Y.; Yu, R.; Wang, X.; Wang, J.; Liu, Z.; Guo, X. Impact of increasing maize densities on agronomic performances and the community stability of productivity of maize/peanut intercropping systems. Agronomy 2019, 9, 150. [Google Scholar] [CrossRef]
  47. Haug, W.; Lantzsch, H. Sensitive method for the rapid determination of phytate in cereals and cereal products. J. Sci. Food Agric. 1983, 34, 1423–1426. [Google Scholar] [CrossRef]
  48. Mohsin, A.U.; Ahmad, A.U.H.; Farooq, M.; Ullah, S. Influence of zinc application through seed treatment and foliar spray on growth, productivity and grain quality of hybrid maize. J. Anim. Plant Sci. 2014, 24, 1494–1503. [Google Scholar]
  49. Bouis, H.E. Micronutrient fortification of plants through plant breeding: Can it improve nutrition in man at low cost? Proc. Nutr. Soc. 2003, 62, 403–411. [Google Scholar] [CrossRef]
  50. Cakmak, I.; Kalayci, M.; Kaya, Y.; Torun, A.A.; Aydin, N.; Wang, Y.; Arisoy, Z.; Erdem, H.; Yazici, A.; Gokmen, O.; et al. Biofortification and localization of zinc in wheat grain. J. Agric. Food Chem. 2010, 58, 9092–9102. [Google Scholar] [CrossRef]
  51. Zhao, A.Q.; Tian, X.H.; Cao, Y.X.; Lu, X.C.; Liu, T. Comparison of soil and foliar zinc application for enhancing grain zinc content of wheat when grown on potentially zinc-deficient calcareous soils. J. Sci. Food Agric. 2014, 94, 2016–2022. [Google Scholar] [CrossRef]
  52. Cakmak, I. Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytol. 2000, 146, 185–205. [Google Scholar] [CrossRef]
  53. Karim, M.; Zhang, Y.; Zhao, R.; Chen, X.; Zhang, F.; Zou, C. Alleviation of drought stress in winter wheat by late foliar application of zinc, boron, and manganese. J. Plant Nutr. Soil Sci. 2012, 175, 142–151. [Google Scholar] [CrossRef]
  54. Sasaki, H.; Edo, E.; Uehara, N.; Ishimaru, T.; Kawamitsu, Y.; Suganuma, S.; Ueda, D.; Ohsugi, R. Effect of sucrose on activity of starch synthesis enzymes in rice ears in culture. Physiol. Plant. 2005, 124, 301–310. [Google Scholar] [CrossRef]
  55. Haslett, B.S.; Reid, R.J.; Rengel, Z. Zinc mobility in wheat: Uptake and distribution of zinc applied to leaves or roots. Ann. Bot. 2001, 87, 379–386. [Google Scholar] [CrossRef]
  56. Kutman, U.B.; Yildiz, B.; Ozturk, L.; Cakmak, I. Biofortification of durum wheat with zinc through soil and foliar applications of nitrogen. Cereal Chem. 2010, 87, 1–9. [Google Scholar] [CrossRef]
  57. Zou, C.; Zhang, Y.; Rashid, A.; Ram, H.; Savasli, E.; Arisoy, R.; Ortiz-Monasterio, I.; Simunji, S.; Wang, Z.; Sohu, V.; et al. Biofortification of wheat with zinc through zinc fertilization in seven countries. Plant Soil 2012, 361, 119–130. [Google Scholar] [CrossRef]
  58. Chomba, E.; Westcott, C.M.; Westcott, J.E.; Mpabalwani, E.M.; Krebs, N.F.; Patinkin, Z.W.; Palacios, N.; Hambidge, K.M. Zinc absorption from biofortified maize meets the requirements of young rural Zambian children. J. Nutr. 2015, 145, 514–519. [Google Scholar] [CrossRef] [PubMed]
  59. Graham, R.D.; Welch, R.M.; Saunders, D.A.; Ortiz-Monasterio, I.; Bouis, H.E.; Bonierbale, M.; De Haan, S.; Burgos, G.; Thiele, G.; Liria, R.; et al. Nutritious subsistence food systems. Adv. Agron. 2007, 92, 1–74. [Google Scholar]
  60. Maqbool, M.A.; Beshir, A. Zinc biofortification of maize (Zea mays L.): Status and challenges. Plant Breed. 2019, 138, 1–28. [Google Scholar] [CrossRef]
  61. Gomez-Coronado, F.; Poblaciones, M.J.; Almeida, A.S.; Cakmak, I. Zinc (Zn) concentration of bread wheat grown under Mediterranean conditions as affected by genotype and soil/foliar Zn application. Plant Soil 2016, 401, 331–346. [Google Scholar] [CrossRef]
  62. Foy, C.D.; Montenegro, G.; Barber, S.A. Foliar feeding of corn with urea nitrogen. Soil Sci. Soc. Am. 1953, 17, 387–390. [Google Scholar] [CrossRef]
  63. Pearson, J.N.; Jenner, C.F.; Rengel, Z.; Graham, R.D. Differential transport of Zn, Mn and sucrose along the longitudinal axis of developing wheat grains. Physiol. Plant. 1996, 97, 332–338. [Google Scholar] [CrossRef]
  64. Fernández, V.; Bahamonde, H.A.; Peguero-Pina, J.J.; Gil-Pelegrín, E.; Sancho-Knapik, D.; Gil, L.; Goldbach, H.E.; Eichert, T. Physico-chemical properties of plant cuticles and their functional and ecological significance. J. Exp. Bot. 2017, 68, 5293–5306. [Google Scholar] [CrossRef] [PubMed]
  65. Schreiber, L. Polar paths of diffusion across plant cuticles: New evidence for an old hypothesis. Ann. Bot. 2005, 95, 1069–1073. [Google Scholar] [CrossRef] [PubMed]
  66. Leakey, A.; Ainsworth, E.; Bernacchi, C.; Rogers, A.; Long, S. Elevated CO2 effects on plant carbon, nitrogen, and water relations: Six important lessons from FACE. J. Exp. Bot. 2009, 60, 2859–2876. [Google Scholar] [CrossRef] [PubMed]
  67. Giordano, P.M.; Mortvedt, J.J. Rice response to zinc in flooded and nonflooded soil. Agron. J. 1972, 64, 521–524. [Google Scholar] [CrossRef]
  68. Chakraborti, M.; Prasanna, B.; Hossain, F.; Singh, A.; Guleria, S. Genetic evaluation of kernel Fe and Zn concentrations and yield performance of selected Maize (Zea mays L.) genotypes. Range Manag. Agrofor. 2009, 30, 109–114. [Google Scholar]
  69. Aref, F. Zinc and boron fertilization on concentration and uptake of iron and manganese in the corn grain. J. Anim. Sci. 2010, 6, 236–242. [Google Scholar]
  70. Zeidan, M.S.; Mohamed, M.F.; Hamouda, H.A. Effect of foliar fertilization of Fe, Mn and Zn on wheat yield and quality in low sandy soils fertility. World J. Agric. Sci. 2010, 6, 696–699. [Google Scholar]
  71. Zhao, A.; Bao, Q.; Tian, X.; Lu, X.; Gale, W. Combined effect of iron and zinc on micronutrient levels in wheat (Triticum aestivum L.). J. Environ. Biol. 2011, 32, 235–239. [Google Scholar]
  72. Qin, H.; Cai, Y.; Liu, Z.; Wang, G.; Wang, J.; Guo, Y.; Wang, H. Identification of QTL for zinc and iron concentration in maize kernel and cob. Euphytica 2012, 187, 345–358. [Google Scholar] [CrossRef]
Agronomy 09 00386 g001 550
Figure 1. Relationships between Zn and Fe concentrations in maize grains across all foliar spraying treatments at different nitrogen (N) application rates and different experimental locations. * indicates significance at p ≤ 0.05; **, significance at p ≤ 0.01.
Figure 1. Relationships between Zn and Fe concentrations in maize grains across all foliar spraying treatments at different nitrogen (N) application rates and different experimental locations. * indicates significance at p ≤ 0.05; **, significance at p ≤ 0.01.
Agronomy 09 00386 g001
Table
Table 1. Detailed site locations (geographic coordinates) and soil basal properties in 0–20 cm soil layers before maize sowing.
Table 1. Detailed site locations (geographic coordinates) and soil basal properties in 0–20 cm soil layers before maize sowing.
YearExperimental SiteGeographic CoordinatesSoil TypepH (2.5:1 Water:Soil Ratio)Organic MatterTotal NitrogenAlkaline HydrolysisOlsen PExchangeable KDTPA-Extractable Zn
(g/kg)(g/kg)Nitrogen (mg/kg)(mg/kg)(mg/kg)(mg/kg)
2010Quzhou115°0′ E, 36°54′ NCalcareous alluvial soil8.314.50.92-14.9130.52.8
2016Licheng117°04′ E, 36°42′ NCalcareous alluvial soil8.015.7-90.520.2142.61.5
Table
Table 2. Foliar spraying treatments.
Table 2. Foliar spraying treatments.
TreatmentsSolution Composition
T1ControlDeionized water
T2Sucrose10.0% (w/v)
T3ZnSO4·7H2O (Zn)0.2% in Quzhou and 0.3% in Licheng (w/v)
T4Zn + SucroseA combination of T2 and T3
Table
Table 3. Effects of different foliar treatments and N application rates on maize grain dry weights (GDW), total dry weights (TDW) including grain and straw, hundred grain dry weights (HGDW) and grain Zn concentrations and contents in the field experiment at Quzhou.
Table 3. Effects of different foliar treatments and N application rates on maize grain dry weights (GDW), total dry weights (TDW) including grain and straw, hundred grain dry weights (HGDW) and grain Zn concentrations and contents in the field experiment at Quzhou.
ParametersTreatmentsN application Rates (kg/ha)ANOVA
0105Mean
GDWT1Deionized water67.6 ± 1.7 a104.9 ± 16.4 a86.2 ± 7.3 AN0.0052
(g per ear)T2Sucrose66.8 ± 19.3 a104.6 ± 13.6 a85.7 ± 16.3 AT0.4983
T3ZnSO4·7H2O (Zn)75.6 ± 19.0 a114.6 ± 25.2 a95.1 ± 22.1 AN × T0.9898
T4Sucrose + Zn65.9 ± 10.0 a99.7 ± 10.9 a82.8 ± 10.5 A
Mean69.0 ± 11.3 B106.0 ± 8.9 A87.5 ± 9.9
TDWT1Deionized water136.5 ± 12.0 a224.3 ± 26.6 a180.4 ± 9.0 AN<0.0001
(g per plant)T2Sucrose134.3 ± 30.2 a206.0 ± 12.2 a170.2 ± 20.9 AT0.4732
T3ZnSO4·7H2O (Zn)143.4 ± 33.9 a221.7 ± 29.5 a182.5 ± 30.7 AN × T0.8051
T4Sucrose + Zn134.1 ± 13.1 a201.5 ± 10.0 a167.8 ± 11.3 A
Mean137.1 ± 20.7 B213.4 ± 8.8 A175.2 ± 14.4
HGDWT1Deionized water28.3 ± 2.9 a32.5 ± 2.5 a30.4 ± 0.5 AN0.0001
(g)T2Sucrose28.1 ± 1.3 a30.7 ± 1.1 a29.4 ± 0.6 AT0.2814
T3ZnSO4·7H2O (Zn)27.3 ± 1.5 a31.4 ± 1.4 a29.4 ± 0.9 AN × T0.6057
T4Sucrose + Zn27.5 ± 2.2 a31.0 ± 1.4 a29.2 ± 0.7 A
Mean27.8 ± 1.9 B31.4 ± 1.3 A29.6 ± 0.5
Grain ZnT1Deionized water18.4 ± 1.1 b19.9 ± 1.0 b19.1 ± 0.5 BN0.4941
concentrationT2Sucrose19.5 ± 2.8 b18.7 ± 2.7 b19.1 ± 2.4 BT<0.0001
(mg/kg)T3ZnSO4·7H2O (Zn)28.6 ± 1.0 a28.0 ± 1.1 a28.3 ± 0.3 AN × T0.2453
T4Sucrose + Zn25.2 ± 1.4 ab29.6 ± 5.6 a27.4 ± 2.4 A
Mean22.9 ± 0.6 A24.1 ± 2.2 A23.5 ± 1.0
Grain ZnT1Deionized water1.2 ± 0.1 b2.1 ± 0.3 b1.7 ± 0.1 BN0.0357
contentT2Sucrose1.3 ± 0.2 b1.9 ± 0.2 b1.6 ± 0.1 BT0.0008
(mg per plant)T3ZnSO4·7H2O (Zn)2.2 ± 0.6 a3.2 ± 0.6 a2.7 ± 0.6 AN × T0.5642
T4Sucrose + Zn1.7 ± 0.3 ab2.9 ± 0.6 a2.3 ± 0.3 A
Mean1.6 ± 0.3 B2.5 ± 0.2 A2.1 ± 0.2
Grain FeT1Deionized water13.4 ± 1.4 a17.1 ± 0.9 ab15.2 ± 1.2 BN0.0091
concentrationT2Sucrose14.4 ± 1.4 a15.4 ± 2.0 b14.9 ± 0.3 BT0.0587
(mg/kg)T3ZnSO4·7H2O (Zn)17.2 ± 3.3 a17.9 ± 1.6 ab17.6 ± 2.1 AN × T0.1656
T4Sucrose + Zn15.2 ± 1.6 a18.5 ± 1.2 a16.8 ± 0.6 AB
Mean15.0 ± 1.8 B17.2 ± 0.9 A16.1 ± 0.8
Grain FeT1Deionized water0.9 ± 0.1 a1.8 ± 0.2 ab1.3 ± 0.1 BN0.0325
contentT2Sucrose1.0 ± 0.4 a1.6 ± 0.1 b1.3 ± 0.2 BT0.0470
(mg per plant)T3ZnSO4·7H2O (Zn)1.3 ± 0.6 a2.0 ± 0.4 a1.7 ± 0.5 AN × T0.7565
T4Sucrose + Zn1.0 ± 0.3 a1.8 ± 0.1 ab1.4 ± 0.2 AB
Mean1.1 ± 0.3 B1.8 ± 0.1 A1.4 ± 0.2
Values are means ± standard deviation (n = 3). Values in the same column followed by different lowercase letters are significantly different among various foliar treatments according to Fisher’s Protected LSD test (p < 0.05). Values followed by different capital letters are significantly different between different N application rates (horizontal comparison) or among various foliar treatments (vertical comparison) according to Fisher’s Protected LSD test (p < 0.05).
Table
Table 4. Maize agronomic traits among various foliar spraying treatments in the field experiment at Licheng.
Table 4. Maize agronomic traits among various foliar spraying treatments in the field experiment at Licheng.
TreatmentsGrain Dry Weight (g/ear)Hundred Grain Weight (g)Number of Kernels per EarEar Diameter (mm)Ear Length (cm)Bald Tip Length (cm)Bald Tip Length/Ear Length (%)
T1Deionized water142.8 ± 15.7 a37.8 ± 2.2 a485.6 ± 119.5 a50.9 ± 3.1 a20.8 ± 3.5 a1.5 ± 0.4 a7.2 ± 2.2 a
T2Sucrose139.6 ± 10.4 a38.6 ± 1.7 a518.4 ± 103.4 a48.5 ± 5.2 a21.9 ± 1.5 a2.2 ± 1.1 a10.0 ± 2.0 a
T3ZnSO4·7H2O (Zn)143.6 ± 13.2 a36.1 ± 1.3 a523.4 ± 96.6 a46.0 ± 4.8 a21.3 ± 1.3 a2.2 ± 0.4 a10.3 ± 4.9 a
T4Sucrose + Zn150.9 ± 20.1 a37.9 ± 1.3 a500.0 ± 120.7 a50.0 ± 2.7 a20.0 ± 1.2 a1.6 ± 1.1 a8.0 ± 5.5 a
Values are means ± standard deviation (n = 3). Values in the same column followed by same lowercase letters are not significantly different among various foliar treatments according to Fisher’s Protected LSD test (p < 0.05).
Table
Table 5. Effects of different foliar treatments on Zn and Fe concentrations, contents and molar ratios of PA/Zn, PA × Ca/Zn, PA/Fe, and PA × Ca/Fe in maize grains in the field experiment at Licheng.
Table 5. Effects of different foliar treatments on Zn and Fe concentrations, contents and molar ratios of PA/Zn, PA × Ca/Zn, PA/Fe, and PA × Ca/Fe in maize grains in the field experiment at Licheng.
TreatmentsZn Concentrations (mg/kg)Zn Contents (mg/plant) PA/ZnPA × Ca/ZnFe Concentrations (mg/kg)Fe Contents (mg/plant)PA/FePA × Ca/Fe
T1Deionized water24.9 ± 0.8 b3.6 ± 0.1 b34.9 ± 3.6 a70.1 ± 3.5 a24.0 ± 2.8 b3.4 ± 0.3 b31.4 ± 4.3 a63.0 ± 5.2 a
T2Sucrose23.8 ± 0.6 b3.3 ± 0.1 b32.6 ± 2.8 a37.9 ± 1.9 b23.1 ± 0.5 b3.2 ± 0.1 b28.9 ± 2.8 ab33.6 ± 2.1 b
T3ZnSO4·7H2O (Zn)36.8 ± 2.0 a5.3 ± 0.3 a22.1 ± 2.0 b35.8 ± 7.6 b30.0 ± 3.9 a4.3 ± 0.5 a23.7 ± 4.1 bc37.9 ± 7.1 b
T4Sucrose + Zn34.8 ± 0.8 a5.3 ± 0.2 a18.9 ± 2.4 b36.7 ± 11.5 b27.7 ± 1.2 ab4.2 ± 0.2 a20.4 ± 2.3c39.5 ± 10.8 b
Values are means ± standard deviation (n = 3). Values in the same column followed by different lowercase letters are significantly different among various foliar treatments according to Fisher’s Protected LSD test (p < 0.05).
Table
Table 6. Effects of different foliar treatments on the concentrations of carbon, nitrogen, phytate P, total P, and Ca, and ratios of C/N and phytate P/total P in maize grains in the field experiment at Licheng.
Table 6. Effects of different foliar treatments on the concentrations of carbon, nitrogen, phytate P, total P, and Ca, and ratios of C/N and phytate P/total P in maize grains in the field experiment at Licheng.
TreatmentsCarbon Concentration (%)Nitrogen Concentration (%)C/NPhytate-P Concentration (g/kg)Total P Concentration (g/kg)Phytate P/Total P (%)Ca Concentration (mg/kg)
T1Deionized water42.8 ± 0.5 a1.78 ± 0.02 a24.07 ± 0.06 b2.49 ± 0.18 a3.24 ± 0.08 a76.8 ± 7.5 a80.8 ± 6.1 a
T2Sucrose42.7 ± 0.6 a1.69 ± 0.03 b25.27 ± 0.27 a2.22 ± 0.25 ab3.01 ± 0.10 ab73.8 ± 6.8 a46.6 ± 1.7 b
T3ZnSO4·7H2O (Zn)42.8 ± 0.1 a1.76 ± 0.03 a24.36 ± 0.40 b2.33 ± 0.17 ab3.07 ± 0.25 ab76.2 ± 7.2 a65.4 ± 17.0 ab
T4Sucrose + Zn42.7 ± 0.3 a1.70 ± 0.01 b25.11 ± 0.12 a1.88 ± 0.27 b2.79 ± 0.07 b67.4 ± 8.2 a77.5 ± 19.0 a
Values are means ± standard deviation (n = 3). Values in the same column followed by different lowercase letters are significantly different among various foliar treatments according to Fisher’s Protected LSD test (p < 0.05).

Share and Cite

MDPI and ACS Style

Xia, H.; Kong, W.; Wang, L.; Xue, Y.; Liu, W.; Zhang, C.; Yang, S.; Li, C. Foliar Zn Spraying Simultaneously Improved Concentrations and Bioavailability of Zn and Fe in Maize Grains Irrespective of Foliar Sucrose Supply. Agronomy 2019, 9, 386. https://doi.org/10.3390/agronomy9070386

AMA Style

Xia H, Kong W, Wang L, Xue Y, Liu W, Zhang C, Yang S, Li C. Foliar Zn Spraying Simultaneously Improved Concentrations and Bioavailability of Zn and Fe in Maize Grains Irrespective of Foliar Sucrose Supply. Agronomy. 2019; 9(7):386. https://doi.org/10.3390/agronomy9070386

Chicago/Turabian Style

Xia, Haiyong, Weilin Kong, Lan Wang, Yanhui Xue, Wenlong Liu, Chunyan Zhang, Shenggang Yang, and Chong Li. 2019. "Foliar Zn Spraying Simultaneously Improved Concentrations and Bioavailability of Zn and Fe in Maize Grains Irrespective of Foliar Sucrose Supply" Agronomy 9, no. 7: 386. https://doi.org/10.3390/agronomy9070386

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop